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with essayson the social and political sienificance of evolutionary biology today. A second, encyclopedic section travels the spectrum of topics in evolution with concise, informative, and accessibleentries on individuals from Aristotle and Linnaeus to Louis Leakey and Jean Lamarck; from T. H. Huxley and Edward O. Wilson to Joseph Felsenstein and Motoo Kimura; and on subjects fronr altruism and an-rphibiansto evolutionary psychology and Piltdown Man to the Scopestrial and social Darwinism. Readers will find the latest word on the history and philosophy of evolution, the nuancesof the scienceitself, and the intricate interplay anong evolutionary study,religion, philosophy, and sociery. Appearing at the beginning of the Darwin Year of 2oo9-the
zooth anniversary of the
birth of Charles Darwin and the rjoth anniversary of the publication of the Origirt o-f Species-this volume is a fitting tribute to the s c i e n c eD a r w i n s e t i n n l o t i o n .
M TcHAEL
RUSE
i s L u c y l eT . W e r k n r e i s t e r
Professor of Philosophy and Director of the Progranr in the History and Philosophy of Science, Florida State (Jniversiry.He is the founder and ediBiologyand Philosophyand has ap-
tor ofthejournal
peared on "Quirks and Quarks" and the Discovery Channel. His books include Tlrc Euolution-Crcdtiort Struggleand Danyin and Desigtrftoth from Harvard). J oS EPH
T R A V T S i s D e a n o f t h e C o l l e g eo f
Arts and Sciencesand Robert O. Lawton Distinguished Professor of Biological Science at Florida State Universiry.
The BelknapPressof HarvardUniversiryPress Cambridge,Nlassathusetts, attd Lturdon,England
www.hup.harvard. edu
Jacket illustration: DEA
Picturr Librarv/(letn
Jacket design: Jill Breitbarth
Inrrqes
"One of the first and likely to be the most comprehensive in scope of the many books occasionedby the zoog sesquicentennialofDarwin's Origin." -Edward
FROM
THE
O.Wilson
EDITORS'
INTRODUCTION
This book presentsevolutionary science as a modern, dynamic discipline and allows the reader to explore evolution according to his or her interestsand background. The reader who wishes to be immersed in the science can focus on the major scientific themes, while the reader who is interested in the intellectual history and influence of the subject away from science can enter through a separateset of essays. A reader interested in very specific topics or historical figures can find the appropriate entries, along with essayson related topics. Our goal was to provide an exciting and compelling introduction to evolution along with a basic reference work that could point the way toward a deeper study of individual issues. The essaysinclude bibliographies, which serve as guides to further and deeper reading.The essaysin this book show not only how far we have come but where the scientific horizons lie and how we might move toward those horizons.
rsBN378-0-b7rr-03175-3
90000
llillfflilllilllllllllll ilililil]tl
ЕVoLUTloN The First Four Billion Yeаrs
EDlтЕD BY
MlсHAЕL RUsE JosЕPH TRAVls W|тH A FoRЕWoRD BY
ЕDWARD o. WlLsoN
т H E в E L K N A PP R Е s s o F н A R V A R DU N l V Е R s | т YP R Е s s с A t ' 4 B R I D GМ ЕA . ssAсHUsЕттs L o N D o N ,Е N G L A N D 2009
Сontеnts
Сopyright o 2009 by thе Prеsidеntand Fеllows of Нarvаrd Collеgе All rights rеsеrvеd Printеd ir-rthе Unitеd Stаtеs Of Amеriс:r Librаrу of Сoпgrеss Саtаlogiпg-iп-Publiсаtion Dаtа Еvоlution : thе first fсlur Ьillion yеars / еditеd by Мiсhaеl Rusе, Josеph Trаvis ; with a forеword Ьу Еdwаrd O. Wilson. p. сm. InсludеsЬiЬliogгаphiсalrеfеrеnсesand indеx' I S B N 9 7 8 . 0 - 6 74 - 0 3 | 7 5 . з ( a l k . p a p е r ) 1. Еvolution (Biotogy) I. Rusе, Мiсhaеl. II. Travis,Josеph, 1953QH366.2.Е86з zО09
576.8-dс22
2008030270
Fоrеword Еdшаrd О.Wils,
Introduсtion NIiсhаеl Ruse аl
Thе Histoгy of Еvolu Мiсhаеl Rцsе
Thе origin of Lifе Jеffrеу L' Bаdа c
Palеontolоgy and thе МiсhаеI Bеnton
Adaptation Josеph Trаuis аt Мolесulаr Еvolutiоn FrаnсisсoJ.Aуа
Еvolution of thе Gеnr Briаn Сhаrlesш
Thе Pattеrn and Proс Маrgаrеt B. Ptа,
Еvolution and Dеvеlо Grеgorу A. IVrа
Soсial Bеhavior and S Dапiеl I. Rubеп Human Еvolution Hеnrу М. МсH
ЕvotutionагyBiоlogy Мiсhаеl F' Аnto
Contеnts
nd Fеllows of Hаrvard Сoliеgе sеrvеd 'tаtеsof Amеriсa ,пg-iп- Pub liсаtklп D аtа геd by Miсhаеl Rusе, Josеph Travis ; ward O. Wilson. эfеrеnсеsand iгrdех. '5-3 (alk. paреr) haеl. II. Travis,Josеph' 1953-
3 2009 20080зО270
Foгеword Еdшаrd O' Wilson Introduсtion Мiсhаеl Rusе апd Josеph Trаuis
UTl
iх
Thе History of Еvolutiоnary Thought Мiсhаеl Rиsе Thе origin of Lifе JеffreуL. Bаdа аnd Aпtonio Lаzсаno
49
Palеontologyand thе History of Lifе Мiсh,lеl Bепtoп
80
Adaptatiоn Josеph Тrаuis аnd Dаuid N. Rеzпiсk
105
МolесulaгЕvolution Frаnсisсol. Ауаlа
1З2
Еvоlution оf thе Gеnomе Briап Сbаrlеstuorthаnd Dеborаh Сhаrlеsшorth
152
Thе Pattеrn and Proсеssof Spесiation Маrgаrеt B, Ptасеk аnd Sbаlа l. Наnktsoп
177
Еvolution and Dеvеlopmеnt Crеgorу A' Wrау
208
Soсial Bеhaviоr and Soсiоbiolоgy DаnielI,Rиbеnstein
2З7
Human Еvolution Неnrу М. МсНеnrу
256
ЕvolutionaryBiolоgy of Disеasеand Darwinian Меdiсinе МiсhаеlF. Anto|ш
281
Contепts Bеyond thе Darwinian Paradigm:UndеrstandingBiolоgiсal Foгms Briаn Goodtuiп
299
Philosоphy of Еvolutionary ThougЬt Kim Stеrеlпу
31З
Еvolution and Soсiеty Мапfrеd D. Lаubiсblеr апd Jапе Маiепsсhеin
ЗЗ0
Forеwor
Еvolution and Rеligion Dаuid N' Liuiпgstonе
З48
ЕdшаrdО
Amегiсan Antiеvolutionism: Rсtrospесt and Prospесt ЕugепiеС. Sсott
З70
Alphabеtiсal Guidе
401
сontriЬЦtors
9ЗS
IllustrationСrеdits
949
Indех
951
Two сеnturiеs aftеr i Сharlеs Darwin's ozz important Ьook еvеr. tЬe Оrigiп havе not t arе not prеaсhеd frоп oath of offiсе with a drеssеd thе living wol ity's plaсе within it, v massivе sсiеntifiс еvid havе grown сontinuo undеrstanding and tht So solidly havе thе of еvolution that it ml (univеrsal prinсiplеs i: first law is that all thе ultimatеly obеdiеnt tс has Ьееn thе driving f half сеntury. Thе sес Ьiology as wеll as mu( еlеmеnts and proсеss еvolution through nat Тhе two laws havе 1 for thе rесognition of grее thеy arе bеing сo logiсal phеnomеna. T thе sесondaddrеssеs еxamplе, arе built and not somе othеr. Еaсh lvIodеrn biology as a l proaсhеs guidеd Ьy th Еvеn without thе iп samе as thе Darwin Ьil
еrstanding BiologiсaIForms
299
З1З
Маiепsсhеiп
сt аnd Pгospесt
ЗЗ0
Forеword
З48
ЕdьuаrdО. Wilson
З70 401 935 949 951
Two сеnturiеs aftеr its author's Ьirгh and 150 yеars aftеr its puЬliс:rtion, Сhаrlеs Darwin's Оп the Оrigin of Speсiеs сan fairly Ье rаnkеd as thе most important book еvеr writtеn. Not thе most widеly rеad, to Ье surе. Сopiеs of thе origiп havе not bееn plaсеd in hotеl rooms aсross Amеriсa; its vеritiеs arе not prеaсhеdfrom pulpits еaсlr Sunday; and no politiсal lеadеr takеs an oath of offiсе with a hаnd on its сovеr. It is thе mastеrрiесе that first ad. drеssеdthе living world and (with Тhe Descеnt of Мап following) humanityЪ plасе within it, without rеfеrеnсеto any rеligion or idеology and upon massivеsсiеntifiс еvidеnсе providеd aсross suссеssivе dесаdеs. Its argumеnts havе grown сontinuously in еstееm as thе Ьеst foundation for hцпran sеlfundеrstаndingand thе pЬilosophiсal guidе for human асrion. So solidly havе thе fiеlds of Ьiology Ьuilt upоn thе Darwinian сonсеption of еvolution that it makеs sеnsе tоday to rесognizе it as onе of thе two laws (univегsalprinсiplеs if you wish) that govеrn ouг undеrstanding of lifе. Thе firsг law is that all thе еlеmеnts and proсеssеs thаt dеfinе living organisms arе ultimatеly oЬеdiеnt to thе laws of physiсs and сhеmistry. This formulation has bееn thе dгiving forсе of molесular and сеllular Ьiology during thе past half сеntury' Thе sесoпd law, thе foundation :rnd produсt of еvolutionary Ьiology as wеll аs muсh of organismiс and еnvironmеntal Ьiology, is that all еlеmеnts and proсеssеs dеfining living organisms havе Ьееn gеnеratеd Ьy еvolutionthrоugh natural sеlесtiсln. Thе two laws havе provеn to Ье frrlly сomplеmеntary, a primе rеquirеmеnr for thе rесognition of sсiеntifiс laws gеnеrally. Furthеr' to an inсrеasing dеgrееthеy arе Ьеing сomЬinеd to aсhiеvе sеamlеssanalysеs of partiсular Ьiоlogiсal phеnomеna. Thе first law addгеssеs how a phеnonrеnon oссurs and thе sесond addrеssеswhy it oссurs. Mitoсhondria and othеr organеllеs, for еxamplе, arе built and work thus and so; and thеy originatеd in onе way and not somе othеr. Еaсh dеsсription сomplеtеs thе еxplanation for thе othеr. Мodеrn biology as a wholе has littlе mеaning without thе joining of both approaсhеs guidеd Ьy thе two lаws. Еvеn without thе impеtus of thе origin sеsquiсеntеnnial-fortuitously thе samеas thе Dаrwin Ьirth Ьiсеntеnniаl-2009 is an аppropriаtе timе to prеsеnt uп
ultx
Foreшord еvolutionary Ьiology in its еnсompassing modеrn form. I douЬt that any singlе writеr, or any еnsеmЬlе of sеveral writеrs, сould summarizе this Ьurgеoning disсiplinе in a сomprеhеnsivе and authoritativе form. Thе multipliсity of authors in Еuolutioп: The First Foиr Billioп Yeаrs has gonе far to*ard that goal. Its array of ехpеrts providе statе of thе art for еaсh suЬjесt in turn. Thе sсiеnсе is prеsеntеd hеrе' Ьut also somе of thе main praсtiсal сonsеquеnсеs and in. еvitably, with fundamеntal rеlеvanсе, thе сonsеquеnсеs of Ьiologiсal еvolutionary thought for philosophy and rеligion. Thе grеat quеstions-..Who arе wе?'' ...Whеrеdid wе сomе from?'' and ...Whyarе wе hgrg}''-gan Ье аnswеrеd only, if еvеr, in thе light of sсiеntifiсally Ьasеd еvolutionary thought.
Introduс
NIiсhаеlR
Тhе disсovеry of еvolr .W.еstеrn thought, ranl аmong sсiеntifiс disс< From sееing naturе aI forеvеr сhanging, wе dеrstanding еvolution In sсiеnсе thе word idеas. First, thеrе is tl ganisms, living and dt natural proсеss of сh othеr, diffеrеnt onеs. l of thе anсiеtlt Grееks. ganisms еvolvеd rеally sidеrеd a Ьasiс elеmе puЬlishеd Ьis on tbe organisms on thе plar that opеratеd rеlеntlеs thе natцral world. An tology to moleсular Ьi еvidеnсе that еvolutiol Sесond, еuolution is gloЬе. This сan rеfеr t еvolution of orсhids, suсh as thе еvolution < reptilе iaw. Еvolution: еvidеnсе that rangеs fi to similaritiеs and diff tiоn of somе fеaturеs. stood, whilе thе еvolu organеllеs of сеlls, is lс Тhе third idеa is th that еvolution has not <
ldеrn form. I douЬt that any singlе сould summaгizеthis Ьurgеoning tivе form. Thе multipliсity of au,аrs has gonе far toward that goal. lr еaсh suЬjесtin turn. Thе sсiеnсе in praсtiсal сonsеquеnсеsand in:onsеquеnсеsof Ьiologiсal еvolu. Thе grеat quеstions-cGWho arе Y arewe hеге?''_сan Ье answеrеd d еvolutionarythought.
Introduсtion Мiсhаеl Rиse апd JosеphTrаuis
Thе disсovеry of evolution is onе of thе grеatеst intеllесtual aсhiеvеmеnts of .Wеstеrn thought, rаnking with thе сalсulus and gеnеrаl and spесifiс rеlativity among sсiеntifiс disсovеriеs that сhangеd indеliЬly how wе sее our world. From sееing naturе as fiхеd torеvеr in form and сomposition to sееing it as forеvеr сhanging, wе havе Ьееn transformеd uttеrly Ьy disсovеring and undеrstanding еvolution. In sсiеnсе thе word euolцtion is usеd to ехprеss thrее diffеrеnt Ьut rеlatеd idеаs. Fiгst, thеrе is rЬe fасt of еvolution. This is thе rеalization that all organisms, living and dеad' irrсluding humans, arе thе еnd produсts of a long natural proсеss of сhangе through whiсh еaсh spесiеs is dеsсеndеd from othеr, diffеrеnt onеs. Although protoеvolutionary idеas datе Ьaсk to the timе of thе аnсiеnt Grееks, only in thе еightееnth сеntury did thе сlaim that organisms еvolvеd rеally start to gain сurrеnсy. Howеvеr' thе idеa was not сonsidеred a Ьasiс еlеmеnt of sсiеntifiс knowlеdgе until aftеr Сharlеs Darwin puЬlishеd his ozl the Оrigiп of Spесiеs in 1859. Darwin arguеd that all thе organisms on thе planеt еmеrgеd through a singlе, straightforward proсеss that opеratеd rеlеntlеssly from thе dawn of lifе and that сontinuеs to shapе thе natural world. An еnormous amount of sсiеntifiсrеsеarсh,from palеontology to molесular biology' has providеd thе сompеlling and ovеrwhеlming еvidеnсеthat еvolution is indееd a faсt. Sесond, еuolиtion is oftеn usеd to rеfеr to the pаth of lifе's history on this gloЬе.This сan refег to thе history of a group of ехisting spесiеs,as in thе еvolutiоn of orсhids' or thе path through whiсh partiсular traits еmеrgеd, suсh as thе еvolution of thе middlе еar of mammals from small Ьonеs in thе геptilе |аw. Еvolutionary historiеs arе гесonstruсtеd from a widе variеty of еvidеnсеthat rangеs from sеquеnсеs of spесiеs and forms in thе fossil rесord to similaritiеs and diffеrеnсеs in thе DNA of ехisting organisms. Thе еvolution of somе fеaturеs,suсh as thе hoovеs of ungulatеs,is vеry wеll undеrstood, whilе thе еvolution of othеrs, partiсularly vеry old fеatures likе thе organеllеsof сеlls, is lеss wеll undеrstood. Thе third idеa is the theorу of еvolution. This rеfеrs not to a suggеstion that еvolution hаs not oссцrrеd or that thе historv of oаrtiсular fеaturеsсannot
Introduсtion Ье rесonstruсtеd Ьut to orrr idеas aЬout thе forсеs that drivе еvolutionarу сhangе.In the Оrigiп Darwin propоsed what today is almost univеrsallyсonsidеrеd thе major forсе in organiс сhangе, natural sеlесtion.But natural sеlесtion is not thе only importаnt еvolutionary forсе; natural sеlесtion opеratеs on thе variation in shapеs, sizеs, and iorпrs of organisms сгеatеd Ьy mutations in thеir gеnеs' and thе rаtе and mirgnitudе of thе сhangеs that arе drivеn Ьy natural sеlесtiоnare govегnеdЬy hоw thosе gеnеsсontrol dеvеlopment. An enormous amount of oЬsеrvation and eхpеrimеnt has doсumеntеd thе aсtion of naturаl sеlесtionand somе of thе gеnеtiс rеsPonsеsto sеlесtion. But modеrn disсovеriеsin gеnеtiсsand dеvеlopmеnt have raisеd many nеw quеstions and guidеd us toward soпrеsurprising answеrs аЬout how all thеsе forсеs сomЬinе to drivе еvolution. Outsidе sсiеnсе thе word еuolution rеfers to a natural proсеss сonsidеrеd the inspiration for а host of soсiologiсal, litеrary, politiсal' philosophiсal, and rеligious idеаs. From writегs еxploring thе animal naturе of humans to psyсhоlogistssеarсhirrgfor thе origirrof humаn Ьеhavior in еvolutionary his. tory to thеologians grappling with thе impliсations of еvolution for ouг undеrstanding of thе Divinе, thе influеnсе of еvolution outsidе sсiеnсе fаг ехсееds that оf any othеr sсiеntifiс disсovеry еvеr madе. And as modеrn сontrovеrsiеs in thе sсhools illustratе, partiсularlу in thе Unitеd Statеs' it pro. vokеs rеасtiolls аlmost аs stгong as issuеssurrounding thе Ьeginningand еnd of hцnran lifе. In this Ьook wе еxplorе all thеsе fасеts of еvolution. Our аuthors prеsеnt thе еvidеnсе for еvolution as faсt from thе fossil rесord to gеnomiсs, illustratе thе histоry оf groups from Ьaсtеriа to Ьirds, and dеsсriЬе our сurrеnt idеas about how гhеsе historiеs and tlris еvidеnсе сamе to bе. Our аuthors also еxplorе tlrе influеnсе of еvoltrtion on plrilosopЬy, rеligion, soсiology, psyсhology, and many othеr arеas and addrеss thе сurrеnt сontгovеrsiеs aЬout thе tеaсhingof еvolution in sсhools.Thе Ьook сovеrs thе historiсal disсoveriеs, suсh as homology, that opеnеd thе path for disсovеring еvolution; thе phеnomena' suсh аs industrial mеlanism, that playеd maior rolеs in inspiring ехpеrimеntal studiеs of еvolution; thе appliсations of еvolutionary prinсiplеs to arеas sееmingly far аfiеld, suсh as сomputеr sсiеnсе;and thе сontributions оf thе major figurеswho shaped thе history
bеhavior. Thеrе arе fс whiсh rеvеal that dеs1 сovеrеd. Not that th. rathеr' thеrе is muсh spесiеs or fеaturеs' pa laг lеvеls' and to rеfinr аstonishing divеrsity с Ьook show пot only h liе and how wе might This Ьook is organi on rhе оvегarсhing tt thought to thе сontro origin of lifе to thе pгс m a j о r f е a t u r е so f е v o аrеas likе molесular е. Thе sесond paгt сonti topiсs. Thеsе inсludе t p е o p l е a г е f а m i l i a r ,t с urеs in thе disсovегy Ьоoks that rесount tht
a disсiplinе' This organizat\on a or hеr intегеstsand Ь; thе sсiеnсе сan foсus < intеrеstеd in thе intеlI sсiеnсе сan еntеr throl spесifiс topiсs or hist with еssays on rеlatеd pеlling introduсtion to point thе way towaгd biЬliogгaphiеsw , hiсh Although wе hopе t volumе to inform, ес sсholars. Wе find еvol intеrеsting, and indес еmеrgе with thе samе t i o n , i t i s i m p o г t a n tt .
сhallеngе of antiЬiot tious disеasеs,it shor a l t е r a t i о n so f h a Ь i r a t ехplanations of who '
m a n y o f o u r с l o s е l yh Тhе last of thеsе r Provеn so сontrovеrs pеoplе in thе Unitеd S of lifе on еarth. lt is u
lпtroductioп thе lЪrсеs thаt dгivе еvolutionary hat today is almost univеrsallyсon:, natural sеlесtion'But natural sеarу forсе;nаtuгаlsеlесtionopегatеs ms of organisms сrеated Ьy mutaragnitudе of thе сlrаngеs that arе y how thosеgеnеsсontrol dеvеlopln and ехpсrimеnthas doсumеntеd f the gеnеtiсrеsponsеsto sеlесtion. еvеlopmеnt havе raisеo many nеw lrising answеrsabotrthow all thеsе :rs to а naturаl Proсеss сonsidеrеd l, litеrary, politiсal, philosophiсal, lg thе animal naturе of humans to цmаn bеhavior in еvolutionary hispliсationsof еvolution for our unоf еvolution outsidе sсiеnсе far ry еvеr madе. And as modеrn сonr l a r l y i n t h е U n i t е d S t a t е s 'i t р r o ;urroundingthе Ьеginning and еnd of еvolution.our authors prеsеnt rе fossil rесord to gеnomiсs, illusto Ьirds, and dеsсriЬеOur сurrеnt :vidеnсесamе to Ье. our authors n philosophy, rеligion, soсiology, addrеss thе сurrеnг сontrovеrsiеs Thе Ьook сovегsthе historiсal dishе path for disсovеring еvolution; sm' that playеd major rolеs in inthе appliсations of еvolutionary rсh as сomputеr sсiеnсе; аnd thе lеd thе history of еvolutionarysсints еvolutionarysсienсeas a modssionsof еvolution outsidе thе sсisubjесt Ьесamе fossilizеd in thе lhеn thе suitaЬilityof еvolution as rеingarguеd.Thе irоny is thаt thе ular Ьiology to сomputational inсе that Darwin сould only drеam c сomе appliсations that Darwin Lianmеdiсinе.Prinсiplеs of еvolu.sсiеntifiсproЬlеms, from undег]sеrvation to ехplaining human
Ьеhavior. Thеrе arе fеw topiсs in sсiеnсе with so many еxсiting nеw faсеts' whiсh rеvеal that dеspitе all wе havе lеarnеd, thеrе is muсh morе to Ье disсovеrеd. Not that thеrе is fuгthеr neеd to suЬstantiatе еvolution as faсt; rathеr' thеrе is muсh morе to Ье donе to traсе thе еvolution of groups of spесiеsor fеaturеs, partiсularly сomplеx fеaturеs аt thе сеllular and molесular lеvеls, and to rеfinе our thеory of еvolution to aссoцnt morе fully for thе astonishing divеrsity of lifе as wе сontinuе to disсovеr it. Thе еssays in this book show not onlу how far wе havе сomе but whеrе thе sсiеntifiс horizons liе and how wе might movе toward thosе horizons. This Ьook is organizеd into two parts. Thе first part сontains long еssays on thе ovеrarсhing thеmеs in еvolution. From thе history of еvolutionary thought to thе с
хi
Introduсtion undеrstanding of еvolution and thе еvidеnсе aЬout it and how muсh is Ьasеd on thе сhallеngеs that it offеrs. Yеt opposition to еvolution Ьy rеligious pеoplе, еspесialiy Ьy Сhristians' is Ьy no mеаns inеvitaЬlе; somе of thе'most distinguishеd Ьеliеvеrs havе aссеptеd еvolution without many qualms. NИе arе сonvinсеd that thе Сhristian-with thе Jеw and Мuslim and other rеligious bеliеvеrs-should Ье at thе hеad of thе quеuе of thosе who welсomе evolutionary idеas. Finding thе idеa, Ьuilding and еlaЬorating upon it, and looking at its influеnсе and importanсе arе' as thе сontriЬutors to this volumе show again and again, truly thе Ьеst of proofs that wе arе madе in thе imagе of God, сеlеЬrating сrеation in all its wondеrful manifеstations. This Ьook is a tеstamеnt to onе of mankind's 8rеatеst disсovеriеs, a disсovеry that offеrs unparallеlеd insight into what сrеation rеally is. Iй/еlovе еvolution, and if wе and our fеllow сontriЬutors сan inspirе you еvеn in a small way with our еnthusiasm' thеn wе shall Ье happy indееd.
Thе Hir Thougt
NIiсbаеlR
Thе idеa that all org mеans from othеr forl (fifth сеntury в.с.в.) tr еightееnth сеntrrry an( idеa of natural dеvеlo portеrs. Тhеrе arе rеa Ьеgan to gain momеnl
Thе Еarly Days
Thе Grееks had no grt turе did not havе a plz Spесifiсally, thе Grееk going, inсrеmеntal o Plato and Aristotlе-l isms) showеd ordеr ал simply havе appеarеd tainly was not somеtt thе сomplехity of tod; and dеsign: ..Sinеw,sl and toеs. Thе miхturе of a singlе stuff, a piес on to put things in сol
Now thеse Werе ml nеnt сausе of its prс gеnеrations: our сI rеalm of wild Ьеast ular thеy knеw that and сlaws or hoofs
се aЬout it and how muсh is Ьasеd tion to еvolution Ьy rеligious pеors inеvitablе;somе of thе most dis.!7е on without many qualms. arе w and Мuslim and othеr rеligious rеuеof thosе who wеlсomе еvolud еlaЬorating upon it, and looking сontributors to this volumе show that we arе mаdе in thе imagе of [ul manifеstations. indЪ grеatеstdisсovеriеs,a disсov.s7е lat сrеation rеally is. lovе еvo. )rs сan inspirе you еvеn in a small happy indееd.
Thе History of Еvolutionary Thought Мiсhаel Ruse
Thе idеa that all organisms (inсluding humans) arе gеnеratеd by natural mеans from othег forms has anсiеnt roots. Aristotlе tеlls us that Еmpеdoсlеs (fifthсеntury в.с.в.) toyеd with suсh thoughts.Howеvеr, it was not until thе еightееnthсеntury and thе Еnlightеnmеnt that еuolutioп (as wе now сall this idеa of natural dеvеlopmеnt) rеally startеd to gain a sеrious numЬеr of sup. portегs. Thеrе aге rеasons Ьoth for thе long dеlay and why thе idеa finally Ьеganto gain momеntum.
Thе Еarly Days Thе Grееks had no grеat rеligious oЬjесtion to еvolution, Ьut thеir world piсturе did not havе a plaсе for any kind of signifiсantdеvеlopmеntalproсеsses. Spесifiсally,thе Grееks thought that thеy had irrеfцtaЬlе rеasons to rеjесt ongoing, inсrеmеntal organiс сhangе. Thеy-partiсularly thе philosophеrs Plаto and Aristotlе-thought that thе world (еspесially thе world of organisms)shоwеd ordег and intеntion and, as suсh, was not somеthing that сould simply havе appеarеd thrоugh Ьlind, ungovеrnеd proсеssеs of law. It сеrtainly was not somеthing that сould havе grown from simplе Ьеginnings to thе сomplехity of today. Plato usеd human fingеrnails as an ехamplе of ordеr and dеsign: ..SinеW,skin and Ьonе wеrе intеrwovеn at thе еnds of our fingеrs and toеs. Thе miхturе of thеsе thrее was driеd out' rеsulting in thе formation of a singlе stuff' a piесе of hard skin, thе samе in еvеry саsе.'' Plato tЬеn wеnt on to put things in сontеХt. Now thеsе wеrе mеrеly auxiliary сaцsеs in its formation-the prееminеnt саusе of its produсtion was thе purposе that took aссount of futurе gеnеrations: our сrеators knеw that onе day womеn and thе wholе rеаlm of wild Ьеastswould onе day сomе to Ье from mеn, and in partiсular thеy knеw that many of thеsе offspring would nееd thе usе of nails and сlaws or hоofs for many purposеs. This is why thеy took сarе to
The Historу of Еuolutioпаrу Thought inсludе nаils formеd in a rudimеntaгy Way in thеir dеsign for humаnkind, right at thе start. This was thеir rеasoц, thеn, and thеsе thе profеssеd aims that guidеd thеm in making skin, hair and nails grow at thе еxtrеmitiеs of our |imЬs. (Timаеus, 76d_e, in Сoopеr 1997, 1277)
humаn thought and pгogrеss. Thе British physiсi; Сharlеs) Was a para mankind:
In an inсrеdiЬly influеntial disсцssion, Aristotlе in Dе pаrtibиs аnimаlium (1,984\identifiеd thе faсtors at work hеre as ..final сausеs.'' Thеsе arе сausеs that oссur not just to produсе or do somеthing (thе fingеr parts dry and makе пails) Ьut foг the sakе of somе kind of purposе (thе nails protесt thе fingеr еnds). Thеy show somе kind of forethought or intеntion. For this rеason, fi. nal сausеs сannot Ье rеduсed to Ьlind, unguidеd law, as is dеmandеd in еvolution. Thе world, partiсularly thе world of orgаnisms' must in somе sеnsе havе Ьееn dеsignеd rathеr than just produсеd undеr its own stеam tly natuгal proсеssеs.(Sеdlеy2008 is thе dеfinitivеstudy.) Thе Jеws, and following thеm thе еarly Christians, had religious rеasons for thе rеjесtion of еvolution. It goеs against thе сrеation storiеs of thе еarly сhaptеrs of Gеnеsis, whiсh portray a world сrеatеd miгасulously Ьy God and thеn pеoplеd Ьy him through divinе fiat ovеr a short timе span. But do not think that rеligion as suсh was thеn and always an aЬsolutе Ьar to еvolutionism. Thе сhurсh fathеrs (thе major Сhristian thеologians of thе еarly сеnturiеs) workеd toward an undеrstanding оf thе ЬiЬliсal tеxt thаt wоuld allow intегprеtation, partiсularly in thе faсе of advanсеs of sсiеnсе. Sаint Augustinе was еagеr not to lеt anсiеnt сrеation aссounts stand in thе way of modеrn thought. Hе himsеlf, Ьеliеving that God stands outsidе timе, spесulatеd in a kind of protoеvolutionary fashion that thе Divinе had foгmеd sееds of lifе that thеn sprang into full Ьеing whеn thеy wеrе plaсеd hеrе on еarth. Howеvеr' onе should not геad too muсh into any of this. Likе thе Grееks, thе Jеws and Christians wеrе simply not looking in thе dirесtion of еvolution and would havе thought final сausеs an unаnswеrablе oЬiесtion to signifiсant dеvеlopmеntalism. As is wеll known, thеsе kinds of сausеs Ьесamе a founda' tion of onе of thе major proofs of God's ехistеnсе, thе Argumеnt from Dеsign, whiсh movеs frоm dеsign herе on еarth to thе еxistеnсе of thе divinе artifiсеr. .!Иhy, thеn, did еvolution start its rise in the еightееnthсentury? Thе an. swеr is simplе. It was at this time that pеoplе startеd to сhallеngе thе Christiаn piсturе of world histоry-a providеntial piсtuге of a world сrе. atеd Ьy God, whеrе humans arе madе in his imagе Ьut havе fallеn and arе ablе to aсhiеvе salvation only through his undеsеrvеd graсе. Somе Ьеgan to arguе that pеrhaps humans hеld thеir fatеs in thеir own hаnds and сould progrеssivеly improvе thеir own lots. It Was this idеa of pгOgrеssthе Ьеliеf that thе world and its dеnizеns arе on a trajесtory upward аnd that this upward risе is madе possiЬlе Ьy (and only Ьy) thе unaidеd еfforts of thе world's human inhabitants-that gavе risе to thе idеa of organiс еvolution (Rusе 1996). Еnthusiasts for progrеss ехtеndеd thеiг thinking into naturе and dеvеlopеd thе idеа of еvolution-progrеssivе сhangе upward from thе simplе to thе сomplех. They thеn rеad this idеa Ьaсk into
Impе: Of la With And r Arost An еr (Е.D This is all rhе еnd pr. gеnсе' whiсh сausеs а
Hоw lo From е. Нow fr. Тhе pilt
Similar idеas wеrе tс Pbilosophiе zoologiq produсеd thе first ful to our own spесiеs fr Ьееn produсеd from l ity and othеr natural Although thе mеta1 risе of еvolutionary i< еvidеnсе. Aristotlе ha shaге сommon pattеrl
and thе еvolutionists triеs (Figurе 1). Likеr 8o unnotiсеd (Figurе sition. Thе fossil rес would invokе first as ful. As a systеmatiс p
were mеagеr indеed. faсt that no onе haсl l lцtion. Мost assцm forсеs, Ьut littlе mor that сharaсtеristiсsa ately to thе futurе g
that thе inhеritanсе Lаmаrсkism*Ьut bt
Thе Historу сэfЕuolutioпаrу Thougbt fу waУ in thеir dеsign for huthеir rеason, thеn' and thеsе thе king skin, hair and nails grow at 76d-r, in Coopеr 1997,|277) 'ristotlе iп Dе pаrtibиs апimаlium as ..final сauses.''Thеsе arе сausеs :hing (thе firrgеrparts dry and makе urposе (thе nails protесt thе finger ;ht or intеntion. For this rеason, figuidеd law, as is dеmandеd in еvoof organisms)must in somе sеnsе сеd undеr its own stеam by natural
udv.)
y Сhristians,had rеliglous rеasons nst thе сrеation storiеs of thе еarly d сгеatеdmiraсulously Ьy God and эvеr а short timе spаn. But do пot lwаys an absolutе Ьar to еvolutionstian thеologians of thе еarly сеn'f thе ЬiЬliсal tеxt that would allow dvanсеs of sсiеnсе.Saint Augustinе ounts stand in thе way of modеrn tands outsidе timе, spесulatеd in a rе Divinе had formеd sееds of lifе F wеге plaсеd hеrе on еaтth. How. , any of this. Likе thе Grееks, thе ng in thе dirесtion of еvolution and wеraЬlеoЬjесtion to signifiсant dеkinds of сausеs Ьесamе a foundaj's ехistеnсе, thе Argumеnt from еarth to thе ехistеnсе of thе divinе n thе еightееnthсеntury? TЬе an: pеoplе staгtеd to сhallеngе thе ovidеntial piсturе of a world сrеhis imаgе Ьut havе faliеn and are is undеsеrvеdgraсе. Somе Ьеgan ir fatеs in thеir own hands and )ts.It was this idеa of progrеssi arе on a trajeсtory upward and (and only Ьy) thе unaidеd еfforts gаvе risе to thе idеa of organiс progrеss еxtеndеd thеir thinking .olution-pгogrеssivе сhаngе up1еy thеn rеad this idеa Ьaсk into
human thought and soсial praсtiсе as сonfirmation of thеir Ьеliеfs about progrеss. Thе British physiсian and man of sсiеnсе Еrasmus Darwin (grandfathеr of Сharlеs) was a paradigm who hymnеd in vеrsе lifе's upward risе to humankind: Impеrious man, who rulеs thе Ьеstiаl сrowd, of languagе'rеason' arrd rеflесtionproud, .With brow еrесt who sсorns this еarthy sod, And stуlеshimsеlf thе imagе of his God; Arosе from rudimеnts of form and Sеnsе, An еmЬryon point' or miсrosсopiс еns! (Е. Darwin 180З' 1: Сanto I,linеs з09-з14) This is all thе еnd produсt of thе progrеssivеdеvеlopmеnt of human intеlligеnсе,whiсh сausеsarrd is rеflесtеdin humans' sсiеntifiсaсhiеvеmеnts: How lovеs аnd tastеs,and svmpathiеsсommеnсе From еvanеsсеntnotiсеs of sеnsе; H
3
4
The Нistorу of Еuolutioпаrу Thought A
DARWlnl tсфl8D
l,
Figurе 1. Homologiеs. Thеse аre thе forelimЬs of (froп lеft to right) the Ьat (its wing), the porpoisе(itspaddlе),thе horsе (itsleg),and thе human (its arm). Thе Ьonesarе oЬviouslysimi[ar,аs if modеledon a singlеаrсhetypе'and yеt thе usеs to whiсh thеy arе Put arе verУ diffеrеnt.It was thе British anatomlst Riсhard owеn who сallеd them ..homologiеs'''аlthough it wаs not until аfter Darwin's on thе origiп of Spесiеs(1859)that thеy Ьесamеuniversallyaссеptеd as proof of desсеntfrom a сommon аnсestor.
Thе idеology of progrеss was whаt сountеd, and it was for this rеason that most pеoplе around 1800 would havе rеgardеd еvolutionism lеss as a rеal sсiеnсе and moге as a pгеtеndег,sоmеwhat likе animal magnеtism (mеsmеrism) and thе rеading of сharaсtеr from skull shapе (phrеnology). Еvеn !udgеd by thе standards of that timе, еvolution was what may fairly Ье сallеd a psеudosсiеnсе. OЬviously, Сhristian opponеnts of еvolution dislikеd intеnsеly the antiprovidеntial undеrpinnings of thе doсtrinе. But еvolution was not assoсiatеd with total nonЬеliеf, athеism, or еvеn what latеr in thе ninе. tееnth сеntury Thomas Hеnry Huxlеy was to сall agnostiсism. Мost еvolutionists wеrе dеists who Ьеliеvеd in God as unmovеd movеr' a Ьеing who had sеt thе world in motion and now lеt it unfurl without nееd сlf miraсulous intеrvеntion. For thе dеist' indeеd, еvolution was proof of God,s powеr and intеntion rathеr than disproof. Еvеrything was plannеd Ьеforеhаnd and wеnt into еffесt through thе lаws of naturе. In Еrasmus Darwin's words: ..\)Иhatа magnifiсеnt idеa of thе infinitе powеr of тнв GRЕAT ARснITЕсT! Tнв сдusв oF сAUsЕs! PARЕNT oF PARЕNTS!ЕNs ЕNTIUМ!' (1801' 2: 247|. Thеrе is a link hеrе, еspесially in Еngland, with thе Industrial Rеvolution. Pеoplе wеrе harnеssing thе forсеs of naturе-watеr, сoаl' and othеrs-to produсе goods through maсhinеs rathеr than Ьy hand. Thе god of thе dеist was thе ultimatе
li
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Figurе 2'Prize pig. Al сountrysidе and go to on thе land to produс rеvolution, and at thе mаjor kеy to suссessl hаiriеr shееp,and Ьig
divinе industгialist a of thе world througt Critiсs of еvoluti Gеorgеs Сuviеr, m; mummifiеd bodiеs o from Еgypt. Althou1 tеmporary forms an, with thе positivе сat that rеally сountеd. hatrеd of a doсtrinе than thеy сould dо z lution, whеn oppon. provеd truе and saft as for еvеry othеr o final сausе. Thе Frе not Ье ignorеd; indr lifе. Thе kеy to unс
The llistorу of Еuolutioпаrу Thought A
Dlnwl*tAн lr
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os of (from left to right) thе Ьat (its s lеg),and thе humаn (itsarm). Thе r a singlearсhеtypе,and yet thе l г w a sr h е B r i г i s hа n a t o m i s r s,''althoughit wаs not until after at thеy Ьeсameunivеrsallyaссеptеd
tеd, and it was for this rеasоn that 4aгdеdevolutionism lеss as a rеal hat likе animal magnеtism (mеsm skull shapе (phrеnology). Еvеn tion was what may fairly bе сallеd |Ponеntsоf еvolution dislikеd inof thе doсtrinе. But еvolution was m' or еvеn what latеr in thе ninеs to сall agnostiсism.Мost еvoluunmovеd movеr' a Ьеing who had ш] without nееd of miraсulous inwas proof of God's powеr and inlas plannеd Ьеforеhand and wеnt lrasmus Darwin's words: "What a нЕ GRЕATARсHITЕсT! Tнв сдusв tuм!'' (1801,2: 247).Thеrе is а ndustrialRеvolution. Pеoplе wеrе al, and othеrs-to produсе goods э gоd of thе dеist was thе ultimatе
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Figure2. Prizе pig. An industrial rеvolution means that pеople lеavе thе сountrysidеand go tо thе faсtoriеsin thе сitiеs. Неnсе, far fеwer peoplе аге left on the land to produсе thе nation's food. Thеrе has to Ье an agriсultural revolution,and at thе еnd of thе еightеenthсеntury pеoplе disсovеrеdthаt a major key to suссesswas thе Ьrеedingof Ьеttеr-qualitylivеstoсk-fattеr pigs' hairiеrshеep,and Ьiggеrсattlе.(From Punсh, |865.)
divinе industrialist as hе harnеssеd thе forсеs of naturе to produсе thе goods of thе world through law rathеr than miraсulously or Ьy hand. Сгitiсs of еvolution, notаЬly thе grеаt Frеnсh сompаrativе anаtomist Gеorgеs Сuviеr, madе rеfеrеnсе to еmpiriсal proЬlеms. Cuviеr сitеd thе mummifiеd Ьodiеs of humans and animals Ьrought baсk Ьy Napolеon's army from Еgypt. Although thеy wеrе vеry old, thеir forms wеrе idеntiсal to соntеmPorary foгms and hеnсе сountеd against ongoing оrganiс сhangе' But as with thе positivе сasе for еvolution' in thе nеgativе сasе it was thе idеology that rеally сountеd. AЬovе all, for Сuviеr, thеrе was hatrеd of progrеsshatrеd of a doсtrinе that had lеd humans to think that thеy сould do morе than thеy сould do and had lеd ultimatеly to thе tеrrors of thе Frеnсh Rеvolution, whеn opponеnts of thе ехisting statе had triеd to сhangе all that had provеd truе and safе for mаny gеnеrations. СomЬinеd with this, for Cuviеr, as for еvеry othеr opponеnt of еvolution, was thе still-цnsolvеd problеm of final сausе. Thе Fгеnсhman еmphasized that this was somеthing that сould not Ье ignorеd; indееd, it was thе most important distinguishing fеaturе of lifе. Thе kеy tо undеrstanding thе organism lay in thе fасt that it was not
5
Thе Historу of Еuolutioпаrу Thought simply suЬjесt to thе physiсal laws of naturе Ьut was organizеd. Thе parts wеrе dirесtеd to thе еnd of thе funсtioning wholе, and еaсh individual fеa. turе playеd its rolе in thе ovеrall, purposе-dirесtеd sсhеmе of things: Natural history nеvеrthеlеss has a rational prinсiplе that is ехсlusivе to it and whiсh it еmploys with grеat advantagе on many oссasions; it is the сoпditioпs of eхisteпсe or' popular|у, fiпаl саusеs. As nothing may ехist whiсh doеs not inсludе thе сonditions whiсh madе its еxlstеnсе possiblе, thе diffеrеnt parts of еaсh сrеaturе must Ье сoordinatеd in suсh a Way as to makе possiЬlе thе wholе organism, not only in itsеlf Ьut in its rеlationship to thosе whiсh surround it, and thе analysis of thеsе сonditions often lеads to gеnеral laws аs wеll foundеd as thosе of сalсulation or еxpеrimеnt. (Сuviеr 1817' 1: 6\ Сuviеr's point simply was that thе organism is far too intеgratеd-organizеd and сomplех-to allow signifiсant сhangе in any dirесtion. It is сеrtainly too intеgratеd to allow сhangе from onе spесiеs to anothеr. organisms at mid. point would Ье litеrally nеithеr fish nor fowl and hеnсе would simply Ье unaЬ]еto еxist or survivе. Еvolution was in somе sеnsеa thеorеtiсal impossiЬility, as wеll as еmpiriсally unfoundеd. Rеligion was involvеd too. Progrеss goеs against thе Сhristiаn doсtrinе of Providеnсе. Nеvеrthеlеss, although Cuviеr thought that thеrе was еvidеnсе of Noаh's flood, nеithеr hе nor othеr serious sсiеntists wantеd to makе thе сasе by simplе rеfеrеnсе to Gеnеsis. Indееd, Ьy thе Ьеginning of thе ninеtееnth сеntury' all wеrе starting to rеalize that thе еаrth's history must Ье far oldеr than thе traditional 6,000 yеars that onе сan work out from thе gеnеalogiеsgivеn in thе BiЬlе. It is not that thе BiЬlе is falsе, Ьut rathеr that it nееds intеrprеtation. Somе solved thе proЬlеm Ьy thinking of thе siх days of сrеation as siх long pеriods of timе; othеrs solvеd it Ьy supposing that thеrе wеrе long, unmеntionеd gaps Ьеtwееn thе ЬiЬliсal days. God's сrеation thеreforе was a long, drawn-оut proсеss' Ьut it was not еvolutionaгy. Thе сontrovеrsywas at an impassе,and not muсh had сhangеd Ьy thе middlе of thе ninеtееnth сentury. on the onе sidе wеrе thе еvolutionists' сommittеd to progrеss and ardеnt in thеir Ьеliеf that organiс dеvеlopmеnt was thе perfесt сomplеmеnt to this idеology, with еnthusiasm outstripping еmpiriсai knowlеdgе. Сonfirming this pattеrn' ]n 1844 thе Sсottish puЬlishеr Robеrt СhamЬеrs wrotе (anonymously)a highly popular work on еvolution, Vеstiges of tbе Nаtиrаl Historу of Сrеаtioп, in whiсh hе arguеd that еvеrything was in a statе оf upward Ьесoming and that whаt happеnеd in thе soсial world mirrorеd what happеnеd in thе Ьiologiсal world: Thе quеstion whеthеr thе human raсе will еvеr advanсe far Ьеyond its prеsеnt position in intеllесt and morals, is onе whiсh has еngagеdmuсh attеntion. Judging from thе past' wе сannot rеasоnaЬly douЬt that grеat advanсеs arе yеt to Ье madе; Ьut if thе prinсiplе of dеvеlopmеnt Ье admittеd' thеsе arе сеrtain, whatеvеr may Ье thе spaсе of timе rеquirеd for thеir rеalization. A progrеssion rеsеmЬling dеvеlopmеnt may Ье traсеd
in human naturе, t Now all of this is i of organiс сrеation thе hour hand is t wе do of that lattс rеtrogrеssion of th. missiЬlе, but a forl Ьеrs 1846, 40040
On thе othег sidе aЬout thе signifiсanс modifiеd Ьut thinkin1 еral man of Sсottish gеrs: ..It would augеl wеrе infесtеd with th taintеd with Matеria rеflесtions that still fi thе slaсknеss of sсho diсating thе unsoun< startеd into puЬliс fa. еnсе, and of sapping tеrеstingly' this kind viеws. Although, fro fеlt thе nееd to makr aЬovе is from thе fifl morе сrеdit to thе Cr of сoursе, nеithеr rеal еvidenсе, and fin all to miraсlе may Ье good sсiеntifiс soluti<
Charlеs Darwin
Сharlеs Robеrt Darl train in thе family droppеd out, Ьorеd r rеady Darwin had st еstеd in thе living w anatomist and an а-v work (thе young Сh' tion was an idеa to r nеvеrthеlеss, that thl wholе of Сhristianit; was a faсtor in his rе thе еstaЬlishеd Chur'
Тbе Historу of Еuolutioпаrу Thought LturеЬut was organizеd.Thе parts ng wholе, and еaсh individual fеa'-dirесtеdsсhеmеof things: lnal prinсiplе that is еxсlusivе to /antagеon maпy oссаsions;it is |у, fiпаl саusеs.As nothing may litions whiсh madе its ехistеnсе turе must bе сoordinatеd in suсh гganism'not only in itsеlf Ьut in Lit, and thе analysisof thеsесonvеll foundеd as thosе of сalсula;m is fаr too intеgrаtеd-organizеd , in any dirесtion. It is сеrtainly toо ;iеsto anothеr. organisms at midlwl and hеnсе would simply Ье unmе sеnsеa thеoгеtiсalimpossiЬility, эs agаinst thе Christian doсtrinе of lr thought that thеrе was еvidеnсе ious sсiеntists wantеd to makе thе эеd, Ьy thе Ьеginning of thе ninеthаt thе еаrthъ history must Ье far at onе сan work out from thе gеthе BiЬlе is falsе' Ьut rаthеr that it Ьlеm Ьy thinking of thе siх days of .s solvеd it Ьy supposing that thеrе ЬiЬliсal days. God's сrеation thеrеWas not еvolutionary. not muсh hаd сhangеd Ьy thе mid: s i d е w е r е t h е е v o l u t i o n i s t sс' o m liеf that oгganiс dеvеlopmеnt was i t h е n t h u s i а s mo u t s t r i p p i r r еg m p i r ,, in \844 thе Sсottish puЬlishеr highly popular work on еvolution, lz, in whiсh hе arguеd that еvегyand that what happеnеd in thе soЬiologiсal worid: will еvеr advanсе faг Ьeyond its is onе whiсh has еngagеd muсh LnotrеasonaЬlydoubt that grеat prinсiplе of dеvеlopmеnt Ье adЬе thе spaсе of timе rеquirеd for ing dеvеlopmеnt may Ье traсеd
in human naturе' Ьoth in thе individual and in largе grouPs of mеn . . . Now all of this is in сonformity with what wе havе sееn of thе progrеss of orgaпiс сrеation. It sееms Ьut thе minutе hand of a watсh, of whiсh thе hoцг hand is thе transition from spесiеs to spесiеS. Кnowing what wе do of that lattеr transition' thе possiЬilitу of a dесidеd and gеnеral rеtrogrеssionof thе highеst spесiеs towards a mеanеr typе is sсaгсе admissiЬlе, Ьut a forward movеmеnt sееms anything Ьut unlikеly. (ChamЬегs 1846.400402| on thе оthеr sidе wеrе thе opponеnts' сommittеd to Providеnсе, voсаl aЬout thе signifiсanсе of final сausе' and aссеpting that Gеnеsis must Ье modifiеd but thinking that this сould Ье rеadily donе. David Brеwster' gеnеral man of Sсottish sсiеnсе and Ьiographеr of Nеwton, сould sее thе dan. gеrs: ..It would augеr ill for thе rising gеnеration, if thе mothеrs of Еngland wеrе infесtеd with thе еrrors of Phгеnology: it would augеr Worsе wеrе thеy taintеdwith Мatеrialism.'' Thе proЬlеm, Brеwstеr gloomily сonсludеd with rеflесtionsthat still find muсh support in many сirсlеs today, stеmmеd from thе slaсknеss of sсhools and univеrsitiеs: ..Prophеtiс of infidеl times, and indiсating thе unsoundnеss of our gеnеral еduсation, .Thе Vеstigеs . . .' has staгtеdinto puЬliс favour with a fair сhanсе of poisoning the fountains of sсiеnсе)and of sapping thе foundations of rеligion', (BrеWstеr1844' 503). (Intеrеstingly, this kind of attaсk sееms to havе сonfirmеd СhamЬers in his viеws. Although, from thе start, progrеss was thе lеitmotif of his Ьook' hе fеlt thе nееd to makе his point еvеr morе еxpliсit. Thе passagе just quotеd aЬоvе is from thе fifth еdition of Vеstigеs and rеplaсеs a passagе that givеs morе сrеdit to thе Сrеator. [Figurе 3]) of сoursе, nеithеr sidе was геally satisfaсtory. Idеology is no substitutе for rеal еvidсnсе, and final сausе сan bе ignorеd Ьut doеs not go away. Rеfеrгing all to miгaсlе may Ье soсially and psyсhologiсally сomforting, Ьut it is not a good sсiеntifiс solution. Thе timе had сomе for a signifiсant stеP forward.
Charlеs Darwin Сhагlеs Robеrt Darwin (1809_1882) was sеnt to Еdinburgh Univеrsity to train in thе family tradition of mеdiсinе (Figurе 4). Aftеr two yеars hе droppеd out, Ьorеd with thе lесturеs and геvoltеd Ьy thе opеrations. Yеt alгеady Darwin had startеd to miх with sсiеntists, еspесially naturalists intеrеstеdin thе living world. Onе of his aсquaintanсеswas RoЬеrt Grant, an anatomist and an avowеd еvolutionist. So, quitе apart from his grandfathеr's woгk (thе young Сharlеs rеad Еrasmus's major trеatise,Zooпomia), еvolution was an idеa to whiсh Darwin was introduсеd at an еarly agе. It sееms' nevеrthеlеss,that thе youthful Darwin aссеptеd in a fairly litеral form thе whоlе of Сhristianity, inсluding thе еarly сhaptеrs of Gеnеsis, and that this was a faсtor in his rеdirесtеd сhoiсе of а сarееr: to Ье an ordainеd ministеr in thе еstablishеdСhurсh of Еngland. To aсhiеvе this еnd onе nееdеd a dеgrее
8
The Historу of Еuolutionarу Tbought
B R
Figurе 3. СhamЬеrs'sеvolution.This is the piсturеof еvolutionthаt СhаmЬеrs gаve in Vestiges of thе Nаturаl Historу of Сreаtioп. Apparеntly' for no apparеnt сausе' a primitivе organism wеnt on dеvеloping in thе womЬ аnd tuгned into a fish; thеn a fish Went on dеvеlopingand turnеd intсl a rеptilе;thеn a Ьird; and finally a mammal. Note thе intertwining of thinking abouj the history of thе individual and the history of thе gгoup, somеthiй that wаs to Ьесomе сommonplaсе in evolr'tionarythinking latеr in the ninеiееnthсеntury. (From Vestigеs of the NаturаI Historу of Сreаtioп.|
from an Еnglish univеrsity, and so, in 1828, Darwin was paсkеd off to Сhrist's Collеgе, СamЬridgе. In 1831 Darwin (who сontinuеd mixing with sсiеntists)got his Ьig Ьrеak. Aftеr hе graduatеd, his сarееr as a сlеrgyman Was put on hold through thе offеr of a lеngthy voyagе on HМS Beаgle,just about to start on a survеying trip around South Ameriсa (Figurе 5). A major influеnсеаt this point was (viсariously) thе Sсottish gеologist Charlеs Lyеll, who at thе Ьeginning of thе dесadе Ьegan puЬlishing his massivе Priпсiplеs of Gеolr>gу(thеrе wеrе thrее volumеs; Darwin took thе first with him and had thе othеrs sеnt out). AIthough hе was no еvolutionist, Lyеll insistеd that thе physiсal world must Ье еxplainеd in tеrms of natural сausеs of a kind now still working (Figurе 6). This had a great еffесt on Darwin, whosе first systеmаtiс work was in gеology, аnd prеpaгеd him to think aЬout thе oгganiс world likеwisе lеss in biЬliсal tеrms and morе in tеrms of natural сauses. In 1835, lеaving South Amеriсa, the Beаglе sailеd into thе Paсifiс oсеan and visitеd thе Galipagos Arсhipеlаgo' a 8roЦp of islands on thе еquator, far from land. Thanks to thе governor' who pointеd out that thе giant tortoisеs indigеnous to thе arсhipеlago wеrе diffеrent from island to island, Darwin сamе to sее that this hеld for thе Galipagos fauna gеnеrally-thе Ьirds in partiсular, thе finсhеs and thе moсkingЬirds, wеrе pесuliar to thеir spесifiс homеs (Figurе 7). Thе diffеrеnсеs had to bе signifiсant, and thе only way thе signifiсanсе сould Ье
Figurе 4. Сharlеs Darl 1 8 3 9 j u s t Ь е f o r еh e m l likеnеss(no surprisе's portraitist in Еngland from a very riсh, midd .Wеd wifе' was JosiaЬ mass produсtion.Alth woгk for a living. Thе ехplains wЬу Оn thе | friеndly fashion. Darц Wеdgwood family.
ехplainеd was throu[ Ьraсеdin еarly 1837 liег thinkеrs, what w .Without са еvolution.
The Historу of Еuolutioпаrу Thought
-/B ---B _---F
liсtuге of еvolution that СhamЬers "eаtioп. Apparеntly, for no ,n devеloping in thе woпlЬ and rping and turned into a гeptilе; thеn twining of thinking аЬout thе hс group, something that was to 'ng latеr in the ninеtеenth сеnturY. еаtioп.)
[828, Darwin was paсkеd off to ;with sсiеntists)got his Ьig Ьrеak. an was put on hold through thе of;tаbour to start on а survеying rrip .influеnсе at this point wаs (viсarl, who at thе Ьеginning of thе dе)les of ceologу (thеrе wеrе thrеe and had thе othеrs sеnt out). Alld that thе physiсal world must Ье
Figurе4. СhaгlеsDarwirr'This is а wеddingportrait of Dаrwin, paintеdin 1839just Ьеforеhе marriеdhis first сousin Еmma.Wedgwood.It is a vеry good likеnеss(no surprisе,sinсеthе paintеrwas GеorgеRiсhmond, thе Ьеst portraitistin Еngland at thе tiпrе),whiсh points to thе faсt that Darwin сamе from a vеryriсh, middlе-сiirss family. Onе of his grandfathеrs,sharеdЬy his wifе, wаs Josiаh Wеdgwood, rеsponsiЬlеfor Ьringing thе pottеry tradе lnto massproduсtion.Although hе was a full-timеsсiеntist,Darwin nеvеrЬad to work for a living. Thе faсt that hе was living off thе family fortunе pеrhaps eхplainswЬу Оп tbe Оrigitt of Spесiеswas writtеn in a vеry opеn аnd userfriendlyfаshion.Darwin wаs wгiting ir-rpаrt for his sponsors,thе Darwin.!ilеdgwood family.
ехplainеdwаs through ..dеsсеntwith modifiсation,',an idеa that Darwin еmbгaсеd in еarly 18З7, shortlу after thе Bеаglе voyagе (Figurе 8). Unlikе еarliеr thinkеrs, whаt was of grеat сonсеrn to Darwin was thе сausе or сausеs of еvolution.\Х/ithoutсausеs'hе wаs no morе than onе among many еvolutionists.
9
10
The Historу of Еuolutioпаrу Тbought
iiiЁ,i:.:.'.:'
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Figurе 5. }{МS Beаgle.The Bеаgle was сaptаinеd Ьy RoЬеrt Fitzroy, thеn only 2З уearsold. Bеing a сaptainon а warship would Ье a very lonеly Post Ьесausе onе would Ье sеt asidе from thе сrеw. Fitzroy thегеforеlookеd for somеonе who сould bе his сompаnionon thе trip, somеonеnot in the navy Ьut а gеntlеmanablе to pay his own bills. Darwin fit thе joЬ pеrfесtly,rapidly еvolving from сaptаin's friеnd to full-timе ship's naturalist.Thе сrеw usеd to сall him ..Philos,''short for Natural Philosophеr_the tеrm thеn usеd for sсiеntists.
.sИithout сallsеs' hе сould nеvеr Ье thе Nеwton of Ьiology. Darwin wantеd to find a biologiсal forсе that would explain thе еvolution of lifе and was univеrsal in thе world and thе kеy Ьеhind all organiс motions' and to this еnd hе workеd fеvеrishlyfor thе nеxt 18 months, spесulatingаnd dоing an ехtеnsivе litеraturе rеviеw. Darwin soon rеalizеd that thе proЬaЬlе kеy to сhangе lаy in somеthing parallеl to thе way in whiсh animal and plant Ьrееdеrsеffесt сhangе, namеly, thе sеlесtiоn of thе dеsiгаЬlе and thе rеjесrion of all othеrs. Brrt how was oDе to gеt a natural еquivalеnt to thе Ьrееdеrs' artifiсial sеlесtion? At thе еnd of SеptеmЬеr 1838 Darwin rеad Аn Еssау on thе Prinсiplе of Popиlаtioz (sixth еdition, 1826| Ьу thе Rеvеrеnd Thomas RoЬеrt Malthus. In his work Мalthus arguеd that food suppliеs would always bе outstrippеd Ьy potеntial population growth. Hеnсе' unlеss thеrе was ..prudеntial rеstraint,'' thеrе wеrе bound to Ье ongoing struggles for еxistеnсе as pеoplе сompеtеd for thе availаЬlе food and suppliеs,inсluding living spaсе (Figurе 9). Darwin turnеd Мalthus's rеasoning on its hеad. Hе pointеd out that thеrе сould Ье no prudеntial rеstraint in thе animаl and plant wоrld' and hеnсе,bесausеpopulation growth сеrtainly Was not rеstriсtеd to humankind, thеrе would Ье an ongoing' organiс-widе strugglе for еxistеnсе. Мorе than this, suссеss and failurе in thе strugglе would (on avеragе) Ье a funсtion of thе diffеrеnt
сII
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Figurе 6. Prinсiples o his mеthodolоgiсalin
Tbe Historу of Еuolutioпаrу Thought
PRINCIPLBS
GЕ o Lo GY, вElIiтG
AN ATгЕlшPт To EхPLAIN TIIЕ FORMЕR сIIANGES oF тIIЕ DARтII'S sURFAcЕ' вY REaEBЕNoE тo сAusЕs Now lN oPEBAтloN.
linеd Ьy RoЬеrt Fitzroy' thеn only lould Ье a vеry lonеly post Ьeсause y thеrеforеlookеd for someonе nеonеnot in the nаvy Ьut a fit thе joЬ pеrfесtly,rapidly ip's naturalist.Thе сrеw usеd to сall --thе rеrmthеn usеdfor sсiеntists.
lton of biology. Darwin wantеd to thе еvolution of ]ifе and was uni'rganiс motions' and to this еnd hе ; p е с u l a t i n agn d d o i n g a п е х t е n s i v е : kеy to сhangе lay in somеthing LntЬrееdеrsеffесt сhangе, namеly, ion of all othеrs. But how was onе ' artifiсial sеlесtion? At thе еnd of tbе Priпсiple of Рopulаtioz (sixth s Robеrt Malthus. In his work rlways bе outstrippеd Ьy potеntial was ..prudеntial rеstraint,', thеrе stеnсеas pеoplе сompеtеd for thе 8 spaсе (Figurе 9). Darwin turnеd ntеd out that thеrе сould Ье no : world, and hеnсе, Ьесausе popuгo humankind, thеrе would Ье an nсе. Мorе than this, suссеss and :) Ье a funсtion of thе diffеrеnt
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сIIARLEs LYЕLL, Еs Q., F.R.s. FOe.
9J8C. TO TflD
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тwo vol.uмЕs. Yol. I.
LONDON: JoIIN lvIURRAY' ALBE},IARLE.SтREЕT. "oБ**.
Figurе6. Principles of Gеologу' The full titlе of Lyell's work tells you all aЬout his mеthodologiсalintеntions. Еventually, thеrе wеre thrее volumes.
11
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Тbe Historу' of Еuolutioпаrу Thougbt
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Figurе 7. Thе Gal;ipagostortoisеs.Darwin did not Ьесomean еvolutionistuntil hе rеtrrгnеdhomе and hе сould show his сollесtionof Ьirds to John Gould' a lеadingornithologist.It was whеn hе wаs told that thеrewеrе unаmЬiguously diffеrеnt spесiеstЬаt he movеd асross to еvolution. Notе that еvеn Ьeforе hе Ьесamеan еvolutionist,Darwin was moving in сirсlеswhеrе hе сould сall on thе tоp minds foг supPort and informatioп. He madе powеrful friеnds аt СamЬridgеand thеy spottеdhis talеntеarly.
Figurе 8. Thе trее of lifе. This littlе skеtсh,drawn inJuly 18З7, is from a private notеbook that Dаrwin was kееping on thе sPесiеsproЬlеm. Lаmarсk had а trееof-[ifеpiсturеand in thе еightееnthсеnturyonе сan find thеm in thе writings оf nonеvolutionistswho wеrе nеvегthеlеsstrying to shorмthе oгdеr in whiсh God hаd сrеаtеd.
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rawn in July 1837' is from a privatе lесiеsproЬlem.Lamarсk had a trее. )nесan find thеm in thе writings of g to show thе ordеr in whiсh God
Figurе 9. Thе Мalthusian еxpltlsion. This сartоon appеarеd in the Сomiс Аlmапасk in 1851. Onе of tlrе rеasons thаt l)аrwin was aЬlе to сonvinсе pеoplе of thе truth of еvolrrtion Was' apart frtlrn lris friеndly stylе, thе faсt that hе rеliеd on idеas tlrаt wеrе widеlv ассеrltеd in Viсtorian Britirin.
1З
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Thе Historу of Еuolutionаrу Thought сharасtегistiсspossеssеdЬv organisms. Неnсе tl-rеrеwould bе an ongoing natural sеlесtion in whiсh thе winnеrs would pаss on fеaturеs to thе nеХt gеnеrаtion and thе losеrs would gеt nothing. Ovеr timе' this sеlесtion would lеad to full-Ьlown organiс сhangе. But this organiс сhangе would Ье of a partiсular kind' for thе fеaturеs that mаkе for suссеss,known as ..adaptаti6n5''-f61 g;amplе, еars' еyеs' tееth, hands, lеgs, lеavеs, Ьаrk, and roots-would show that purposеful naturе that еpitoпizеs final сirusе. Darwin sat on his еvolutionary idеas for 15 yеars' during whiсh timе hе 's7'е turnеd to a massivе study of Ьarnaсlеs. arе not quitе surе why this dеlay oссurrеd, although Ьy this timе Darwin hаd fallеn siсk with a mystеriousail. mеnt that W21sto plaguе him for thе rеst of his lifе, and so undouЬtеdly hе Was not rеlishing thе hugе dеЬatеtlrat his idеas wеrе Ьound to сausе. Also a major faсtor must havе Ьееn his rеluсtanсе to upsеt powегful sсiеnсееstaЬlishmеntfigurеs (inсluding СаmЬridgе mеntors) who had еnсouragеd thе young Darwin in his work. Onе of thе things hе did during thе pausе was to nеtwоrk with youngеr sсiеnrists'who сould rally around him whеn hе did go publiс. Finally, howеvеr, Dzrrwin was pushеd into aсtion whеn, in thе .Wallaсе, middlе of 1858, hе rесеivеdа short еssay Ьy Alfrеd Russеl a сollесtor in thе Malay pеninsula' that had virtually thе samе prеmisеs and сonсlusion that hе had disсovеrеdsomе 20 yеars еarliеr.
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oN тнЕ oRlGlN oF sPЕсlЕs Darwin quiсkly wrotе up his idеas, and ()n thе Оrigin of Spесies bу Мeапs of Nаtиrаl Selесtion, or thе Preseruаtioп of Fаuсlиred Rасes iп thе Struggle for Lifе appеаrеd in thе fall of 1859 (Figurе 10). Thе work Ьеginswith a disсussion of artifiсial sеlесtion аrrd animal and plant Ьrееdеrs'grеat suссеssеs. This is partly hеuristiс,tо prеparе thе rеаdеr by following thе path thаt Dar. win himsеlf had takеn to disсovеry, and partly justifiсatory,suggеstingthat what wе сan do, naturе сan surеly do Ьеttеr.Following is a disсussion of thе variation thаt аlways oссurs in thе wild, somеthing that Darwin oЬviously nееdеd as thе building Ьloсks of сhangе. If еvсry organism Wеrе еxaсtly likе its parеnts, thеn thеrе сould Ье no еvolution' At this point Daгwirr was rеady to introduсе thе strugglеfor ехistenсеаnd' following on this, thе mесhanisnr of natural sеlесtion: A strugglе for ехistеnсе inеvitaЬly follows fr
Figurе 10. Thе titlе pag сhееky in quoting thе p thе topiс of thе law-gor Dаrwin's mеntorswhеr сontinuеd in this r
Notе that еvеn mor for rеproduсtion. lt is sеxцal dеsirеsof a phi way' givеn naturally с
Canit...Ьеthou1 havе undouЬtеdl1' . еaсh bеing in thе g сur in thе сoursс o doubt (rеmеmbеri siЬly survivе) that ovеr othеrs' would
Tbe Нistorу of Еuolutioпаrу Thought . Неnсе thеrе would bе an ongoing ould pass on fеaturеsto thе nеxt gеn;. ovеr timе, this sеlесtion would lеad ganiс сhangеwould Ье of a partiсular эss,knоwn as ..adaptation5''-f91 91еs' bark, and roots-Would show that :ausе. for 15 yеаrs, during whiсh timе hе !Ие arе not quitе surе why this dеlay had fallеn siсk with a mystеrious ailst of his lifе' and so undouЬtеdly hе Lisidеas wеrе Ьound to сaцsе.Also a -lсtanсе to upsеt powеrful sсiеnсеidgе mеntors) who had еnсouragеd tе things hе did during thе pausе was сould rally around him whеn hе did as pushеd into aсtion whеn, in thе .sИallaсе, y Ьy Alfrеd Russеl a сollес:uallythе samе prеmisеsand сonсlurs еarliеr.
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oп the Оrigiп of Speсies bу Мeаns n of Fаuourеd Rасes iп the Struggle urе 10). Thе work Ьеginswith a disand plant Ьrееdеrs' grеat suссеssеs. adеr Ьy following thе path that DarI partly justifiсatory, suggеsting that ttеr. Following is a disсussion of thе l, somеthing that Darwin oЬviously If еvеry organism Wеrе ехaсtly likе ion. At this point Darwin was rеady Ld,following on this' thе mесhanism
lws from thе high ratе at whiсh all y Ьеing' whiсh during its natural s' must suffег dеstruсtion during 1е sеason or oссаsionаl yеar' othсal inсrеasе, its numЬеrs would hat no сountry сould suppоrt thе е produсеd than сan possiЬly sur. gglе for еxistеnсе,еithеr onе indi, or with thе individuals of distinсt of lifе. (С. Darwin 1859' 6З)
15
Figurе 10. Thе titlе pagе of Оn tbе Оrigin of Spесiеs.Darwin wаs Ьеing a littlе Whеwеll, oppositеthе titlе pagе' on сhееkyin quotingthе philosophеr.!Иilliam .!Иhеwеll had Ьееn onе of thе topiс of thе law-govеrnеdnaturе of thе univеrsе. Darwin'smеntoгswhеn thе lattеrWas a studеntat СаmЬridgе,аnd hе сontinuеdin this ro1еin thе еarly yеars aftеr tЬe Bеаglе voyagе.Llе was a wеllknown opponеntof еvolutionand was sсathingon thе suЬjесtof Vеstigеs' Darwin sеnt a сomplimеntary сopy of the Оrigiп to.Whеwеll, who rеspondеd by Ьanningthе Ьook from thе shеlvеsof thе liЬrаry of Trinity Сollеgе' of whiсh hе was Mastеr (hеad)
Notе that еvеn morе than a strugglе for еxistеnсе,Darwin nееdеd a strugglе for rеproduсtion. It is no good having thе physiquе of Tarzan if you havе thе sеxualdеsirеsof a philosophеr. But with thе strugglе undеrstood in this sort of Way' givеn naturally oссurring variaгiоn, natural sеlесtion follows at onсе: Сan it . . . Ье thought improЬaЬlе' sееing that variations usеful to man havе undouЬtеdly oссurrеd, that othеr vаriations usеful in somе way to еaсh Ьеing in thе grеat and сomplех Ьattlе of lifе, should somеtimеsoссur in thе сoursе of thousands of gеnеrations?If suсh do oссur' сan wе douЬt (rеmеmЬеringthat many morе individuals arе born than сan possibly survivе) that individuals having any advantagе' howеvеr slight, ovеr othеrs, wоuld havе thе Ьеst сhanсе of surviving аnd of proсrеating
tb
The Historу of Еuolutioпаrу Тbrшgbt tlrеir kind? On tlrе othеr hаnd Wе шIаyfееl surе that any r,аrizrtionin thе lеast dеgгее injurious worrld Ье rigidly dеstrсlyеd.This prеsеrvatiorrof favouraЬlеvariations and thе rеjесtionof ilrjurious variations,I сall Nаt. u r а l S е l е с t i t l n(. 8 0 _ 8 1 ) In latеr еditiсlrrsDaгwin intгodtrсеd thе аltегrrаtivеtеrm gtruiuаl of thе fittest, wlriсh was pеrhаps a littlе unfoгtulratе,for it has lеd to еndlеss сlaims that sеlесtion is a tаutolсlgy, rеduсing simply to thе сlairn thаt thosе who survivе arе thosе who survivе. But althouglr this is oЬviously truе, sеlесtionmеans morе than tlrat. It сlaims, ior Ьеttеr сlr fсlr worsе' th21ton аvеragе tlrosе who survivе thosе whtl do not, and thilt suссеssin tlrе strugglе is a funсaге diffеrеnt fгсrr-n tiorr of thosе diffеrеnсеs.This may ()r may not Ье truе, Ьut it is not a tautology. Darwin inсludеd a sесondary sеlесtivе mесhanism. Hе arguеd that thе stгugglеis not always for food irnd spaсе Ьut сan Ье dirесtly foг matеs. This mесhanisrn, sехtlаl seleсtiс>tl, Darwirr dividеd into twtl Pаrts. Thеrе was sеlесtion through пlalе сomЬat (fсlrfе;rralеs). Tlrе antlеrs of thе dееr would Ье thе produсt of this. Тhеn thеrе was sеlесti
Thе anаlogywith anirnalЬrееdinglеd Dаrwin ro Figurе 11. Sеxual sеlесti
lесtion partiсularly pr thе samе spесiеs:sеlес istiсs rаthеr thаn spес sее sеlесtion (inсludin Нaving thus prеsе duсеd thе famous mе samе сlass havе somеl ilе largеly spеaks thе spесiеs еxtant today. еvolutionary paths of vеry first sharеd orig and thеsе, if vigorou Ьranсh, so Ьy gеnеrz whiсh fills with its dе еrs thе surfaсе with i
win 1859, 129-130) Now, with somе prеsеnt thе sесond р Darwin took thе rеa< instinсt, palеontology and showеd that ph through natural sеlес support thе mесhan
Figurе 12. Thе trее < this piсture is lеss or sprеads.
Thе Historу o|.ЕuolutiсllzаrуlT1',,,''' fееl surе that any variation in thе r"dеstroyеd.This prеsеrvation of of injuriousvariаtions'I сall Nat-
tеrnativе tсJm suruiuаl сlf the fittest, ,r it has lеd to еndlеssсlairns that sег Ь ес l а i n lt h а t t h r l s еw h o s t t r v i v еа г е bviously truе, sеlесtion mеаns morе э' that on avеragеthosе who survivе thаt strссеssin thе strtrgglеis а funсnot Ье truе' Ьut it is not a tautology' е mесhanism. Не arguеd that thе bllt сan Ье dlrесtly for mаtеs. This idеd into two parts. Thеге was sе_ ;). Thе antlеrsof thе dееr would Ье :tion through fеr-nalе сhoiсе (of thе or gеnеral plurr-ragе of thе pеaсoсk ; (Figurе11). Notiсе how sехual sе-
h animalЬrееdinglеd Dаrr,vrnto :сtion.Naturаl sеlесtion rеlpsurvival,likе thiсkеrсoars, сtion fоr аttriЬutеsthat givе plеamorе fегoсiousfightingquаlitiеs. [aи.(Bссаusеtl.tе()rigin wаs writtеn or illustrating. Most of Darwin's iouslyillrrstratеd.)
lесtion partiсulaгlyputs thе еmphasis on сompеtition bеtwееn mеmЬеrs of thе samеspесiеs:sеlесtionis dirесtеd toward individual-Ьеnеfitingсharaсtеristiсsrathеr than spесiеs-Ьеnеfiting сharaсtеristiсs.Darwin tеndеd always to (inсluding sееsеlесtion natural sеlесtion)aсting in this way. Having thus pгеsеntеdthе mаin Inесhanisms of сhangе, Darwin intro. duсеdthе famous mеtaphor of a trее: ..Thе affinitiеs of all thе Ьеings of thе samесlasshavе somеtimеsЬееn rеprеsеntеdЬy a grеat trее. I Ьеliеvеthis similе largеly spеaks thе truth.'' Thе lеavеs and twigs at thе top reprеsеnt thе spесiеsеxtant today. Thеn, as wе go down thе branсhеs' wе havе thе grеat еvolutionary pаths of yеstеrday. All thе way down wе go until wе rеасh thе .,As vеry fiгst sharеd origins of lifе. Ьuds givе risе Ьy growth to frеsЬ Ьuds, and thеsе,if vigorous, Ьranсh out and ovегtop on аll sidеs many a fееblеr Ьranсh, so Ьy gеnеration I Ьеliеvе it has Ьееn with thе grеat Trее of Lifе, whiсh fills with its dеad and ЬrokеrrЬranсhеsthе сrust of thе еагth, and сovеrs thе surfaсе with its еvеr branсhing and Ьеautiful ramifiсations'' (С. Darwin 1859, 129_130) (Figuге 12). Now, with soпlе minor problеms brr.rshеdaway, Dаrrvin was rеady to prеsеnt thе sесond part оf his thеory. For a good two-thirds of thе Оrigiп, Darwin took thе rеadеr through thе vaгious Ьranсhеs of Ьiologiсal sсiеnсеinstinсt,palеontology,Ьiogеography,сlassifiсаtion,m
Figurе 12. Thе tгееof lifе аs given in tЬе Оrigiп. Notiсе that thе еmphasis in this piсturеis lеss on showing lifе rеaсhing up and morе on thе way in whiсh it spreаds'
17
18
The Historу of Еuolutiсlпаrl Thought
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Figurе 1.3.Thе struсturеof Darwin's аrgumеnt.l)arwin did not hit Ьy сhanсеon this kind of argumеntаtion,whеrе a unifyir-rg hypсlthesis ехplainsin many 'Whеwеll, diffеrеntarеasand in turn is justifiеdor suрportеdЬl.thеsеаrеas. who сallеd it a ..сonsiliеnсе of induсtiсlns,''madе muсh of it whеn disсr.rssing suссеssfulthеtlriеsof physiсs,еspесiall1' Nеwttlnianmесlrаniсsand thе wavе thеory of light.Whеwеll idеntifiеdthе сirusеsat thе сеntеrof а сonsiliеrrсе аs ..truесausеs,''whаt Nеwttln hаd сallеd Uеrdес(l|tsае. Showinga сonsiliеnсеwas thеrеforеаn еssеntiаlstfatеgyfor а worrld-bеNеwtсlt-lof Ьiology.
Wеrе somе proЬlеmatiс issttеs.Soсial Ьеhlvior, pаrtiсtrlагlyth:rt shown by thе soсial insесts (thе hymеnoptеra-thе ants' thе Ьееs, and thе wasps), would Ье еasily ехpliсaЬlе if sеlесtion favсlrеdthе group. But frсrm an individualistiс pеrspесtir,е,why slror"rldol1е gеt stеrilе lr,orkеrs lvlro sееmirrgly spеnd thеir wholе livеs dеvotеdto thе lvеll-Ьеingof othеrs irl thе nеst or hivе? How сan natural sеlесtion,with its еmphasis on thс importanсе of rеproduсtion, рroduсе organisms that сaлn
would сall thе СаnrЬг е х p l a i n е ds i t n р l уз s e n o l o n g е r Ь е t h е r е ,Ь r . Ьrought out all of D whеrе now thеге Wrrе not find it. Еvеn if wе dotrЬtftll that wе wou prеssеd and mеtamor1 М o s t o t Ь е r а r е a so f triЬr-rtion(Ьiogеograph is that onе finds thе va Why, foг instanсе,doе that arе еxhiЬitеd Ьy tl simply that thе foundе thе mainlаnd, аnd onс. sify undеr thе nеw sе Figurе 7). Systеmatiсs еvolution. As Linnaеu сally in nеstеdsеts,thu МoгpЬology lrаrsthosс diffеrеnt spесiеs.oЬvi. Ьryology likеwisе was . еmbryos of soпrе diffеwhеrеas thе adults аrе faсt thаt in thе wonrЬ similaг (thеywould nor thе rwo adults would l Hеrе' as аlways thгouр analogy with thе worlс ..Fanсiеrssеlесt hand: arе nеаrly 8rown up: struсturеs lrаvе Ьееn a possеssеsthеm'' (С. D' So wе arе lеd to tt Сhristianity lrаd еvolr mеmЬеrs of thе \Х/еd сеаlеd that hе Was W unsеlf-сonsсiousrеfеr sееm to Ье fully satis dеntly сrеatеd.''This r tеr with what wе kno thе produсtion and ех shоuld hаvе Ьееn duс and dеath of thе indi Whаt God doеs not d nеss in supposing oth
Тhе Нistorу of ЕuсllиtiсlпаrуThoцgbt
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ЕmЬryoIogy
lеnt. Dагwin did not hit Ьy сhanсе on lg hypсlthеsisсхрl:rins in many эportеd by thеsе :rrеzrs.Whеwеll, who е n l t l с h r l f i t r rh с n d i s с u s s i n g :wtoniаn mссhаniсs and thе wavе еs at thе сепtеr of a сonsiliеnсе as ае саusае. Showing a сonsiliеnсе was Ье Nеwton of Ьiology.
,havior,partiсr-rlаrlvthat shown Ьy tе ants, thе Ьееs, and thе wаsps)' vorеd thе group. But from an indigеt stеrilе ч,orkегs who sееmingly l-Ьеingof othеrsirr thе nеst or hivе? asis on thе importanсеof rеproduсlroduсе? Finally, Dаrwin, who alovеr group approaсhеs Ьесausе hе Ldехploitation,dесidеdthat in suсh gratеdthat it is pеrnrissiЬlеto trеat r in whiсh thе individшalinsесtsarе lork on thе еvе, ft>rехamplе, whiсh m' so thе u.orkеr ехists fоr thе Ьеnhad its good points-for instanсе, gly wе find orgarrismsthat sееm to )f ехtant organisrтs that arе widеly .hеrеwеrе gaps irr thе fossil rесord, r aЬruptly at thе starг of what wе
would саll thе СzrnrЬriаn;thеrе Was l1()rес()rdЬеforе that' Thе gaps Darwin ехplairrеdsirlplу as a produсt of ilrсtlmplеtеfrrssilization.T.hеrеmains might no longеrЬе thеrе,Ьut thе linking anсеstorsdid еxist. Thе aЬrupt Ьеginning Ьrought out all of Darwin's invеntivе Powеrs. Еarly lifе proЬaЬly еxistеd whеrеnow thегеwеrе oсеans;this would еxplain why wе on dry land сould not find it. Еvеn if wе wеrе aЬlе to drill Ьеnеaththе oсеans, howеvеr, it was douЬtfulthat ъ.е would find lifе; thе prеssurе from abovе had surеly сomprеssеdand mеtirmоrphosеdthе fossil rеmains lrеlow (Figurе 14). Мost othег arеаs of Ьiology fеll int<-l plaсе witlr morе еаsе.Gеographiс disrvas а triumph ЬесаttsеD:rrwin ехplainеd iust why it triЬution(Ьiogеogrаplry) is thаt onе finс]sthе variolts pattеrns of arriпrаland plant lifе aгourrd thе gloЬе. !Иhy, for instаt-lсе, doеs onе havе thе strаngе sorts of distriЬutions and pattеrns that arе ехhiЬitеd Ьy thе Gal5pagos Arсhipеlago and othеr island groups? It is simply that thе ftrundеrsof thеsе isolatеd islirnd dеnizеns сamе Ьy сhanсе from thе mainland, alld onсе thеy wеrе еstaЬlishесl,thеy startеd to еvolvе and divеrsify undеr thе nеw sеlесtivе prеssurеs to wlriсh thеy wеrе now suЬjесt (sее Figurе 7). Systепrirtiсslikеwisе ехhiЬits thе kind of pattеrns onе ехpесts from еvolution. As Lirrrraеttsdеmonstratеd, organisnrs сan bе сlassifiеd hiеrarсhiсallyin nеstеdsеts,tlrusslrowinga pаttегnthat геvеаlspast history (Figцrе 15). Morpholog1,hirs thosе similaritiеs,саllеd lromologiеs,bеtwееn orgаnisms of diffеrеntspесiеs.oЬviously thеsеspеаk to slrarеdanсеstry(sееFigurе 1). ЕmЬryologylikеr,l,isеWas a partiсular point of рrгidеfor Dаrwin. Why is it tlrаt thе еmЬryosof soгtlеdiffеrеnt spесiеs,suсh as man and thе dog, arе vеry similar, whеrеasthе adults arе vеry diffегеnt? Darwin arguеd thаt this follows frorn thе faсt thаt in thе womЬ thе sеlесtivе forсеs on thе two еmЬryos would bе vеry similar (thеywсlr"rldnot thеrеforе Ье torn apart)' whеrеas thе sеlесtivеforсеs on thе rwo adults woшld Ье vеry diffеrеnt(thеy wor"rldЬе torn apart) (Figurе 16). Darwin turnеd to thе Неrе, as always tlrrouglror-rt his disсussions сlf еvсllr-trion, anabg,vr,r,ithtlrе world of Ьrееdеrsin tlrdеr to сlarify and support tlrе point аt sеlесtthеir horsеs, dogs, аrld pigеons, for Ьrееding' wlrеn thеy hand: ..Fiu-rсiеrs arе nеarly gro\vn up: thеy arе indiffеrеrrt rvhеthеr thе dеsirеd qualitiеs аnd struсturеshavе bееn aсquirеd еarliеr or latег in lifе, if thе full-grown animal possеssеs thеm', (С. Darwin 1859,446). So wе arе lеd to thе сonсluding passаgеsof the Оrigiи. Darwin, whosе Сhristianityhad еr,olvеdinto a form of dеisrn (Lyеll, a Unitariаn likе many mеmЬеrsof thе Wесlgwood family' Was а mаjor influеnсе hеrе), nеvеr сon' сеalеd that hе w,:rsr,vсlrkingin a God_Ьасkесl modе, and thеrе arе frеquеnt геfеrеnсеsto thе Сrеаttlг' ..Authors of thе lrighеstеnrinеnсе unsеlf-сonsсiot'ts sееmto Ье fulh. satisfiеdwith thе viеrv tlrlrt еaсh spесiеshas Ьееn indеpеn,.To my mind it dеntlyсrеatесl'''This was not Darwin's ptlsition. aссords Ьеttеr with whаt wе know of thе laws irnprеssеdon mattеr Ьy thе Сrеator' that thеproduсtionalrd ехtinсtion of thе past and prеsеntinhaЬitantsof thе world should havе Ьееn duе to sесondary сausеs' likе thosе dеtеrmining thе birth and dеath of thе irrdividual'' (С. Г)аrwin 18's9' 488). God Ьaсks thе world. What God doеs Irot с1ois gеt involvеd in thе world, and sсiеnсеhas no busin е s si n s u p p t l s i n gr l r h е r r r ' i s е .
19
20
Тhе Hist<.lrу сlf Еuolutioпаrу тABLв
oв STRATA
Tbought дttu Oвpsв or' AРPЕAR,ANолоr Aшrмдr, I,rrв UPoN
o N o z ц o
s
F A, UJ t-
o N
N ц'l
5
ч
o z
o o lrl
U'
TпrЬaгy. Shetl-Мarl. Glacial Drift. i fl Brick EвrtЬ. E8 Noтwiсh 1 Red }Crшg. Comllinе ) Fвlunн. Моlaвse. "" .'"-"-.. Gypr.
BonoBed.-мArи
l!ARтЕ.
Ьy Wеaponв.
Ф 3 . . . ;I
!9o{9n }сt"",. rlаяtlс, Мaеstricht' Uppeг Chalk. Iюweт Chalk'. Uppeт Сlгeensand Iюver Grеensand 'lYeвld Сla1.. ТIaвtingвSan.l PuгЬеck Bеdв. Kimmeгidgian. oхfoгdian. Кellovian. ltoгest Матble. Bath-Stone. StonoвfieldSlшtе' Grеat oolitе. Liдв.
гIlE
й
E fтпgu]аta. Caгnivоrа
s
Cyсloid. l _ Мoввsauгnв. Ci"ooid. l !rg,Еg' РolyptyсЬodoп' Brвоs, Ьу Boneв. Prосrlian Cтoсodilia.
e €
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Iguаnodоn. _l\Iaтsupialв' - Cheloniв Ьy Boneя. P]iosauгuв'
EE o
Мaгsupialв.
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Iсthуopteтуgia.
гvrAL|
"{-*-";:":"w
Е.
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Figurе 14. Тhе history of lifе as sееnin 1860. Тhis is takеn trom Riсhard owеn's Pаleoпt
Figuтe 15. Thе Linnaеa w i t h t h е m е m Ь е r so f | o с o m P г е h е n s i v еs)е r sa t l s e t ( k n o w n a s t a х a ,s i n 8 sharеd past' althoughas without rеgardto еvolu interprеtationgavеit nе hypothеsisof shаrеddе
тl1Е DEscENт
|
What аЬout humans? that humans aге part i on thе Bеаgle voyagе Тiеrra dеl Fuеgians' hс сally Darwin dесidеd l want to сonсеal his th points aЬout еvolution mеnts of all timе, hе si and his history.' (С. D thе topiс and dеal wi two-volume work, ТЙ.
Тhe Нistсlrу of Еuolutioпаrу Thougbt
)F APPЕAпANOE or ANIмAт, Т,rFE lдвтц' >1.0o0,oo0speсies
(аnimа|s)
I 6
Н
..-;;H'r't"+$:s Ф d
€
,d.l. Мoввsauгuв.l id. r дl8lrЕs' PoIуptyсЬodоn. I ' Ъy Boneв. l liвn Cтoсodilia. l I
trl
#;dseж rffi
€"*Wehf?
di d
я
.";;i;.^-"6. a--;.;"; ;.
5,,l60 sрeсies
(songbirds)
odoв. pialв,- CheloniшЬy Bonев цгu8.
&ж ldЖ
"-t#
,hyopteгygiш.
i, by Foot-pfints. эtotygia. iдtЬodontia.
'ia, by Toot.pгints. lL|A ganoоерh. Inвeсta
-si
Ei
I ganOld.
Figure15. Thе Linnaеanhiеrarсhy.organisms саn all Ье plaсеd in a hiеrarсhy with thе mеmЬеrsof lowеr-lеvеlsеts Ьеing groupеd into еvеr fеWеr(Ьut morе сomprеhеnsivе) sеtsаt highеrlеvеls.All organismsЬеlongto onе and only onе sеt(knownas taхa, singulartaхon) at еaсh lеvеl (саtеgory).This reflесtsa sharedpast, although as With thе fossil rесord' muсh of this was workеd out without regardto еvolution. Hеnсе, giving thе hiеrarсhy an еvolutionary interprеtationgavе it nеw mеaning and at thе samе timе сonfirmеd thе hypothеsisof sharеd dеsсеnt.
.oф
."f
I plaсo.ganoid.+ig.{ plaоoid.-
ь$1'Ё$:'*:Ъw т
Fuсoids.
zoopl\уI,os.
60. This is takеn from Riсhard wеn Ьесamеan implасaЬlееnemy of е matеrialistiс; Ьut, as young mеn эn proЬaЬlyЬесamеa ing thе сourseof history)'Ьut onе <еthesеas implying еvolution. As re fossil rесord thinking that it might entially сrеatеdorganisms.
21
тl]Е DEscЕNт oF MAN What aЬout humans? From thе first, Darwin was always stonе.сold сеrtain that humans arе part and parсеl of thе еvolutionary proсеss. His еnсountеr on tЬe Bеаglе УoУagewith thе nativеs at thе Ьottom of South Amеriсa, thе Tiеrra dеl Fuеgians' had сonvinсеd him of this. In the origiп, howеvеr, taсtiсally Darwin dесidеd not to makе muсh of thе human quеstion. Hе did not wаnt to сonсеal his thinking; hе simply did not want it to swamp his gеnеral pointsaЬout еvolution and its proсеss.Hеnсе, in onе of thе grеat undеrstatе. mеnts of all timе, hе said mеrеly' ..Light will Ье thrown on thе origin of man and his history'' (С. Darwin 1859' 488). Darwin fully intеndеd to gеt Ьaсk to thе topiс and dеal with it at lеngth. This hе did in 1871, offеring a major two-volumе work,The Desсent of Маn.
22
Thе Historу of Еuolиtiсlпаrу T'htlugbt
naturаlistiс pеrsPесtivе tlе еssay on how humal with spiritualism and с. natural еvеnt. Thеrе ml
}.lg.l.
Uppеl ffgпrеlruвltrп.'rJ}*3f;Ji:kоr'
l,oweтfi$tre thlt of s dog,
Рoff of this сonсlusion, tеristiсs that сould not human hairlеssnеssanс ally livеd with nativеs, powеr unusеd by pril prodцсеd Ьy sеlесtion. thе Thеorу of Nаturаl ' Suсh a сonсlusion w good ar8umеnts. Natul tivе human fеaturеs, Ь that is сharaсtеristiс o Ьеaury and dеsirabilit; .Wаllaсе wеrе not suсh сеrtainly not out of th( sion of sеxual sеlесtio .Why arе mеn Ьig and s сеstors who wеrе got tl domеstiс? Bесausе thе Ьеst joЬ with thе famil; anсеstors found sехua womеn (using Darwin' thе standard of Ьеаut1 Е x p е с t е d l y ,a l l o f t h i s i timеnts aboцt thе геlat dесidеd еminеnсе ovе mеntal powеr in man
326-з27). o. Forе.broln, сeтсtл.оl lrсtпispherсs, tс. r,. ]шld.brдin. с.,rln,г8 (lltа'lгigеn'iПs. с. Ilind.lrraiш. сerеlлllunt, medulla obloug8tд. d. Еуe. с. Iйг.
;f. Fiгst visсегal arсb' g. sосolrdvisсетдlarсh. I{. veгtсbгsl сolurnns and muасltlа in pтшeв:or d0vоloрвr(.ut.
ties. it.**'ltli]l. }ехtгеnri 'Гвil I,.
oг tiв соссyx.
Figurе 16. Similarityof thе еrnЬryoof humirnand dog. Again, Wе sееthе strеngthof the Оrigiп in r.r.raking шsеof fасts likе rlrеsе'wеll known to all Ьiologists.(Еrom ТЙe Dеsсепtrl|-Мап.|
No argumеnt is nеес his thinking wеrе star may havе Ьееn a rеvol triЬе. It is littlе wondеt By univеrsal aссlaim, that Еnglish Valhalla,
Aftег Darwin \й/hеnonе looks at this Ьook, it is rеally rathеr pесuliar. Most of thе Ьook is not on thе lrun-ranspесiеsаt all Ьut сonsists сlf an ехtеndеd еssay on thе seсondary mесlrаnism of sехu,rlsеlесtion.Tlrе pесuliarity of tlrе topiс yiеlds thе сluе to its gеnеsis. Alfrес] Russеl !Иallасе startеd Ьy shaгing Darwin's
Bеforе the origiп was of progrеss, it was op1 to that of mеsmеrisп Darwin сhangе thing was сеrtainly a сultur
The Historу of Еuolutionаrу Thought
f
J
noЕсkсг.
Iюweт figrrrе that olя dog'
naturalistiсpеrspесtivе on human origins and еvеn pеnnеd a stimulating littlе еssayon how humans might havе еvolvеd. But thеn hе Ьесamе еnamorеd with spiritualismand сonvinсеd that humankind сould Ье no сhanсе, purеly natural еvеnt. Thеrе must havе Ьееn a Mind guiding human gеnеsis. In sup.sИallaсе port of this сonсlusion' arguеd thаt thеrе Wеrе many human сharaсtеristiсsthat сould not havе Ьееn thе produсt of natural Sеlесtion, suсh as human hairlеssnеssаnd humans' grеat intеlligеnсе. \Wallасе,who had aсtually livеd with nativеs, maintainеd that thеrе wаs a vast аmount of Ьrain. powеr unusеd by primitivе man, and thеrеforе it сould not havе Ьееn produсеd Ьy sеlесtion. (\7allaсе's еssays arе сollесtеd tnЬts Сoпtribиtioпs to thе Thеorу of Nаturаl Selесtioп, 1870.) .Wallaсе Suсh a сonсlusion Was anathеma to Darwin, Ьut hе fеlt that had good argumеnts.Natural sеlесtion unaidеd сould not produсе many distinсtivе human fеaturеs, Ьut sехual selесtion сould. Darwin arguеd that muсh that is сharaсtеristiс of humans сamе aЬout through varying standards of Ьеauty and dеsiraЬility. Hеnсе, although distinсtivе' thе fеaturеs сitеd Ьy .!Иallaсе Wеге not suсh as to tаkе mаttеrs out of thе rangе of еvolution and сеrtainly not out оf thе rangе of sсiеnсе. Thus Darwin Wrotе a long disсussion of sеxual sеlесtion in gеnеral and thеn its appliсation to humankind. 10fhyarе mеn big and strong and powеrful and intеlligеnt? Bесausе thеir anсеstorswho wеrе got thе Ьеst womеn. \7hy arе Womеn soft and yiеlding and domеstiс? Bесausе thеir anсеstors who wеrе got thе Ьеst mеn and did thе .Why ЬеstjoЬ with thе family. arе humans hairlеss? Bесausе that is whаt thеir anсеstorsfound sехually ехсiting. Why (tо gеt morе spесifiс) do Hottеntot Womеn(usingDarwin's languagе)havе suсh Ьig Ьaсksidеs?Bесausе this was thе standard of Ьеauty of thе triЬе, and thе Ьravеst Ьravеs got first сhoiсе. Еxpесtеdly,all of this is wrappеd up with somе fairly standard Viсtorian sеntimеntsabout thе rеlativеaЬilitiеs of mеn and wоmеn: ..If mеn arе сapaЬlе of dесidеd еminеnсe ovеr Womеn in many suЬjесts' thе avеrage standard of mеntalPowеr in man must Ье aЬovе that of woman'' (С. Darwin |871,2,:
З26-З27\.
jf. First visсегal sтс}t. 9. Sссond visсeгal дтсh. H. Vеrtсbгal соlumns and in рrше8{ ot dсvсloрnrt,ut. d. Antеriог l I{. Рostегiог Jеxtгenrllleз. Il. Твil trг oя сoссyx.
muвсlt:!
tan and dog. Again, Wе sее thе :ts likе thеsе,wеll known to all
No argumеnt is nееdеd to alеrt us to thе faсt that by thе 1870s Darwin and his thinking wеrе starting to sеttlе into somе fairly сonvеntional modеs. Hе may havе Ьееn a rеvolutionary, Ьut hе Was not always that far ahеad of his triЬе. It is littlе wondеr that Darwin Ьесamе a major sourсе of national pridе. By univеrsal aссlaim, whеn hе diеd, hе was Ьuriеd next to Isaaс Nеwton in that Еnglish Valhalla, Iй/еstminstеrAЬЬеy (Figurе 17).
Aftеr Darwin ly rathеr pесuliar.Most of thе Ьook :onsistsof an ехtеndеdеssay on thе :r.Thе pесuliаrityof thе topiс yiеlds Иallaсе startеd Ьy sharing Darwin's
Bеforе thе Оrigiп was puЬlishеd, еvolution rodе on thе Ьaсk of thе doсtrinе of progrеss,it was opposеd Ьy thе idеa of final сausе, and its status was akin to that of mеsmеrism and phrеnology-it was a psеudosсiеnсе. Нow did Darwin сhangе things? As far aS progrеss was сonсеrnеd, Darwin himsеlf was сеrtаinlya сultural progrеssivistand saw еvolution itsеlf as progrеssivе.
1)
z-)
24
Thе Нistorу of Еuoltttioпаrу Tbсlught
Figurе 17. Сartoon of Dаrwin as аn apе. TЬс hr-lmorwas аlw.avsgеntlе and nеvеr sаvagе. Thе Еnglish Wеrе vеr}' pr
Нowеvеr, hе аlso saw that thе link Ьеtwееn progrеss and еvolution Was somеthing that Ьrought down thе stаtus
RеmеmЬеr that as f nаtural sеlесtion spеal blind.law ехplanation foг thе еnd-diгесtеd n. thiswаs no minoг mаt thе organiс world is it Hе was Ьrought up oI sеntеd in thе сlassiс dl Thеologу (1802). Hov Darwin may havе Ьееl аny kind had no plaс plainеd without rесoul T h е s t а t u so f е v o l u t i and surprising answеr: tionary thought up to еnсе, funсtioning wit praсtitionеrs using n:rt organiс ехistеnсе and might сall a profеssio man' so thе fatе of hi Thomas Неnгy Huхlе1 in Gеrmаny. Unfortun all Ьесamе ardеrrtеvoll Оrigin, whiсh showеd gеthеr undеr thе umЬr vеry kееn on natural s that thе wholе issuе o was unnееdеd, and ot and that sеlесtion сou othеr putativе сausеs' today might саll maсr е v o l u t i o nt h r o u g h a k i Admimеdly' thеrе w' thеory. onе was thаt t sее how suffiсiеnt nеw tions that sеlесtion сor unfortunatеly Darwin thаt whеn two orgаni turеs blеnd with thosе variation, within a gе What was nееdеd was nеw fеаturеs from gе Was that on thе bаsis t ing physiсists (notaЬl suсh a lеisurеly proсе But in a way thе sсiеr
Thе Historу of Еuolutioпаrу Tbougbt
]hеhumor was alwavsgеntlеand l of Darwin, and thеy still arе. Hе is :hеn,Darwin is as muсh а part of t tЬeHornеt mаgazinе.)
]twееn progrеss and еvolution Was s of thе lattеr, and hе rеalizеd that lеniеs thе inеvitaЬility of Ьiologiсal Darwin Ьrokе thе link Ьеtwееn thе lеd that natural sеlесtionсould lеad lay's еvolutionistswould сall a kind lming from сoпlpеtition with rivals. Lnisation,thе amount of diffеrеntia3ans in еaсh Ьеing whеn adult (and Ьrain for intеllесtualpurposеs),nat;tаndard:for all physiologistsadmit сh as in this statе thеy pеrform thеir . Ьеing;and hеnсеthе aссumulation tion is within thе sссlpе of natural frоm thе third еdition of the origiп
RеmеmЬеrthat аs far аs {inаl сausе Was сonсеrnеd' Darwin thought that naturalsеlесtionspеaks to thе dеsignlikе aspесt of living Ьеings. It givеs a blind.law ехplanation: sеlесtion lеаds to adaptation, and this is thе rеаson for thе еnd-dirесtеdnaturе оf suсh fеaturеs as еyеs and hands. For Darwin this was no minor mattеr. Hе always rесognizеd that thе dеsignlikе naturе of thе оrganiс wоrld is its most distinсtivе fеaturе аnd should not Ье ignorеd. Не wаs Ьrought up On thе Argumеnt from Dеsign' еspесially as it was prеsеntеdin thе сlassiс disсussion of Arсhdеaсon \Villiam Palеy in Ьls Nаturаl Thеologу(1802). Howеvеr' what was no lеss inrportant was that although Darwin may havе Ьееn a dеist (latеr hе Ьесamе agnostiс)' for him a god of any kind had no plaсе in a sсiеntifiс ехplanation. Еvеrything must Ье ех. plainеd without rесoursе to mirасlеs or othеr spесially guidеd forms of forсе. Thе statusof еvolutionary thought raisеspartiсularly intеrеstingquеstions and surprisinganswеrs.Darwin himsеl{ wantеd to raisе the status of еvolutionary thought up to thе lеvеl of physiсs and сhеmistry-аs a maturе sсienсе, funсtiоning within univеrsitiеs and rеsеarсh сеntеrs, with skillеd praсtitionеrsusing natural sеlесtion as a toсll to сut through thе proЬlеms of organiс еxistеnсе and funсtion. Hе wantеd еvolution to Ье what Wе today might сall a profеssional sсiеnсе. But it was not to Ье. Darwin was а siсk man' so thе fatе of his idеas had to Ье еntrustеd to othеrs-followеrs likе Thomas Hеnry Huхlеy in Еngland, Asa Gray in Amеriсa, and Еrnst Haесkеl in Gеrmany.Unfortunatеly, thеy had aims othеr than thosе of Darwin. Thеy all Ьесamеardеnt еvolutionists,аnd all agrееdthat Darwin's аrgumеnt in thе Оrigin, whiсh showеd how many arеas of Ьiologiсal inquiry сould Ье tiеd togеthеrundеr thе umЬrеlla of еvolution, was dеfinitivе. But fеw, if any' wеrе vеry kееn on natural sеlесtion.No onе dеniеd it outright, but somе thought that thе wholе issuе of finаl сausе Was ovеrЬlown аnd hеnсе that sеlесtion was unnееdеd,and othеrs thought that final сausе still nееdеd еxplanation and that sеlесtionсould not really do thе joЬ. Еithеr way, pеoplе turnеd to othеr putativе сausеs' suсh аs Lamarсkism, еvolution Ьy jumps or what wе today might сall mасromutations (thе thеory is known as saltationism)' or еvolutionthrough a kind of intеrnal momеntum (orthogеnеsis). Admittеdly,thеrе wеrе somе signifiсantЬiolоgiсаl pгoЬlеms with Darwin's thеory.onе was that hе had no working thеory of hеrеdity.Pеoplе сould not sееhow suffiсiеntnеw variation сould arisе and Ье maintainеd within populations that sеlесtion сould havе a lasting еffесt (Vorzimrnеr 1970). Somеwhat unfortunatеlyDarwin сompoundеd his proЬlеms in this rеspесtЬy аssuming that whеn two organisms Ьrееd, thе usual еffесt is that thеir distinсtivе fеaturеs Ьlеnd with thosе of thеir matеs. Неnсе, if only onе has a nеw' valuaЬlе variatiоn, within a gеnеration or two it is Ьlеndеd into virtually nonЬеing. !Иhatwas nееdеdwas a ,.partiсulatе''thеory of hеrеdity,that prеsеrvеdgood nеw fеaturеs from gеnеration ro gеnеration. Anothеr proЬlеm of Darwin's Wasthat on thе Ьasis of саlсulations aЬout the agе of thе еarth madе Ьy lеading physiсists (notaЬly thе futurе Lсlrd Kеlvin), thеrе Was too littlе timе for suсh а lеisurеly proсеss аs naturаl sеlесtion to takе еffесt (Burсhfre|d |975). But in a Way thе sсiеntifiс proЬlеrns Wеrе not thе dесiding faсtor. lfhat was
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Тhе Historу of Еuolutioltаrу Thoиght signifiсant wаs that еvеn Darwin's most ardеnt followеrs wеrе gеnеrally not that intеrеstеd in turning еvolution into a profеssional sсiеnсе' at lеast not as Dаrwin еnyisioned it. This wаs thе timе of grеat fossil disсovеries in thе Nеw \world-all of thosе dinosаur rтlonstеrsof thе past-and naturally thеrе was grеat intеrеst in woгking out thе truе pаths of lifе's history (Figurе 18). In сombination with not-аltogеthеr_rеliаЬlеmеthodologiеs liftеd from еmЬryology' most famously Haесkеl's so.сallеd Ьiogеnеtiс law thаt ontogеny (thе history of thе individual) rесаpitulatеsphylogеny (thе history of thе group), muсh еffort was еxpеndеd on working out thе full dеtails of thе еvolutionаry trее of lifе. But as a сausal thеory of origins, еvolution was somеwhat of a flop. Its еnthusiаsts Wеrе сontеnt to kееp it morе аt thе lеvеl of a ..popular sсi. еnсе,'' whеrе it сould hаvе a diffеrеnt rolе. Why? By thе sесond half of thе ninеtееnth сеntlrry, mеn likе Huxlеy wеrе working haгd to Ьring thеir soсiеtiеs сrut of thе еightееnth сеntury and into thе twеntiеth (Dеsmond 7994, 1997)' Thеy triеd to геform thе military, mеdiсinе, thе сivil sеrviсе'еduсation, and othеr institutions' A strЬjесtlikе pЬysiology oЬviously hаs а pragmatiс payoff in suсh arеаs as mеdiсinе (F.igurе19).
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Еvolrrtion sееms to hav Ьinеd with thе idеologу thе nеw rеfornlеd soсiс C h г i s t i a n i t v ,a k i n d o f s origins, а story of hurn they wеrе going arrd wh bаsiсаlly this wаs how l
Figurе 18. Dinosaur modеls'It wаs Riсhard owеn, in thе еаrly 1840s,who lаЬеlеda major grouр сlf rеptilеsas dinosaurs.From thе firstthеy сaptuгеd pеoplе'simaginations'as thеy still do. Thеsесonсrеtе,paintedmodеlswеrе madе foг thе Grеat ЕхhiЬition of London in 1851' whеrеBritain showеdits prowеss to thе world. Thеy arе now prеsеrvеdin а park in south London. Notе that thеy show dinosaursas rаthеrhеavy,сluпrsyЬrutеs'Tсldаy,wе think thеm muсh morе aсtivе.
rus of thе day, of whol еnсr Неrbеrt Spеnсеr. J anything from thе еigh from thе undiffеrеntiat thе homogеnеous to th thе Еarth, in thе dеvеlt Soсiеty, of Govеrnmеn aturе, sсiеnсе' Art, tl thгough suссеssivеdif]
Тhе Нistorу of Еuolutiсlпаrу Tboиgbt ardеnt followеrs wеrе gеnеrally not a profеssional sсiеnсе,at lеast not as of grеat fossil disсovеriеs in thе Nеw lf thе past-and naturally thеrе was ,aths оf lifеЪ history (Figurе 18). In mеthodologiеsliftеd from еmЬryol,iogеnеtiсlaw that ontogеny (thе hisylogеny (tlrе histоry of thе group), ut thе full dеtails of thе еvolutionary 'igins, еvolution was somеwhat of a it morе at thе lеvеl of a ..popular sсiеnth сеntury' mеn likе Huхlеy wеrе t of thе еightееnthсеntury and into iеy triеd to rеform the military, mеdrеr institutions. A suЬjесt likе physir suсh arеasas mеdiсinе (Figurе 19).
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Figurе19. Thе ..GrеatStink.''In thе suпrmеrof 1858 London Ьесаmеnеаrly uninhabitaЬlе bесausеthе Thamеs had Ьесorтеsuсh a vilе, odifеrousrесеptaсlе of еvеryonе'sraw sеwagе.Fеw things Ьrоught homе morе vividly to thе Viсtoriansthе nееdfor trainingin modеrn tесhnolоgiсalsr.rЬjесts, likе сivil (From Рuпch' 1858.) enginееring.
l owеn, in thе еarly 1840s,who rrs. From thе first thеy сapturеd e сonсrеte'paintedmodеls wеrе n 1851,whеrеBritainshowеdits ',еdin a park in south London. Notе lumsy Ьrutеs.Today, wе think thеm
Еvolution sееms to havе no suсh immеdiatе funсtion. But' еspесially сomЬinеd with thе idеology of progrеss, it сould funсtion as thе philosophy of thе nеw rеformеd soсiеty-it сould havе a rolе as а kind of altеrnаtivе to Сhгistianity,a kind of sесular rеligion in its own right. It сould Ье a story of origins,a story of humans' еxaltеd plасе in thе proсеss, a vision of whеrе thеywеrе going and what thеy should do to еnsurеsuссеssand triumph. And basiсallythis was how еvolutiс-ln Was prolnotеd, еspесiallyЬy thе lеading gurus of thе day' of whom nonе Was morе voсal than thе Еnglish man of sсiе n с еH е г Ь е r rS p е n с е r .P l а y i n g u p е v t l I u t i t l l lh, i s v i s i t l п W a s a s p r с l g r е s s i v aе s anythingfrom the еightееnthсеntury. Spеnсеr saw progrеss as Ьеing a movе from thе undiffеrеntiatеd to thе diffеrеntiatеd, or what hе сallеd a movе from thе homogеnеousto thе hеtеrogеnеous:..Whеthеrit Ье in thе dеvеlopmеntof thе Еarth, in thе dеvеlopmеntof Lifе upon its surfaсe' in tlre dеvelopment of Soсiеty,of Govеrnmеnt,of Manufaсturеs, of Сommеrсе, of Languagе, Litеraturе, Sсiеnсе,Art, this sаmе еvolution of thе simplе into thе сomplеХ' throughsuссеssivеdiffеrеntiatiсlns,holds throughout'' (Spеrrсеr1857,2_З).
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2 8 Tbe Historу of Еuolutioпаrу Тhought Еvеrything oЬеys this law. Humans arе morе сomplеx or hеtеrogеnеousthan othеr animals, Еuгopеans arе morе сomplеx or hеtеrogеnеous than savagеs' and thе Еnglish languagе is moге сomplеx oг hеtеrogеnеousthan thе tonguеs of othеr pеoplеs (Figurе 20). Inсidеntаlly, it was НеrЬеrt Spеnсеr who popularizеd thе word euolutioп, Until thе middlе of thе ninеtееnth сеntury' thе tеrm was gеnеrally rеsеrvеd for thе dеvеlopmеnt of thе individual (ontogеny). For evolution in thе mod..trаnsformation'' еrn sеnsе (phylogеny), most pеoplе usеd words likе (Riсhards 1'992). Sееing no еssеntiаl diffеrеnсе Ьеtwееn thе dеvеlopmеnt of
thе individual and thе d. just-quotеd еssay on prl tеrm for both. In thе С ..dеsсеntwith modi was ..еvolvеd.''Darwin alwa him a woolly and loosе t in the Оrigiz, a work tl tеndеd as a maior сontr usе a tеrm thаt appеaгеd to philosophy, litеratur timе of Tbe Dеscеnt of 1
day had Ьесomе univеrs and as сomfortaЬly as a A good rеligion' sесu of еvolution' thе artiсul; winism. Thе Ьasiс pattс ai
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Figurе 20. Thе trее of lifе as drawn Ьy Еrnst Haесkеl. Notiсе just how thе idеa of progrеssinfluеnсеdhis piсturе of lifе's history. (From HаeсkeL1897, 2:188.)
nеss of еvolution-sirг monаd to man. This is а vеry lеast, not impеdе i with thе еvolutionary p should promotе it and < Ьy еvolution. Start wit} nеvег oссurs-аnd it is : soсioесonomiс soсial p< pеtition, and thе wеak
supportеd amеlioration thе faсt that undеr thе r its unhеalthy' imbесilе ing,thoughwеll-mеani thе purifying proсеss br thе multipliсation of tt failing provision, and , providеnt by hеightеni ( S p е n с е r| 8 5 1 , з 2 3 _ 3 2 Christians diffеr, soI mеanings of thеir rеlig from anything еlsе, ma: world than in thе Ьiolo1 wеrе liЬеrtarian; othеrs еvolution; and still oth' appеaling to a kind оf low mеmbеrs of a spе сhism. Somе wеrе fеmi Somе wеrе paсifists (S
All usеd еvolution lеss living world-as a full-
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Thе Histсlrу of ЕuсllиtiсlпаrуThoиght for thе nеW soсiеty. No longеr:r psеudсlsсiеtlсе, еvоlutit)nwаs сегсainlyrro morе than a populаr sсiеnсе. l"{
Thе Synthеtiс Thеory Things pеrsistеdthis way into thе еarly dесасlеsof thе twепtiеth сеntuгу аnd in somе rеspесtsЬесamе еvеn worsе whеn Сontinеntal thirrkеrs,notaЬly thе еmbryologist Hans Driеsсh in Gеrmany and thе philosophеr Неnгi Bегgson in Franсе, Ьеgan pLrshinga kind of nеo-Aгistorеlianthеory of lifе thаt szrw spесiаl, nonphysiсal final forсеs guiding tlrе path of еvolution. DriеsсЬ's еntеlесhiеsаnd Bеrgson,sёlапs uitаuх' thе foundatiоns of ..vitalisпr,''wеrе iust not thе еlеmеnts of а forward-looking modеrn sсiеnсе.Rеliеf finally сamе with thе dеvеlopmеntof Mеndеliаn gеnеtiсsаnсl its mеlding rvith Darwiniurn sеlесtiorr,although еvеtrhеrе thе proсеss took til-r-rе аnd lvirs not stri]ishtforward (Рrovine |97I). Grеgor Меndеl, а Morаvian mtlпk who livеd irr thе Austro-Hungагian Еmpirе, disсovеrеdthе еssеntialprinсiplеs of hеrеdity in thе 1860s. Unlikе Darwin, hе sa'ur, thе trаnsmissionof сharасtеristiсsas ..pzlrtiсulatе,'' Ьеliеving thаt fеaturеslikе сolor аnd sizе саn Ье p.rssеdon without thе thrеat оf Ьеing Ьlеndеd аwаy (Figurе 2l ). Howеvеr, it was not Llntil thе bеginning of thе twеntiеth сеnttrrythat pеoplе сamе to аppгесiаtеthе impor. tanсе of Mеndеl's work and saw thаt it providеd а kеy еlеmеntin thе story of еvolution. You miglrt think thаt this was a tеrriЬlе missеd opportunity, and that, hаd Dагwin rеad Mеndеl's kеy papеr, hе would hllvе rеаlizеd thаt гtow hе had thе answеrs to all of tlrе issuеs of hеrеdity thаt his thеory of nаtural sеlесtion dеmandеd. Henсе, thе thеory would havе mсlvеd forward morе quiсkly' muсh еаrliеr. This is proЬaЬly not sO. Еvеn whеn thе work of Mеndеl was disсovеrеd, it to
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F i g u r е2 l . T h е p е a p l a n Меndеl to work out thе many diffеrentvariеtiе so forth. Меndеl сould passеdfrom onе gеnеfа rеsultswеге a littlе too l he was only rесordingr ovеrzеalouslytrying to plа sevеntееnth-сеntury
was rеvеalеd, and it с Finally, around 1930, taЬly R' A. Fishеr (19 Wright (19З7' t9Зz) sеlvеs and arе transmi works оnly in thе grou work to rhе соmplеtiс
Tbe Historу rlf Еuolutionаrу Тbought osсiеnсе'еvolution was сеrtainly no
dесаdеsсlf thе twеntiеthсеntury and LеnСсlntinепtalthinkеrs, notably thе 'and thе phiiosophеr Hеnri Bеrgson l-Aristotеlianthеory of lifе that saw thе path of еvolution.Driеsсh's еntfoundаtionsof ..vitalism'''wеrе just modеrn sсiеnсе.Rеliеf finally сamе еtiсsand its mеldirrgwith Darwinian s took timе and wаs not straightfora Моravian monk who livеd in thе hе еssеntialprinсiplеs of hеrеdity in rnsmissionof сharaсtеristiсsas ..parэr and sizе сan Ье passеdon without е 21). Howеvеr. it was not until thе lеoplе сamе to apprесiаtеthе imporlrovidеd a kеy еlеmеnt in the story of 's a tеrriЬlеmissеd opportunity' and lеr, hе would havе rеalizеd thаt now lf hеrеditythat his thеory of natural . would havе mсlvеd forward morе y not so. Еvеn whеn thе work of l assimilatеit. Many pеoplе at first )r than a ссlmplеment(sееЬеlow). So гhе monk's work was puЬlishеd in a ;еarсhеd,Darwin would havе found :е would havе Ьееn a ..еurеka'' m
Figurе21. Thе pеa plant.This lowly gаrdеnvеgеtаЬlеWas thе organismusеd Ьу Меndеlto wоrk out thе prinсiplеsof hеrеdity.lt wаs еasyto grow аnd сamе in manydifferеntvariеtiеsand forms-sееd аnd pod shapеand сolor, hеight'and so forth.Меndеl сould thеrеforеdistinguishаnd rесord hоw fеаturеsWеrе passеdfrom onе gеnеrationto thе nехt. It now sееmsсеrtainthat Меndеl's rеsultswеrеа littlе too good to Ье truе. It сould havе Ьееnthаt suЬсonsсiously hеwas only rесordingrеsultsthat fit his hypothеsis,or that thе gardеnеrwas ovеrzеаlously tryingto plеasеhis mastсr.This stylizеdpiсturеis from a latе. seventееnth-сеntury рlant Ьook.
was rеvеalеd,and it сould Ье sееn as thе сomplеmеnt tO natural sеlесtion. Finally,aгound 1930, a numЬеr of highly giftеd mathеmatiсal biologists,not a Ь l yR . A . F i s h е r ( 1 9 3 0 )a n d J . B . S . H а l d a n е ( \ 9 з 2 \ i n Е n g l a n d a n d S e w a l l !Иright (|9З1, I9З2) in Amеriса, showеd how Меndеlian gеnеs sort thеmsеlvеsand arе transmittеd irr groups (arrеssеntial finding, givеn that sеlесtion works only in thе group situation),and thеn it wаs possiЬlеto bring Darwin's work to thе сomplеtion that it nееdеd.Along with mutation (thе сoming of
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Тhе Historу of Еuolutionаrу Thought new variation, сausеd Ьy spontanеous сhangеs in gеnеs),nаtural sеleсtion сan truly Ье a signifiсant forсе for сhangе. Sinсе Ьy thе 1930s thе quеstion of thе agе of thе еаrth was no longеr prеss. ing (thе disсovеry of thе warming еffесts of radioасtivе dесay showеd that thе еаrth is quitе old еnor-rghfoг thе slow workings of sеlесtion),Ьiologists movеd rapidly forward with nеw idеas (known as popиlаtion genеtiсs) tЬat woцld put еmpiriсal flеsh on thе mathеmatiсal skеlеtons. In Britain a highly voсal supportеr of гhе thеoгy was Thomas Неnry Huxlеy's grandson Julian Huхlеy (thе oldеr brothеr of novеlist Aldous Huxlеy)' who produсеd a major work that pullеd idеas togеther:Еuolution: T|эe Мodеrп Sуnt|lesis(|942). Sсiеntifiсally, aftеr Fishеr thе most important figurе was thе oxford Ьiologist Е. B. Ford (|964), who did groundЬrеaking studiеs of sеlесtion in populа. tions of Ьuttеrfliеs and who gаthеrеd around himsеlf in а sсhool of ..есologi. сal gеnеtiсs''a numЬеr of youngеr rеsеarсhеrslikеwisе interеsrеdin sеlесtion and its еffесts in naturе. Notеworthy wеrе Aгthur Сain (1954) and Philip Shеppard (1958), who workеd on Ьanding pattеrns in snails, and Bernard К е t t l е w е l l1l 9 7 3 ) ' w h o s е i n t е r е s т w s е r е i n i n с l u s t r i am l еlanisnl-rhе wаys in whiсh Ьuttеrfliеs сhangе adаptivе сolor pattеrns as thеir haЬitats arе сhangеd Ьy thе еffесtsof smokе and pollLrtion.[n Amеriсa thе influеntial figurе was thе Russian-Ьorn gеnеtiсistThеodosius DoЬzhansky' whosе Geпеtics апd thе Оrigiп of Spесies |\9З7) wаs an inspiration to zrwholе gеnеrаtion of еvolu.s7orking tionists (Figurе 22). аlongsidе him wеrе othеrs' notaЬly thе oгnithologist/taхonomist Еrnst Мayr (author of Sуstemаtiсs апd the Оrigin of Spесiеs, 1942), thе palеontologist Gеorgе Gayloгd Simpson (Tеmpo апd Мodе iп Еuolutioп, 1944), and thе Ьotanist G. Lеdyard StеЬbins (Vаriаtioп апd Еuolutioп iп Plапts,1950). By thе 1950s Darwin's drеam of a maturе' profеssional sсiеnсе of еvolutionary Ьiology was rеalizеd. Мorеovеr, it was gеnuinеly Darwinian, for although thеrе had Ьееn prеtеndеrs to thе сausal thronе, notaЬly Sеwall .lfright's proсеss of gеnеtiс drift (random сhаngеs in gеnе frеquеnсy in small populаtions duе to thе vаgariеs of Ьrееding),it was гесognizеdthat thе kеy faсtor in organiс naturе is its adaptivеnеss, its manifеstation of final сausе' and thаt natural sеlесtionis a full :rnd satisfying way of еxplaining this phеnomеnon. At thе same tilтrе' proЕlress-and all thе moralizing and philosophizing that wеnt along with it-hаd Ьееn еxpеllеd.No onе was going to usе this kind of profеssional Ьiology as an ехсusе for quasi-rеligiousspесulations aЬout thе stаtus of humankind and thе oЬligations thаt naturе lays upon hum a п s ( F i g u г е2 3 ) ' Yеt, for all this, thеrе is onе morе important faсtor to thе story, and this partly еxplains why to this day еvolutionаry idеas rеmаin so сontrovеrsial to so many. Although еvolutionary Ьiology wаs upgradеd from thе lеvel of a popular sсiеnсеto thе lеvеl of a profеssional sсiеnсе,this did not oссur simply out o{ a disintеrеstеdquеst for thе truth Ьу mеn who hаd no aims Ьut thе finding of thе workings of naturе. Virtually еvеry onе of thе nеw profеssional biologists' from Fishеr to StеЬЬins,Ьесamеаn еvolutionistЬесаusеlrе was attraсtеd to thе suЬjесt Ьy thinking that it was morе than just a sсiеntifiс thеory.
Figuге 22. ThеodosiusDo fourth from left) at а сonf sсienсеmеаns having stud Hаrvard gеnеriсistRiсhаr Сornеll genеtiсistBruсе V was a Spаnishpriеst Ьеfor right in thе front row. Сlе sеxеswas а long-lastingp
For somе, likе DoЬzh: Ьгought pгogrеss-prog piсturе that saw God wс divisions that wеrе сru God's gгaсе аnd аn rrnfu was attraсtеd to thе idс ( 1 9 5 5 ) ,w h о p r o m o t е d and Мayr and Simpson too likеd thе idеa of prс somе kind of dirесtion r Bесausе all thеsе sеп еarly twеntiеth сеntury, dripping with mеtaphv surprisе if this had not h i m s е l f ,t h i s n е w l l r е е d sional status for thеir a< sсiеntists-thеn thеy wt pесts. Thеy nееdеd to d
Тhe Нistor,-oi Еuolutionаrу.[,hought 3.] эhangеsin gеnеs),natural sеlесtion е. agе of thе еarth Was no longеr press:s of radioaсtivе dесay showеd that w workings of sеlесtion),Ьiologists known as populаtiotl gепеtiсs) t,Ьat i]atiсalskеlеtons. In Britain a highly ras Flеnry Huxlеy's grandson Julian ous Huxlеy), who produсеd a major ioп: The Мodеru Sуnthesis (1,942). 'tant figurе was thе oхford Ьiologist king studiеsof sеlесtion in popula'und himsеlfin а sсhool of ..есologiсhеrs likеwisе intеrеsted in sеlесtion .еrеArthur Сain (1954) and Philip ing pattеrns in snails, and Bеrnard n industrial mеlanism-thе ways in attеrnsas thеir haЬitatsarе сhangеd -rAmеriсa thе influеntial figurе was )oЬzhansky,whosе Gепеtiсs апd tbe ion to a wholе gеnеration of еvoluhim wеrе othеrs, notaЬly thе or. or of Sуstеmаtiсsапd thе Оrigiп of гgе Gaylord Simpson (Tempo апd nist G. Lеdyard StеЬЬins(Vаriаtion
Figure22. ThесldсlsiusDoЬzhansk1''This piсturе of DoЬzhanskу froпt rrlш, fourtbfrom lеft) at a сonfеrеnсеwith his studеntsundеrlinеshow suссеssful mеanshаvingstudеntswho rvill саrry on and dеvеlоpyour idеas.Thе sсienсе HarvаrdgеnеtiсistRiсhard Lеwсlntinis sесondfrom thе lеft in thе front rсrw; lWаllaсеis riglrt Ьеhindhim; anс1FrаnсisсrlAyаlа (whсl СornеllgеnеtiсistBrr"rсе wasa SpanisЬpriеstЬеforеlrе Ьес.rпlеan Amеriсan еvolutionist)is on tlrе far rightin thе front row. Сlеarly' Dаrц,in'sviеrvson tlrе rеlаtivеaЬilitiеsсlf tЬе sехеswas a long-lastingprеjudiсеirl еvсllutionаryсirсlеs.
lturе' profеssiоnаl sсiеnсе of еvoluit was gеnuinеly Darwinian, for althе сausal thгonе, notаЬly Sеwаll r сhangеs in gеnе frеquеnсy in small ing), it was rесognizеd that thе kеy :ss, its manifеstationof final сausе' tisfying way of еxplaining this phеlnd all thе moralizing and philoson е х p е l l е dN . o onе was goingto usе сusеfor quasi-rеligiousspесulations Ьligations that lraturе lays upon hu-
For somе, likе Dobzhansky, thе i1ttrz1сtionwаs ехpliсitly rеligious. Не ЬroughtpгogГеss-progrеssto httmаns,that is-inttl a kind of ovеrirll world piсturеthat saw God working his way through thе foгсеsof nаturе. Ignoring divisions that wеrе сruсial to еarliеr thinkеrs, DoЬzhansky thought that God,sgraсеand irn unfrrrlingсrеаtion сould Ье сomЬinеd. Unsurpгisingly, hе was attraсtеdto thе idеas of thе .[еsuitpalеontolсlgistTеilhard dе Сhаrdin Huхlеv in Еngland (1955),who pronrсltеdsimitаr idеas. Othегs, likе .[r.rliаrr and Мayr and Simpson in Amегiсa, wеrе sесцlal.iп thеir thinking, Ьtrt thеy too likеd thе idеa of progrеss and thought that it showеd thаt еvolutitln had
)ortant faсtor to thе story' and this ary idеas rеmain so сontrovеrsiаl to , was upgradеd from tlrе lеvеl of а > n a ls с i е n с еt,h i s d i d n o t o с с u r s i m LthЬy mеn who had no aims Ьut thе ly еvеry onе of thе nеw profеssional tе an еvolutiоnist bесausе hе was at'as morе than just a sсiеntifiс thеory.
somеkind of dirесtiсlnand mеаning. Bесausеall thеsе sеminal еvolutiоnists wеrе pеoplе whо grеw up irr thе еarlytwеntiеthсеntr.lry,whеn rnuсlr
uldhavе Ьееn a surprisеif this Ьad not Ьееn tЬе lnаin motivating fасtсlr. But' likе Darwin saw that if thеy wеrе to havе profеshimsеlf,this nеrv Ьrееd of еvolr"rtionists sionalstatusfor thеir асtivitiеs-soп1еthingthеy аrdеntly dеsirеd as full-timе sсiеntists-thеnthеy would nееd ttl purify thеir work Of its ехtrasсiеntifiсaspесts.Thеy nееdеdto dеal witlr dсlсrrinеsof prсlgrеss:rnd with еХtгapolаtеd
34
Тhе Historу of Еuolutionаrу Thought
STUDIЕS oi\ IltliADIATЕD POPULAT]ONS D no So P Н I I, А M l] I' А N oG А S1,]tr]l*
oI..
By BRUCE WALLAс]] Bio|фc,ot I,a|пralorу,CoIdSqriщ llа'rbor, N.Y. (With Fivе Teхt.figures) (Recеiod 28 Jdу |95б) rштвoоuстloш It iв well kпorтn thаt the тridеspгead use of ionizing гвdiations, beсsuse of tlrеiг gеnetiс effeсts, posoв в pгoЬlem futurе genегations. The*е гadiвtions induсe gene .""g""diog mutations. TЬe vast majority of mutвtions haie dеletегiousеffесtson individuals свгrying them. Undег the pгеssuгe of сontinued mutatiоn, thеse deleteгious mutationв will aосumulatе in populвtionв. Thereforе, an iтгadiated population will, on thе avеrage, be lцrmеd-havе its .fitnesв' reduced'-by a сontinual u*р.o." to irгadiation. The pгеsеnt aгtiсle вummarizев obsrгvдtions made on iгrаdiatвd po|oйi1"". oi lиo. so1lhilamе|юnчавtюr.Somе of thе.mвterial presentedteгe haв Ьееn p"ьri'ьa pгeviously (Wallaсе, 1950, lg5l; wl]tryе & King, l95i, 1952). This summвгy,^ho,n".'',u., will intro. duсe lrew mдtоrial in вddition to еxtйding the oгiginai obsеrvatiЬns. Мдтввlдr, AND DtEтЕoDs Thе erpет'imеntnlnop]nlion.s. Tire eхpетimental population в of D' mеIюn,чoslerarе kept in luсite and sсгееnсageв.The огiginal fliев *eгe oЪйinеd fгom an oгчoniR stгвin kept' lry mass tгвnsfеr for mвny yearв. Fouгtеen letЬal. and sеmi.letЬвl-fгee sесond сhгomosomes wеге extrвсted fгom thig.stгвin thгough the usе of a вeriевof matings identiсal to tJrовedesсribed later (Fig. 2.)'.Flies сaгrying thеsе sесond сhгomosomes and miхtures of orеgon.R and .markеd stoоk' сhromosomeвotheг than thе ..""od ;;;; йlarental fliеs оf thс populвtions. Rгief dевсriptions of thе рpulationв aге given in Tаblе 1. Thе left-hand сolumn gives thе identifying numbег foг eaсh populвtion. Thе весondсolumn indiсateв tircoгrgin of thо .Stoоkв'indiоatеs populations whoвеoгiginal flies сaтгiedluth'l.г."u рopulation. *uсond сhгomosomes of oregon-R. deгivation. Tlrтeе more rеоent populations aгe subpopulations оf populationв 5 вnd 6; the deвignation in the tablе gives tie^pвгent,r p"p"ьt,l"" and the gеnегation duгing whiеh eggs wеIе removеd to вtaгt tЬе nеw The tЬird р"p'i*;;;. сolumn indiсвtеs the numlrег.ofвdulЬ in thе population .Ь,gu' .uiu.* to popotu. ".g"*, tions of aliout ]0,000 indir'iduals,.small'fo рpulвtionsЪ"qo"oТly *]iti гu'u. tь"n 1000 ildividuals. Thе last thгee сolumns of TaБlе l givе thЁ typJ ot."*po*uге, the
Figurе 23. A papеr on fruit fliеs Ьy Bruсе \Х/allaсe.Sее thе aсknowlеdgmеnt at thе^bottomof thе pagе. By thе 1950s' evсllutionistswеrе Ьесomi.'g u.iy сrеativе at finding funds for thеir work. DoЬzЬаnsky pеrsuadеdthe U.S. Aiomiс Еnеrgy Сommission that fruit fliеs wеге thе pеrfeсtmodеl organism for studyof the effeсtsof nuсlеаr rаdiation, a majсlr worry at thе timе givеn thе o.'goi.,g tеstlng of ЬomЬs (in.thеatmosphеrе). In Еnglanj, Е. B. Fоrd fеrsuadеdthБ шurя"ld Foundation that thе study of Ьuttеrfliеsgavе insight inio thе sprеad of gеnеsin populаtionsаnd hеnсewas of grеatvaluе in studyinghuman gеnеtiсallv саused аilmеnts.
moral ехhortations. so 1 Progrеss' morality, and l duсеd as profеssional rеs foundеd journal Еuolutiс authors' dеpositеd with t ing aЬout his intеntions l еnсеs аs possiЬlе. On tЬ ..Thе fiеld hаs rеaсhed Also, еvolutionary rеsеa from thе phylogеnеtiс ir еvaluаting thе faсtors of on thе othеr hand, it ha sеаrсh has suffеrеd in thl tion'' (lеttеr to G. G. Fеr Yеt, having donе thеir tionists thеn wrotе othеr еxhortаtion as anything 1 rrсtivеs wеrе foсusеd on l ninеtеenth. ..Thе most еs Ье just this: knowlеdgе' t As a first proposition of еvolution, it is suЬmittеd aсquisition of nеw truths ly the mutations of thе n. to othеrs and Ьy thеir aс< ity)'' (Simpson 1949, З1 Stаlinism was at its pеal undеr thrеat Ьесausе of t surprisingly, thеrеforе, .. and undеr somе сurrеnt ( ogy whiсh сan Ье madе t< of еthiсs hеrе maintainеd
Thе Past Half Сеntt
That was all 50 or morе synthеtiс thеorists in Am sidеrеd just as a sсiеnсе, thеory dеsеrvеdly is onе еmpiriсаl inquiгy. Еvery flourishеs as nеvеr Ьеfort еmpiriсal, havе rеaсhеd Rosеmary and Pеtеr Gral paradigmatiс еxamplе of hаs Ьееn vеry imoortant ]
сD PoPULAT]olt,s ol. LАNoGАS1,Eht* rALLАcli фniщ llarbor, N'Y. кt.figureв) uJу |9bб) ,тIoN
nizing radiations, bесause of t}reiг genetiс nегвtionв. TЬese гвdiвtions induсi gene l delеtегiouвеffeсtson individu"l. ."..}ьg ,tвtion, thеsе delеteriouв mutations wil.i tiвtod рpulation will, on the avеrвge, Ь ;inual ехрвuге to iггдdiвtion. r mдd-e. on iггвdiдted populations of Drosentedheгеlrвв bеen puЬlished pгеviously 952)'Thiв summвгy, howeveг,will intro. е oгiginвl obsеrvations. }lEтвoD8
tal populationвot D' mеlл,nчasler aге kept
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oгеgon-R stгainkeit
::lb*iid 1n iial- and sеmi.lethвl-fгee seсond the use of a seгieвof mвtings identiсвl "h.on,Ьtо resевесondсhromosomesand miхtuгes of heтthgn thе вeеondrveгethe paгеntal flies
эn in Tablе l. Thе left.hand сolumn gil,es e seсondсolumn indiсates tй" o.lgi,, #tьu rвe original flies сaггied lethal.frer seсoпj oJe recrnt poрulationsaгe вubpopulations вbIеgivesthе pвтеntalpopulation and thе .o ..11' tbе nеw р
/allaсе.Sееthе aсknowlеdgmentat riсlnistswеrе Ьесominguеiy сгеarivе ,,pеrsuadеdthе U.S. Atomiс Еnеrgy modеl organismfor study of thе ...i'.. givеnthe ongoingгеsring l. f :. б. l.ord pеrsпаdеdrhе Nuf6еld : insightinto thе spreаd of яеnеsin s г u d y i n gh u m a ng е n е t i с a l Iсyа u s е d
Tbе Нistorу
Thе Past Half Сеntury Тhаt wаs all 50 oг morе yеars ago. Thе nеo.Darwinians in Britain and thе synthеtiсthеoristsin Аmеriса Ьuilt good foundations for thеir sсiеnсе.Сonsidеrеdjust as a sсiеnсе,whiсli it h,. .u..y right to Ье, modеrn еvoluttonary thеorydеsеrvеdlyis onе of thе most fo,-n,j-looking and е*сitinf аrеas of еmpiriсal inquiry. Еvеry onе of thе аrеаs trеatеd Ьy Dаrwin in t|te Оrigin flourishеsas nеvеr Ьеforе.Sеlесtion studiеs thеmsеlvеs,Ьoth thеorеtiсаl and еmpiriсal' havе геaсhed a УerУ high dеgreе of sophistiсation. The work of Rosеmaryand Pеtеr Grant (1989) on thе Ьеak sizе of Gal5pagos finсhеs is a paradigmatiсехаmplе of ехсеllеnt sсiеnсе.Тhе аdvеrrtof -oГ...'ln. biology has Ьееnvеry important hеrе for offеring Ьotl-rnеw insights (for instanсе, thе
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Figlrе 24. Thе сovеr of thе first issuе сlf Еuсllиtir.пt. onе сlf thе ЬiggеstprсrЬlеms of thеsееarly profеssionalеvolutionistswas of findingpеoplе,working to thеir standards,who wеrе nоt studyingfruit fliеsor similar organisrns.Thе journal was launсhеdwith а gгаntfrom thе Amеriсаn PЬilosophiсalSoсiеty(fсlundеdЬy BenjaminFranklin) in PЬilаdеlphia.Rеvеаlingly,tЬе only pеrsonOn thе grxnts сommittееwho opposеdthе fundingWаs thе еmЬryologistЕdwin Сonklin. ЕmЬryologyWas thеn thе quееnof thе Ьiсllogiсalsсiеrrсеs and Сonklin was not сonvinсеdthаt еvolutionсor-rldЬе thе Ьasisof rсal profеssionirlsсiеnсе.Pеrhaps bесausеоf thеsеdisсiplinarytеnsions,еvolutionistsrеspсlndеdЬv ignorrng Ьiology еmbryologyand it was not until thе 1980s,Ьy wЬiсh timс m
signifiсanсеof drift at thе nеtiс fingеrprinting for dс .W dеtailеd in Еdward o. Sуnthеsis (1975), havе po tion and rесiproсаlaItrui t o е х p l a i n t h е i n t г i с a с i е sl from an individualistiс pе е m p i r i с а ls t u d i е s - f o r i n s t (|982) on thе rеd dееr of S a powеrful faсtor in thе е sially, thе fiеld (oftеn hеrе Darwinian fаshion looks ' fantiсidе and sехual Ьеha tion. Pаlеontology has Ьt major fossil finds-rесеntl twееn fish and amphiЬial mеntion thе finding in Ind srs, naturally known as tJ tесhniquеs havе еnaЬlеd g еvеr gгеаtеr pгесision. At pгoposеd (for instanсе, th аnd thе lаtе Stеphеn Jay othеr arеas of еvolutionar t е r n so f t h е p а s t ( f o r i n s t а | | 9 7 6 | u s е d е с o l o g i с a lt h t pаst pаttеrns of animal с сhangе, an еvеnt that oсс
Figure25. Punсtuatеdеqu g r a d u a l i s m .Ь. у Е l d г е d g еi r а l t е r n а t i v еp i с r u г е( B ) ' i t g l sаltationist,whiсh rathеr s сomparativеtimеsсalеs.Fс сhangесan tаkе plасе duri Ьarеlygеts rесordеdand a
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Morphology
|v]orphoIogу
Figurе25. PuпсtuatеdеquiliЬriurn.lrr thе Dаrrviniаnpiсturе,lаЬеlеd..phуlеtiс grаdualism,' Ьy Еldrеdgеаnd Gсluld (A), еvolutiongoеs smoothly.in thеrr piсture(B),it goеsЬy jumps. Gould dеniеdstronglythat hе was a alteгnаtivе whiсh rathеrsuggеststhat muсl-rof thе dеЬаtеwas aЬout saltationist, For а fгuit fly gеnеtiсist,1,000 1'еаrsis an agе аnd muсh соmparаtivе timеsсаlеs. 1,000 yеars сhаngесan takеplaсеduring thаt pеriod.For a pа[еoIltologist, Ьarеlvgеtsгесordеdаnd any сhаngеsarе gоing t()sееnlinstintanеOlls.
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Тhe Нisttlr1'tf ЕuolutirlпаrуlT|,с,"r'' Nrlrth Amеriса ioinеd and irrrinralsm
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Cynognathus Тriasвic ReptiIe
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Anteaters Armаdi||os Capybaras Glyptodonts Monkeys Opossums Porсupines
Figurе 27. Pаttеrns of foss y o u a s s u m еr h а t t h е с o n t i г how muсh еvolutioniststo wе hаvе сome from thе ol
Phorusrhaсids Bears
Sloths
Camels
Тouсans
Cats
Тoxodonts
Dogs EIephаnts Horses Peсcaries Rаbbits Raссoons Skunks Тapirs Weаse!s Figurе 26. Тlrе Grеat Amеriсаn Intеrсhаngе. By trеating North Arrrеriса and Sсluth Arrlеriса аs if thеy wеrе t''vо islands Ьеing сolonizеd, onе сan rvork out thе ехpесtесl гаtеs сli ехсlr.lпgс anсl thс numЬеrs tlf invadirrg gr.ouPs сlnе wсluld Ii Ьrium. ехpесt at еqr"ri
Systеmatiсs has bееn tran thе сoming of сomputеrs absorbеd, quantifiеd, сal likеwisе is opеn to nеw u! thе synthеtiс thеorists tе oame euolutioпаrу det,el сеptual baсkwatеr to thе еvolutionary studiеs (Сar
instаnсе,aЬout thе ways mans sharе thе samе un thе ways in whiсh orgс among thе hottеst arеas ( Thеrе arе' of сoursе' с thе importаngg-1hg ygr
еvolutionists' partiсularl; s o m е t i m е sq u е s t i o n s o f .
Thе Historу of Еuсllutioпаrу Tbought )vеdnorth to south and south to north rеoriеsof gеographiсdistribution Wеrе есtoniсs.Until this point, in a tгadition еvolutionistshad spеnt many happy lridgеsand finding ways in whiсh sееds эdiеs of watеr. Now thе moving of thе Lystrosaurus,a mammal-likе hеrЬivo00 million ),еarsago' is fat, short, and t would havе гoamеd far and widе. To. i г s( L o w е rT r i a s s i с )o n t h е с ( ) n t i n е n гos f l. This would Ье inехpliсablе wеrе it not l yеars ago аll thоsе сontinеnts touсhеd ly havе sinсе driftеd apart (Figure 27). Antаrctiса
Mesosaurus Permiаn Reptile
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Anteaters Armadillos
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Cаpуbaras Glyptodonts MonkeУs Opossums Porсupines
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Figurе27. Pattеrnsof fossil organisms.ThеsеdistriЬutionsmakе sеnsеonly if youassumеthat thе сontinеntswеrе joinеd. Phеnomеnalikе thеsеshow jusr howmuсhеvolutioniststoday still work in thе Darwinian modе аnd yеt how far we havесomе from tЬe Оrigiп itsеlf. (Unitеd StatеsGеologiсal Survеy.)
Phorusrhaсids Sloths Touсans Тoxodonts
аngе.By trеating North Amеriсa and rds Ьеing сolonizеd, onе сan wсlrk out numЬеrs of invаding groups onе would
Systеmatiсs has Ьееn trаnsformеd Ьy nеw сladistiс tесhniquеs,muсh aidеd Ьy thе сoming of сomputеrs that hаvе allowеd massivе amounts of data to Ье aЬsorЬеd,quantifiеd,сalсulatеd, and undеrstood (Hull 1988). Мoгphology likеwisеis opеn to nеW undеrstandings.AЬovе all' еmЬryology' a suЬjесtthat thе synthetiсthеorists tеndеd to ignorе, has now, еspесiaily undеr thе nеw nameеuolutiсlпаrуdeuеlopmепt (evo-dеvo), Ьееn сonvеrtеd from a nonсon. сеptualЬaсkwatеrto thе most еxсiting arеа of rеsеarсhtoday in thе fiеld of еvolutionarystudiеs(Сarroll 2005). Fantаstiс nеw findings havе еmеrgеd,for instanсе, aЬout thе ways in whiсh organisms аs divеrsе as fruit fliеs and humans sharе thе samе undеrlying gеnetiс mесhanisms for dеvеlopmеnt, and thе ways in whiсh organisms arе Ьuilt and vаriations arе produсеd arе amongthе hottеst arеas of rеsеarсh (Figurеs 28 and 29). Thеrеarе, of сoursе, сontrovеrsiеsand diffеrеnсеs.No onе wants to deny thе importanсе-thе vеry grеаt importаnсе-of natural sеlесtion.But somе partiсularly in arеas likе palеontology and еmЬryology, whеrе еvolutionists, quеstionsof adaptivе signifiсanсеarе (as was еarliеr thе сasе for somеtimеs
39
40
Tbе Historу of Еuolutiсlnаrу Thrlught
pеoplе likе Thomas Hеnr. pеrhaps othеr сausal faсtс of thе thеory of punсtuatе many fеaturеs arе not рal that is, nonfunсtional byL е w o n t i n l 9 7 9 ) ( F i g u r е s. ..Just rеlying tоo oftеn on yard Kipling (Figurе 32).
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Figurе 28. Dеvеlopmеnt in thе fruit fly. In thе сеntеr Wе hаvе thе gеnеs that сontrol dеvеlсlpmеnt, in thе ordеr in whiсh thеy Oссur on thе сhromosomе. Bеlсlw wе havе thе lаrvа and aЬovе wе hаvе thе grown fly.
L|vn{d P K в o в т A Y | в H o I L Е L L K I - F н Y | \ R Y L l в п н в } . е t д н t t V L s Е в o U K I W F o N в п м к wKкLкPф\ т К N v R т K в s в т A Y т в o o V L Е L Е K Е l H F N в Y L т п п в н t ! : в t д н s r с r т Е в o I K l W l o N R R M K W K K D йR$L P N l к т в s дi."iiн."д к LDPl .Nl т K | в s PKRsRIAYтRoovLtLFKЕFнYNвYLтRвRRVLIAF{ALсLsLRoIKIWFoNJRвMKWKK м^i'."н.,вд t R o I K I W F o N в R M К W K K DKнL P N т K I R s н " й l " н . ^ Ъ q P K R s R т A Y . l R o o V L Е L L к Е F н Y ' \ ] R Y L t п в я в v в tслLфs Е KKL D PN P K в s в т A Y т в o o v L F L Е K Е t t ] Y l \ R Y L т в R R в v F I A н s L с L s t R o l K I W l o N в R M K W K н тKIRs сhtсkHoхB4 KKH Lк PD\нт к | * s ;;;;;";;; f. fЁKкввss в т A l вRRRRRвVVEЕI A | Aн нт LI Lс Lf fsLEsRЕoвI oK Il W K IFW FR oN в RK М д vYтI ввoooovVLLЕЕLLЕtKKЕEFFнHYYNNR вY YL тL R oN RM WKK W KD K L P N тKVвS i'.],u"'Ъo KLPNтKцю] )lЁi"?i'ьi.Ъ"* miisЗщvтвooY!ELЕKЕFнYIIцLIRпвпvвtnнтrtllrsввqIKIWFoNRRМKWK!qц
F.igurе29. Homologous amino aсids.On thе lеft is а сolumn tlf thе nаmеsof gеnеsin diffеrеntоrganisms.All of thеsеgеnеsarе сruсial,kiсking in at similar stagеsof dеvеlopmеnt.Thе rows irr thс main Ьoх irrеmadе up of lеttеrs сorrеspondingto amino асids,produсеdЬy thеsеgеnеs,in turn produсinga vital protеin.It саn Ье sееnthat thе gеnеsof frrritfliеsand humans arе virtually idеntiсal,lеаdingto thе сonсlusiоnthаt dеvеlopmеntis likе Ьuildingmodеls with l,еgo Ьriсks.You startwith thе samе piесеsand thеn put thеm togеthеrin vеry diffеrеnt Ways.
Figure З0. A spandrel froп and assistants.Gould's сla spаndrеls(асtually,thе tru sРаndrеlssееm dеsignеdfс rеsultof othеr nееds.Hеn< p е r h а p sn a t u r а ls е | е с t i o ri
Тhe Historу сli l:,uсllиtioпаrуThought pеoplеlikе Thomas Неnry Huхlеy) not ovеrwhеlmingly prеssing' think that pеrhapsothеr сausаl faсtors wеrе sigrrifiсant.This Was thе undеrlying thеmе of thе thеoryof punсtuatеdеquiliЬri;r,with Gould in partiсr.rlararguing that manyfеatuгеsаrе not pагtiсLllarlyadаptivе Ьut arе moге ..spandrеl-likе''that is, nonfunсtional Ьy-prоduсts of thе еvolutionаry proсеss (Gould аnd Lеwontin1979) (Figurеs30 and 31). Hе aссusеd Darwinian еvolutionists of rеlyingtoo oftеn on ..Just so'' storiеs' thе fantaЬulous.likе talеs told Ьy Rudyard Kipling (Figurе 32). Today many еvo-dеvo еnthllsiasts fееl muсh thе
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[n thе сеntеr \4,еЬаvе thе gеnеs thаt iсh thеу ()ссur On thе сhromсlsomе. tаvе thе gгorvn flv.
вфr днтivGйoUKIWI oNRвMкWккф кrешткг.tvв B q f ж jЕA F l s L G Lт Е R o I K I W F oN R в M к W к к D i s R L P N т K т R s в в V Е|A l - s L с L s t п o I K I W F o \ в R M K W к K D H K L P N I K | в s R в V EI A | - f f L с L s Е п IoK I W lo N в R M K W K к D H к L P N т K | в s R я V Е |A H S L с L s Е R o IK I W F o N R R MK W K K D H к L P N т K I R s п в v в t n н т ф r s с п o l K l w t o N R R М K W к к o н к t .в t , ' l т кt s $ R R v t I А Hт L с L s Е R o| к | W F o NR R | vK]W K K D H K t P N т K V R s R B Y q l4 ! . г ф ц s Е R o I K I W t o N R R М K W ц ц q н ]щ L р ш т к ф .
n thе lеft is a сolumn of thе namеsof 3 gеnеsarе сгttсiаl,kiсking in аt sirrlill.rr main Ьoх arе madе up of lеttеrs l Ьy thеsеgеrrеs,in turn prtldr-rсing a rs of fluit fliеsаnd humans аrе r'irtually is likе Ьuilding moс1еls dеvеlopmеnt 1еpiесеsand thеn put thеm togеthеrin
FigurеЗ0. A spandrеlfrom thе Villа lr:rrrrеsinа in Romе, pаintеd Ьy Raphaеl аndassistants. Gould's сlаim is thаt rrrаnyfеаturеsof organismsarе likе (aсtuzrlly, spandгеls thе truе tесhniсаlnamе is pеndеntivе).Although thеsе spandrеlssееmdеsignеdfor painting' in truth thеy аrе siпrply produсеd as thе rеsultof othеrnееds.Hеnсе, onе shсlr-rld not аlways look for adaptation and pеrhaps naturalsеlесtiсln is ovеrratеd.
41
42
Тhе Historу of Еuolиtioпаrу Тhought
Figuге32. Thе elephant's nosе сamе aЬout Ьесausе, that many storiеsaЬout a<
Figurе 31. Thе Irish еlk. Aсtually, this now-ехtinсtЬеast,found in thе Ьogs of Ireland,is not a truе еlk. lt is rеmarkaЬlеfor its antlеrs.Thеy arе so largе it is hard to imaginе that thеy сould еvеr havе Ьееn of adaptivе аdvantagе.A popu. lar hypothеsistoday is that thеy grеWthrough sехualsеlесtion'thе еlks with Ьiggеr horns dеfеatingthеir rivаls and gеtting thе fеmalеs.It is suggеstеdthat thе еlks Ьесаmеfеrtilе Ьеforе thеy stoppеd growing and pеrhaps аn immаturе еlk would pass on his gеnеs,еvеnthough latеr in lifе hе and his offspringwould Ье at a disadvantаgе. An еxplanationlikе this shows how сarеfulonе should Ье in tаlking aЬout adaptationаnd its aЬsеnсе.In onе sеnsе,thе аntlеrsarе аdaptivе,but not nесеssarilyfor survivaland pеrhapsnot for muсh of thе animal'slifе.
samе way. ..Thе homologiеs of proсеss within morphogеnеtiс fiеlds providе somе of thе Ьеst еvidеnсеfor еvolution-just as skеlеtal and organ homologiеs did еarliеr. Thus, thе еvidеnсеfor еvolutiсlnis Ьеttеrthan еvеr. Thе rolе of natural sеlесtion in еvolution' howеvеr, is sееn to play lеss an important rolе. It is mеrеly a filtеr for unsuссеssful morphologiеs gеnеratеd Ьy dеvеlop. mеnt. Population gеnеtiсsis dеstinеdto сhangе if it is not to Ьесomе as irrеlеvant to еvolution as Nеwtonian mесhaniсs is to сontеmDorarv ohvsiсs''
(Gilbеrtet a|. 1996, З68, likе thеsе arе wisе and p, asts for a nеW disсiplinе way' thе vigor and еxсir firmеd. Doеs this thеn mеan tl tionary thinking has nor many pеoplеas a kind ol numЬегs of artiсlеs and grams) show oг justify i еvolution. Еdward o. W of books dеsignеd to sh flows not iust moral ех} forеsts-Ьut an aItеrnati
But makе no mistakе еnts thе human mind v wаys, point foг point i narrativе form is thе е1
Тbе lIistorу of Еt,сllutiсlпаrуТhoиght
Figurе32. Thе еlеpЬant'snosе.In his stсlriеs,Kipling сlaimеdthаt thе еlеphаnt's nosесamеaЬoutЬесausеа сroссldilеgraЬЬеdit and pullеd. Gould suggеstеd thatmanystoriеsaЬout adaptivеadvantagеhavе аЬout аs muсh plausiЬility.
)w-ехtinсtЬеast,found in thе Ьogs of э for its antlеrs.Thеy arе so largе it is 'е Ьееnof adaptivеadvantagе.A popu' roughsеxualsеlесtion,thе еlks with )ttingthе fеmаlеs.It is suggеstеdthat е d g r o w i n gа n d p е r h a p sа n i m m a t u r е r later in life hе and his offspring would е this showshow сarеfulonе should bе rсе. In onе sеnsе'thе antlеrs аrе I and pеrhapsnot for muсh of thе
;s within morphogеnеtiс fiеlds providе n-just as skеlеtaland organ homoloеvolution is Ьеttеr than еvеr. Thе rolе е v е r ,i s s е е nt O p l a y l е s s a n i m P o r t а n t пl morphologiеsgеnеratеdЬy dеvеlopo сhangе if it is not to Ьесomе as irrеl:сhaniсsis to сontеmporary physiсs''
(GilЬеrtet a|. |996,368). No douЬt postеrity will tеll us whеthеr sеntimеnts likе thеsеarе wisе and prеsсiеntor mеrеly thе unjustifiеdеffluvia of еnthusiastsfor a nеw disсiplinе thаt is trying to еstaЬlish itsеlf as important. Еithеr way' thе vigor and ехсitеmеntof сontеmporaгy еvolutionаry thеory arе сonfiгmеd. Doеs this thеn mеan that thе nonsсiеntifiс'morе idеologiсal sidе to еvolutionarythinking has now vanishеd? Doеs еvolution nо longеr funсtion for manypеoplеas a kind сlf sесular rеligion? Not at all. on thе сlnе hand, hugе numЬеrsof artiсlеs and Ьoсlks (not to mеntion radio and tеlеvision programs)show or justify idеologiсal impliсations аsсriЬеd to or drawn from .Wilson is а paradigm, for hе has pourеd out a strеam еvolution.Еdward o. of Ьooks dеsignеdto show that еvolution is progrеssivе аnd that from this .Wilson' thе prеsеrvation of thе rаin flowsnot just mоral ехhortations-for forеsts-Ьutаn altеrnativеviеw of сrеation to that of trаditiona1rеligion: But makе no mistakе aЬout thе power of sсiеntifiсmatеrialism. It prеsеntsthе human mind with an altеrnativе mythology that until now has always,point for point in zonеs of сonfliсt, dеfеatеd traditionаl rеligion. Its narrativеform is thе еpiс: thе еvolution of thе univеrsе from thе Ьig Ьang
4З
Г 11
Тhс Нistrlrуrlf Еuоlutitlпа1'Tbought сlf fiftееn Ьillion \Iеаrsago thrсlugh thе origin of thе еlеrrrеntsand сеlеstial Ьodiеs to thе Ьеgir.rnings of lifе on еartlr. Thе еv
10,000 yеaгs old and that i еrgy in just six days' follor vеrsal flood' savе only for (Rusе 2005; NumЬеrs 20( story hеrе' Ьut thе сonstan еnthusiastsfor this kind of thеory Ьut as somеthing m. tionаl Ьеliеf systеms that с hеld morаl norms. In thе' ..It rаl is Hеnry М. Мorris: punishmеnt for murdеr аn mеnt for othеr sеriousсril е v o l u t i o n а r yd е t е r m i n i s mt гis 1989, 148). Appаrеntl ..ath Rusе,'' а wеll_known thе morаl rot. lvlorе rесеn has morphеd into thе morr gеnt Dеsign Thеory, whiсh q u i r е s p е с i a lс r е a t i v еi n t е r is morе than just a сonfliс pеting idеologiеs. Thе fou Bеrkеlеу law profеssor Ph о l d t е r m s :. . T h е C h г i s t i а n an еasy targеt Ьесatrsе it ] with worldly idеаs likе hul whiсh аrе aсtually profoun ingly, this humanistiс mеt: gay marгiagе, aЬortion, ar
Conсlusion
Тhе history of еvolutiona until 1859, it was littlе m. idеology of progrеss, thе r It was opposеd to traditiol litеral truth of thе BiЬlе Ьl that сhangе сomеs only t on thе Оrigin of Spесiеs ,
truth of еvolution onсе an tion was ignorеd or down Darwin, notaЬly Thomаs еvolutionary idеas as a ki аn altеrnativе idеology to to soсiаl rеform. Thе thir. of Меndеliаn gеnеtiсs. I
Thе Нistorу of Еuolиtioпаrу,Thought tlrе origin of thе еlеrrrеntsаnd сеlеsе on еarth. Thе еvolutiсlrraryеpiс is ws it аdduсеs hеrе аnd nсtw arе Ьеy provеd ttl form a сausе.irnd-еffесt сial sсiеnсеs,from this woгld to аll :, and Ьасkward througЬ tinlе to thе lart of ехistеt-lсе is сonsidеrеd ttl Ье I1O ехtеrnal сontr
s kind of spесulatiоr-r-zrltl-rough hе disrrrсlwantеd to suЬstitшtеlris own idеаs s StерhеnJay Gould, partiсularly in his puЬlishеd mсlnthly in |хJаturаlHistorу. :rеkind of moral mеssagеfrсlm his writLiсin our soсiеtyсlr thе nеес]for сonsеrnal rеligiсlnmuсh morе sсopе than did Lеf:rvorеdсhiidrеn of Goсl, thаt wе lrurеation' arе simply hLrЬris...Sinсе dirrkedly largеr Ьrains, and sinсе suсh a iеs of rеptilian dеsign , We tnust asvе еvolvеdon our planеt if а сosmiс сasaurs as viсtims. In an еntirеly litеral аnd rеastlningmamtnаls, to our luсky J antiсipаtесlthе so-саllеdllеW аthеists' г h с r е а l m o f p o p u l : r rs с i е n с е w г i t i n g . tsitm(2О06)Dawkins argLlеsthat Сhrist)r sourсеsof humankind's rlls, and that )stitutе-a sесular philosophy informеd akеs appеalsto traditional rеligions not lsophегDaniеl Dеnnеtt's I)опuiп's Dапrr of tЬis kind of litеraturс' 'ny сгitiсs of еvolr.rtiorr:rry thinking. In rrfiгmsthat most Amеriсans do not ЬеrjorityЬеliеvеthat thе еi.rгthis lеss than
10,000yеars old and that all organisms wеrе сгеatеdin а Ьurst of divinе еn. еrgyin just siх dirys, followеd somе timе latеr Ьy thеir dеstruсtion in a цnivеrsalflood, savе only for thosе luсky pairs that floatеd away in Noah's ark (Rusе2005; NumЬеrs 2006|. Amегiсan еvangеliсal Сhristianity is not our storyhеrе,Ьut thе сonstant attасks on modегn Darwinism show сlеarly that for this kirrd of rеligion do not rеgard еvolution as just а sсiеntifiс еnthusiasts thеoryЬut as somеthing пlorе' a mаtеrialistiс,sесular altеrnаtivеto thе traditionalЬеliеf systеlllsthat сarriеs lvithirr it opposition to аll dесеnt and long..сrеation sсiеntist,'' hеldmoral norms. [n thе words of thе lеаding thе latе ..It HеnryМ. Morris: is rathеr oЬvious that thе modеrn opposition to сapital punishmеntfor murdеr аnd thе gеnеral tеndеnсy towаrd lеniеnсy in punishmеntfor othеr sеrious сrimеs аrе dirесtly rеlatеd to thе strong еmphasis on еvolutionarydеtеrminismthat has сhaгaсtеrizеdmuсh of this сеntury'' (Mor..notorious Dirrwinian philosopЬег Miсhaеl ris 1989, 148). Apparеntlv' thе ..athеistiс hltпratrist'''has madе а rnirjorсontгibution to Rusе'''a wеll-krrown сгudе litеrаlism of сrеation sсiеnсе thеmoral rot. МOrе rесеntly' thе rz.rtlrеr hasmorphеd into thе morе sophistiсatеdanti-Dаrwinism ot so-сallеd IntеlligеntDеsignThеory' whiсh sееsaspесtsof oгganiс lifе as so сomplех as to геquirеspесial сrеativе intеrvеntions Ьy thе Dеsignеr. But still thе dеЬatе today is morе than just a сonfliсt of sсiеnсеvеГsl'lsrеligion and onе Ьеtwееn сompеtingidеolсlgiеs.Tlrе foundеr of thе lntеlligеnt Dеsign movеlnеnt' formеr BеrkеlеylzrwprotЪssсlrPhiilip Jсlhrrsorr,is ехpliсit ir-rsееing еvolutiоn irr thе ..Thе oldtеrms: Сhristian philosophy that Was ovегthrown in thе 1960s was an еasy targеt Ьесausе it had Ьесomе idеntifiеd with Amеriсan сulturе аnd with worldly idеas likе human pеrfесtiЬilityand thе inеvitaЬility of progrеss, whiсharе aсtually profoundly un-Сhristian'' (Johnson 1997,106), Unsurprisingly,this humanistiс mеtaphysiсsis linkеd to moral failings-pornography' gaymarriаgе,aЬoгtiol-l'аnd likе transgгеssionssuсh as soсialisrl.
Сonсlusion Thе history of еvolutionary thеory falls into thrее stagеs.From aЬout 1700 until 1859, it was littlе morе than a psеudosсiеnсеriding on thе Ьaсk of thе idеologyof progrеss,thе notion that humirns сan makе сЬangе for thе Ьеttеr. Itrvasopposеdto tгаditional rеligion not so r-nuсhЬесausеit wеnt against thе it lеft no plaсе for Prсrvidеnсе,thе Ьеliеf litеraltruth of rhе BiЬlе Ьut Ьесаr-rsе thatсhangесoп-lеsonly through Goсl's undеsеrvеdgraсе. Сharlеs Darwin's Оп thе origiп
4S
46
Tbе Historу of Еuolиtioпаrl, Thought pгotЪssional sсiеnсе oi еvolutior.rary сlrangе. This oссurrеd, arrd it is this thеOry that flourishеs today. Yеt еvсllr-rtiorrisrsshould nеvеr fсlrgеt thе past and its influепсе On thе prеsеnt. Alorrg witlr thе sсiеnсе thеrе is still an ongсling dеbatе about idеolog1. аnd thе ехtеnt to lvhiсh еvсrltrtion in somе wаY рrovidеs a sесulаr altеrnatir,е to oldеr' Ovеrtly rеligiorrs ways Of viеwing thе world and humankind's status within it. вlBLloGRAPHY Aristotlе. 1984. Dе pаrtibиs апimаIium.In J. Bаrnеs, еd'' Тbе Сomplеtе Works tf Aristotlе,1087_-l1 10. Prinсеton, NJ: Prinсеton University Prеss. Bаnnistеr, R. 1979. Soсiа! Dапuiпism: Sсiспсе dпd М1,уfiiп Апglo-Аmеriсшt Sсlсiаl Тhtlught' Plrilаdеlphia: Теrnрlе Univеrsitv Prеss. Brеwstеr,D. 1844. Vеsтigеs.Nortb ]]ritish RеL,iеlu3: 470_51'5. .W. Saptorno,and Brown, P., T. Sutikna, М' J. Мorwood' R. P. Soеjono' Jatrnikсl'Е. R. A. Duе. 2004. A nеw slnall.Ьodiеd horninin from thе Late Plеisttlсеrrсof Еlorеs, Indtlnеsia. Nсltцrе 43 1: 10.55-106 1. Burсlrfiеld,J. D. 197'5.Lord Kеluiп апd tЬе Аgе сlf thс Лarrl:. Nеrv Yoгk: Sсtеnсе History Publiсatiоns. Сain, A. I. 1954, Aпimаl Spесiеsапd.Гhеir I'uolиtioп. London: HutсhiIrson. Сarroll, S. B. 2005. Епdlеss Fсlrпts Мtlst Bеаutiful: Тhе Ncц, Sсiеttсеllf Еuс, Dсt,,tl апd thе Маkiпg of thе Aпimаl Кiпg&mt. Nец, Yсlrk: Nсlrton. СhamЬеrs, R. 1844' Vеstigеs of tbе Nаturtll Histrlrу сlf Сrеаtigу'of Tu,сl Sс;сe-с. Indianаpolis:Haсkеtt. Сooреr, J. М., ed. 1997 ' Plаto: Сomplеtе V(/or&s. Сuviеr, G. l817. Lе rёgпе апimаl distribиё d'аprёs soп rlrgшtisаtiсlп,ptlur sеruir dе bаsе i l'histoirе п,ltиrеllе dеs апitпсtttхеt d'iпtrotlисtioп i l'апаtrlпliе сrлпpаrёе. 4 vols. Paris: Dёtеrr.illе. Daеsсhlеr, Е. B.' N. H. Shubin, and F. A. Jеnkins Jr' 2006. A Dеvoniаn tеtraроd.likе fish and thе еvolution of thе tеtrapod Ьildy plan. Nсrиre 44О:757_76З. Darwin, С. l859. Оп thе Оrigiп о|.Spесiсs.Londсlrr:.|olrnN,tr-rrrаy. 1871. Thе Dеsсе|1trlf Мап,2 vols. London: .JohnМuгra,v. 19 59 . Тhе Оrigiп of Spесiеs bу Сhаrlеs Dаrшiп: А Vаriltuпl Техt. М. Pесkhаm, еd. Philadеlphia:Urrivеrsitуof PеnnsylvilniaPrеss. сlr, Thе Lаtus сl|.ОrgаltiсLifе,3rd еd. 4 vсlls.Lоndon; Darwin, Е. 1801. Z,сlсlllсlltliа; J. Johnsоn. 180З. Тbе TеnryIе of Nаtt,trе.Londсln: J. Johnson. Dawkins, R. 2006. Thе God DеIиsirlп' Boston: Houghton Мiff]in. Dеnnеtt, D. с. 1995. Dаrшiп's Dапgсrrllts1rlса.Nеш. Ytlrk: Siпrсlnаrrd Sсhustеr. Dеsпrond, ^. |994. Нuхleу,,thе Dеuil's Disсiрlе. I-ondon:Miсhaеl Jоsеph. 1997, Нuхlеу, Еuоlиtiспt'sHigh l,riеst,I,сlndсln:Мiсhаеl Josеph. DoЬzhаnsky, т ' 19з7. Geпеtiсs аlld thе Оrigiп of Spесles.Nеrv Yоrk: СolumЬia Univеrsity Prеss. Еldrеdgе' N., arrd S. J. GoLr[d.l972. PunсtuаtеdеqiriliЬriа:An irltеrllаtir.еttl ph1,lеtiс gradualism. ln T. ]. М. Sсhopf, еd.,Мodеls iп Pаlеobiсlklgу,tt2-1l.5. Sаn Frаnсisсo: Frееman, (,oopеr' Fishеr, R. A. 1930. ТЬе Gепеtiсаl Тhеor1' of Nаturаl Sеlесtitltt,Oхfсlгd: oхt.oгd Univеrsitу Prеss. Ford, Е. B. 1964' Есologiсаl Gепеtiсs, London: ]\4еthuеn. еvolutiorraryand GilЬеrt, S.F., J.M. Opitz, and R. A. Rаff. 1996. Rеsyrrtlrеsizing dеvеlopmеntаlЬiсllogy.Dеuеk)pmultаl Bklltlgу |7 З: З57_З72.
Gould, S. J. 1989. Woпder Nеw York: W. !7. Nor Gould, S. J., аnd R. C. Lеw Panglossianpаradigm of thе Roуаl Soсiеtу сl Grаnt, B' R., аnd P. R. Gra Populаtioп:Тhе Lаrgе Сhiсago Prеss. H a е с k е l ,Е ' 1 8 9 7 . . Г h сЕ u l l Poiпts of Humап oпtс аnd сompilny.
H а l d а n еJ, . B . S . 1 9 3 2 . . Г h H u l l , D . L . 1 9 8 8 .S с i е п с eа ,1942.Еuolut Huхlеy,]. S. Johnson,P. Е. |997. Dеfеа IntеrVarsityPrеss. Jonеs,G. |98О.Soсiаl Dаr Kеttlеwеll,Н. B. D. 1973. L a m а r с k J, ' B ' | 8 0 9 . P h i l o L y е l l ,C . l 8 3 0 - l 8 3 3 . P r i п с Сhаngеsof thе Еаrth's 3 vols.London:John l М a l t h u s ,T . R . I 1 8 2 6 11 9 1 L o n d o n :Е v е г y m а n . Маrshall' L. G., S. D. IWе еvolutitlnаnd thе grеа М а y г , Е . | 9 4 2 .S у s l с m а l i UnivегsityPress. М o r г i s ,H . М . | 9 8 9 . T h e I Сrеаtirln/Еuсllutio п С< N u m Ь е г sR , . L . 2 О 0 6 .Т h e Dеsigп.2ndеd. Сamb Owеn' R. |860. Pаlаесlпt G еologiсаl Rеlаtiсlпs. P a l е y ,W . [ 1 8 0 2 ]18 1 9 . N а Rivington. -W. Provinе, B. |971. Тhe с Univегsityof Chiсagс -Гhе Riсhаrds,R. I. 1992. Prеss. Rusе,М. 7996.Мoпаd to СаmЬгidgе,МA: Har 2ОО5.Тhе Еt',olut UnivеrsityPrеss. Sеdlеy,D. 2008. Сrеаtiсlп CalifоrniaPrеss. S е p k o s k iJ,. J . ' J r . 1 9 7 6 .S Pаlеlэbblogу2, no.4 S h е p p а r dP, . М . l 9 5 8 . N . Simpson,G. G. |944. Теr UnivеrsityPrеss. | 9 4 9 .T b е М с а n i Spеnсеr'Н. 185|, Soсiаl Spесifiеdап,l thе Fir.
Тhе Histrlrу of Еuolutioпаrу
angе.This oссllrrеd' and it is this thеnists shоulсirrеvегforgеt thе past аnd .h thе sсiеnсеthеrе is still irrr ongoing to whiсh еvolution in somе Way рro)Vеrtlyrеligious Ways of viеwing thе t.
J. Barnеs' ed.,Tbс Сomplеtе Worhs of ) г i l r с е t o nU n i v е r ч i t rP.r е s ч . 'ltcе апd Nl1'thiп Апglo-Апte riсttп Sсlсiаl 'sityPrеss. Rеuiеl.e'3: 470_.j 1.5. .W. P' Soеjono,Jatmiko, Е. Sаptomo, and hoп-rininfrоm thr'-Lаtе Plеistoсеnt-of
r061.
с Аgе of thе ЕлrfД. Nеw York: Sсiеnсе , Еuolutioп. London: Hutсhinson. еаutiful: Thе Nеu, Sсiепсе of l:url Dеuo 'zll.Nеrv York: Noгtоn. il Histсlrуоi Сrеаtiсlп.London: Сhurсhill. vу of Сrеаtioп. .5thеd. London: Сhurсhill. S' D. АlЬon. 1982, Rеd Dееr: Bеhаuior Jnivеrsityсlf Сhiсago Prеss. lVorДs.lndiаnapolis:Haсkеtt. i d'аprёs soп tlrgапisаtiсlп,ptlнr sеruir dе . еt d'iпtrodисtitlп Й l'аllаtomiе с()mpаrёe. еnkinsJr. 2006. А Dеvсlniantеtгapсrd-likе Ьodv plan. Nаturе 440:757_76З' s. London: John N,luгrav. . London;John Мurray. |аrlеsDаrlui|I: А Vаriоrum Tехt. \4. of Pеnns1.lvаnia Prеss. s of Оrgапiс Lifе. 3rd еd. 4 vсlls. London: 1orr:J. Jсlhnson. ;tоn: Houghton Мifflin. 1deс.Nеw York: Simоn arrd Sсhustеr. .sсlple.London: NIiсhaеlJosеph. riс,-s,' Lсlndon: Мiсlrаеl Josеph. rigiп сlf Spесiеs.Nсw Yоrk: СoiumЬia uаtеd еquilibria: An аltеrnativе to phylеtiс сldеlsiп Pаlеobioklgу, 82_1 15. San ,f Nаturаl Sеlесtit-lп,Oхford: oхf
Thought
Gould, S. I,1989.\ilrlпderful I-ifе: Thе Bиrgess ,Shаlеапd thе Nаtнrе of Нisttlrу' Nеw York: W. W. Nсlrrсlп. Gould,S. J., and R. С. Lеwontirr. |979. TЬе spandгеlsof San ]vIаrсoand thе Panglossianpi1гadigm:A сritiquе of thе аdaptationist progr:rmme. Proсееdiпgs of thе Roуаl Soсiеtу of Londoп' Sеriеs B 205: 581_598. Gгаnt' B. R., and P. R. Grant. 1989. ЕuolutiLlпаr1l f)уn47niсs оf а Nаtиrаl Populаtion:ТЬе Lаrgе Сасtus Fiпch of thе Gоltipаgоs. Сhiсirgo: L}nivеrsity of Сhiсago Prеss. Haесkеl,Е. 1897. The Еuсllutil.lпof Мап: A Po1lulаr Ехpсlsitioll of thе Priпсipаl Poiпts of Humап oпtogепу апd Phуlсlgепy. 2 vols. Nеw York: D. Applеton and Company. Haldanе'J. B. S. 1932. Thе Сацses сlf Еuolutioп. Nеw York: Lоngtnans, Grееn. Hull, D. L. 1988. Sсiепсеаs а Proсеss.Сhiсаgo: Llnivеrsityof Сhiсagо Prеss. Huхlеy,J. S. 1942, Еuolиtioп: Thс Мodеrп Sуtthеsis. London: Allеn and Un'*,in. Johnsоn,P. F,. 1997. Dеfеаtiпg DLlrшiпism bу Оpепiпg Мiпds. Downеrs Grovе, IL: IntеrVarsityPгеss. Jonеs,G. 1980' Soсiаl Dаrшiпism апd Епglish Thсlиght, Brightor-r,U.K.: Наrvеstег. Kеttiеwеll,Н. B. D. 197З. Thе ЕuпsЕssеntiаl tсl Hиmап Hаp|liпеss Specifiеdапd thе First of TЬеllt Dеuеlopеd. Lоndon: J. Chapman.
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Тhe Historу of Еuсэlutioпаrу Тhсlltght 1857. Progrеss:Its law and сausе. WеstmiпsterReuieш 67:244-267, Stеbbins,G. L. 1950. Уаriаtioп апd Еuolutiсlп iп Plапts' Nеw York: СolumЬiа Univегsity Prеss. Tеilhаrd dе Сhardin. P. 1955. Lе phёпomёпе hнпшiп. Pаris: Ес]itionsdu Sеrril. Vorzimmеr, P. J. 1970. Сhаrlеs Dаrшiп: Thе Yеаrs сlf Сoпtrouеrsу. Philadеtphil: Tеmplе Univеrsity Prеss. .Wallaсе, A' R. 1858. On thе tеndеnсv of variеtiеsto dеpart infinitеly from thе оriginal tvpe. .|tlurпаl of thе Proссеtliпgs сlf thе Liппаеап Soсiеtl,,Zсlologу 3: 5з-62. 1870. Сoпtrillцtitlпs to thе Thеorу of Nаtltrаl Sеlесtiсlп:A Sеriеs of Еssауs. London: МасmiIlan. .Wilson, Е. o. |975. Soсiсlbiсllсlgу: Тbе Neш Sупthеsis,СamЬridgе' МA: Bеlknap Prеss сlf Hаrvаrd Univеrsitv Prеss' |978. Оп Htttпап Nаturе. Сambridgе, МA: Нarvard Univеrsity Prеss. Wright, S. 1931. Еvolrrtion in Mеndеlian populаtions. Gепеtiсs 16:97_1,59. 1932'Thе rolеs of mutatiOn' inЬrееding,сгossЬrееdingand sеlесtionrn еvo]ution. Proсcеdiпgs rlf thе Siхth Iпtеrпаtitlпаl Ссlпgrеss oi Gепеtiсs 1: з56_З66.
Thе orig
JеffreуL. Bа
Gеnеrаtions of sсiеnt tiоn of thе origin of ally is as сеrtain as surround us.
Нow. whеrе. and whеn r wаs геluсtant to addrеss r |, 1871.,to his friеnd Jr paragraph that ..it is oftе of a living Ьеing arе now (and oh what а Ьig if) w sorts of ammonia аnd ph a Protеin сompoulrd Wа сomplех сhangеs' at thе ] аЬsorЬеd, whiсh would l formеd'' (Darwin 1887, Cambridgе. It is геfеrеnс rеproduсed in Сalvin 19t Darwin's lеttеr nоt onl; of lifе Ьut also providеs сt naturе of thе Ьasiс Ьiolog sсiеntifiс сirсlеs. Althоugl сallеd thеm nuсlеin) in 18 in gеnеtiс proсеssеs woul trast' thе rolеs plаyеd bу firmly гесognizеd. Еquall' jor advanсеs had Ьееn m. wЬiсh for a long timе hаr ganiс сompounds. Thе ех Alеksandr Butlеrov, who laЬorаtory synthеsis of r starring matеrials, wеrе r sеpаratingorganisms frol
WеstminstеrRсuiеtl,,67: 244_267 . tiсlп iп Plаnts, Nеw York: СolumЬia эnc humаin. Pаris: Еditions du Sеtril. 'hе Yeаrs of СlлtroL,,еrsу.Philаdеlphia: а r i е т i е rso d е p a r ti n f i n i t е I yГ r o m г h е tgsсlf the Liппаеап Soсiеtу, Z
Thеorigin of Lifе leffreуL. Bаdа аnd Аntonio Lаzсапo
ш Sупthesis,СamЬridgе, MA: Bеlknap idgе,МA: Hаrvаrd Ur-rivеrsity Prеss. loрulations.Gеnеtiсs |6: 97-| 59 . эеding,сrossЬrееdingаnd sеlесtionin tеrnаtioпаl Сгlпgrеss of Gепеtiсs I:
Gеnеrationsof sсiеntistsmаy ).еthavе to сomе and go Ьеforе thе quеsгion of thе origin of lifе is finаl11'sсllvеd.That it lvill Ье solvеd еvеrttually is аs сегtаin аs аnything сan еvеr Ье amid thе unсеrtaintiеs that suгroundus. Еari AlЬеrt Nеlson, TЬеrе Is Lifе oп Маrs (1956\
How, whеrе,and whеn did lifе appеar on еarth? Although Сharlеs Darwin wasrеluсtantto addrеssthеsеissuеsin his Ьooks, in a lеttеr sеnt on FеЬruary 7, 1877, to his friеnd Josеph Dalton Нookеr, hе wrotе in а now_famous paragraphthat ..it is oftеn said that аll thе сonditions for thе first pгoduсtion of a livirrgbеing arе now prеsеnt,whiсh сould еvеr havе Ьееn prеsеnt.But if (аndoh what a big if) rvе сould сonсеivе in somе warm littlе pond with аll sortsof ammonia and phosphoriс salts,-light, hеat, еlесtriсityprеsеnt' that a protеinсompound was сhеmiсirlly fornrеd, rеady to undеrgo still morе сomplеxсhangеs,at thе pгеsеntsuсh mattеr would Ье instantly dеvourеd' оr absorЬеd,whiсh wоuld not havе Ьееn thе сasе Ьеforе living сrеaturеs wеrе formеd''(Darwirr 1887, 'i, 18). (Thе lеttеr is in thе Darwin Сollесtion in Сambridgе.It is rеfеrеnсеdas Lеttеr 747 | in Burkhаrt and Smith l994 and is rеproduсеd in Сalvin 7969,4_5.) DагwirrЪlеttеr not onlv summаrizеs in a nutshеll his idеas on thе еmеrgеnсе of lifе but also providеs сonsidеraЬlе insights on thе viеws aЬout thе molесular naturеof thе basiс biologiсal proсеssеsthat wеrе prеvalеnt at thе timе ln mаny sсiеntifiссirсlеs.Although Friеdriсh Мiеsсhеr had disсovеrеd nuсlеiс aсids (hе сallеdthеm nuсlеin) tn 1869 (Dahm 2005)' thе dесiphегing of thеir сеntral rolе in gеnеtiсproсеssеswould rеmаin unknown for morе than 80 yеars. In сon. trast'thе rolеs playеd Ьy protеirrs in mаnifold Ьiologiсal pгoсеSsеshad Ьееn firmlyrесognizеd.Еqually signifiсant, by tlrе timе Darwin wrotе his lешеr, major advanсеshad beеn madе in thе undеrstandingof thе matеrial Ьasis of lifе, whiсh tЪr a long timе had bееn сonsidеrеd fundaпrеntally diffеrеnt from inoг.!76hlеr, ganiссompounds.Thе ехpеrimеnts of Friеdriсh Adolph Streсkеr, and AlеksаndrButlеrov, who hаd dеmorrstrаtеdirrdеpеrrdеntlyгhе fеаsiЬility of the laboratorysynthеsis of urеa, alаninе, and sugars, rеspесtivеly' from simplе startingmatеrials,Wеrе rесognizеd as a dеmonstration that thе сhеmiсal gap sеpаIating organisms fronr thе nonliving was not insurпrtlr.rntaЬiе. 19
F 50
The Оrigiп of Lifе But how had this gap first Ьееn Ьridgеd? Thе idеa that lifе Was an emеrgеnt fеaturе of naturе has Ьееn widesprеad sinсе thе ninеtееnthсеntury. Thе major Ьrеakthroughs that transformеd thе origin of lifе from purе spесula. tion into workaЬlе and tеstablе rеsеarсh modеls wеrе proposals that wеrе suggеstеdindеpеndеntly in thе 1920s Ьy Alеksandr I. oparin and J. B. S. Haldanе, as wеll aS othеrs (sееBada and Lazсano 200З). Thеy hypothеsizеd that thе first lifе forms wеrе thе outсomе of a slow, multistеp proсеss that Ьеgan with thе aЬiotiс synthеsisof organiс сompounds and thе formation of ..primordial soup.'' Hеrе thеir proposals divеrgеd. Whilе Haldanе arguеd a that virusеs rеprеsеntеda primordial stagе that had appеагеd prior to сеlis' opаrin arguеd that сolloidal, gеl.likе systеms had formеd from thе soup, lеading to anaеroЬiс hеtеrotrophs that сould takе up surrounding organiс сompounds and usе thеm dirесtly for growth and rеproduсtion. Although thе dеtails of thеsе idеas havе Ьееn supеrsеdеd' thе oparin-Haldanе hypothеsis of сhеmiсal еvolution providеd a сonсеptual framеwork for thе еxpеrimеntal dеvеlopmеnt of thе study of thе оrigin of lifе. LaЬoratory еxpеrimеnts havе shown how еasy it is to produсе a variеty of organiс сompounds, inсluding Ьioсhеmiсally important monomеrs' undеr plausiblе сosmiс and gеoсhеmiсal сonditions. Thе roЬust naturе of thеsе rеaсtions has Ьееn dеmonstratеd Ьy thе finding that organiс сompounds arе uЬiquitous in thе univеrsе, as shown by thеir prеsеnсеin сarbon.riсh mеtеoritеs'сomеtary spесtra' and intеrstеllar сloцds whеrе star and planеtary formation is taking plaсе.
A Timеsсalе for thе Еmеrgеnсеof Lifе Although traditionally it had Ьееn assumеd that thе origin and еarly еvolu. tion of lifе involvеd sеvеral Ьillion yеars (Lazсano and Millеr 1994), suсh viеws arе no longеr tеnaЬlе. It is truе that it is not pоssiЬlе to assign a prесisе сhronology to thе appеаranсеof lifе, Ьut in thе past fеw yеars еstimatеS of thе timе within whiсh this must havе oссurrеd havе Ьееn сonsidеraЬly rеduсеd. Dеtеrmination of thе Ьiologiсal origin of what havе Ьееn сonsidеrеd thе еarliеst traсеs of lifе is now a rathеr сontеntious issuе (van Zuilеn еt al. 2o0z). This is not surprising. Thе gеologiсal rесord of thе еarly Arсhеan is sparsе' and thеrе arе vеry fеw roсks that arе morе than 3.5 Ьillion yеars old. Thе roсks with agеs grеatеr than 3.5 Ьillion yеars that arе prеsеrvеd havе bееn еxtеnsivеly altеrеd Ьy mеtamorphiс proсеssеs(van Zg||en et a|.2002|, and thus any dirесt еvidеnсе of anсiеnt lifе has apparеntly Ьееn largеly oЬlitеratеd. Although the Ьiologiсal naturе of thе miсrostruсrurеsprеsеnt in thе 3.5 Ьillion.yеar-old Apех сhеrts of thе Australian !Иarrawoona formation (Sсhopf 1993) has Ьееn disputеd (Brаsiеr еt a|. 2002; Garсia-Ruiz еt al. 2003), thеrе is еvidеnсе that lifе еmеrgеd on еarth vеry еarly in its histоry. Thе proposеd timing of thе onsеt of miсrobial mеthanogеnеsis,Ьasеd on thе low 1зС valuеs in mеthanе inсlusions, has Ьееn found in hydrothеrmally
prесipitаtеdquartz in thе (Uеno еt a|' 2006), аlthou МсCollom 2006). Howеv diсatе Ьiologiсal sulfatе-r 3.4 billion-yеar-old Sout} rinе еnvironmеnt inhaЬit аnd Lowе 2004\' Thеsе r old stromatolitеs from W idеa thаt thе еarly Arсhеa origin of lifе must havе ta pеrmit thе survival of thе Thе еarly Arсhеan foss quirеd for thе origin and r сritiсal faсtor may havе Ь. siЬlе аs soon as thе planе watеr. Unfortunatеly, tht с o n d i t i o n so n t h е е а г l у е а lесulаr or physiсаl rеmni еvolutionаry proсеssеs th ganisms found in the еarl ing not only on thе сoп pегiod of thе origin of lifr gеnеral and loсal еnvlroг impoгtant for thе еmеrgе
Thе Primitivе Еarth
ConsidеraЬlе progrеss ha сonditions of thе еarly е сhеmistry may havе oссr thеrе arе still еnormous сompounds assoсiatеdwi ing еntitiеs and how thеs t u а l е v i d е n с еo f t h е i r е х i havе bеgun on еarth' wе ] history and undеr what thе origin of lifе took pl. liquid watеr and oгganiс availablе еvidеnсе suggе lасkеd protеins and dеpе сlеotidеs, Ьut watеr was vidеs thе mеdium for сh сomponеnts, as far as wе It is unlikеly that Watе ing thе Hadеan pеriod tl
Thе Оrigiп of Life dgеd?Tlrе idеa that litе was an еmеrlrеad sinсе tlrе ninеtееnth сеntury. Thе d thе origin of lifе from prrrе spесulaLrсh modеls Wеrе proposals that wеrе s Ь y A l е k s a n d rI . O p а r i n а n d J . B . S . nd Lаzсano 2003). Thеy lrypothеsizеd omе of a slow, multistеp proсеss that 4aniссomptlundsand thе formation of osals divеrgеd'Whilе Haldanе arguеd stаgеthat had appеared prior to сеlls, 3 systеms lrаd formеd frorn thе soup, at сould takе up surrounding organiс r growth and rеproduсtion. Although supеrsеdеd,tlrе Oparin-Наldanе hy_ idеd a сonсеptual framеwoгk for thе 'rdy of thе origin of lifе. LaЬoratory s to produсе a variеty of organiс сom)rtant monotnеrs,undеr plausiЬlе сos. э robust natuГе of thеsе rеaсtions has г organiс сompounds arе uЬiquitous in с е i n с а r Ь o n - r i с hm е t е o r i r с sс, o m е t a r y star and planеtary formation is taking
е of Lifе sumеd that thе origin аnd еarly еvoluе a г s ( L a z с a n oа n d М i l l е r 1 9 9 4 ) , s u с h . t h a t i t i s n o r p o s s i Ь l еr o a s s i g n a p r е l i f е ' Ь u t i n r h е p a s t f е w у е . r r sе s t i m a t е s vе oссurrеd havе Ьееn сonsidеraЬly rеal origin of wlrat havе Ьееlrсonsidеrеd 1егсontеntiousissuе (varrZuilеn еt al. clogiсal rесord of thе еarly Arсhеan is |ratarе morе than 3.5 Ьillion yеars оld. i Ьillion yеars that arе prеsеrvеd havе lhiс prосеssеs(van Zuilеn et a|.2002|, ;iеnt llfе has apparеrrtly Ьееn |arge|у thе miсrostruсtrrrеsprеsеnt in thе 3.5 э Australian NИarrawoonа formation ,гasiеrеt a\' 20021 Garсia-Ruiz еt al. rgеd orr еilrth vеry еarly in its history. niсroЬiаlmеthanogеnеsis,Ьasеd on thе ts, has Ьееn found in hydrothеrmally
prесipitatеd qtlartz in thе З..SЬillion-yеar-old Drеssеr Formation in Australia (Uеnoеt al. 2006), although tlris finding has i.rlstlЬееn сhallеngеd (Lollar and МсСollom 2006). Howеvеr, sulfur isotopе invеstigationsof thе samе sitе indiсatеЬiologiсalsulfatе-rеduсingасtivity (Shеn еt al.2001), and analysеsof 3'4 Ьillion-yеar_old South Afriсan сhеrts suggеstthat thеy forrnеd ln a marinе еnvironmеntinЬaЬitеd Ьv anaеroЬiс photosynthеtiс pгokaгyotеs (Tiсе and Lowе 2004). Thеsе rеsults' сomЬinеd with rеports on З.43 Ьillion-yеаrold stromatolitеsfrom .JИеstеrnAustralia (Allwood et a|.2007), support thе ideathat thе еarl,vArсhеan еarth Was tееming rvith prokaryotеs' and that tlrе originof lifе mr"rst hаrvеtakеn plaсе as soon as tlrе сonditions wеrе suitaЬlе to pеrmitthе survivаl of thеsе tvpеs of organisnrs. Тhе еarly Arсhеan fossil rесord spеaks for thе rеlativеly short timеsсalе rеquirеdfor thе origin and еarly еvolution of lifе on еarth and suggеststhat thе сritiсalfaсtormaу havе ЬееrrtЬе Prеsеnсеof liquid watеr' whiсh Ьесamеpossiblеаs soon as tlrе planеt'ssurfасе finаlly сoolеd Ьеlorv thе Ьoiling point of wаtеr.Unfortr-rnatеiy, thеrе is no gеologiсal еvidеnсе of thе еnvironmеntal сonditionson thе еarly еarth at thе timе of tlrе origin of lifе, nor arе any molесuiar or physiсal rеmnants pГеsеrvеd that providе infornration aЬout thе еvolutionaryproсеssеsthat prесеdеd thе appеaranсе of thе fiгst сеllular organismsfound in thе еarly fossil reссlrd.Dirесt inforпratiorris gеnеrally lасk_ ing not only on thе сomposition of thе tеrrеstrial atmosphеrе during thе pеriodof thе origin оf lifе Ьut also on thе tеrnperaturе' oсеan pH, and othеr gеnеraland loсаl еnvironmеntal сonditions that may or may not havе Ьееn impoгtantfor thе еmеrgеnсеof living systеms'
Thе Primitivе Еarth Еnvironmеnt progrеsshаs Ьeеn lrradеin our undеrstandingof еnvironmеntаl СonsidеraЬlе сonditionsof thе еarly еarth аnd how tlrе transition frorn аЬiotiс to Ьiotiс сhеmistrymay havе oссurrеd (for ехаmplе. sее Bada 2004). Nеvеrthеlеss, thеrеarе still еnormous gaps in our dеsсription of how thе simplе Orgаnrс сompoundsassoсiatеdwith lifе аs wе know it геaсtеdto gеnегatеthе first liviпgеntitiеsand how tlrеsеin trrrn еvolvеd into orgаnisms thаt lеft Ьеhind aсtuаlеvidеnсеof thеir ехistеnсеin thе roсk rесоrd. Тo еvaluatе how lifе may havеЬеgunon еarth' Wе must aссеsswhat thе planеt was likе during its еaгly historyand undеr what сonditions thе proсеssеsthought to bе involvеd in thе origin of lifе took plaсе. Lifе as wе know it dеpеnds on thе prеsеnсе of [iquidwatеr and oгganiс polr,mеrs suсh as rruсlеiс aсids аnd proteins. Thе аvаilaЬlееvidеnсе suggеsts tl-ratduring arr еarly stagе, Ьiologiсal systems laсkedprotеinsand dеpеndеdlargеly on сatalytiс and rеpliсativе polyriЬonuсleotidеs'Ьut watеr was likel1.еssеntial fronr thе vеry Ьеginning, as it providеsthе mеdium for сhеmiсal rеaсtions tсl tirkе plaсе' Withоut thеsе Ьasiс сomponеntsJ i1sfar as wе know, lifе is irrrpossiblе. It is unlikеly that watеr mаdе its first appеaranсеon еartlr as a liquid. During thе Hadеan pеriod thе volatilе сomponеnts that wеrе trappеd insidе thе
52
Тhe origiп of Lifе aссrеting planеt wеrе rеlеasеd (dеgassеd)from thе intеrior of thе juvеnilе еarth to form a sесondary atmсlsphеrе.Any primary atmosphеrе (if onе ехistеd at all) must havе Ьееn lost' as еvidеnсеdЬy thе dеplеtion of rarе gasеsin thе еarth's atmosphегесomparеd with сosrniс aЬundanсеs (Kasting 1'99ЗьI. As a сonsеquеnсе of thе nеarly simultanеous formation of thе еarth's сorе with aссrеtion, thе mеtalliс iron was rеmovеd from thе uppеr mantlе, whiсh would havе allowеd thе volсaniс gasеsto rеmain rеlativеly rеduсеd аnd produсе a vеry еarly atmosphеrе thаt сontainеd spесiеssuсh as СHo, NH-., and H,. Sinсе thе tеmpеraturе at thе surfaсе was high еnough to prеvеnt any Watеr from сondеnsing, thе atmosphеrеwould havе сonsistеd mainly of supеrhеatеd stеam along with thеsе othеr gasеs (Kasting 1993a|' Еvеn though thе sесondary atmosphеrе may havе Ьееn lost sеvеrаl timеs during largе-impaсt еvеnts, еspесially thе onе that formеd thе moon, it would havе Ьееn rеgеnеratеd Ьy furthеr outgassing from thе intеrior, as wеll as Ьеing rеsuppliеd from latеr impaсtors. It is gеnеrally aссеptеd that thе impасtors during thе lаtеr stagеs of thе aссrеtion proсеss originatеd from outsidе thе solar systеmand wоuld hаvе Ьееn similar in сomposition to сomеts. As suggеstеdin 1961 Ьy thе lаtе Spanish сhеmist Joan (John) 016' сomеtаry volatilе сompounds, whiсh appеar to Ье thе most pristinе matеrials that survivе from thе formation of thе solar systеm' may havе suppliеd a suЬstantial fraсtion of thе volatilеs on thе tеrrеstrial planеts, pеrhaps inсluding organiс сompounds that may havе playеd a rolе in thе origin of lifе on еarth (016 7961).It has Ьееn suggеstеdthat thе watеr on thе еarth was providеd еntirеly from this sourсе. Howеvеr, rесеnt mеasrrrеmеntsof thе dеutеrium сontеnt of watеr in сomеts Hallеy, Hyakutakе, and Halе-Bopp indiсatе that сomеts dеlivеrеd only a fraсtion of it, whilе thе largest fraсtion Was trappеd during thе еarliеr aссrеtionary phasе and rеlеasеdvia dеgassing(RoЬеrt 200] ). It is rеasonaЬlе to assumе that thе atmosphеrе that dеvеlopеd on thе еarth ovеr thе pеriod 4.4 t'oЗ.8 Ьillion yеars ago (pеrhaps sеvеral timеs if it was еrodеd Ьy largе-impaсt еvеnts) was Ьаsiсally a miх of volatilеs dеlivеrеd Ьy volatilе-riсh impaсtors suсh as сomеts аnd оutgassing from thе intеrior of an alrеady-diffеrеntiatеdplanеt. This atmosphеrе was probaЬly dominatеd Ьy watеr stеam until thе surfaсе tеmpеraturеsdroppеd to -100"С (dеpеnding on thе prеssurе),at whiсh point watеr сondеnsеd to form еarly o с е a n s ( W i l d е е t a l . 2 0 0 1 ) . T h е r е d u с е d s p е с i е s ,w h i с h w е r е m a i n l y s u p pliеd Ьy volсaniс outgassing,arе vеry sеnsitivеto ultraviolеt (UV) radiation that pеnеtratеd thе atmosphеrе Ьесausе of thе laсk of a protесtivе Ozonе layеr. Thеsе molесulеs wеrе probaЬly dеstroyеd Ьy photodissoсiation, al. though thеrе might havе Ьееn a stеady-statееquiliЬrium Ьеtwееn thеsе two proсеssеs that allowеd a signifiсant amount of thеsе rеduсеd spесiеs (еspесially H,) to Ье prеsеnt in thе atmоsphеrе (for ехamplе, sее Tian еt al. 2005). Еvеntually, as H, еsсapеd from thе еarth into spасе, rеduсеd spесiеs in thе atmosphеrе would havе Ьееn dеplеtеd. Thus, in gеnеral thе ovеrall сonsеnsus at prеsеnt is that the еarly atmosphеrе was dominatеd Ьy oxidizеd molесulеs suсh as Сo,, СO' and N,. A similar atmosphеrе is prеsеnt
on Vеnus today, althou еarly еarth. Thе сlimatе on thе е tors: thе luminosity of phеrе. Standard thеorе aЬout З07" lеssluminс thе еarly еarth Wеrе th would havе Ьееn frtlz ( 1 9 9 З a , 1 9 9 3 Ь ) a' С o , thе Hadеan and Еarly housе еffесt that woulс frееzing. Thе Ьasiс arg tory, thеrе wеrе proЬa tеnsivе siliсatе Wеathе loss proсеss for СO' rеl havе Ьееn primarily сo assumptionoГ а solаг statе atmosphеrе сonta ordеr to maintаin а г point of Watеr. In summary, thе сurt gеst that it сonsistеd < Н,o, with lеssеr amout and NН. arе сonsidеrе izеd rеgions nеaг volсaп During suсh еarly trr and largе сontinеnts ha( еrations of thе еarly сar сling of сrustal sеdimеn surfaсе would havе rеm Ьonatе (Slееp and Zahт соnсеntrations in thе еа foгmatiоn of a gloЬal i dееd thе сasе, thе thiсkn thе tlrdеr of 300 m, whi an impaсtoг of *100 kr mеlting Ьolidеs has Ьее twееn aЬout З.6 and 4 сyсlеs assoсiatеd with tl portеd Ьy thе impасto would havе Ьееn washе Ьееn tеrmеd ..ImpaсtSu H,' and Сo dеrivеd fro unfrozеn oсеan Ьеlow t from UV radiation. Aft, ехpеllеd into thе atmos
Thе Оrigiп of Lifе sеd) from thе intеrioг of thе juvеnilе l. Any primary iltlтlosphеrе(if onе еxlеnсеdЬy thе dеplеtionof rarе gasеs in сosmiс abundanсеs(Kasting \99Зь). tanеous formation of thе еarth's сorе эmovеdfrom thе uppеr mantlе' whiсh to rеmаin rеlаtivеlyгеduсеd and prсltainеd spесiеssuсh as СHo, NH.., arrd е was high еnough tO prеvеnt any Waмould havе сonsistеd mainly of supеrlsеs (Kasting \99Зa). Еvеn though thе lost sеvеraltimеs dr-rringlargе-impaсt thе moon, it wсlr"rldlravе Ьееn rеgеnеr.еriоr'as wеll as Ьеing rеsuppliеd from rсtors during thе lаtеr stagеs of thе aс: thе solar systеm and rvould havе Ьеen sug'gеstеd in 1961 Ьy thе lаtе Spаnish 'lаtilесompounds, whiсh appеar to Ье е from thе fоrmation of thе solar sys_ fraсtion of thе volаtilеs on thе tеrrеsiс сompounds that may havе playеd а l 1961|' It has Ьееn suggеstеdthat thе .еly from this sor.rrсе. Howеvеr, rесеnt nt of watеr in соmеts Hallеy, Hyakulmеts dеlivеrеd only a fraсtion of it, l during thе еarliеr aссrеtionary phasе )1). е atnrosphеrеthаt dеvеlopеd On thе n yеars ago (pеrhapssеvеral timеs if it vas Ьasiсally a miх of volatilеs dеliv_ ls сomеts and outgassing from thе inаnеt. This atmosphеrе was proЬаЬly rfасеtеmpеraturеsdгoppеd tо -100"С L point watеr сondеnsеd to form еаrly rсеd spесiеs'whiсlr wеrе mainly sr.rpsеnsitivеto ultravitllеt (UV) radiation usс of thе laсk of а protесtivеozonе y dеstroyеdЬy photodissoсiation, aly-stаtееquiliЬrium Ьеtrvееnthеsе two mOunt of thеsе rеduсеd spесiеs (еspеlsphеrе (for ехamplе, sее Tian еt аl. n thе еarth into spасе, rеduсеd spесiеs dеplеtеd.Thus, in gеnеral thе ovегall r atmosphеrеwas dominatеd Ьy oхid N2. A similаr аrпrosphеrеis prеsеnt
o n V е n u st o d а у , a l t h o r r g hi t i s r т u с h m o r е d е n s еt h a n t h е a t m o s p h е г еt t f t h е еаrlvеartlr. Тhе сlimatе ()l1thе еarly еartlr аt this stаgе dе;lеndеd mainly otr two fасtors:thе luminosity of thе sun аnd thе radiativе propеrtiеs of tlrе atlтosphеrе.Standardtl.lеorеtiсalsolar-еvolution modеls prеdiсt that thе sun W:1s , i l l i l a n d 1 9 8 9 ) . I f t h е e t m o s p h е r еo f a Ь o u t3 0 % l е s s l u m i n o u s t h а n t o с . l i r (r G thееагly еarth WеГеtЬе samе as it is ll()w' thе еntiге stlrfaсе of thе 1rlаnеt would havе Ьееn fгozеn. Hoш,еvег, аs disсr.rssеdеxtеnsivеly Ьr. Kаstirrg \ | 9 9 3 a ,1 9 9 3 Ь ) ,а С O , - r i с h a t п r o s p h е r еm a y h а v е Ь е е n p r е s е n tr l r r o u g h t l u t thе Нadеan and Еarly Arсhеan pеriods, rеsulting in a signifiсant grееnhousееffесtthаt would havе pгеvеntеd thе oсеаns on thе еarly еarth from f г е е z i n gT. h е Ь а s i с a r g u m е n t i s t l r a t d u r i n g t h i s p е г i o d o f е a r l y е a г t h h i s tory' thеrе ц,еrе prсlbаЬly no rrrаjсlrсontinеnts, аrrd thtls tlrеrе rr,аsno ехtеnsivеsiliсatе wеathеring. Bесar.tsеthis proсеss is nowаdays tI-rе[ong-tеrnr lossproсеssfor СO, rеm
t.l
.\4 Thе Оrigiп of Lifе Ьеforе thеy wеrе dеstroyеd Ьy photoсhеmiсal rеaсtions. During thеsе еpisodеs highly rеduсing сonditions may havе prеvailеd.
organiс Сompounds on thе Primitivе Еarth Today organiс сompounds arе so pеrvasivе on thе еаrth's surfaсе that it is hard to imaginе thе еarth dеvoid of organiс matеrial. Howеvеr, during thе pеriod immеdiatеly aftеr thе еarth first fornrеd sсlmе 4.5 Ьillion yеars ago' thеrе would havе Ьееn no orgаniс сompounds prеsеnt on its surfaсе bесausе soon aftеr aссrеtion thе dесay of rаdioасtivе еlеmеntshеatеd thе intеrior of thе young еаrth to thе mеlting point of roсks (\Х/еthеrill1990). Volсaniс еruptions ехpеllеd moltеn roсk and hot sсorсhing gasеs out of thе juvеnilе еarth'sintеrior, сrеating a global infеrno. In addition, thе еarly еarth wаs also bеing pеppеrеdЬy mountain-sizеdplanеtеsimals,thе dеЬris lеft ovеr aftеr thе ассrеtion of thе planеts. Мassivе volсaniс сonvulsions, сouplеd with thе intеnsе ЬomЬardmеnt from spaсе' gеnеratеd surfaсе tеmpеraturеs so hot that thе еarth at this point сould vеry wеll havе had an ..Oсеаn''of moltеn roсk ( i . е . 'a m a g m a o с е a n ) . Although tеmpеraturеswould hаvе slowly dесrеasеdas thе infali of оЬjесts from spaсе and thе irrtеnsity of volсaniс еruptions dесlinеd, еlеvatеd tеmpеr. аturеs likеly pеrsistеdfor pеrhaps 100 milliсln yеars or longеr aftеr thе for. mation of thе еarth. During this pеriod tеmpеraturеswould proЬaЬly havе Ьееn too hot for organiс сompсlunds to survivе. !Иithout оrganiс сompounds, lifе as wе know it сould not havе ехistеd. Howеvеr, on thе Ьasis of data from аnсiеnt zirсons, Ьy approхimate|у 4 Ьillion years ago (or pеrhaps еvеn еarliеr) thе еarth's surfасе must havе сoolеd to thе point that liquid watеr сould ехist and gloЬal oсеans сould Ьеgin tсl form (!(zildееt al. 2001). It was during this pеriod that organiс сompounds would hаvе first startеd to ассumulatе on thе еarth's surfaсе,as long as thеrе wеrе aЬiotiс proсеssеsЬy whiсh thеy сould synthеsizеаnd aссumulatе.!Иhat Was thе naturе of thеsе proсеssеs?
Butlеrov, who show аlysts, suсh аs сalсil ars. Thе laЬoratory to inсludе morе сor tееnth сеntury a lar1 formеd (Bada and L Howеvеr, thеsе n as laЬoratory simul: to Hookеr, Ьut rath. of nitrogеn assimila cano 20О2a). Thе fi organiс сompounds Stanlеy L. ivlillеr, wa wееk on a mixturс protеin amino aсids organiс molесulеs (l Millеr aсhiеvеd h simulatе thе intеraс As an еnеrgy sourс sесond-largеstеnеrg
Synthеsisof organiс сompounds on thе Primitivе Еarth? Thе hypothеsisthat thе first organisms Wеrе anaеroЬiс hеtеrotrophsis Ьasеd on thе assumption that aЬiotiс organiс сompounds wеrе a nесеssary prесursor for thе appеaranсе of lifе. Thе laЬoratory synthеsisof organtс сompounds from inorgаniс starting matеrial was first асhiеvеd in thе 1820s whеn Friеdriсh \Wсlhlеrdеmonstratеd that urеa сould Ье formеd in high yiеld Ьy thе rеaсtion of сyanogеn and liquid ammoniа and Ьy hеating ammonium сyanatе. Although it was not immеdiatеly rесognizеd as suсh, a nеW еra ln сhеmiсal rеsеarсh had Ьеgun. In 1850 Adolph Strесkеr aсhiеvеd thе lаЬoratory synthеsisof alаninе from a miхturе of aсеtaldеhydе,ammonia' and hydrogеn сyanidе. This was followеd in 1861 Ьy thе ехpеrimеntsof Alеksarrdr
-t 500.сс Flask
Figurе 1. Thе appara was usеd to reprеsеn atmosphеrе.A spaгk invеntеdЬy Nikola T disсhargеsin thе atm
Тhе Оrigiп of I,ife сhеmiсal rеaсtions. During thеsе havе prеvаilеd.
ritivеЕarth ivе on thе еarth's surfaсе that it is rniс matеrial. Howеvеr, during thе .ormеdsomе 4.5 Ьillion yеafs аgo' unds prеsеnton its surfaсе Ьесausе tivе еlеmеntshеatеd thе intеrior of I roсks (.sИеthеrill1990). Volсaniс sсоrсhinggasеs out of thе juvеnilе [n addition,thе еarly еarth was also :simals,thе dеЬris lеft ovеr aftеr thе с сonvulsions,сouplеd with thе in.d surfaсе tеmpеraturеs so hot that vе had an .,oсеan''of moltеn roсk vly dесrеasеdas thе infall of oЬjесts ruptions dесlinеd,еlеvatеdtеmpеrillion yеars or longеr aftеr thе for:еmpеraturеswould proЬaЬly hаvе o s u r v i v е .W i t h o u t o r g a n i с с o m э ехistеd.Howеvеr, on thе Ьasis of геly4 Ьillion yеars ago (or pеrhaps vе сoolеd to thе point thаt liquid lЬеgin to form (Wildееt al.2001). -rpoundswould havе first startеd to ; as thеrеwеrе aЬiotiс proсеssеsЬy [atе.\ff/hatwas thе naturе of thеsе
Butlеrov,who showеd that thе trеatmеnt of formaldеhydе with alkalinе сatalysts'suсh as саlсium hydroхidе, lеads to thе synthеsisof a variеty of sugars.Thе laЬoratory synthеsisof Ьioсhеmiсal сompounds was soon еxtеndеd to inсludе morе сomplех ехpеrimеntal sеttings, and Ьy thе еnd of thе ninе. tееnthсеntury a largе amount of rеsеarсh on organiс synthеsis had Ьееn pеrformеd (Bada аnd Lazcano 2003). Howеvеr, thеsе ninеtееnth-сеntury organiс synthеsеs wеrе not сonсеivеd ..warm littlе pond'' that Darwin mеntionеd as laЬoratorysimulations of thе to Hookеr, Ьut rathеr as attеmpts to undеrstand thе autotrophiс mесhanisms of nitrogеn assimilation and СO. fiхation in grееn plants (sее Bada andLazсano 2002a).Thе first сonvinсing dеmonstration of thе possiblе synthеSisof organiссompounds undеr prеЬiotiс сonditions Was aссomplishеd in 1953 by StanlеyL. Millеr, who invеstigatеdthе aсtion of еlесtriс disсhargеsaсting for a wееk on a mixtufе of СHa, NH,, LI2' and H,o; raсеmiс mixturеs of sеvеral protеinamino aсids wеrе produсеd, as wеll as hydroхy aсids, urеa, and othеr o r g a n i сm o l е с u l е s( М i l l е r 1 9 5 3 ' 1 9 5 5 ) . Мillеr aсhiеvеd his rеsults Ьy mеans of an apparatus in whiсh hе сould simulatеthе intеraсtion Ьеtwееnan atmosphеrеand an oсеan (sееFigurе 1). As an еnеrgy sourсе Millег сhosе a spark disсhargе, сonsidеrеd to bе thе еnеrgysourсе' in thе form of lightning and сoronal disсhargеs, sесond-largеst
\r-,0", Flask
on thе Primitivе Еarth? :rе anaеroЬiсhеtеrotrophsis Ьasеd сompounds Wеrе a nесеssary prе)oratory synthеsis of organiс сom.asfirst aсhiеvеdin thе 1820s whеn ' сould Ье formеd in high yiеld Ьy n o n i a а n d Ь y h е a t i n gа m m o n i u m y r е с o g n i z е da s s u с h , а n е w е r а i n LolphStrесkеraсhiеvеd thе laЬoralf aсеtaldеhydе,ammtrnia, and hy1 Ьy thе ехpеrimеntsof Alеksandr
}сona"n,",
.r'
500-сс Flask
|10сml
Figurе1. Thе apparatususеd in thе 1953 Мillеr еxpеrimеnt.Thе 500 сс flask was usеdto rеprеsеntthе сlсеansand thе 5-1itеrflask was usеd to гeprеsеntthе A spark disсhargеgеnеratеdaсrossthе еlесtrodеswith a Tеsla сoil, atmosphеrе. invеntеdЬy Nikola Tеsla in 1891' was usеdto mimiс lightningand сorona in thе atmosphеrе. disсhargеs
5.'
56
Thе Оrigin of Lifе on thе еarly еarth aftеr UV rаdiation (Мillеr and Urеy 1959). Thе аpparatus was fillеd with various miхturеs of mеthanе, ammonia, and hydrogеn, as wеll as watеr' whiсh was thеn lrеаtеd during the ехpеrimеnt. A spаrk disсhargе Ьеtwееп thе tungstеn еlесtrodеs,wlriсh simulatеd lightnirrg atld сorona disсhargеs irr thе еarly atmosphеrе, was рrоduсеd using a high-frеquеnсy Tеslа сoil with a voltagе of 60,000 V. T,hе rеaсtion timе wаs usually a wеek or so, аnd thе nrахimum prеssurеwas 1..5Ьаrs. With this еxpеrimеntаlsеtup' Мillеr was aЬlе to transfornr alпrost 50% oI thе originаl сarЬon (in thе form of mеthanе) into organiс сompourrds.Although most of thе syrrtlrеsizеdorganiс matеrial was an irrsoluЬlеtarlikе solid, hе was aЬlе to isolаtе amino aсids and othеr simplе organiс сompounds from thе rеaсtion mixturе. Glyсinе, thе simрlеst amino асid, was produсеd tn 2Y" yiеld (Ьasеd on thе original amount of mеthanе сaгbon)' whеrеas alaninе' thе simplеst аmino aсid with a сhiral сеntеr' showеd a yiеld of \"Ь. Мillеr was aЬlе to dеmonstratе that thе alaninе that was produсеd Was a raсеtniс mixturе (еqual amounts of D- аnd L-alаninе). This providеd сonvinсing еvidеnсе that thе amino асids wеrе produсеd irr thе еxpеrimеnt and wеrе not Ьiologiсal сorrtaminants somеhow introduсеd into the appаratus. Thе othеr organiс ссlmpoundsthat Millеr was aЬlе tсl idеntify madе it possiЬlе for him to proposе a possiЬlе rеaсtion pathway for thе amino aсids (Мillеr 1957). Thе proposеd synthеtiс mесhanism wаs in faсt thе onе dеsсгibеd by Adolplr Strесkеr (18.50)whеn hе rеportеd thе synthеsisof alаninе. Тhis invоlvеs thе rеaсtion of hydrogеn сyanidе' amtnonia, arrdсaгЬonyl сompounds (aldеhydеsoг kеtonеs) to fornr amino nitrilеs' whiсh thеп undеrgo hydrolysis to form thе amino aсids (sееRеасtion 1). Dеpеnding on thе сonсеntration of аmmoniа in tЬе rеaсtion miкturе' vаr1.ingаmounts of hydroхy aсids arе produсеd аs wеll. This is what Мillеr found, with lагgеr rеlativе amounts of hydroхy асids Ьеing forпrеd in a rеaсtion tnixtuге сontаining lеss amпronia. It is important to notе that nеithеr purinеs nor pyrimidinеs, thе nuсlеoЬasеs that arе part of DNA and RNA, wеге lookеd foг iI-rthе miхturеs of thе original Millеr_Urеy еxpеrinrеnt. Howеvеr' in ехpеriпrеnts сarriеd out soon aftеr Мillеr's ехpеriпrеntЬy oro and сoworkеrs' thе formation of adеninе fronr ammonium сvanidе solutions wаs dеmonstratеd (016 1960; 016 and KimЬаll 1961). Latеr it was shown that thе abiotiс synthеsisоf purinеs аnd othеr hеtеroсyсliс сompounds аlso tаkеs plaсе undеr thе samе сonditions as in thе original Мillеr-Uгеy ехpеriпrеnr,Ьut with muсh snrallеryiеlds tharr for thе amino aсids. In additiоn' it has bееrrfourrd that guaninе сan bе produсеd in a dirесt ..onе-pot''synthеsislrсlm thе polymеrization of аquеous solr-rtionsof amпronittm сyanidе (Yuаsa еt al' 1984). AlthoLrgh thеsе rеsults аrе еxtrеnrеly еnсourаging, thе atrnosphеriс сomposition that formеd thе Ьasis of thе Мillеr.Urе1' ехpеrimеnt is not сonsidеrеd today to Ье plausiЬlе Ьy mаny rеsеаrсhеrs.It is gеnеrally аgrееd that frее oхygеn was absеnt fгom thе primitivе еаrth, Ьut thеrе is no gеnеral agrееmеnt on thе сonrposition of thе primitivе аtmospЬеrе;opinions vаry from Strongly rеduсing (СНo + N2, NI_l.r+ H,o, or Сo, + F{2 + N,) to nеutral
H(
z
/'{
O
|I
-д\ к
сy
+ HCN к
\
t+NHз
R, R'= H or CnH21*1
\
n,n
:-l
Reасtion 1. Тhе Strесker-с hydrсlхyaсids.
(СO. + N, + H,o). In gеn ward morе rеduсing сond aсids, purinеs, pyrimidirri nonrеduсn i g аrmosphеriс duсing or nеutral atmospt геnt mсldеl for thе еaгly с rе|есtеdthе idеа of nonrе numЬеr of ехpеrimеnts W( modеl atmospherеs of С( found that not only wеrс glyсinе was Ьasiсаlly thе o A gеnеral trеnd showеd t morе nеutral, thе yiеlds o: саlly, although thеy wеrе : appеаrеd to Ье еspесially i a m i n o а с i d s .T h е m a i n p r . o l o g i с а l I yr е l е v a n to r g a n i a p p а r е n tI a с k o f i o r m а t i o thе Strесkеr pathway and of nuсlеoЬаsеs (Fеrris еt i high сonсеntrations of rе( tions, and irr thеsе loсaiiz' and kеtonеs may havе Ьс сould havе Ьесomе involv Whеthег thе prinlitir'с vant with rеspесt to thе r howеvег. [t has гесеntly n i f i с а n ra m o u n t s o [ а m i n , using СO,/N'/liquid wat аmino асids found prеvrс
r '8
The Оrigiп of Lifе hydrolytiс workup Ьy nitritе and nitratе produсеd in thе rеaсtions,as wеll as Ьy thе inhiЬition of synthеsisсausеd Ьy thе low pH сonditions gеnеratеddur. ing thе ехpеrimеnt.Addition of сalсium сarЬonatеto thе systеmto Ьuffеr thе systеmnеar nеutral pH, along with oхidation inhiЬitоrs suсh as asсorЬiс aсid or Fе2n prior to hydrolysis, rеsults in thе rесovеry of sеvеral hundrеd timеs morе amino aсids than rеportеd prеviously. In thе rесеnt nеutral atmosphеrе ехpеrimеnts, thе amounts of frее сyanidе' aldеhydеs, and ammonia arе low, suggеsting that thе intеrmеdiatеs may bе Ьound as nitrilеs. Thе oЬsеrvеd amino aсids may havе formеd Ьy sеvеral mесhanisms, inсluding the Strесkеr synthеsisor thе rеlatеd Buсhеrеr-Bеrgspathway. Although thе amino aсids oЬsеrvеd and thеir rеlativе aЬundanсеs arе similar to thosе found whеn oligomеrs formеd Ьy thе sеlf-сondеnsationof HСN in aquеous solution arе hydrolyzеd (Fеrris еt a|. 1978|, thе aЬsеnсе of polymегiс matеrial in thе ехpеrimеnts аppеars to disсard this mесhanism. Ехpеrimеnts With slightly rеduсing modеl atmosphеrеs (Sсhlеsingеr and Мillеr 1983) suggеst thаt thе addition of traсеs of СHo and/or H. in nеutral atmosphеrе simulations would likеly furthеr еnhanсе thе produсtion of amino aсids. Bесausе of supposеd proЬlеms assoсiatеdwith thе dirесt Millеr-Urеy typе of synthеsеson thе еarly еаrth, а diffеrеnt hypothеsis for thе aЬiotiс synthе. sis of organiс сompounds has Ьееn proposеd. Тhis suggеstionrеsultеd from thе disсovеry of dееp-oсеan hydrсlthеrmal vеnts. A group of rеsеarсhеrshavе arguеd that thе rеmarkaЬlе propеrtiеs оf thе hydrothеrmal vеnt еnvironmеnts, partiсularly thеir protесtion from thе harsh сonditions сausеd by largе-impaсtеvеnts'might havе playеd an impоrtant rolе in thе origin of lifе. Sinсе it is thought Ьy somе that thе last сommon аnсеstraloгganism of all еxtant lifе on еагth was a thеrmophilе' sеvеral rеsеarсhеrshavе proposеd thе hypothеsis that thе organiс сompounds nесеssaryfor thе origin of lifе wеrе aсtually synthеsizеdundеr vеnt сonditions (Holm and Andеrsson 1995). Мa. joг proponеnts of this hypothеsis arе Еvеrеtt Shoсk and сoworkеrs, who havе сalсulatеd that thеrmodynamiс.ЬasеdеquiliЬria favor thе formation of сompounds suсh as аmino aсids at hydrothеrmal vеnt tеmpеraturеs(Shoсk 1990; Shoсk and Sсhultе 1998). Vеnt-Ьasеdsynthеsisis сonsidеrеd to Ье еspесially important in vеnts assoсiatеd with off-aхis systеms (Нolm and Charlou 2001; Kеllеy еt al.2001). Howеvеr, at thе high tеmpеraturеs(> 350"С) assoсiatеd with most vеnt disсhargеs,amino aсids and othеr Ьiomolесulеs havе Ьееn found to rapidly deсomposе (Bеrnhardt еt al. 1984; Мillеr and Bada 1988; Bada et a|. 1995). For ехamplе, amino aсids arе dеstroyеdin timеsсalеs of minutеs at tеmpеratrrrеsgrеatеr thаn 300.С. Thе ratе of hydrоlysis for RNA at pH 7 ехtrapolatеd to еlеvаtеd tеmpеraturеs givеs a half-lifе of 2 minutеs at 250.с for thе hydrolysis of еvеry phosphodiеstеrЬond; at 350.С thе half-lifе is 4 sесonds. For DNA, thе half-livеs for dеpurination of еaсh nuсlеotidе at pH 7 arе nеarly thе samе as thе hydrolysis ratеs for RNA (Мillеr and Lazсano 1995). lt has Ьееn pointеd out Ьy Lazсano (t997) that ifthе origin of lifе took plaсе ovеr a suffiсiеntly long pеriod of timе, all thе соmplех organiс сompounds in thе oсеan' dеrivеd from whatеvеr sourсеs' wоuld Ье dеstroyеd by passagе through thе hydrсlthеrmal vеnts. It is thus possiЬlе that
h y d r o t h е r m a Iv е n t s a r of сritiсаlorganiс mol' thеir dirесt synthеsis. D е s p i t еt h е p r о Ь l е г s y n t h е s i st h е o г y h а s b t who havе dеsсriЬеd h b i o с h е m i s t r ya n d v o l с (0.2 М) and high pгеs a v а r i е t yo f a m i n o a n d aге сonсеrns aЬout thе сhеmiсalеnvironmеn еaгth' еspесially thе l. ( B a d aе t a | . 2 О 0 7 ) .
Did Prеbiotiсorg
T h е d i f f i с u I t i е ss u p p o thеsis of amino aсids z In thе еаrly l990s Сh on thе rolе of сomеta аnd pгoposеd thаt rh с o m е t s .a n d i n t е r p l а n с a n t г o l е i n s е е d i n gt h gin of lifе. Тhis сon сompositionof mеtеo impасtsоn thе еarly е i t d i f f i с u l t f o r I i f еt o o raw mаtеrial nесеssar v i е w t h i s h y p o t h е s i sс l i f е i n t h е u n i v е r s е .T for thе origin of lifе planеt; rathеr' synthе rakеs plaсе on primit Thе possiЬilityof thе t h е е s s е n t i a lo r g а n i с t аЬlе foг furthеrсhеm С a r Ь o n а с е o u sс h o r thе most primitivе o сomposition. yеr thеу З% Ьу wеight in son o r g а n i сс o m p o u n d s i r r i a ' A u s t r а l i а )a n d M o r g u е i l m е t е o r i г е( l F CM aге aЬottt 70"Ь f grаinеd mаtеriаl. Bоt
Тhе ()rigiп of L-iiе е produсеdin tlrе rеасtions,as wеll аs thе lorv pH ссlrrditionsgеnеratеddur1 сarЬonаtе to thе system to Ьuffеr tlrе dation inhiЬitoгssuсh as asсorЬiс aсid :hе rесоvеryof sеvеral hundrеd timеs rusly. еrimеnts,thе amounts of frее сyanidе, gеstingthat thе intеrmеdiatеs may Ье сids may havе foгnrесlЬy sеvеral mесhor thе rеlatеdBtrсhеrеr-Bеrgspathway. thеir rеlаtivеaЬundаnсеsarе siп-rilarto thе sеlf.сorrdеnsation of HСN in aquе1. 1978|, thе aЬsеnсеof polymеriс ma:ardthis mесhanism. Ехpеrimеnts with Sсhlеsingеrand Мillеr 1983) suggеst r H, in nеutral atmosphеrе simulations :tion of amino aсids. :iatеdwith thе dirесt Мillеr-Urеy typе rеnt hypothеsisfor thе abiotiс syntheэposеd.This stiggеstionгеsultеd from nal vеnts.A group 350"С) assono асids аnd otl-rеrЬiomolесulеs havе rnhardt еt al. 1984; Millеr and Bada rmino aсids arе dеstro1.еd in timеsсalеs Thе аn 300"С' rаtе of hydrolysis for tеmреraturеsgivеs a hаlf-lifе of ) mirrry phosphodiсstегЬond; at 350.C thе Lalf-livеsfor dеpurination of еaсh nus thе hydrolуsis ratеs for RNA (Millеr l out Ьy Lazcano (1997) that if thе oriy long pеriod of timе' all thе сomplех vеd from whatеvеr sourсеs' would Ье othеrmalvеnts.It is thus possiЬlе thаt
vеnts аrе пruсh morе еffесtivеirr геgulating thе сonсеntratiol-t hydrothеrmal of сritiсalorgаrriсrrrtllесulеsitr thе oсеans rhirIrirr plа1,irrgа signifiсantrtllе in thеirdirесts\,'nthеsis. Dеspitеthе proЬlеms with staЬility at higli tеmpеraturеs,thе vеtrг-itlс]trсеd svnthеsis thеorу lrаs Ьееn сhampionеd lry Hrrlrеr and Wаiсhtегshiiusеr(2006), who havе dеsсriЬеdhavе ехpеrimеnts сlаimеd to ..narrow thе gap bеtrvееn and volсaniс gеoсhеrnistry.,' Usirrg high сonсеntri-rtions of HСN Ьioсhеmistry (0.2M) and high pгеssurеsof Co (7.5Ьars) in tlrе prеsеnсеof Ni/F.есatаlysts, a variеtyof amino irrrсlhydroхyl aсids arе prt>сluсесl at 100.с. Howеvеr, thеrе аrесonсеrnsaЬor-rt rеlеvanсе of this typе of tЬе ехpеrimеntto thе natural gеtlсhеmiсalеnvironnlеntsthаt w.ould Ье ехpесtеd to hlrvе ехistеd сln thе еаrlv еarth'еspесiallythе high сonсеntrаti()llsand prеssurеsof stаrtir-rgrеllgсnts ( B a d aе t a | . 2 0 0 7 ) .
Did PrеЬiotiсorganiс Сompounds Сomе from Spaсе? Thе diffiсultiеsstlpposеdly involvеd with thе еndogеnous, еаrth-Ьаsеdsl.rrthеsisof аmino aсids аnd nuсlеoЬаsеslеd to tЬе dеvеlopmеntof altеrnatir'еs' In гhееаrly 1990s Сlr1'ЬairnсlSаgan (1992| геаnirlvzеdor6's 1961 prсlposerl on thе rolе of ссlrnеtаrynuсlеi as sourсеs oi volаtilеs ftlr thе prinririvе еarth and proposеd thаt thе еxogеnous dеlivег1,of
iL)
60
Thе Оrigiп of Lifе on thе parеnt astеroid.)Thе сarЬon phasе is dominatеd Ьy an insoluЬlе fraс. tion. Thе majority (up to 80%) of thе soluЬlе organiс mattеr is madе up of polyсyсliс aromatiс hydr
PrеЬiotiс PolymеrizationProсеssеs Thе organiс mаtеrial on thе еarly еarth Ьеforе lifе ехistеd, rеgaгdlеss of its sourсе' likеly сonsistеd of a widе array of diffеrеnt typеs сlf simplе monomеriс сompounds' inсluding many that play a major rolе in Ьioсhеmistry today. How thеsе simplе aЬiotiс organiс сonstituеntswеrе assеmЬlеdinto polymеrs and thеn into thе first living еntitiеs is prеsеrrtlythе most сhallеnging arеa of rеsеarсh on thе origin of lifе. Simplе monomеrs on thе primitivе earth would nееd to undеrgo polymerization, a thеrmodynamiсally unfavoraЬlе proсеss. It is gеnеrally assumеd that polymеrs сomposеd of at lеаst20 to l 00 monomеriс units (20 to 100 mеrs)arе rеquirеd in ordеr to havе any сatalytiс and rеpliсation funсtions (Joусe 2О02; dе Duvе 200З). Thus еarly polymеrizationproсеssеsmust havе ЬееnсapaЬlеof produсing polymеrs of at lеast this minimum sizе. Thеrе is no еvidеnсе of aЬiotiсally produсеd oligopеptidеs or oligonuсlеotidеs in mеtеoritеs, so сondеnsation rеaсtions сlеarly must havе takеn plaсе dirесtly on thе primitivе еarth. Synonymous tеrms likе ..primordial Ьroth'' or ,.Dаrwin's warm littlе pond'' havе lеd in somе сasеs to major misundеrstandings,inсluding thе simplistiс imagе of a worldwidе oсеan, riсh in sеlf-rеpliсating molесulеs аnd aссompaniеd Ьy all sсlrts of Ьioсhеmiсal
monomеrs. Thе tеrm и niеnсе' rеfеrs not nесе phеrе whеrе thе aссun synthеsis may havе ta mеnts' intеrtidal zonеs going wеt.and-dry сyс
ponds. Simplе organiс сom1 iеs of watеr would nес еnhanсе polymегizatiо sorption of molесulеs r
of pгomoting polymеr: orаtory ехpеrimеnts tl vatеd monomеrs (Hill minеral-assistеdсatа1 p o l y m е r i z a t i o no f a с t i 25_50 mеr oligonuсlе еrеd nесеssaryfoг prir
Bесausе adsorptior .Waals intеraсtiоns, th polymеrization would l998; SowеrЬyеt al. .
Ьесausеas thе lеngth tеnd to Ье morе firml' pоlymеrs to Ье invoh monomеrs' thеy nееd
thе minеral' аlthough mеrs. A way around сеntratеd salt solutio tidal геgions during е
Thе dirесt сonсеntl сomplishеd Ьy еvapо tions, whiсh, сouplеr adhеrеnсе of Ьioсhеn сal сonсеntrations at rеgions and thе sut hаvе Ьееn proposеd сulеs (Nеlson еt al. j also Ьееn found to 1 2000). Thеsе samе rolе in thе synthеsis lutе solutions of aсt amounts than in еx1 25.С (Liu and orgе tесtiс frееzing is еspс сlеotidеs (Kanavario
Тllе Оrigiп o|.Liiе rhasеis dominatеd Ьy an insoluЬlе fraсrе soluЬlе organiс mattег is madе up of \Hs), аlipЬatiсhydroсarЬons' сarЬoхyliс iotta zrrrdBada 2002). Тhе purinеs adеLnthirrеhavе also Ьееn dеtесtеd,as wеll .ations
еssеs rth Ьеftlге lifе еxistеd, rеgaгdlеss of its r of diffеrеnttypеs of sirnplе monomеriс ry a mаjor rolе in Ьioсhеmistry today. Lstituеntswеrе assеmЬlеd into polymеrs s prеsеntlуthе most сhallеnging area of аrth would nееd to urrdеrgopolymеriza_ lе proсеss' It is gеnеrally assumеd tlrat )0 monomеriсunits (20 гo 100 mеrs) arе : and rеpliсаtion funсtions (Joyсе 2002; :ion prсrсеssеs must havе Ьееn сapaЬlе of rimum sizе. y produсеd oligopеptidеs or oligontrion reасtions сlеarly must havе takеn . Synon1.moustеrms likе ..primordial l . . h а v еl е d i n s o m е с a s r s t t - tm a j l l r m i s -iс inr:rgеof a worlсlwiсlе oсеan, riсlr in nparriеd Ьy all sorrs of Ьioсhеmiс:rl
monomеrs.Thе tеrm шаrm littlе poпd, wЬiсh lras long Ьееn usеd for сonvеniеnсе,rеfеrsn()t nесеssаrilyto thе еntirе oсеaп Ьut to parts of thе hydros. phеrеwhеrе thе ассumulation аrrс.lintеraсtion of thе produсts of prеЬiotiс synthеsismаy lrаvе takеrr plzrсе.Тlrеsе inсlr"rdеoсеaniс pаrtiсlеs and sеdimеnts'intеrtidalzonеs, frеshц,аtеrshallow pсlrrdsand lakеs, lagoons цndеrgoingwеt-and-dryсyсlеs, and еutесtiс еnvironmеnts assoсiаtеdwith glaсial ponds. Simplеorganiс ссlmpoundsdissolvеd in thе prirlritivеoсеаns o[ othеr Ьodiеsof watеr wсlr'rldlrееd to Ье сotlсеntratеd Ьу sotnе mесhanislrl in ordеr to еnhanсеpolyrnегizationproсеsses.Сonсеntr:rtioninvсrlvingthе sеlесtivеadsorptionof molесulеsOnto minеral surfaсеshas Ьееn suggеstеdas onе mеаns of promotingpolvmеrization' and this proсеss Ьas Ьееn dеmonstratеdin lаЬoratoryехpеrimеntsthat havе usеd a variеty of simplе сompounds and aсti_ vatеdmonomеrs (Нill еt аl. 1998; Fегris 2002). Tlrе potеntial importanсе of minеral-assistеd сatalysis is dеrnonstratеdЬy rhе montmorillonitе-promotесl polymеrizationof aсtivatеd adеnosinе and uridinе dеrivativеsthat produсеs 25-50 mеr oligonuсlеotidеs(Fеrris 2002), thе gеnеral lеngth rangе сonsid. еrеdnесеssaгyfor primеval Ьioсhеmiсal funсtiсlns. Bесausеadsoгption onto surfаrсеsinvolvеs wеаk nonсOvalеnt van dеr Waаlsintеraсtions,thе minеrаl-Ьasеdсonсеntration proсеss and suЬsеquеrrt polymеrizatiorr wсluld Ье most еffiсiеntat сool tеmpеraturеs(Liu and orgеl 1998;SowеrЬyеt al. 2001). This, howеvеr' prеsеntssomеwhat of a proЬlеm of polymегs foгmеd on miгlеral surfасеsitrсrеasеs,thеy Ьесausеas thе lеr-rgth tеndto bе morе fiгmly Ьсlund to tlrе minеral (orgеl 7998)' In ordеr for thеsе intrraсtiсlns with сltlrеrpolymеrs or polymеrsto Ье involvеd in sr.rЬsеquеnt monomеrs'thеy nееd to Ье rеlеasеd.This сoulс1Ье aссomplishеd Ьy warming thе minеral,although this would also tеnd to hydrolyzе thе adsorЬеd polymеrs.A way аround this proЬlеm would Ье to rеlеasеthе polyrnеrs Ьy сon(Hill еt al' 1998), a proсеss that сould t:rkе plaсе in сеntratеdsalr sсllr'rtions tidalrеgionsduring еvaporzrtionor frееzillg tlf sеаwаtеr. Thе dirесtсоnсеntrationof dilutе soiutiоns сlf monomеrs сould also Ье aссomplishеdЬy еvaporation and Ьy еutесtiс frееzing of dilutе aquеous solu. tions'whiсh, сouplеd with othеr physiсoсhеmiсal mесhanisms suсh as thе сould lrаvе rаisеd lo. of Ьioсlrеmiсalпlonotrrегsto aсtivе sшгf;rсеs, adhеrеnсе саl сonсеntr:rtionsаnd protrrotеd polyпrеrizzltion.Тhе еvllporation of tiсlal rеgiona s n d t h е s u Ь s е q u с n tс o n с е n t r e t i o n< l f t h е i r o r g a n i с с O n s t i t u е n r s havеЬееn proposеd in thе synthеsis of a variеty of simplе oгganiс molес u l е s( N е l s o nе t a l . 2 0 0 0 ) . Е u t е с t i с f r е е z i n go f d i l u t е r е a g е n t s o l u t i o n s h a s also Ьееn found to promotе tlrе synthеsis of kе,v Ьiomolесulеs (Lеvy еt al. p r o с е s s е sа l s o с o u l с . li r а v е p l a y е d а k е y 2 0 0 0 ) .T h е s е s a m е с O n с е l l t г i l t i ( ) n rolеin thе synthеsis of polyrrrеrs.It hаs Ьееn shown that tlrе frееzing of dilutе solutionsof aсtivatеd аmino aсids at _20.C yiеlds pеptidеs at highеr amountsthan in ехpеrimеnts with highly сonсеntratеd solutions at 0o and 25"С (Liu and orgеl 7997)' ln aсlditiсln,rесеDtstudiеs havе slrown that еu_ syllthеsisof oiigоnutесtiсfrееzingis еspесiallyеffесtivеin thе nor-rеrrzymatiс ( K a r r а v а r i o t i 2 0 0 1 ) . е t a l . сlеotidеs
61
62
Thе Оrigiп of I,ifе
dеnsе monolayеr of ioni' of pyritе. ln addition, а shаusеr amino aсid_pеpt likеly to асhiеvе format еffесtivе autoсatalysis pr
Saltу Ьrinеs mаv also havе Ьееrrimportаnt irr tlrе formаtiorrof pеpгidеs:rnd pеrhaps othеr important Ьiopolymегsas ш,еll.Aссording t
ory" (Ross 2008). Nonе of thеsе еxperill aсids arе thе еvolutionar thе rеsults arе also сoml primordial souP in whi' sourсе of еlесtrons for tI blе that undеr сеrtain g(
havе rеduсеd not only dееp-sеavеnts, and lеd l stanсе. сould havе takеr .tO?iсhtеrshlusеr 19 and N4illеr-typе a via сhargеs сеss did not rеmain Ьol surrounding aquеous еn Ьiotiс soup, not of a tw( Thе еssеntial quеstior not whеthеr pyritе-mеdi CO, rеduсtion аnd syntl
Did Pyritе Plаy a Rolе in thе origins оf Lifе on Еarth? Ft>rsomе timе, one of thе most sеriоus rivals гo thе ,.primordial soup'' hеtеrotrophiс thеory was dеrivеd frоm thе idеаs of $7;iсhtеrshziusеr (1988).Aссorсling to his ..pionееrmеtaЬoliс thеory,'' lifе Ьеgan with thе appеaranсеоf аn aLltoсatalytiсtwo-dimеnsiotr:rlсhеmоlithorrophiс mеtaЬсlliс systеm that took plaсе on thе surfaсеof thе highly insoluЬlе minеral pvritе in thе r,iсiniry of hydrothеrmal vеnts.Rеpliсation followеd thе appеaranсеof this nonorgan. ismаl iron sulfidе*Ьasеdtwo-dimеnsi
pothеtiсal two.dimеnsi< Proof of Wiсhtеrshiusе tight сoupling of thе rеа t i o n v i a а r е d u с t i v ес i t r i of homologotls сyсlеs th wеll as rеpliсation (Мaс
imеntal геsults aсhiеvеd and Co arе сonsistеnt ! thе rolе of sцlfur-riсh п mulation of organiс сor
Ьееп shown to providе an еffiсiеnt sourсе tlf еlесtrons for thе rеduсtiсln of organiс сompounds undеr mild сonditions. Pyгitе formation сan produсе mol е с t r l a rh y d r o g е n : r r r dr е d u с еп i r r a t еt o a m m < l n i aa, с е t y l е n ег < еl t h y l е n е ,a n d thioасеtiс асiс.lttl aсеtiс aсiсl, .rs wеll as L)гolrrotingmorе сomplех syDthеsеs (Мadеn 1995), inсluding pеptldе Ьсlnds thаt геsult fronr thе aсtivatioп of amino aсids with сarЬon monохidе and niсkеl/iron sulphidеs (HuЬеr and \й/dсlrtеrshiusеr1998). Although pyritе-mеdiirtеdСO, rеdLrсtionto orgаtriс сompour-rdshas not Ьееn aсhiеvесl,thе fiхatiсlп undеr plzrusiЬlepгеЬi
How Did Rеpliсati
Thе pгimordial Ьroth r dеrland in whiсh a wid sizеd' dеstroyеd, or in Rеgardlеss of thе сoпrp сould not havе еvolvеd guarantее thе maintеnl Ponеnts undеr thе aсt molесular еntitiеs сa] would hаvе markеd tl
: 5
Тhе Оrigiп of Life oгtаntin thе formation сlf pеptidеs and rs wеll. Aссording to Rodе and сoworkэ formatiоn rеасtion'' (SIPF)provides a pеptidеsand possiЬly protеins dirесtly ltеd NaСl solutions сontaining Сu(II). gе of 0.4 to 4oЬ Ьaуe Ьееn rеportеd us; in thе 40_50mМ rangе. Сlay minеrrtly promotс thе rеaсtion. Again, thе o r t h е f г е е z i n go f t h е p г i m i t i v еo с е a n 5 salt.riсhЬrinеsnееdеdto promotе this
)riginsof Lifе оn Еarth? rs rivals to thе ..primordial soup'' hеt. еi d е a so f W i с h t е r s h i u s е r ( . l 9 8 8 ) .A с lry,'' lifе Ьеganп,ith thе appеаranсе of molithotrophiс mеtаЬoliс systеm that insoluЬlеminеral pyritе in thе viсinitу owеd thе appеaranсеof this nonorgannal ..lifе,''in whiсh сhеmoаutotrophiс :tivесitriс aсid сyсlе, or rеvеrsе KrеЬs Or thе photosynthеtiс grееn sulfr.rrЬaсlar phyiogеnеtiсtrееs show that this fiсations(suсh аs thе rеduсtivе aсеtyl)athways)аrе found in anаеroЬiс ar:uЬасtеria'whiсh has Ьееn intеrprеtеd Madеn 1995\. But is thе rеvеrsе KrеЬs , is vеry еnеrgеtiсallyfavorаЬlе. It has ]tеrWith а stаndard frее еnеrgy сhangе sponds to a rеduсtion potеntial Е., = tion is a strongrеduсing agеnt and has :сеof еlесtronsfor thе rеduсtion of orns. Pyritе formаtion саn produсе mol ammonia, aсеtylеnеto еthylеnе, and ts promoting morе сomplех synthеsеs rds that rеsult from thе aсtivation of rnd niсkеl/iron sulphidеs (HuЬеr and tе-mеdiatеdСo, rеduсtion to organiс hе fiхation undег plausiЬlе prеЬiotiс :tivatеdaсrtiс aсid Ьy a miхturе of сolortеd (HuЬеr and $7гiсhtеrsh:iusеr thе rеaсtionsсlссur in аП aquеOus еnhas Ьееn аddеd: thеy d
dеnsеmonolayеr of ioniсally Ьound molесulеs or takе plасе on thе surfасе of pyritе.In addition' a сarеful ехaminatiorr of thе HuЬеr and !Иziсhtеrshiusеramino aсid-pеptidе synthеsissсhеmе hаs found that it is highly un. likеly to aсhiеvе formation of oligomеrs that had thе aЬility to promotе ..pionееrmеtaЬoliс thееffесtivе аutoсatalysisproсеssеsassoсiatеdwith thе o r y " ( R o s s2 0 0 8 ) . Nonе of thеsееxpеrimеnts provеs Ьy itsеlf that Ьoth еnzymеs and nuсlеiс aсidsarе thе еvolutionary outсomе of surfaсе-ЬoundеdmеtaЬolism. In faсt, thе rеsultsarе also сompаtiblе with a morе gеnеral' modifiеd modеl of thе primoгdial soup in whiсh pyгitе formation is rесognizеd as an important sourсеof еlесtronsfor thе rеduсtion of organiс сompounds. It is thus possiЬlеthаt undеr сеrtain gеologiсal сonditions thе FеS/H,S сombination сould havеrеduсеd not only Сo Ьut also СO. rеlеasеd from moltеn mаgnа in dееp-sеavеnts, and lеd to Ьioсhеmiсal monomеfs. Pеptidе synthеsis' for instanсе,сould havе takеn plaсе in an iron and niсkеl sulfidе systеm (HuЬеr and Wiсhtеrsh:iusеr 1998) involving amino асids formеd Ьy еlесtriс disсhargеsvia a Millеr-typе synthеsis.If thе сompounds synthеsizеdЬy this pro. сеssdid not rеmain Ьound to thе pyritе surfaсе Ьut driftеd away into thе surroundingaquеous еnvironmеnt, thеn thеy would Ьесomе part of thе prеЬiotiсsoup, not of a two-dimеnsional autoсatalytiс rеaсtion sсhеmе. Thе еssеntial quеstion in dесiding Ьеtwееn thеsе two diffеrеnt thеoriеs is not whеthеr pyritе-mеdiatеd organiс synthеsis сan oссLlr' Ьut whеthеr dirесt Сo, rеduсtionand synthеsisof organiс сompounds саn Ье aсhiеvеd by a hypothеtiсal two-dimеnsional living systеm that laсks gеnеtiс information. Proof of !7ziсhtеrshiusеr's hypсlthеsisrеquirеs dеmonstration not only of thе tightсoupling of thе rеaсtions nесеSsаryto drivе autoсatalytiс СO, assimilationvia a rеduсtivесitriс aсid сyсlе Ьut also of thе intеrwеavingof a nеtwork of homologousсyсlеs that, it is assumеd,lеd to all thе anaЬoliс pаthways' as wеll as rеpliсation (Мadеn 1995). This has not Ьееn aсhiеvеd.ln faсt, ехpеrimеntalrеsults aсhiеvеd so far with thе FеS/H,S сomЬination in геduсing N. and Сo arе сonsistеnt with a hеtеrotrophiс origin of lifе thаt aсknowlеdgеs thеrolе of sulfur-riсh minеrals аnd othеr сatalysts in thе synthеsisand aссumulationof organiс сompounds.
How Did Rеpliсation First originatе? Thе primordial Ьroth must havе Ьееn a Ьеwildеring organiс сhеmiсal wondеrlandin whiсh a widе array of diffеrеnt molесulеs Wеrе сonstantly synthеsizеd,dеstroyеd' or inсorporatеd into сyсlеs of сhеmiсal transformations. Rеgardlеss of thе сomplехity of thе prеЬiotiс еnvironmеnt' lifе as wе know it сouldnot havе еvоlvеd in thе aЬsеnсеof a gеnеtiс rеpliсating mесhanism to guarantееthе maintеnanсе,staЬility' and divеrsifiсation of lifе's Ьasiс сomponеntsundеr thе aсtion of natural sеlесtion. Thе appеaranсе of thе first molесulаr еntitiеs саpaЬlе of rеpliсation, сatalysis' and multipliсation .What wеrе thе would havе markеd thе orisin of Ьoth lifе and еvolution.
o.)
64
The (.)rigiпof Lifе furrdamеntalсhаraсtеristiсsof thеsе first mсlIесr-rlar living еntitiеsthat distinguishеd thеrт fr
thе PNA-RNA and P] pеaling as possiЬlе сar titiеs, both PNA and nеgativе faсtors arе t that would prоduсе t сonditions and thе laс PNA is attraсtivе l whiсh еliminatеs thе r origin of lifе. Its сorn havе Ьееn produсеd ur Howеvеr, PNA is susс rеarrangеd PNA. Thil thе N-tеrminal positiс on thе Ьasis of an Pеars to Ье supеrior t. to its Ьasе-pairing attr Sсhсiningеt al. 2000). during thе rеaсtion сa dеsсriЬеd Ьy Butlеrov сould havе bееn rеad (sееRеaсtion 2), whiс tion of formaldеhydе. rеduсеs this proЬlеm oligonuсlеotidеs сom1 sizеd undеr prеЬiotiс r It is possiЬlе that P] to thе fiгst TNA molе сomponеnt of TNA w in opеrаtion. orgе1 aI сhiral sugar dinuсlеot сurrеd simply Ьy сhan PNA.induсеd oligom. providеd а mеans of с сhirality into polymеr tеntially solvеs an onf Ьеforе thе origin of lil
I{снo
нснo ..--..---.-.--f
Formaldehyde
G.
Reасtion 2. Тhе forma formaldehydeand glyс of rеaсtions'and Ьoth suЬsеquеntгеaсtions.
The Оrigiп of Life irst molесulаr living еntitiеs that distinry? rеrs аnd smali oligomеrs to living еntithе uЬiquit
thе PNA-RNA and PNA-DNA hеliсеs arе both right-handеd. Although appеalingas possiЬlесandidatеsfor thе first sеlf-rеpliсatingmolесular living еntitiеs,Ьoth PNA and TNA havе positivе and nеgativе aspесts. Thе main nеgativеfaсtors arе thе laсk of аny dеmonstratеd oligomеrization proсеss that would produсе thеsе nuсlеiс aсid analоguеs undеr plausiЬlе prеЬiotiс сonditionsand thе laсk of any dеmonstratеd сatalytiс propеrtiеs. PNA is attraсtivе Ьесausе its ЬaсkЬonе is aсhiral (lасking handеdnеss), whiсh еliminatеsthе nееd for thе sеlесtion of сhirality Ьеforе thе timе of thе origin of lifе. Its сomponеnts, AЕG and nuсlеoЬasеs linkеd to aсеtiс aсid' havеbееnproduсеd цndеr simulatеd prеЬiotiс сonditions (Nеlson еt al. 2000). Howеvеr'PNA is stlsсеptiЬlеto an N-aсyl migration rеaсtion that produсеs a rеarrangеdPNA. This proЬlеm сould Ье minimizеd, howеvеr, Ьy Ьloсking thеN-tеrminal position Ьy асеtylation' for еxamplе. on thе Ьasis of an ехtеnsivеstudy of sugar-Ьasеdnuсlеiс aсids' TNA appеafsto bе supеrior to othеr possiblе sugar-Ьasеd nuсlеiс aсids with rеspесt to its Ьasе-pairingattriЬutеs,еspесiallywith RNA (Еsсhеnmosеr1999, 20041 Sсhбningеt al. 2000). Thе tеtrosеsugar in TNA сould havе Ьееn synthеsizеd duringthе rеaсtion сasсadе that takеs plaсе during thе formosе rеaсtion first dеsсriЬеdЬy Butlеrov in 1861. Thе 4-сarЬon sugars thrеosе and еrythrеosе сould havе Ьееn rеadily synthеsizеd Ьy thе dimеrization of glyсolaldеhydе (sееRеaсtion2), whiсh in turn сould havе Ьееn produсеd from thе dimеrization оf formaldеhydе. Еvеn though thе prеsеnсе of a 4-сarЬon sugаr in TNA rеduсеsthis proЬlеm to 2 sugars and 4 stеrеoisomеrs' to dеmonstratе how oligonuсlеotidеsсomposеd only of L-thrеosе сould Ье prеfеrеntially synthеsizеdundеr prеbiotiс соnditions is a formidaЬlе сhallеngе. It is possiЬlе that PNA prесеdеd TNA and in faсt assistеd in thе transition to thе first TNA molесulеs. As statеd еarliеr, thе sеlесtion of thе сhirаl sugar сomponеntof TNA would havе rеquirеd somе sort of sеlесtion proсess to Ье in opеration. orgеl and сoworkеrs havе suggеstеd that thе inсorporation of сhiral sugar dinuсlеotidеs at thе еnd of a PNA сhain' whiсh сould havе oссuгrеdsimply Ьy сhanсе, сan induсе сhirality into a nuсlеiс aсid produсеd Ьy PNA.induсеd oligomеrization (Kozlov еt al. 2000). PNA сould thus havе providеda mеans of сonvеying thе сritiсally impоrtant Ьiologiсal propеrty оf сhiralityinto polymеrs nеar thе timе of thе origin of lifе. This possiЬility potеntiallysolvеs an ongoing dilеmma whеthеr thе origin of сhiгality oссurrеd Ьеforеthе origin of lifе оr during thе еvolution of еarly living еntitiеs.
tlснo
HCНo'нoсн?-сHo
Formaldehyde
н9SЦr91o ЕIoсн2-сFIoH.Co-CH2oH
Glyсolaldеhydе
Reaсtion2. Thе formation of tеtrosеsugars from thе dimеrization of and glyсolaldеhydе.This is оnly part of the ovеrаll formosе sеriеs formaldеhydе and ЬotЬ hеxosеsаnd pеntosеswould havе Ьееn produсеd Ьy of reaсtions, rеaсtions. subsеquent
Тhе ()rigitt оf 1,ifе Rеgardlеssof thе typе of analoguе simiIar to nuсlеiс aсid or othеr typе of rеpliсator sуstеm that wаs usеd Ьy tl-rеfirst self-rеpliсatingеntitiеs, polvmеr staЬility and survival would havе Ьееn of сritiсal importanсе. Nuсlеiс aсidsin gеrrеralhаvе vеry shсrгtsurvival timеs at еlеvatеdtеllpеraturеs. RNA is r,еrу Ьond involvirtgthе 2'unstablе Ьесausеof thе prеsеnсеof thе phсlsphсldiеstег Ьydroхyl group of riЬоsе. Thе staЬiIiryof TNA is unkrrorvnat prеsеnt' Ьut it is proЬaЬly somеwhаt similar to thе staЬility of DNA. It is possiЬlеtlrat otlrеr tеtrosе sugar-Ьasеdnuсlеiс aсids wеrе lеss staЬlе thirn TNA Ьесаusеof thеir tеndеnсy ttl forш lеss staЬlе hеliсal stfrrсtul]еs(ЕsсЬеnmtlsеr|L)99|аrrd tlrаt thе sеlесtion of TNA Was thе rеsult of this faсtсlr,althotlgh this is also not known. Tlrе stаЬility of PNA lrаs Ьееn pаrtly invеstigatеd,and providеd thе N-aсyl migration rеaсtion сan Ье rninimizеd, thе аmidе linkagе in PNA rvould Ье еxpесtеdto havе a staЬilitу at nеutral pH similar to that of pеptidе rvith tеmhonds in prno.,di-' аnd triglусеridеsur-rdегrтild ссlnditions (Hargrеavеsеt аl. 1977)' It is vеry atrraсtivеtO assulте thаt сorтpartmеntalization within liposot-llеsformеd Ьy amphiphiliс molесulеsof prеЬiotiс origin асlsorЬеdorltо сlaуs \vаs еssеntiillfor thе еmеrgеnсеof lifе. RNA nr
thе Ьasiс maсhinеry . partmеntalizеd into Dеspitе thе suссеsl ..with lеms with this ordеr to maintain a s сating systеm insidе layеr barriеr. This г as amino aсids. As a sidе thе vеsiсlе'' (Gr surfасеs сould havе сules that usеd thе сz volvеd in polymеrizа сomplеxity, synеrgis of thе сomponеnts il portеd into thе vеsiс formеd a singlе сom rеsults showing that сomе polymеrizеd ч pidiс Ьarriег may no
Thе Transition l
Thе еvolution of thс tirеly on RNA (i.е. еvolution toward m< onе molесulе that са ..t LaЬoгatory-basеd сatalytiс RNA molе rangе of important RNA fragmеnts (lig
1999|. Thе list of dt that thе RNA world есulеs, pеrhaps funс 2002). Thе сomplеx tiс transfеr, аnd vaI dеmonstratеd in thе immatuгity of tlris Cесh 2002; Joусe2| Thе invеntion of сhinегy nееdеd for l Four of thе bаsiс rеа Ьozymеs, and it has tions is not likеly a oгigin, most prоЬaЬ thе сasе' thеn thе рr
Thе Оrigin of Life similar to nuсlеiс aсiсl or othеr typе of е 6rst sеlf-геpliсаringеntitiеs' pthеr lеss staЬlеtharrТNA Ьесausеof rhеir rllсturеs(Еsсhеnmosеr1999) and tlrat lf this faсtor, altЬough this is also not l pагtly invеstigatеd,and providеd thе 'inirnizеd' thе amidе lirrkagе in PNA tt nеutrаlpH sinrilar to that of pеptidе uggеststhat in еnviгonmеntswith tеmtiпlе would Ье in thе rangе of 101_105 rolе in еarly nuсlеiс aсid survival Ьеэеn found to еnhanсе nuсlеiс aсid stаsеvеrаltransfеr RNAs (tRNAs) wеrе solution in сompzrristlсliрidiс molесr-rlеs mаv als
thеЬasiсmaсhinегуnееdеd for RNA sеlf-rеpliсatiсlnсould hаvе ЬееIrсomirrto pгoto-typесеils (Наriсzyс еt :rl.200З; Сhеn 2006). pаrtmеntalizеd Dеspitеthе suссеssof thе RNA еnсapsulatioIrехpеrimеnts,thеrе arе proЬ..rvithin lеmswith this thе vеsiсlе'' sсеnario (Griffiths 2007). For ехаmplе, in ordеrto maintain a stеаdy supply of molесulеs nееdеd for survival of a rеpliсatingsystеminsidе a vеsiсlе, molесulеs would nееd to сross a lipid-likе ЬilayеrЬarriеr'This rrlay havе Ьееn а mirjor oЬstaсlе foг сhargеd spесiеs suсh ..outas aminoaсids.As a rеsult' pеrlrirpsthе first rеpliсating systеm еvolvеd sidе thе vеsiсlе'' (Griffiths 2007). In this сasе, vеsiсlеs attaсhеd on minеral surfaсеsсould hаvе Ьееn in сlosе proхimity to sirnplе sеlf-rеpliсating molесulеsthat usеd thе сatalytiс propеrtiеsof thе minеrаl to еnhanсе rеaсtions involvеdin polymеrizationand rеpliсаtion. As thеsеtlrе two systеmsеvolvеd in сomplехity,synеrgistiсintеrirсtiotrsсould iravе dеvеloреd thar аllсlwеd somе of thесomponеntsinvolvеd in thе rеpliсating systеm to Ьесomе frееly transportеdinto thе r,еsiсlе.At this point thе two systеms сould havе rrrеrgеdand formеda singlе сomрartmеntalizеd, sеlf-rеpliсation systеm. Howеvеr, rесеnt rеsultsshowing thаt aсtivatеdnuсlеotidesсan diffrrsеinto liposomеs and Ьесomеpolymеrizеdwithin thеm suggеstthаt undеr сеrtain сonditioпs tl-rеlipidiсbarriеrmаy not havе Ьееn irnpеnеtraЬlе(Маnsy еt al. 2008).
Thе Transition toward a DNA/RNA/Protеin
World
Thе еvoiutionof thе first livirrg rrrolесularlir,ing еrrtitiеsinto onеs basеd еntirеlyon RNA (i.е.,thе RNA rvоrld) would lravе Ьееn thе nехt stеp in thе еvolutiontoward modеrn Ьiосhеrnistry.RNA has Ьееn found to Ье an all-inonеmolесulеthat сan not only storе information Ьut also сatalyzе rеaсtions. ..tеst-tuЬе-еvolution'' ехpеrimеtrtshavе dеmonstгatеdthat LaЬoratory-Ьasеd (riЬozyrnеs) havе thе саpасitv to сaгry Out a widе сatаlytiсRNA molесulеs rangеof iпrportant Ьioсhеnriсal геaсtions,irrсluding thе joining togеthеr of RNA fragmеnts (ligation) and pеptidе-Ьond formation (Bartеl and Unrau 1999).TЬelist of dеmonstratеdсatalytiс rеaсtions is ехtеnsivе aпd suggеsts thatthе RNA world сould havе had a lаrgе rеpеrtoirеof сatalytiс RNA mol. in сonсеrt with onе an()thеr(Doudna irnd Cесh есulеs,pеrhаps fr"rпсtiоning rnultipliсаtion'gеnе2002).Thе сotrrplехsеriеsof rеасtionsnееdеdto pеrr-r.rit tiс transfеr,and variation rеqr.lirеdin thе RNA wоrld has so filr not Ьееn in thе laЬoratсlry,Ьut optimism rеlrrainsbесausеof thе rеlativе dеmonstratеd immaturityof tЬis arеa of rеsеаrсh (Bartеl аnd Unrau 1999; Doudna and Сесh2002;Joyсе 2002). Thе invеntion сlf protеin synthеsisand thе еnсаpsulation of rеасtioll maсhinеrynееdеd for rеpliсation n1аy have takеn p[асе during thе RNA world. Fourofthе Ьasiс rеaсtitlnsinvolvеd in protеin Ьiсlsynthеsisarе сatаlyzеdЬy riЬozymеs,and it has Ьееn notеd that thе сomplеmеntary naturе of thеsе rеaсtions is not likеlv aссidеntal Ьut rathеr suggеstivе that thеy had a сommon origin,most proЬably in thе RNA wсlrld (Kumar atrс]Yarus 2001)' If this was thесasе,thеrrtlrе primitivе nltсlеoЬasесodе usеd tor protеin Ьiosyntlrеsislrad
67
Thе Оrigiп сlf l,ifе its origin in thе RNA worlсl, аlthough thе b:rsеsusеd in thе early сodе сould hаvе Ьeеn diffеrеrrtfгorn tllе onеs usесJtodаy (KolЬ еt аl. 1994). It is possiЬlе thаt Ьy thе timе RNA-Ьasеd lifе appеaгеd
Did Lifе Arisе in a High-TеmpеraturеЕnvironmеnt? Еvеn tlrouglrDNA is nrorе st:rЬlеthan RNA, it is still rарidly dеgrаdеdat еlеr,atеd tеmpеraturеs.In addition, Protеin еnzymеs dеnaturе rapidly at еlеvatеd tеmpеraturеs.This rтtrsthаr,еat lеаst irtitiаllylimitеd thе еnr,ironmеntswhеге DNA/protеin-Ьasеd lifе сould survivе for anr. signifiсzrntpеriоd of timе, аnd as was thе сasе for аll othеr еarliег living еntitiеsЬаsеd tln nuсlеiс aсid, sr.lrvivаl would havе Ьееn most likеly undег сool сonditiorrs(Bаda and [,azсаno2002Ь). Nеvеrthеlеss, sevеral rеsеarсhеrslravе advoсatеd high tеп1pеraturеs,еspесiаllу thosе zrssoсiatеdrvith [rydrсlthеrnralvеrrt systеnrs,as thе еnr,ironmеnt whеrе DNA/protеin_Ьasеd еntitiеs first аrosе. Prсlponеntsfor а high.tеmpеrаturеOrtgin сitе thе f:tсtthаt thе trnivеrsаltrее сlf ехtаI1tlifе irppеаrst
Pеrthеrmophiliс organt modеrn Ьiology was a DNA/protеin-Ьasеd lift At first glanсе, Ьoth аPPеаr to support a }
еarly. Largе-sсalе anal of primitivе еarth was rrmainеd moltеn for (Nfеthеrill 1990), but n hydrosphеrе impliеs th Howеvеr, thеrе is thес wеnt latе ассrеtion im. may havе Ьoilеd thе oс Could modеrn bioсh ditions? Thе proposals lеms, inсluding thе сhе сompounds suсh as ar molесulеs, whosе ha] 250_350.с arе at thе n
It is truе, of сoursе, fаstеr. Primitivе еnzyI аnd thus thе ratе еnha: onе way to ovеrсome rizеd еlsеwhеrе (Islasi
1. rеduсеd сonсеntr and NH.; 2. lowеr Stеady.stat whiсh at tеmpеra fоrmamidе and tl 3. instability of rеaс
(RсFIo(Nt{,)СЬ
o f a m i n o a с i d s ;a 4. loss of organiс сс s t a Ь i l i t yo f g е n е t
Thе rесognition thz arе oссupiеd Ьy hypе itsеlf сonсlusivе proо lifе (Broсhiеr and Phi sсriptions of thе еvo bioсhеmiсa1сompoul bly nаivе to attеmpt living systеms from п еrаl gеnеtransfеrof. misеd thе gеnеtiс rе сonсlusions aЬout th.
Tbe Оrigiп of Li|.е r thе Ьasеsusеd in thе еarly сodе сoLlld ltodаy (KolЬеt aI.1994). -Ьаsеdlifе irppеarеdOn еartЬ' thе suprnds dеrivеdfrom tЬе sourсеs disсussеd ishеd.М:rrryсlf thе сomporrеnts of thе sivеly сonvеrtеdintrl polymеrs, inсluds, and thus thе rаw mаtеrials neеdеd to tеd.This irrrpliеsthat simplе mеtаЬoliсе in ordеr tO еnsurе a supply of thе inсе oi thе prinlitivеlir.ingеntitiеs.In this iеd to produсе еssеntial сtlnrponеnts - ' r е1 . l е r l i д pt lqr i g i n l I l r n o n е n z v m a t i сo r rlratiatеr Ьесamеfinе гurrеdаs riЬozyoсеssingЬесamеdominаnt. ulаг еntities,thе main limitаtiоn irr thе rеrnеinstaЬility of RNA. Tlris in tr'rrn r v е Ь е е n v е r y е Г f i с i е n ri n с з r r y i n g < l u t rаintainan асlеquatеitlvеntorr.of mol'ility of RNA сould havе Ьееn thе pгi)NA/pгotеirr world, whеrе, Ьесausе of olесulеs,suгl,ir'aIlr'сluldh:rl'еllееn lеss dirrgto.|oyсе(2002), it is p
еrаturеЕnvironmеnt? RNA, it is still rapidl1'dеgraсlеdat еlеn еnzymеsdеnаturегapidly аt еlеvatеd ritially limitеd thе еnvironmеntswhеrе lг any signifiсаntpеriod of tiлlе, and аs еntitiеsЬasеdon nr.rсlеiсaсid, survival сonditions(Badaand I,аzсаno20O2Ь). dvoсаtеdlriglr tеnlpеraturеs,еspесi:rlly nt systеms'as thе еnvironmеnt whеrе P r o p о n е n t Гs o rl h i g , h - t е m p е г а t urrlеr i Еехtаnt litЪ appеars to Ье ro
pеrthеrmophiliсorganisms. Thus if thе lаst сomп]on anсеstor (LСA) of all modеrnЬiоlogy was a hypеrthеrmоphilе, thеn it is сonсluded that tlrе first DNA/protеin_Ьasеdlifе nrust havе arisеn in a similar typе of еnvironmеnt. At first glanсе' Ьoth thе molесular and thе palеontologiсal fossil rесords appеarto support a lrypеrthеrпrophiliсorigin of lifе. LitЪ on еarth arosе еarly.Largе-sсalе analysis suggеsts that soоn aftеr its formation thе surfaсе of primitivееаrth was еxtrеmеlу hot. Thе planеt is gеnеrаlly thouglrt to havе rеmainеdmoltеn for somе timе aftеr its formation 4.6 Ьillion yеars ago (Wеthеrill 1990|, Ьut minеralogiсal еvidеnсeof a 4'З- to 4'4-Ьillion- yеar-old lmpliеs that its surfaсе гapidly сoolеd down (\Уr'ildе еt al. 2001,). hydrosphеrе Howеvеr,thеrе is thеorеtiсal and еmpiriсal еvidеnсе that thе planеt undегWеntlatе aссrеtion impасts (Byеrly et a|.2О02; Sсl-roеnЬеrg еt al. 2002) that yеaгs (Slееp latе еt aL.|989). mayhavеЬoilеd thе oсеans as as 3.8 Ьillion ago Сould modеrn Ьiосhеmistry havе arisеn undеr thеsе high tеmpеrаturе сonditions?Thе proposаls of a high-tеmpеrаturе origin of lifе faсе major proЬlеms'inсluding tlrе сhеnriсal dесomposition of prеsumеd еssеntial Ьioсhеmiсal сompoundssuсh as amino aсids, nuсlеoЬasеs, RNA, and othеr thеrmсllaЬilе molесulеs,whosе half-livеs for dесomposition at tеmPеraturеs Ьеtwееn 250-350"Сarе at thе most a fеw minutеs (!(/hitе1984;Millеr and Bada 1988). It is truе' of сoursе' thаt high tеmpеraturеsаllow сhеmiсal rеaсtions to go fasrеr.Pгimitivе еnzymеs' onсе tlrеy appеared, сould hаvе Ьееn inеffiсiеnt аndthus thе ratе еnhanсеmеnt аssoсiatеd with highеr tеmpеraturеs wouid bе onеWay to ovеrсomе this limitation (Harvеy 1924), Howеvеr, аs summarizеdеlsеwhеrе(Islaset a|.20О7)' high-tеmpеraturеrеgil-tlеs would lеad to: 1.rеduсеdсonсеntratiOnsof volatilе intеrmеdiatеs'suсh as HСN, H2СO, and NH,; 2. lowеr stеady-statесOnсеntrationsof prеbiоtiс prесursors likе HСN' whiсh at tеmpеraturеsa littlе aЬovе 100.С undеrgoеshydrolysis to first forrnamidеаnd thеn formiс асid arrd ammoniа; 3. instabilityof rеaсtivе сhеmiсal intеrnrеdiatеslikе amino nitrilеs (RсHo(NH')сN), whiсh play a сеntгal rolе in thе Strесkеr syr-rthеsis of amino aсids; and 4. loss of оrganiс сompounds Ьy thеrmal dесomposition and diminishеd staЬilityof gеnеtiс polymеrs. Thе rесognitionthat thе dееpеstЬranсhеs in rootеd univеrsal phylogеniеs arеoссupiеdЬy lrypеrthегrnophilеsis сontrovеrsiаl and doеs not providе Ьy itsеlfсonсlusivеproof of a higlr.tеmpеraturеorigin of DNA/protеin-Ьasеd lifе(Broсhiеrand Рhilippе 2002). Givеn thе hugе gap еxisting in сurrеnt dеsсriptionsof thе еvoltrtionarytransition Ьеtwееn thе prеЬiotiс syr-rthеsis of Ьioсhеmiсalсorrrpounds and thе LСA сlf аll ехtarrt living Ьеings, it is proЬаЬly naivе to attrmpt to dеsсriЬе thе origin of lifе аnd thе naturе of thе first livingsvstemsfronr nrolесularplrylogеniеs(Islaset aI. 2007).In addition, lаtеralgеnеtransfеr of thеrmoadaptativеtrаits has apparеntly grеаtly сompromisеdthе gеnеtiс rесord prеsеnt in modеrn organisms, r,vhiсh makеs any сoпсlusions aЬoцt thе еnvironnrеntwhеrе thе DNA/protеin world origirrаtеd
69
70 Тhc Оrigilt of I'ifе q t l е s t i o n a Ь l е( D o o l i t t l е | 9 9 9 , 2 О 0 О 1B е с е г r a е t a l . 2 0 0 7 Ь ) . A r r a n a l y s i so f protеin sеqtlеIlсеshаs f
From thе Origin of Protеin Synthеsistо thе Last Сommon Anсеstor оf Lifе Orrсе DNA/pгotеin_Ьlrsеdlifе, аnd proЬaЬly RNA-Ьаsеd lifе as wеll, Ьесarте dorтinant and еvolvеd in stlphistiсatitln,thе way сarЬon was produсеd аnd оrr thе еаrth,ssurfасе was foгеvеr сhangеd' еspесiallу aftеr phosес1uеstеrеd tosynthеsiseppеarесl.Thе amor.tntof organiс сarЬon produсеd Ьy еaгl1 lifе via the аutotrophiс fiхation of СС),' СН,,, and simplе organiс сompounds suсh as fornriс and :rсеtiсасids rvоuld havе far ехсееdеdthе anr
extant forms of lifе Ьut Ponеnts of thеsе сom; сhangеs in thеm arе vt that no anсiеnt inсipiеr ular struсturеs havе bе сan Ье dеduсеd, аnd th
fаshionеd and сontеm1 For instanсе, thе faсt forming all thе rеaсtion еаrliеr, that protеin Ьiс 1998), that is' that thе 1
RNA. This possibiliry thаt thе ribosomе's сatl сomposеd of RNA (Bar
ganization of primitivе gеnеs, whiсh arе sеquеr pliсadon еvеnt. Foг ins1 gous gеnеs that еnсoс triphosphatе)-dеpеndеr
еvidеnсе of thе ехistеn synthеsis that took plа mеntal еvidеnсе of in ' trations laсking Ьoth (Gаvrilova et a|.1976;
anсеstral protеin syntht Bioinformatiс analy domains сan bе usеd t sеquеnсеs to сharасtеr rеsulting sеt is dominа volvеd in gеnе еxprеss whiсh unwind RNA r сonsеrvеd as many tra еvolution of a сontrol viding additional suPP prominеnt rolе during biosynthеtiс pathway rophosphatе synthasr taЬolism. Although t сorrеsponds only to а poгtеd hеrе are likеly protеin domains сoml Thе high lеvеls of imply not only that r
thе сomplеx Bеnomе dupliсation еvеnts rе. tion is usеd tо Ьuild
Тhе origiп of Lfе B е с е r r aе t а l . 2 0 0 7 Ь ) . A n a n a l y s i s o f : еnzуmе'[еvеrsеg},rаsе'that is sресifiс ]rе appаrеntlynot аnсеstralto thеsе orJ-adaptеdvеrsions of thosе prеsеnt in r е 2 0 0 2 | .Е v е n i f t l r е L С A w a s a h y p е r ,uyand Сhaussiсlorr2008), thеrе arе illl distriЬution,inсluding thе possiЬility hеanhigh-tсrnpеraturе rеgimеsthat may lпе (Slееpеt al. 1989; Gogаrrеl-r-Boеkels гia to ехtrеmе еnr,iгonmеntsЬy latеrаl al. 2000) and otЬеr thеrmoadаptativе (3) outсornpеtionof oldеr nrеsophilеs )tеdto strеss-indr-rсing сonditi
nthеsisto thе Last oЬaЬly RNA-Ьasеd lifе as wеll, Ьесanrе tln, thе way сarЬon was produсеd and s forеvеrсhangеd,еspесiаlly аrftеrphoorganiс сarЬon prоduсеd Ьy еarly lifе СHo, and simplе organiс сtlmpounds ] havе fаг ехсееdеdthе amouгtts of orЬеirrgsynthеsizесl'fгom еithеr hornе. ourсеs undеr thе Ьеst сonditions. Thе on thе еаrth thеn shiftеd frorn onе ini. aЬiotiс origin to t>nеmadе tlp еntirеly ltеin world that Ьioсhеmiсal mасhinеry Ьranе strttсturеs'сomparaЬlе to thosе эsprеаd.This ls tlrus thе first timе that righthavе Ьееnprеsеrvеdin thе form of гliеr stagеswould hаvе lеft Ьс.hind only ot sttrvir.еdthе rar':rgеsof gеoсhеmiсаl : timе. Although traсеs of hydroсarЬon billion-r.еar-old sеdimеntaryroсks, thе s found tсl dаtе (Broсks et tl|. 1999), lation,аnd post-dеpositionalmеtamor. еаrliеr rесord of аЬiotiс organiс сhеm. .ithprimitivеlifе. lе еssеlltialfеattlrеsof gеn
ехtantforms of lifе Ьut also imply that thе sеts of gеnеs that еnсodе thе сomponеntsof thеsе сomplеx traits wеrе frozen a long timе ago (i.e., major сhangеsin thеm аrе vеry stгongly sеlесtеdagainst and arе lеthal). It is truе that no anсiеnt inсipiеnt Stagеsor еvolutionary intеrmеdiatеs of thеsе molесular struсturеshavе Ьееn dеtесtеd, Ьut thе ехistеnсе of gradеd intеrmеdiatеs сan bе dеduсеd'and thеrеforе thе supеrnatural origin advoсatеd Ьy Ьoth oldfashionеdand соntеmporary сrеаtionists is rеndеrеd unnесеssary. Foг instanсе,thе faсt thаt RNA molесulеs Ьy thеmsеlvеsarе сapаЬlе of pеrformingаll thе rеасtions involvеd in pеptidе_Ьondformаtiorr suggеsts'аs statеd еarliеr,that protеin biosynthеsis еvolvеd in an RNA world (Zhang and Сесh 1998|,that' is, that thе first гiЬosomе laсkеd protеins and wаs produсеd only by RNA' This possiЬility is supportеd Ьy сrystаllogгаphiс data that havе shown thatthе ribosomе'sсatalytiс sitе, wlrеrе pеptidе-bond formation takеs plaсе, is сomposеdof RNA (Ban еt al. 2000; Nissеn еt al. 2000). Сlurеsto thе gеnеtiс organizationof primitivе forms of translation arе also providеd Ьy paralogous gеnеs,whiсh arе sеquеnсеsthat divеrgе, not through spесiаtion, Ьut аftеr a dupliсationеvеnt.For instanсе' thе prеsеnсеin all known сеlls of pairs of homologous gеnеs that еnсodе two еlongation faсtоrs, whiсh аrе GTP (guanosinе triphosphatе)-dеpеndеnt еnzymеs that assist in protеin Ьiosynthеsis, providеs еvidеnсеof thе еxistеnсеof a moге primitivе, lеss rеgulatеd vеrsion of protеin synthеsisthat took plaсе with only onе еlongation faсtor. In faсt, thе еxpеrimеntalеvidеnсеof in vitro tгanslation systеms with modifiеd сationiс сonсеntrations lасking both еlongation faсtors and othеr protеin сomponеnts (Gavrilovaet aI' I976; Spirin 1986) strongly supports thе possiЬility of an oldеr prоtеin synthеsisapparatus Ьеforе thе еmеrgеnсеof еlongation faсtors. аnсеstral Bioinformatiс аnаlysis of sеquеnсеd сеllular gеnomеs from thе thrее major domainsсan Ье usеd to dеfinе thе sеt of thе most сonsеrvеd protеin.еnсoding sеquеnсes to сharaсtеrizе thе gеnе сomplеmеnt of thе LCA of еxtant lifе. Thе rеsultingsеt is dominatеd Ьy diffеrеnt putativе ATPasеs' and Ьy molесulеs in. volvеdin gеnеехprеssion and RNA nrеtaЬolisпr.Thе so-сallеd DЕAD gyrasеs' whiсh unwind RNA molесulеs and lеavе thеm rеady for dеgradation, arе аs сonsеrvеdаs many transсription and translation gеnеs.This suggеststhе еarly еvolutionof a сontrol rnесhanism for gеnе еxprеssion at thе RNA lеvеl, providingаdditional support to thе hypothеsis that RNA molесulеs playеd a morе prominеntrоlе during еarly сеllular еvolution. Сonsеrvеd sеquеnсеsгеlatеd to Ьiosynthеtiсpathwаys inсludе thosе еnсoding putativе phosphoriЬosyl py_ rophosphatеsynthasе and thiorеdoхin, whiсlr partiсipatе in nuсlеotidе mеtaЬolism. Although thе information сontainеd in thе availaЬlе dataЬasеs сorrеspondsonly to а minor portion of biologiсal divеrsity, thе sеquеnсеsreportеdhеrе arе likеly to Ье part сlf an еssеntiаl and highly сonsеrvеd pool of protеindomains сommon to all orgarrisms (Bесеrra et a|' 2007a). Thе high lеvеls of gеnеtiс rеdundanсy dеtесtеdin all sеquеnсеdЕ]еnomеs implyпot only thаt dupliсation has plаyеd a major rсllе in thе aссrеtion of thе сomplех gеnomеs foцnd in еХtant сеlls, Ьut also tlrat Ьеforе thе еarly dupliсationеvеnts rеvеalеd Ьy thе largе protеin familiеs, Ьесausе thе dupliсa' tion is usеd to Ьuild morе соmplехity, simplеr living systеms еxistеd that
71
72
Thе Оrigiп of Lifе laсkеd thе largе sеts of еnzvmеs and thе sсlplristiсatеdгеgшlаtoryaЬilitiеsof с о n r е m Г O r i ] г 1о 'г g а n i s m s .Т h е r ' a r i l t i t ' n ' . ' i t r l i t s с o l r ln l o l l t t l е х t an t s p е с i е s сan Ье еasily ехplainеd as thе outсоmе of divеrgеntproсеssesfrom аn anсеstrаl lifе form that ехistеd Ьеforе thе sеparation of thе thrее major Ьiologiсal domains, that is, thе last сommon anсеstor (LсA) or сеnanсеstor.No palеontologiсаl rеmnаnts likеly rеmain that Ье:rrtеstimony of its ехistеnсе'so thе sеarсh for::r fossil of thе сеnilrrсеstoris Ьound to provе fгuitlеss. Analvsis of an inсгеasirrglylargе nulrrlrегof сomplеtеlv sеquеnсеdсеllular gеnomеshas rеvеalеdmajrlr disсrеpanсiеsin thе topology of riЬosomal RNA (rRNA) trееs. Vеry oftеn thеsе diffеrеnсеs havе Ьееn intеrprеtеd as еvidеnсе of horizontal gеnе trаnsfеr (HGT) еvеnts Ьеtwееn diffеrеnt spесiеs,сasting douЬt uporr thе fеasiЬility of thе rесonstrttсtioгr and prсlpегurrсlеrstanding оf еaгly Ьiologiсаl histoгv (Doolittle 1999, 2000). Тhеге is сlеar еvidеrrсеtlrаt gеnomеs havе a mosaiс-likе naturе whоsе сomponеnts сotllе from a widе vаriеty of sourсеs (Oсhman еt al. 2000). Diffеrеnt advoсatеshavе dеsсriЬеda widе spесtrum of mix-and-matсh rесomЬination proсеssеs'ranging from thе latеral transfеr of a fеw gеnеs via сonjugarion, trаnsduсtiorr'оr transformаtion to се|l ftrsionеvеnts irrr,оlvingorganistrrsfrom diffеrеnt domains. Unil,еrsаl gеnе-basеdphylogеniеsultiгnatеlyrеaсh a singlе univеrsal еntitr,, Ьut thе Ьaсtеrial-likе LСA (Gogartеn еt al. 1989) that wе favor Was not alonе. It would havе Ьееn in thе сompany оf its siЬlings, a population of еntitiеs similar to it that ехistеd throughсlut thе samе pеriod. Thеy may havе not survivеd, Ьut somе сlf tlrеir gеnеsdid if rl-rеvЬесamе intеgrаtеdvia lаtеrаl transfеr il-ltotlrе l-СA gеnonlе.Thе сеnanсеstoris thtrsonе t>ftЬе last еvolutionary outсomеs of a sеriеsof anсеstralеvеnts' inсluding latеral gеnе transfеr, gеnе lossеs, and paгalogous dupliсatiсlns, that took plaсе Ьеforе thе sеparation of Bасtеria, Arсhaеa, аnd Еuсarya (I,azсano еt al. 1992; Glansdorff 2000; Сastrеsana 200 1; Dеlayе еt аl. 2004; Bесеrra еt аl. 2007a).
Сonсlusions and Pеrspесtivеs Although tl.rеrеhavе Ьееn сonsidеraЬlе advanсеs in thе undеrstаnding сlf сhеmiсal proсеssеsthat may havе tzrkеnplaсе bеf
thеiг mаintеnanсе аnd r syпthеsizеd Ьy pгеЬiotiс sumеs that thе raw mat tivе сhеmiсal systеms w геquirеd tо drivе thе сh. may hаvе bееn providе high.еnегgyсompolrrrds Thе Ьаsiс tеnet of thr maintеnanсе and rеpro. on prеЬiotiсally synthе hаs Ьееn no shortagе o diаl soup took plaсе.Br It is vеrу unlikеly that z
of organiс сompourlds and that thе сonsеquer еndogеnous synthеsеs synthеsis in dееp_sеav
oritеs, and intеrplrrтlеt thе rеlativе signifiсanс simply гесognizеs thе pounds' thе raw matеri As disсussеd hеrе, th bioсhеmiсalmonomеrs tions is wеll еstaЬlishе еffiсiеnt, Ьut thе widе r
сompounds сan Ье syn Ьuilding bloсks of lifе ; to thеm do not tаkе pl геaсtion сonditions bul Thе synthеsisof сhеп zymatiс proсеssеsundе thеy wеrе еithег еssеnt ronmеnt. Nonеthеlеss,l
stituеntsof living orgzr too striking to Ье foгtui portеd Ьy thе oссuгrеn Ьonасеous mеtеorltеs (
Ьесomеs plаusiЬlе, brpгimitivе еarth. Foг all a P P е а r st o u s т h a t t h е [ еstaЬlishеdеvеnts thзt Mainstrеam sсiеntif vеlopеd within thе fr
wеalth of еxpеrimеntа пarrаtivе thаt links m: issuеs.It is truе thаt th
Thе Оrigiп of Lifе :hе sophistiсzltеd rеgulаtory aЬilitiеs оf l n s o f t r a i r sс o t n m o n г o е х t a n t s p е с i с s е of divergеntproсеssеsfrom an anсrsеparationof thе tlrrееma jor biologiсаl сеstor ([-СA) or сеnanсеstoг.No pi.rlеLtЬеartеstimonvof its еxistеnсе,so thе s Ьorrndto pгovе fruitlеss. mЬеr of сorrrplеtеlysеqr.rеr.rсеd сe[lulzrr сiеs in thе topolсlgyof riЬosomal RNA nсеs havе Ьееn intеrprеtеdas еvidеnсе е n t s Ь е t w е е nd i t f е r е n ts p е с i с s .с а s t i n 8 tstrllсtiс'nand propеr unс{еrstandingсlf }9,2000). Thеrе is сlеar еvidеnсе thаt I o s ес o m p ( ) n е n tсs( ) m еf r t ' n l а w i d е v а . Diffеrеrrt аdvосatеs havе dеsсriЬеd а mЬinаtion proсеssеs'ranging from rhе jugation,transduсtion,or transformaanisms from diftЪrеntdomаins. tirnatеlyrеaсlra singlе ur-rivеrsal еntitу, r еt al. 1989) that wе fаr,or wаs not ' a n y o f i t s s i Ь l i n g s ,а p o p u l a t i o n o f е n hout thе samе pеriod. Thе,v nray havе tid ii thеy Ьесatrrеintеgrаtеdviа latеral nаnсеstoris thus onе
rdvаI-tсеs irr гhе urrdеrsrirrrdir.rg of сhеrn: ЬеtЪrеthе еmеrgеnсеof thе first livirrg " l d е di n m y s t е r ) ' L. i k е v е g е t e г i < linn а al phvlogеnеtiсtгееsarе suЬшеrgеd in t, :rndhow tlrе transition frоm thе nor-rknown. Givеn thе hugе gap that ехists ry transition Ьеtu,ееnthе prеЬiotiс synhе lаst сOmmon аnсеst()rof all ехtant еmpt to сomplеtеlydеsсriЬеthе oгigin ystеmsfrom molесular phylogеniеs. сs, Ьioсhеmistry.сеll Ьiolсlg,v,and thе nismshas сhirllеngеdmarly сlгiginalasThе viеw advoсatеd hеrе assumеs that owеd with minimal synthеtiс аЬilitiеs,
theirmаintеnanсе and rеpliсation dеpеndеdprimагily on organiс сoп-tpounds synthеsizеdЬy prеЬiotiс proсеssеs. An updatеd hеtеrotrophiс hypothеsis assumеsthat thе raw matеrial for аssеmЬling thе first sеlf-maintaining, rеpliсadvе сhеmiсa]svstеп1s\t,as thе оutсomе of аЬiсltiс syrrthеsis,rvhilе thе еnеrg), геquirеdto drivе thе сhеmiсаl rеасtions involvеd in growth irnd rеprodr.rсtion may havе Ьееn prсlvidеd Ь,v сyanamidе, thioеstеrs' glyсinе nitrilе, or othеr high-еnеrgy сomporrnds(dе Dtrvе 199S:Lazсano and Millеr 7996). Thе Ьasiсtеnet of thе lrеtеrotroplriсthеory of thе origirr of lifе is that сhе maintеnаnсе anсl rеproduсtion of thе first living еntitiеs dеpеndеd primarily on prеbiotiсallysvnthеsizеdorganiс molесulеs. As summarizеd hеrе, thеrе hаs Ьееnno shortаgеof disсussitlnaЬottt how tЬе formаtion of thе primordial soup took plасе. But lr:rvеtoo mal1y сooks spoilеd thе sсlup?Not rеally. It is vеry unlikеli,that any singlе mесhanism саn aссount for thе widе rangе of organiссompounds thаr rnay hаvе aссumulatеd on thе primitivе еa]rth' аnd that thе сitnsеquеntprеЬiotiс sollp Was formеd Ьy сorrtгiЬutionsfrсlm еndogеnoussynthеsеsin a rеduсing аtmosphеrе, mеtal sulphidе-mеdiatеd synthеsisin dееp-sеavеnts' and еХogеnous sourсеs suсh as сomеts' lтlеtеoritеs,аnd intегplirnеtarvdust. This есlесtiс viеw dfnrt>stof thеsе Ьioсhеnriсаl сompounds in thе сarmеtеoritеsof 4..5Ьillion yе:lrsago (Еlrrеnfrеundеt al. 2001). So it Ьonaсеous bесomеspiausiЬlе, Ьut ntlt provеl1' that similar synthеsis took plaсе on thе primitivееarth.}-orall thе unсеrtaintiеssurrоunding thе еmеrgеnсеof lifе' it apреаrsto us th21tthе forrrrаti
/)
74
Thе Оrigiп of Lifе lutionary transitiorr Ьеtwееn thе prеЬiotiс synthеsis of Ьioсhеmiсal сompounds and thе last сommon anсеstorof аll ехtirntliving Ьеings' Ьut attеmpts to rеduсе it havе аllowеd а morе prесisе dеsсription of thе Ьеginning of lifе, Nowadays а сеntral issuе in origin-оf-litЪrеsеarсh is to undеrstаnd thе abiotiс synthеsisof an аnсestrаlgеnеtiсpolymеr еndowеd with сatalytiс aсtivity and its furthеr еvolution to an RNA world and ultimatеly to thе DNA/RNA/protеin world сharaсtеristiс of all lifе on еarth. !Ие faсе major unsolvеd proЬlеms, but thеy aге not сompletеly shroudеd in mystеry, unsolvaЬlе, or unknowaЬlе. B|вLloGRAPнY 'W.. Allwood,A. с., I. Burсh,M. R. Waltеr,аnd B. S. KаmЬеr.2007. з.4З billion.Wеstеrn yеar.oldstrom:rt
Burkhaгdt' F., and S. Smi СЬаrlas Dаrшiп, 182 Univегsitl' Prеss. Bvеrlv' с. R.' Г). R. Lorr, l:r}'егfгоnl thе PilЬаr C a l r , i n ,M . l 9 6 9 . С h е m i , LiL,iпg Sуstеms oп tb C а s t r е s a n a ,J . 2 0 0 1 . С o п l Biсlpbуsiса Асtа 150 Сhеn, I' A. 2006. Thе еп. 15.58-15.t9. СhyЬа, С.. and С. Sagan imрасt.shoсk synthе Iiie , Nаturе З55: 12. Сlе:rvеs,I_{..l.' J. Н. Сhal rеаssеssmеntof prеЬ Оrigiпs of l-ifе апd 1 Сoopеr, G., N. Kimmiсh. CirrЬonасеous mеtес thе еarly еarth. Nс/'r Dаhnl' R. 2005. Friеdriс B i с l l t l g l 2, 7 8 : 2 7 4 _ 2 t Dilrwin, F. lE8-. Тhс Li1 Аutobi
D o u d n a , J . A . , a r r dТ . R . Nаturе 418 222_22 Еghсl|m,М.' o. Buсhard (PNA): oligonuсlеo thc Аmеriсап Сhеm P., D. P' G Еhrеlrfгеr'rr-rd, Е х t г . r t е г г е s t r li nl m i СI typе сitrЬon.lсес Sсiепcеs USА 98: 2 ЕiсhЬеrg' .|.,Е. Shеrwoo synthеsеsundеr pla Е u t ' l t t l i t t lп0 : 2 2 | _ Еsсhеnrnosеr, ^. 1999. ( 2t 18-2\24. 2004. Thе TNA origilts сlf 1'ife апd F е г г i s ,J . P . 2 0 0 f . М o n t
Тhе ()rigiп сl| Lifе
otiс synthеsisof Ьioсhеmiсal сomall ехtantliving Ьеings,Ьut attеmpts : dеsсription of thе Ьеginning of lifе. геsеarсhis to undеrstand thе аЬiotiс lndowеdwith сatаlytiс aсtiviгy and its ultimatеly to thе DNA/RNA/protеin /е faсе ma|or unsolvеd prоЬlеms, Ьut еry' unsolvaЬlе,or unknowablе.
n d B ' S . К a m Ь е г2. 0 0 7 .з . 4 3 Ь i l l i o n Austrаlia: Есosystеm-sсalе insightsto h 158 198-227. statusrерort.Еаrth PIапеtаrуSсiencе 4. Impaсtmеltingof frozеnoсеanson in of lifе. Prсlt:ееdiпgs of thе Nаtioпаl ;0. o, H.J. Сlеavеs,R. М. Hazеn,аnd rr thеoriginof lifе on eartЬ.Sсirпсе :vеаlеdnеw waysto studythе оrigins of firstЬiоmоlесu|es. Sсiепсe296: Иillеr ехpеrimеnt. Sсiепсе3ОО:74 5-7 46. Thе stаЬilityof aminoасidsat res.Оrigiпsof Life апd Еuolutioп of d T' Stеitz.2000.Thе сomplеtеatomiс r 2.4A rеsolution. Sсiеltсе289: 905-920. .Гrепds сtingan RNA world. iп Сеll с>.2007a. Vеryеаrlystаgеsof Ьiologiсаl сommonanсеStor of thе thrееmajor сеll iиtioп апd Sуstemаtiсs 38 361-З79. rge|'2007Ь.Protеindisulfidе lrпrophily:Wаsthе last сommon of МolесulаrЕuсllцtioп65: 296*3ОЗ. H. Konig,and K. o. Stеttеr.1984. sпrokеr', сonditions. . i a Io r g a n i с o m p o u n disn m е t е o г i t е s . (. Klеppе,М. vаn Krаnеndonk, F. J. . 2002.Quеsrioningthе еvidеnсеfоr ). ry: A non-hypеrthеrmophiliс anсеstor ].Summons. 1999.Arсhеanmolесulаr сiеtlсе 285 1033-10з6.
Burkhardt,F', аnd S. Smith, ес]s.|994 . А Саlспdаr of tbc Сtlrrеsprlltdепсеtlf СhаrlеsDаru'iп, 1821-1 I]82, \Yith Suрplепtепt. Сzttл|lridgе:()апrЬridgе UnivеrsitуPrеss. .Woodеll, Bvеrlv,G. R., D. R. l-сlwе,J. L. and Х. Хiе. 2002. An Arсhсan irrrpасt laуегfrorrrthе РilЬага аnd K;rаpvaаIсr.аtolls.Sсiепсс 297: |32.5_1З27. Сalvin' М. 1969. Сhеmiсаl Еun Prеss. 2001. Сornparativt.gеllollliсs and lrioеnеrgеtiсs.IJirlt-llimiсаеt Саstrеsаna,J' Biop|lуsiсаАсrа 1.506:|47_162. Сhеn,I. A. 2006. Thе еmеrgспсеof сеlls с1uringtl.rеtlrigin of |ifе.Sсiепсе 374 1558-1-5-59. Сhvba,С., апd С. Sаgаn. l992. ЕrrdоgеnOusproduсtioll. ехOgеl)tlllsdеlivеrv rrrrd impaсьshoсksynthеsisof organiс пlolесulеs:An ilrvеntOrVfсlг thе origins сlf |ife.Nаtt,trе 355: 12.5_1З2. С i е а v е sH, . . l . ' J . Н . С h а l п r с r s .А . [ , a z с а n t lS' . L . N , I i l l е ra, r l d J . L . t ] а d а . 2 0 0 8 .А rеassеssmеnt of prеЬitltiсorg:rrriсsynthеsisin rrеutrаlp1anеtirтvetmсlsplrсrеs. Оrigiпsof Lifе апd Еurllttti,опоf thе Birlsphсrе З8 l0.5_11.5. Сooper,C., N. Kimmiсh, W. Bеlislе'.].Sаrilrаr.rlr' K. BreЬlrarrr,aIlсl L. GаrrеI.2001. СarЬonaсеousпrеtеoritеsаs a sourсе of sugаr-rеlirtесl сlrgаrriсссlmpouridsfor thе еаrly ea|t|1. Ndturе 4l4: 879_88з. Dahm,R. 200.5.FriесlriсhМiеsсhсr аnrl tlrе disсovеrv оf Dп.A. Dcrсlсl1llltспtll Blolo3r'2-8:2-4-28Ь. Darwln,F. ]887. Тhr Lifе апd Lеttеrs rlf Сhаrlеs l)апuiп, ]псlttdiпs аlt Аut o bi ogr а1lh i са l (',hаp tеr, Lorrdoll : M urrir1.' Dеamеr,D. W., arrсlR. M. l)irshlсy.l9tt9. Arnрlriphiliс сtlnlpоurrсlsсlf tlrе Мurсhison сarЬonaсеousсhondritе: SurftrсерropеItiеsanс1mспrЬr:rtrе formation.()rigiпs of Lifс апd Еutllиtion rl|-thеBirlsрllеrе 19 21_З8. dе Duvе,с. l995. \/itаlDLrst:I-it'.е аs а Соsmiс Impеrаtit'c.Nец, York: Birsiс Books. -. 200з. A rеsеаrсhproрosаl oп thе ()riginof |ifс. Оrigills o| I-ifc апd Luolullo1l
О | I п е 1 5 l | ) s D l J с , 1 '. i i : ) . ) y _ ) , / Z t .
DеIаvе,L., A. Bесerrir,апd A. Lаzсаllсl.2004. Тlrе rlаturеоf гhс lаst сопmolt anсеstor.In L. RiЬas dе Pсluplirnаr, еd.,Thе Gепеtiс (,,odеапd tbе origiп of Lifе, 34_47. Gеrrгgеt. 977. Сr.аrlаmiсlс rrlеdiateсl svnthеsеs undеr plаusiЬIсрriIrritil,сеirrth с()llditiotts. '|rlttrпаltlf Мolесttlаr Еuolutioп |0:221-230' Е s с h е n m o s еАr ,' .1 9 9 9 .С h е m i с l r lе t i r l l t l g r ' o n f r-rсIеiсасidstгttсturе.Sсiепсе?81 2118-2124. --. 2004. Thс TNA-family of nuсJеiсасid svstеtns:Рlopегtiеs апс1glrosресts' Оriginsof Lifе аlld Еurlltttioпof thе Bitlsphcrе З4:2-a7-З06. Ееrris,J. P.2002. N{оnгrnorill
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Thе Оrigiп of Liiе LaЬoratory dеmonstrаtion of potеntial stеps in thе origin of thе RNA world. Оrigiпs of Liiе апd Еuсllиtiсlпсlf thе BiospЬеrе З2:311-332. Fеrris, J. P., P. D. Jоshi, Е. I{. Еdеlsоп, аnd.|' (}. Lаrvlеss. l978. HСN: A plausiЬlе souгсе оf purinеs' рyrirnidinеs, аnd aminо aсids on thе primirivе ..afih,.lourпаl оf Мoleсulаr Еuolutioп 1'1':29З.311, Fortеrге' P.2002. A hot storv from с
2006. сr-Hydroхyl аnс1с origin-of-lifе ссlnditiоns'Sсr Islаs,S., A. N4. Vеlаsссl'A. Bесег and tЬе origin of lifе. In Сhr' апd lJillсhеlпistrу of F,хtrеlп J o v . с , G . Г . .2 ( ) 0 ] . Т h с r r r г i q u i t Kаnavarioti, А.' P. A. Mсlnnаrt] faсil itаtе nOnеnzvtтlatlсlltlс K : r s t i n g J, . F . l 9 9 З а . Е : r r I yе v t l l r GrееnЬегg, С. Х. ]Vlеrlсloz Lifе's Оrigiпs, 119_176' Dt PuЬlishеrs. 1 9 9 3 Ь . Е а r t l r ' sе a r l v а t п K е I l е y ,D . s ' . . ] . A . K a г s r l r l ,D . K Buttегfiеld' М. D. l,illеy, Е. Rivizzigntl' and thе AT3-60 vеnt fiеlс] llеar thе Мiсl-Atlа KolЬ, V. M.,.1. P. Dworkin, and wоrld: Tlrе prеЬiсltiсsvnthе Е ul llu t k l tt .]t]: .549_5.57. Kozlсlv, I. A., L. Е. orgеl, and P trаnsmittеd Ьy an aсhiral pt llttcrпаtitlllаl Еditirlп З9 4. Кltmаr, R' lr., and r\l. Yаrus.20 B io с h еmi strl' 40 : 69 9 8-7 0( l-arr:rldе,R.' N,I.P. RoЬегtson,а r i Ь o s е ; r l l dl l t h е г s t t ц l r s - t ; l thе Nаtitlпаl Асаtlеtпу rlf St Lаzсano, ^. 1997. Тhе tеmpo aг S. Bowvеr' lrnd D. \Vсrthinl thе Sеаrсh for Lifс iп thс Ul Lаzсano, A., G. Е. Fсlх, аnd J. С сlf еаrly Aгсhеtrn. еr,oluti
Thе Оrigiп of Lifе ps in thе origin сlf thе RNA worlсl. ,hеrе32:311-З32. i. Lаwlеss.t978. НСN: А plausiЬlе aсids on thе рrimitivе eartЬ.lОurпаl е gеnomiсs:Rеvеrsеgyrasе is thе епds iп Gепеtiсs 18 2.36_2З7. э, аnd М. Duguеt. 2000. Rеvеrsе гensfеo r f t t r h е r m . l а d a p t а t i otnr а i r iсs 16 152_154. l, A. G. Сhristy, Nl. J. van [-assеmЬlеd siliсa.сarЬonаrе lssils.Sсle,сs 302: 1194-7197. and S. A. Bеnnеr.2,008.Irrfеrringthе :hеЬаsisof rеsurrесtеdpr()tеrns. .liansky,N. M. Rutkеvitсh, and A. S. J faсtor-depеndеnтs1.stеmsof hiа сoli riЬosomеs.Jourпаl of d . N а t и r еЗ | 9 : 6 1 8 . IапеtСhапgе 1: 35-55. nсеstor'tЬе univеrsаl lifе-trееаnd llаr Мiсrolliоlog1'38: |77-|85. i. J. Bowman' B. J. Bowman' М. F. , J. Konishi, K. Dепda, and ar l{+-AТPаsе:Impliсations for thе :ionаl Аcаdamу of Sciепсеs USА 86: ,artеn.1995. Thе еffесtsof hеavy :ion of lifе-а nеw look аt thе иtioп of thе Biosphеrе 25:78_83. laсtеriа likе it hot. Nаturе 451 m of mеmЬranе topology. Nаturе
024.
stak.200З. Ехpеrimеntаl m.ldеls
2006. с-Hyсlгсlхyl alrd O(-аminoасids unс]егp
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78
Tbe Оrigiп of Lfe .l 955. Produсtiсln of somе
S l е е p ,N . Н . , K . J . Z a h л r c есosystепls by lаrgе ar S o w е r l ' y .s . . I . 'С . M . М о r аdsогptior.rof adеninе Spirin,A. s. l986. Rlbosс Bеn jamin/Сummings' Springstееn, G., and (]. F. rillоsе |гсlm lr prеlliог 9578-95 8з. Stoks, P. G., аnd A' W. Sс 282 709-710. 1981. Nitrсlgеn-h mесhanisms of foгmа l982. Bаsiсnitrog G есlсhimiса еt Ссlslпt S t r е с k е r ,A . 1 8 5 0 . U Ь е r d i Glyсoсoll homсllсlgе Tеhеi, N4., B. Franzеtti,M 2002. Thе sеarсh foi maсromсllесulеs.Ехlr Tian, F., o. Toсln, A. Pаvl аtmosphеге. SсiепссЗ Тiсе, М. M., аr.rdD. R. l-r Мyr-old oсеan. Na/и . Uеno, Y., K. Yilmасlа,N. from fluid irrсlusions] Nаtltrе 440:5l6-.5 l9 van Zuilеn, N4. A.' A. Lеp thе еаrliеst trасеsof li W;iсhtеrsh:iusеr,G. 1988. mеtirЬolism. Мiсrоbir \й7аng,Х. s. l998. StаЬili сonditions. PhD thеs С i r I i f t l r n i . lrt 5 : l n D i е W е t h е г i | |G, . W . l 9 9 0 . F о Sсieпсе 1t]:20.5-2.56 .!7hitе, R. H. 1984' Нydrс impliсation for lifе аt \}/ildе, S. A.' J. \W.Vаllеy, dеtritаl zirсons foг th Gyr ago. Nаturе 409 Yuasа, S., D. Flory, B. Bas сlthеr hеtеroсyсliс соr Мllleailаr Еuсllutiolt ZaЬn],е,K., N. Arndt, С. t 2007. Еmсrgеt"tсеof с ZЬang, B., and T. R. Сес| riЬсlzymеs. Nаturе 39 с ZllЬaу, G. 1998. Str.rdies Lifе апd Еuсllutiсlп ,,
Thе Оrigiп of Life npоundsundеr роssiЬlеprimitivе СhеmiсаlSoсiеtу 77:2З51_2361 . amino aсids Ьy еlесtriсdisсhargеs. 89. ltiс сhеmistry. N аtttrс StruсturаI hot springsаnсl tlrе origin of litе. n of lifе-diс] it oссur аt high t t i о п4 1 ' : 6 8 9 _ 6 9 2 . o m p o u n ds y n t h е \ i \u n t h е p r i m i г i v с ). Pеptidеnuсlеiс асids rathеr thаn :сuIе.Proсеесliпgstf thе Nаtklпаl LdT. Stеitz.2000..Гhеstruсturаl Ьasеs lеsis. Sсiепсе 2.89: 92О_9З0. nan.2000. Lirtеralgеnе transfеr and , 405 299_3О4. s: Thеorеtiсаlintroduсtion. Оrigins оf 27-234. lnium сyanidе.Biосhеmiсаl аnd 407412. oсhеmiсaiсompounds rln thе pr"rrinеs undеr possiЬlеprimitivе еarth nidе. Аrсhit,еs of Bioсbaпtistrl' аnd d S. A. Bеnnеr.2004. Borаtе minеrаls S c i е n c е2 9 3 : 1 0 5 6 _ 1 0 5 8 . --.]_786. ifе. Pеptidеs20: tlrе iron-sulfurworlсl аnd its rеlеvanсе г i с s y n t h е s i i' r tl t г r t t o s p h е rсеos n г . r i r t i r l g шl of Мolесulаr Еutiutklп !9: . L,аnd S. x,IoorЬаth'2002. Tungstеn h о s е ds е d i m е n t fso r е а r | vm е г е r l r i t е 03-40.5. R . К г i ч h n . r m r r г г' h. rl r r dA . nuсlеiсaсid strllсгurе:Тhе сx. stem.Sсiепсе290: |347_1351, rrсhaеanApех сhеrt:Nеw еvidеnсе -646. sotopiс еvidеr-rсе foг miсroЬiа1 эr'.l.Nаtur е 410: 7 7-8 |. l thе oгigin of rlrgапiсссlпrpoundsin :l Еuolutioп rli tllе Birlspbеrе 2О: с s y n t h е \ i ds u r i r r gf l u i d m i x i n g i r l ,siсаIRеsеаrсh10З: 28.513_28528. эхidе сyсling and irnpliсationsfсlг hуsiсаl Rеscаrсh 106: 1з7з-1з99.
S l е е pN , . H . ' K . J . Z а h п l е , J . F . .K а s r i r r g sа, r r d H . J . M t l r o r v i t z . 1 9 8 9 . A n n i h i l a t i с l пс l f есosystеmsbу lагgе ilstеroid iIтpасts On thе еаIly еarth. Nаturе З42:139_|42.. SowеrЬy,S. J.' с. N,l.Mrirth, and N. G. Holпr.200l. Еffесt сlf tеmpеratuгеOn thе аdsorptionof асlеrrinе.Аstrobirllogl 1: 481487. Spirin,A. S. ]986. Rillоstllпе Struсtttraаltd Pкltеiп tsirlsуnr|2с'i''Меnlo Pаrk, СA: Bеnjamin/Сum nl ings. G.' arrсlG. F. Joyсе. 200,1.Sеlесtivеdеrir'irtiz:rtiсln аnd sеquеstrlltiоnOf Springstееn, riЬosе frсlпl a prеЬitltiс mtх. Jсlurп,tl
79
Narrative
Paleontologyand the History of Life Michael Benton And out of the ground the Lord God formed every beast of the field, and every fowl of the air; and brought them unto Adam to seewhat he would call them: and whatsoeverAdam calledeveryliving creature,that was the name thereof. G e n e s i s2 : 1 9
Peoplehave always been astoundedby the diversity of life, although perhaps in different ways. In prescientifictimes farmers saw how their crops and livestock were merely part of a much larger richnessof life, ar-rdpeople have alwrrys striven to understandthe complexity and arrangementof living things. From Aristotle to Linnaeus,scienristsatremptedto catalog life and to understand where it had come from. During the eighteenth century it becameclear to all savantsthar the earth had beenpopulirtedformerly by strangeand marvelous creaturesthat had since becomeertinct. Bv 1820 some rough picture of the successionof floras and faunas through geological time was beginning to emerge.Charles Darwirr, during the voyage of HMS Beagle in the early 1830s, becameincreasinglyconvincedthat life was more diversethan he had imagined-every island he visited sported a new crop of plants and animals. He saw the lateral (geographic)and vertical (historic) links between species and realizedby 1837 that speciesrvereall linked by a great tree.The tree concept made it clear why speciesthat in his time were geographicallyclose should also be genealogicallyclose. Further, the tree conc€pt made it clear why the fossil mammals he found in Argentina should be similar to the living mammals of the region. This essayaddressesfour concepts:what we know about the sequenceof the history of life, how life has diversified through time, how speciation occurs, and how good (or bad) the fossil record is as a sourceof data on the history of life. These were all issuesthat concernedDarwin (1859), and they concern us still today.
80
There are many ways to re( nren)'fvpical examples,Bent o f l 0 s t a g e sf r o n r t h e o r i g i n
l.The origin of life.The tt fossil recorcl,some 3.6c e l l sw e r e p r o b a b l y l i k e but they lived in the irbs 2. Eukarycttesttnd the oriS nucleus,are reporteclfrr ar.rdhencepresum:rblya o f s e x u a lr e p r o d u c t i o n possibly no eukar,votes, mrrterialancl reconrbin 3. Multicellularity. The hr billion-950 nrillionyea m o l e c u l a re v i d e n c et h a t s o m e 1 . 2 b i l l i o n y e a r si 1 d i r e r s i f yt h e f u n c t i o r rrs 4 . S k c l e t o n sN. l r n y l n r m a skeletonsabout 545 rni Phanerozclic,during thc are known from many I d i v e r s i t yo f p l r v l a r c p r e skeletonsu,ereaccluire skeletonsclearly ofierec g r o u p s t o e n t e rn e w l i f c 5. Pretlation Perhapslink protective outer shells,r predato rs, tnacrosco1't ic strategiesto feed on the prey becamea st:rndar 6. Bictlogical reefs. Reeis l been made from a broa polychaeteu,orms in th l.ate Cambrian and alg tabulate corals in the O groups of algae,sponge through time, but reefs scleractinian c o r a l s .R e rnrrjor physical geograp habitats for life. 7 . Terrestrialization. The t huge arra,vclf new life z
Pаlеoпtolrэg1' апd thе Нistсlrу of Lifе
Naгrativе
d thе History
rnrеd еvеry Ьеast of thе fiеld, and unto Adam to sее whаt hе would еvегy living сrеaturе' tЬat wаs thе
G е n е s i 2s : 1 9
е divегsityof lifе, although pеrhaps гmеtssаW how thеir сrops and livеriсhnеssof lifе, and pеoplе hаvе aly and arrangеmеntоf living things. lmptеd to сatalog lifе and to undеrе еightееnthсеntury it Ьесamесlеar :lаtеd formеrly Ьу strаngеand marкtinсt.By 1820 sonrе rough piсturе эugh gеologiсal tirnе was Ьеginning ,оyagе of F{МS Beаgle in thе еarly rt lifе was morе divеrsе than hе had l a nеw сrop of plants and animals. i с а l ( h i s t t l г i сl)i n k s Ь е t w е е ns р е с i е s linkеd Ьy a greattrеe. Thе trее сonris timе wеrе gеographiсally сlosе hеr, thе trее сonсеpt madе it сlеar ntina should Ье similirr to thе livins tаt wе know аЬout thе sеquеnсеof l through timе' how spесiation oсэrd is as a sourсеof data on thе hislnсernеd Darwin (1859), and thеy
.Гhеrе аrе many ways tO rес()untthе stсrrytlf thе history of lifе. As
8,l
82
Pаlеoпtrllсlgуапd thе Historу of Lifе PrесamЬrian suссеssions,and soils imply lifе on lalrd. Buгrowing animаls arе known from ()rdoviсiаn soils, whilе mаny smаll vasсular plants and artlrropods arе known from thе Siluriаn. Land plants Ьесamе larger z.rndmorе divеrsе in thе Dеvoniаn, аnd tlrе divегsitу of land-dwеlling,animals ехpandеd to inсludе Worms' mсlllusks,many morе arthropсldgroups, and vеrtеЬratеs. 8. Тrеes аnd fсlrеsts.Just as rееfs in thе sеzrarе gеographiсally suЬstantial Ьiologiсal struсturеs,so too arе forеsts.Thе first trееs il-t thе Devoniаn Wеrе largеly isсllatеd,btlt massivе forеstsdеvеlopеd in thе СarЬonifеrous, with trееs up to 20 m tall. Not only did variсlus land-plant groups divеrsify аs trееs' Ьut othеr plants and animals that ехploitеd thе nеw habit:rtsсrеatеd Ьу thе trееs аlsо divеrsifiеd. 9. Flight. A ftlrthеr ехpansion of есosp;rсеwas markеd Ьy thе origin of flight. Insесtsarosе in thе Еarly Dеvonian, Ьut thе first truе flyеrs wеrе CаrЬonifеrous in agе. Inseсtsdominatеd thе skiеs from thеn on. Thе first flying (gliding) vеrteЬratеsarosе in thе Pеrmiiln and Triassiс, whilе powеrеd flight in vеrtеЬratеsarosе at lеast thrее timеs' in ptеrosaursin thе Latе Triassiс, in Ьirds in thе Latе Jurirssiс, аnd in Ьats in thе Tеrtiary. Thе origin of соnsсioust-tеss 10. Ссlnsciсlusnеss. in humаrrsis muсh dеЬatеd.Is this a fеatr'rrеoi Homсl sсtpiепsalonе, and henсе pгеsеnt only in thе past 200,000 vеars or so, or did еarliеr spесiеsof Hсlmo, or еvеn pгесursor gеnеra suсh as АustrаlopithеcИs afld Ardipithесus' possеssсonsсiousnеssas mltсh as 2 tn,сonsсitlusnеss)and major ехpаIlsitrns in haЬitats oссupiеd Ьy lifе (rееfs,tеrrеstrialization,trееs, flight). All 10 arе . doсumеntеd to a gгеаtеrоr lеssеrехtеnt in thе fossil rесord. In a morе Ьiologiсаlly oriеntеd prеsеntation' .|ohn Мaynard Smith and Ебrs Szathmarу (995) idеntifiеd еight major stеps from thе с>riginof lifе to human soсietiеswith languagе: 7. Rеpliсаtiпg molесules. Thе first oЬjесts with thе propеrtiеs of multipliсation, vаriation, аnd hеrеditywеrе probaЬly rеpliсating Inolесulеs,siпrilаr to RNA Ьut pеrhaps simplеr and сapaЬlе of геpliсation Ьut not informationаl Ьесatrsеthеy did nOt spесify othеr struсturеs.A populaг viеw is thаt RNA сamе Ьеforе DNA Ьесausеit саn aсt Ьoth as il gеnе and an еnzymе' viеrvsеnсapsulatеdin thе tеrm RNА шorld' If evrllutiorrwerе to proсееd fuгthег,it rvas nесеssary that diffеrеntkinds of rеpliсatingmolесuIеshould сoopеratе,еaсh pгoduсing еffесts that hеlpеd thе rеpliсаtion of сlthеrs.For this to hаppеn, populations of molесulеshad t
2. lndеpeпdепt rеpliсс or gепеs' аrе linkеd сlrromosomе pеr се wlrеn onе gеnе is rе Pгеvеnts сolllPеtitio с()()pеratiOnon thеI 3. RNА аs gе|1еапd ei laЬor bеtwееn two ( that storеаnd trans rеaсtions and form musсlе, tеrrdоn,hai Ьotlr funсtions. Thе :rnd pгotеin rеquirеr sеquеnсеdеtеrminе 4. Еukаrусltеs апd org h:rvеa singlе сirсtllа с у a n с l Ь a с t е г i a( Ь l u е сontains rod-shapес struсturеs сallеd orд Тlrе еukaryoсеs inсlr сеllеd AmoеЬir and 5. Saхuаl rеproLluсtior i n d i v i d u a l sa r i s е a s . two. In nrost ешkarу сеll division may Ье rvhiсh а nеw individ gаmеtеs' produсеd l 6. D i ffеreпt iаtе d сe lls. сеlls сlf onlу OI1еor pla alтlong anirrrаrls, kinds of сеlls,suсh . Еасh individuаl,thе inforrтation (trvo in pr
l,аlеoпttllogу,аndthе Histor1,of LiIa ; imply lifе on land. Burrowing ln soils,rvhilе mani, small vаsсulаr from thе Silurian. Lаnd plarrts thе Dеvoniаn, and thе divеrsity of l inсludеwoгms' rr-rollusks, mаny Ьratеs. hе sеа аrе gеographiсally c too arе forсsts.Tlrе first trеes in l, Ьut massivеforеstsdеvеlopеd in o 20 m tаll' Not сlnly did vaгious s' Ьut othеr plants and animals :atеdЬу thе trееsalso divеrsifiеd. spaсеWas mаrkеd Ьy thе origin of ]vonian, Ьut thе first truе flyеrs ;dorninatеdthе skiеs from thеn on. s aгosеin thе Pеrnriаn and ]rtеЬratеsarosе at least thrее iassiс,in Ьirds in thе Latе Jur;rssiс, сiousnеssin humans is muсh sаpiепsаlonе, аnd lrеnсеprеsеnt ;o' оr did еаrliеr spесiеsof Нсlmo, \ustrаlop itЬесus aлd Аrdip ith eсиs, 2 ttl 4 million yеars ago? сrеatеthings and to modify thеir rе pгofound impaсt Ьumans irге or Ьiologiсal innovаtions (lifе, sех, r s с i o u s n е s sа)n d r n , jro r е х p i r n s i o n s rialization,trееs' flight). All 10 аrе n thе fossil гесord. ltаtion' John Mayrrard Smith and ajor stеpsfrom thе origin of lifе to jесtswith thе propеrtiеs of J i t у w е r е p r о Ь а Ь l yr е p l i с a r i n g raps simplеrand саpaЬlе of |есatlsеthеy did not spесify othеr lNA саmе ЬеforеDNA Ьесausеit mе' viеws еnсapsuiаtеdin thе tеrm roсееd furthеr, it was nесеssary rolесuiе should ссl
2. Iпdеpeпdепtrepliсаttlrs.In ехisting organisms,rеpliсating molесulеs, or gепеs' arе lirrkеd togеthеr с'nd tO еnd to forлl сhromoso|7'еs (а singlе сhromosomеpеr сеll in пrсlstsimplе оrganisnrs).This has thе еffесt thаt whеn onе gеnе is rеpliсatеd,аll arе. This сoordinatеd геpliсation prеvеntsсonrpеtiti()tlbеtwееngеnеs within a сompаrtmеnt and forсеs сoopеrationсln thеm, sinсе if сlnе fails, thеy all fail. з.RNА оs gеnе апd eпzl,mе.in modеrn organisnrsthеrе is a division of iаЬor Ьеtwееntwo сlassеsof mоlесulе..писleiс', ссids (DNA and RNA) that storе and transmit information aпd protеiпs thаt сatalyzе сhеmiсal rеaсtionsanсl form rnuсh rlf tlrе struсturе of thе Ьody (for ехan-r;llе, musсlе,tеndсln,hair). Pеrhаps originirlly RNА molесr.rlеs pеrfсlrmеd Ьoth funсtions. Thе tгansition frсlm an RNA rvсlrld to a wсlrld of DNA and prrlrеinrеquirеd thе еvсllutionof thе gеnеtiсссldе,r,vhегеЬyЬasе sеqtlеnсd е е r е г m i n е sp r о t е i ns t г u с t u r с . 4. Еuktlrусltеsапd orgаllеllеs.Prсlkаrуr;tсslaсk а nuсlеus аnd usualry hаvе а singlе сirсulаr сhrtrпrosomе.Тhеy irrсlLrdеthе Ьaсtеriа аnd сyarroЬaсtеria(Ьluе-grееnalgaе).Еttkаrуotеs havе а nuсlеus that сontainsrod.shаpеd сlrromosсlmеsanс]usuallу othеr iгltraсеllulаr г strttсtllrеsсa||еdсlrgtlпe//es' inсludirrgmitoсhсlndria .rгrdсhlоroplasts. Thе еuk:rryotеsinсludе all othеr сеlluIar organisnrs,fronr thе singlесеllеdAmt>еЬit,.lnd Сhlаm1,dtlпrlпаsttp to hul.nans' 5. Sехuаl rеprodисtiot;.In prokaryotеs аnd in somе еukагyotеs'lrеw individuals arisе as аsех|tаlсloпеs Ьy thе divisiсln of a singlе сеll into trvсl.Iп most еЦkar\'otеs,in с()iltrastithis prсlсеssof multipliсаti
8l
Раlеoпtoklgу апd thе Historу of Life 8. Primаtе sociеtiеs, bumап soсiеtiеs, апd thе origiп of lапguаge. The dесisivе stеp in thе trаnsition from apе to human soсiеty was proЬаЬly thе origin tlf languagе.In many wаys human languagе is likе thе gеnеtiс сodе; information is storеd and transmittеd,with modifiсatron, down thе gеnеrations.Сommuniсation holds soсiеtiеstosеthеr and allows hunrans to еsсapееvolution. Мaynard Smith and Szаthmiry (1995) arguе that all Ьut two of thеsе еight transitions wеrе uniquе, oссurring just onсе in a singlе linеagе.Thе twсl ехсеptions arе thе oгigir-rsof multiсеllular organisms, whiсh happеnеd thrее timеs, and of сolonial animals with stеrilе сastеs'whiсh has happеnеd many timеs. Had any of thе othеr siх trаnsitions not happеnеd, and thаt inсludеs thе origin of lifе itsеlf (numЬеr 1), thеn wе would not Ье hеrе. Thаt only two of thе еight havе dеmonstraЬly happеnеd morе than onсе spеаks against Simon Сonway Morris's (2003) thеsis that с()nvеrgеnсеtn naturе is so prеvalеnt that humanity and mаny othеr еХtаnt stylеs of lifе аrе virtually inеvitаЬlе.
Divеrsifiсation NUМвЕRs Lifе is astonishingly diversе today, with еstimаtеsrаnging from 5 milliсln to 100 million spесiеs, Ьut pеrhaps' п1OrеsoЬеrly, homing in on a 6gurе Ьеtwееn 10 million and 15 million spесiеs(sееthе mаin еssay ..Thе Pattеrn and Proсеss of Spесiation'' Ьy Мargarеt B. Ptасеk and Shala J. Hankison in this vсllumе).Of thеsе,fеwеr than 2 million hаvе Ьееn rесognizеd and dеsсriЬеd so far. It is сommonly assumеd that iifе today is morе divеrsе than it has еvег Ьееn.This sееmsin somе Ways oЬviсlus,Ьut it сould aIso Ье сonstruеd as еxtraordinary vanity, somеhow akin ttl thе viеw that all еvolution was plannеd to lеad to human Ьеiggs, аnd that somеhow this instant in thе vast span of timе is thе most importаnt of аll. Howеvеr, it is еvidеnt that all living organ. isms and ali organisms known as fossils dеrivе fгom а singlе сommon anсеstor (on thе Ьasis of thе еvidеnсе of shаrеd сomplех сharaсtеrs,sr-rсhas thе DNA-RNA systеm of inhеritanсе,homеoЬoх gеnеs,and thе likе). That сom. mon anсеstor, thе singlе spесiеs that gаvе risе tсl all of lifе, ехistеd somе З.5_з.8 Ьillion yеars ago. But how many spесiеshavе еvеr ехistеd? Biologists аnd palеontologistshavе triеd а rrumЬеrof linеs of rеаsonlng to еstimatе thе totаl numЬеr of spесiеs thаt havе еvеr ехistеd. Pеrhaps living Ьiodivеrsity is only 24Y" of thе total that hаs еvеr ехistеd' as is suggеstеdЬy thrее linеs of rеasoning (Sеpkoski 19921Мaу 1994): 1. Thе first argumеnt is Ьasеd on an assumеd pattеrn оf spесiеsdivеrsity inсrеasе аnd thе known avеragе duratiсln of a spесiеs Ьеforе it Ьесomеs еxtinсt. If spесiеsdivеrsity inсrеasеdroughly linеarly (additivе modеl) through thе Phanеrozoiс' аnd аvегagеspесiеsduration is 5_10 million
yеars' thеn living spе thе past 600 million 2. Thе sесond argumеn past 450 million yеa 1 0 m i l l i o n y е a r s ,a n d tеrrеstrial spесiеs tha 3 . Т h е t h i г d а r g u m е n ri s p е с i е so Г f o s s i l m а r i numЬеr of known m; Allowing for nonprеs lossеs,this сould alsс spесiеs (Sеpkoski 19!
In thеsе disсussions it has саtion foг mасrosсopiс o сroЬеs arе ехсludеd Ьесаu and vеry littlе is known of еvеr ехistеd arе alivе todа to 750 million spесiеs rn t
МoDЕLs
Biodivеrsity, thеn, has ехp todаy. But how? Thеrе ar thеsе сan Ье ехprеssеdin t a straight linе, an ехponеI ruptеd inсrеasе (Figurе 1; i m p o s е d ( F i g u г е1 B ) . The liпеаr modеl rеprеs Ьеr of nеw spесiеs in еасh o t h е r s i s a n е t i n с r е a s е ,i . еvolutionaгy ,Ьrаnсhing m timе spесiation гatеs havе larly at a ratе suffiсiеnt to in rhе гаtе of еvolution in t o t а l n u m Ь е r o f s p е с i е si s t h е Ь o а r d г е m a i n s f i x е d ;h o r p r o Ь a Ь i l i г yo f s p l i t t i n g ally Ьееn rеjесtеd as imprс The eхpoпeпtiаl model i tion. If spесiation and еxt will Ье rеgular douЬling < of еvolution at thе lеvеl of nеlltial ratе of inсгеasе ol modеl has Ьееn appliеd to thе divегsifiсation of lifе ir
Pаlеoпtologу апd thе Historу of Lifе пd thе origiп of lсlпguаgе. TЬe pе to human soсiеtywas proЬaЬly ; human lаnguagеis likе thе gеnеa n s m i t t е dw ' i t h m < l d i сf iа t i o n , cn holds soсiеtiеstogеthеr аnd гguеthat all Ьut two of thеsе еight lсе in a singlе linеagе.Thе tW()еxorgаnisms,whiсh happеnеd thrее ] сastеs'whiсh has happеnеd many ls not happеnеd,and that inсludеs е would not Ье hеrе. That only two :d morе than onсе spеаks against e t с o n V е r g е n сiеn n а t u r е i s s o p r е ехtant stylеs o{ lifе arе virtually
yеаrs,thеn living spесiеsrеprеsеnt2-4"Ь of thosе that ехistеd duгing thе past 600 milliоn yеars. 2. Thе sесond aгgumеnt is Ьasеd on thе divеrsifiсationof insесts ovеr thе past 450 million yеars. If thе avеragеduration of an insесt spесiеsis 10 million yеars, and thе group has divеrsifiеdlinеaгly, thеn 5% of all tеrrеstrialspесiеsthat еvеr еxistеd arе alivе today. 3. Thе third argumеnt is Ьasеd on prеsеrvaЬilityof fossils. Somе 250,000 spесiеsof fossil marinе animals havе Ьееn namеd, similar to thе total numЬеr of known marinе animal spесiеsalivе today (200'000). Allowing for nonprеsеrvationof soft-Ьodiеdorganisms and othеr lossеs'this сould also rеprеsеntonlу 2_4Y" of thе total numЬеr of fossil spесiеs(Sеpkoski 1992). In thеsеdisсussionsit has only Ьееn possiЬlе to еxaminе pattеrns of divеrsifiсation for mасrosсopiс organisms, that is, typiсal plants and animals. MiсroЬеsаrе ехсludеd Ьесausеit has Ьееn hard to еstimatе thеir сurrеnt divеrsity, and vеry littlе is known of thеir еarly fossil rесord. If 24% of all spесiеsthat еvеrеxistеdarе alivе today (10-1 5 million), thеrе must hаvе Ьееn somе 250 to 750 million spесiеsin thе past. MoDЕLs
)Stimatеs ranging from 5 million to ioЬеrly, homing in on а figurе Ьеее thе main еssay..Thе Pattеrn and aсеk and Shala J. Нankison in this tavеЬееn rесognizеdand dеsсriЬеd 'y is morе divеrsе than it has еvеr rut it сould also Ье сonstruеd as еxr,iеwthat all еvolution wаs plannеd tow this instant in thе vast span of :r, it is еvidеntthat all living orgЭn|еrivеfгom a singlе сommon anсеs:d сomplеx сharaсtеrs'suсh as thе boх gеnеs,and thе likе). That сomvе risе to аll of lifе, ехistеd somе spесiеshavе еvеr еxistеd? d a n u m Ь е гo f l i n е so f r е e s о n i n gt o t havе еvеr ехistеd. Pеrhaps living ' has еvеrехistеd,as is suggеstеdЬy tlaу |994): ;umеdpattеrnof spесiеsdivеrsity rtion of a spесiеsЬеforе it Ьесomеs roughly linеarly (additivеmodеl) ;еspесiеsduration is 5_10 million
Biodivеrsity,thеn' has ехpandеd from onе spесiеsto many millions of spесiеs today.But how? Тhеrе arе many Ways to go from оnе spесiеsto many' and thеsесan Ье ехpгеssеdin tеrms of thrее mathеmatiсal modеls, rеprеsеntеdЬy a straightlinе, an еxponеntial сurvе' and a logistiс сurvе' first as аn unlntеrruptеdinсrеasе(Figurе 1A), and sесond with somе mass ехtinсtions supеrimposеd(Figurе 1B). ТЬe lineаr modеl rеprеsеnts additivе inсrеasе' thе addition of a fiхеd numЬеrof nеw spесiеsin еасh unit of timе. (Thе inсrеasеin this ехamplе and thе othеrsis a nеt inсrеasе,i.е., truе inсгеаsе minus еxtinсtions.)In tеrnrs of an еvolutionаryЬranсhing modеl, additivе inсrеasе would mеan that thгough timе spесiationratеs havе dесlinеd, or ехtinсtion ratеs havе inсrеasеdrеgularly at a ratе suffiсiеntto mop up thе ехсеssspесiations.Thе impliеd dесlinе in thе ratе of еvolution in thе linеar modеl сomеs aЬout simply Ьесаusеthе total numЬеr of spесiеsis inсrеasingrеgularly, yеt thе rаtе of inсrеasеaсross thе Ьoard rеmains fiхеd; hеnсе,for any individual еvolutionary linе, thе ratе or proЬabilityof splitting (spесiatiоn)must dесlinе. Suсh a modеl has gеnеrally Ьееnrеjесtеdas improЬaЬlе. The ехponепtiаlmodеl is morе сonsistеntwith a Ьranсhing modе of еvolution. If spесiatiсlnand ехtinсtion ratеs rеmain roughly сonstant' thеn thеrе will Ье rеgular douЬling of divеrsity within fiхеd units of timе. A stеady ratе of еvolutionаt thе lеvеl of individuаl еvolutionary linеs sсalеsup to аn еxponеntialratе of inсrеasе ovеrall sinсе total divеrsity is еvеr inсrеasing. This modеlhas Ьееn appliеd to thе divеrsifiсationratеs of individual сladеs and to thеdivеrsifiсationof lifе in gеnеral (Bеnton 1995; Hеwzulla еt a|. 1999|.
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Pаlеrlпtсllog1' апd thе Historу of Lifе
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Figurе l. Thеorеtiсalmtldеlsfсlr thе divеrsifiсаtionof lifе plottеdfrlr thе last 600 million yеars:(A) in thе aЬsеnсеof major pеrturЬаtionand (B) with two п"rass еxtinсtionssupеrimpсlsеd. In еасh сasеthе uppеr сurvе is thе logistiсor еquiliЬriummtldеl' thе middlе сurvе is thе :rdditivеor linеаr modеl,аnd thе ]owеrсurvе is thе схponеntiaIrnodеl.
Thе logistiс mсiеl involvеs onе or morе сlаssiс S-shapеdсurvеs' еaсh соnsisting of an initial pеriod сlf slсlw divеrsity inсrеаsе,a rapid risе, a slowing of thе ratе of inсrеаsе as a rеsult of divеrsity-dеpеndеntdamping faсtors' and thеn a plаtеau сorrеsponding to a limiting or еquiliЬriurrrvaluе. Thе lсlgistiс modеl has Ьееrrusеd to еxplain pattеrns of divеrsifiсatiсlnof marinе organi s r n s( S е p k o s k i1 9 8 4 ) а n d o f p l a n t s ( N i k l a s е t a l . 1 9 8 3 ) . Thеrе is сlеarly n() сonsеnsuson whiсh modеl Ьеst ехplаins thе divеrsifiсation сlf mаiOr sесtorsof lifе thrоugh timе, or on whеthеr all pattеrnsof divеrsifiсation adhеrе to thе samе modеl of inсrеasе. Thе сhoiсе of modеt is imptlrtant sir-rсе еасh makеs prсlfourrdlydiffеrеnt сlaims аЬout еvoluгion.
Thеrе arе major diffегеnс and in thе sеa, and thе his fеrеnt. Today aЬout 85% land, and thе main grouPs p r е s е n t8 r е а t d i v е r s i t y i n t Ьееn еvolving in thе sеa s rесord is dominatеd Ьy m. sсriЬеd forms. This domir by thе faсts that virtually еarly Рalеozoiс (600-450 history of lifе on land apр Also, fossils in сеrtain ma thаn thosе in many сontin d а y i s a p p а r е n t I yf i v е t с l s i of thе insесts' сould Ье an votеd Ьy systеmatists to сl this diffеrеnсе is еvеn pаrt divеrsifiсаtion on land tha In studiеs of thе divеrsif is еvidеnсе for a short pl. yеars) and a longеr onе frс lion yеars). This is follow ехponеntial inсrеаsе in di rising еlеmеnt of a third lo thе last 25 million yеars o aсhiеvеd 125 million yеars Мarinе invеrtеЬratе divt thе suссеssion of thrее m: Ьlаgеs of diffеrеnt phyla . wеrе thеn rерlaсеd. Thе (
and thеn divеrsifiсation slo proaсhеd. Thе ехponеntiа in thе еаrly ordoviсian, rес largеly supplanting thе Сal thе еnd of thе Pеrmian' wJ fauna dгаmatiсally, thе M tеrm risе in divеrsity. In studiеs of thе divеrsif rium intеrprеtation has аls< сеssion of major Bаиpltiпе vasсular plants in thе Dеv< СаrЬonifеrous to thе Pеrm and angiospеrms from thе ing spесiation ratеs and inr
Pаlеoпtoklgу апd tbe Historу of Life LAND AND sЕA сoМPARЕD
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з сlаssiсS-shapеdсurvеs' еaсh сon. g inсrеasе,a rapid risе, a slowing of y-dеpеndеntdamping faсtors, and 3 or еquiliЬrium valuе. Thе lсlgistiс of divегsi6саtion o f m а г i n еo r g e n tsеtal. 1983). modеl Ьеstеxplains thе divеrsifiсaor on whеthеrall pattеrnsof divеrinсrеаsе.Thе сhoiсе of modеl is iffеrеntсlaims aЬout еvolution.
Thеrе arе major diffеrеnсеs Ьеtwееn thе pattеrns of divеrsifiсation on lаnd and in thе sеa, and thе history of lifе in еaсh rеalm may havе bееn rathеr diffеrеnt.Todаy aЬout 85% of dеsсriЬеd spесiеsof plants and animals livе on land' and thе main groups (plants, arthropods, vеrtеЬratеs)havе rеaсhеd thеir prеsеntgrеat divеrsity in thе past 450 million yеars. Plants and animals havе bееnеvolving in thе sеa sinсе at lеаst 600 million yеars ago' аnd thе fossil rесordis dominatеd Ьy marinе spесiеs,whiсh makе up somе 95o%of all dеsсriЬеdforms. This dominanсе of marinе organisms is partly aссountеd for Ьy thе faсts that virtually thе only organisms known from thе Vеndian and еarly Palеozoiс (600_450 million yеars ago) arе marinе, and that thе еarly historyof lifе on land appеars to havе oссurrеd at rеlativеly low divеrsitiеs. Also, fossils in сеrtain marinе еnvironmеnts arе morе likеly to Ье prеsеrvеd than thсlsеin many сontinеnta1sеttings.Thе oЬsеrvation that lifе on land today is apparеntlyfivе to siх timеs as divеrsе аs lifе in thе sеa, largеly Ьесausе of thе insесts,сould Ье an artifaсt that rеflесtsthе grеatеramount of timе dеvotеd Ьy systеmatists to сontinеntal than to marinе organisms. Howеvеr, if this diffеrеnсеis еvеn paгtly сorrесt' thеn it would imply a muсh morе rapid divеrsifiсationon land than in thе sеa. In studiеsof thе divеrsifiсationof marinе animal familiеs (Figurе 2A), thеrе is еvidеnсеfor a short platеau in thе СamЬrian (lаsting aЬout 40 million yеаrs)and a longеr onе from thе Ordoviсian to thе Pеrmian (аЬout 250 million yеars).This is followеd Ьy a long phasе (250 million yеаrs) of nеarехponеntialinсrеasе in divеrsity through thе Меsozoiс and Cеnozoiс, thе rising еlеmеnt of a third logistiс сurvе, whiсh shows a hint of a slowdown in the last 25 million yеars or so, suggеstingthat a third platеau lеvеl may bе aсhiеvеd125 million yеars in thе futurе (Sеpkoski 7984). Мarinе invеrtеЬratеdivеrsifiсationhas Ьееn ехplainеd (Sеpkoski 1984) as thе suссеssionof thrее major phasеs of еvolution, in whiсh Ьroad assеmЬlagеs of diffеrеnt phу|a (еuolutionаrу fаuпаs) dorninatеd thе oсеans and wеrе thеn rеplaсеd. Thе СamЬrian fauna divеrsifiеd еxponеntially at first' and thеn divеrsifiсationslowеd as thе еquiliЬrium lеvеl of 85 familiеs was approaсhеd.Thе еxponеntial divеrsifiсationof thе Pаlеozoiс fauna thеn bеgan in thе еarly Ordoviсian, rеaсhing an еquiliЬrium divеrsity of З50 familiеs and largеly supplanting thе СаmЬrian fauna. Finally, aftеr thе mаss еxtinсtion аt thе еnd of thе Pеrmian, whiсh rеduсеd thе global divеrsity of thе Palеozoiс fauna dramatiсally, thе Мodегn fauna сontinuеd and ассеlегatеdits longtеrmrisе in divеrsity. In studiеsof thе divеrsifiсаtionof vasсular plаnts (Figurе 2B), an еquiliЬrium intеrprеtationhas also Ьееn givеn (Niklas еt аl. 1983). Thеrе was a suссеssionof major Bаиpliiпe (ground plans or arсhеtypеs)of plant typеs:еarly vasсularplants in thе Dеvonian; lyсopods' fеrns' сonifеrs, and othеrs in thе СarЬonifеrous to thе Pеrmiarr; gymnospеrms in thе Triassiс to thе Jurassiс; and angiоspеrmsfгom thе Сrеtaсеous onwаrd. Thеrе is еvidеnсе foг dесlining spесiation ratеs and inсrеasing spесiеs durations during еaсh of thе first
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(A), Figurе 2. Pattеrnsсlf divеrsifiсationof fаnriliеsof marinе irrvеrtеЬrаtеs ( B ) , ( С ) , ( D ) . p l a n t s n o n m a r i n е i n s е с t s v а s с u l a rl a n d tсtrapods :rnd StratigraphiсaЬЬrеviations:С, СarnЬrian1СrЬ, СarЬonifеrous;(irеt, Сrеtaсеous;D, Dеvonian;Jur, Jurassiс;O, Ordoviсiаn;P, Pеrrnian;S, Silurian; Tеrt, Теrtiаry;Tr, Triassiс;V, Vеndiаn. (Basеdсln Sеpkoski 1984; Niklаs еt al. 1 9 8 3 ;B е n t o n1 9 8 5 ;a n d l , a Ь а n d е i r a n d S е p k o s k i19 9 З . )
thгее radiations as thе nеw sеt of сladеs partially rеplaсеd thе old. Еaсh nеw radiation lеd to an inсrеasеin.total gloЬal divеrsity,whilе thе divеrsity of thе pгесеdingfloras dесlinеd.Angiospеrms apparеntly сontinuеd tсl divеrsify аt a high ratе. It is hаrd to idеntify platеatrsin land-plant spесiеsdivеrsifiсation, and it is hard to find еvidеnсе for lоgistiс modеls of divеrsifiсation.Еqually, thе total сurvе of spесiеsdivеrsitiеsthrсlugh timе is not oЬviously ехponеntiаl, and, if anything, thе pattеrn appеars tO suggеstlinеаr inсrеasе in divеrsity through timе. Thе divеrsifiсationof сontinеntal tеtrapсldfаmiliеs (Figurе 2С) appеаrs to сOrrеspondtO an ехponеntial rтodеl of iпсrеаsе(Bеnton 1985). Divеrsiry lеvеls rеmainеd low, at somе З0 to 40 familiеs, during thе latе Palеozoiс and muсh of thе Меsozoiс. Thеy thеn rosе to aЬoшt l00 faпriliеsat thе еnd of thе Сrеtaсеous and, after rесovеry from thе еnd-Сrеtaсеous ехtinсti()n еvеnt' f:1milial divеrsity inсrеasеdrapidly toward 330 fаmiliеs and shows rro sign of a slowdown. Thе pattеrn of divеrsifiсationmay Ье dissесtеdinto suссеsstvеradiations of thrее gloЬal сladе аssoсiations:Ьаsаl tеtrapods (formеrly tегmеd
Iаbуriпth o dorul amphiЬiar Palеozoiс; arсhosaurs (dir and lissamphiЬians (frogs Ь i r d s ,a n d m a m m a l s f r o m assoсiations rеplaсе еaсh r milial divеrsity lеvеls,Ьut
сiations. Thе divеrsifiсation of ir еspесially in гhе Mеsozo 1,99З). This suggеsts that еxpansion that pеrhaps sl с a t е t h а t i n s е с t d i v е г s i t yi
Plots of thе divеrsifiсa lifе (Figurе 3) by Bеnton сation. Thе сontinеntal с and land plants' is ехpon lеozoiс platеau lеvеl and ward thе Rесеnt, whiсh l approaсhing an еquiliЬri сontinеntal familiеs (Fig ting еxponеntial сurvе (F flесting thе сontriЬurio сannot Ье ignorеd. ЕxPLANAтloNs
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In сomparing logistiс anr thе kеy distinсtion is Ьеtv modеls. Thе formеr imp\ еxpansion modеls assum lеast that suсh a сеiling h Еquilibrium modеIs fol an influеntial Ьody of еr data on divеrsifiсation as (2) intеraсtions Ьеtwееn< iеs show that сlаdеs ma; ratе of divеrsifiсation slov phеnomеna, suсh as сom duсtion of spесiеs rangеs lows еxpliсitly from сlas of onе population supor sourсе. An initial ехpoп lowеd Ьy a platеau whеI (usually food); this сorrе Thе pattеrn of divеrsif prеtеd (Sеpkoski 1984,
Pаlеontologу апd the Нistorу of Life Iаbуrinthodoпt amphtЬians) and synapsids (mammal-likе rеptilеs) in thе latе Palеozoiс;arсhosaurs (dinosaurs,ptеrosaurs' сroсodilians) in thе Mеsozoiс; and lissamphiЬians (frogs and salamandеrs), lеpidosaurs (lizards and snakеs), birds' and mаmmals from thе latе Сrеtaсеous to thе prеsеnt day. Thеsе сladе assoсiationsrеplaсе еaсh othеr and arе assосiatеd with еvеr highеr gloЬal familial divеrsity lеvеls, Ьut it is diffiсult to fit logistiс сufvеs to any of thе asso-
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aгtiallyrеplaсеdthе сlld. Еaсh rrеw divеrsity,whilе thе divеrsity of thе parеntlyсontinuеdtсl divеrsify at а r land-plantspесiеsdivеrsifiсation' modеls of divеrsifiсation.Еquаlly, gh timе is nсlt oЬviously еxponеntO suggеstlinеar inсrеasеin divеrod familiеs (}.igurе2С) appеаrs to r е a s е( B е n t o n1 9 8 5 ) .D i v е r s i t yl е v . [iеs,duгing thе latе Palеozoiс аnd Ьout 100 familiеsat thе еnd of thе l d - С г е t а с е o uеsх t i n с t i о nе V е n t 'f i r 30 familiеsand shows no sign of a r a y b е d i s s е с t е di n r o s u с с с s s i v ег а : Ьasaltеtrаpods(formеrly tеrmеd
сiations. Thе divеrsifiсation of insесts (Figurе 2D) was also apparеntly еxponеntial, еspесiallyin thе Меsozoiс poгtion of thе сurvе (Labandеira and Sеpkoski 1993).This suggеststhat insесts havе had a long and сontinuous pattеrn of ехpansionthat pеrhaps slowеd somеwhat during thе Tеrtiary. This may indiсatеthat insесt divеrsity is approaсhing an еquiliЬrium lеvеl now. ..all'' Plots of thе divеrsifiсation of fаmiliеs of marinе. сontinеntal. and lifе (Figurе 3) Ьy Bеnton (1995) сonfirm thеsе varying modеls of divеrsifiсation.Thе сontinеntal сuгvе (Figurе 3B), dominatеd Ьy tеtrapods, insесts, and land plants, is еxponеntial. Thе marinе сurvе (Figurе 3С) rеtains a Palеozoiсplatеau lеvеl and appеаrs to show a slowdown in divеrsifiсation toward thе Rесеnt' whiсh may indiсatе that marinе divеrsity lеvеls today arе approaсhingan еquiliЬrium lеvеl. Thе сurvе that сomЬinеs all marinе and сontinеntalfamiliеs (Figurе 3A) сould Ье intеrprеtеd as a singlе poorly fitting ехponential сurvе (Hеwzulla et a|. 1'999),Ьut thе Рalеozoiс platеau, rеflесting thе сontriЬution of marinе invеrtеЬratеs (сomparе Figurе 3С), сannot Ье ignorеd. ЕXPLANAтloNs oF PAттЕRNs oF DlVЕRsIF|сAт|oN In сomparing logistiс and ехponеntial modеls for thе divеrsifiсation of lifе, thе kеy distinсtion is Ьеtwееn еquiliЬrium and nonеquilibrium (or еxpansion) modеls.Thе formеr imрly thе ехistеnсеof gloЬal еquiliЬria in divеrsity,whilе ехpansion modеls assumе that thеrе is no сеiling to thе divеrsity of lifе, or at lеastthat suсh a сеiling has yеt to Ье rеaсhеd. Еquilibrium models forthе ехpansion of thе divеrsity of lifе wеrе Ьasеd on an influеntial Ьody of есologiсal thеory. Logistiс modеling of gloЬal-sсаlе data on divеrsifiсationassumеs (1) intеraсtionsamong spесiеswithin сladеs, (2)intеraсtionsЬеtwееnсladеs,and (3) gloЬаl еquilibrium levеls.Many studiеs show that сladеs may radiatе initially at ехponеntial ratеs' Ьut that thе ratеof divеrsifiсation slows at a сегtain point as a result of divеrsity-dеpеndеnt phеnomеna,suсh as сompеtitivе еxсlusion, inсrеasеd spесiеs paсking' and rеduсtionof spесiеsrangеs (Sеpkoski 1,984,1'996).This stylе of rеasoning follows еxpliсitly from сlassiсal еxpеrimеnts in сompеtition whеrе thе inсrеasе of onе populаtion supprеssеs anothеr that dеpеnds on thе samе limiting rеsourсе. An initial ехponеntial inсrеasе of thе suссеssful population is followed Ьy a platеau whеn thе spесiеs Ьеgins to dеplеtе thе limiting rеsourсе (usuallyfood); this сorrеspondsto thе loсal сarrying сapaсity. Thе pattеrn of divеrsifiсation of marinе familiеs (Figurе 2A) has Ьееn intеrprеtеd (Sеpkoski 1984' 1996) in tеrms of a thrее-phasе logistiс modеl that
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Figurе 3. Pattеrnsof thе с in numbеrs of familiеsеx (A)' сontinеntalorganism mахimumand а minimur tn and haЬitat-prеfеrеnсе familiеsгесordеdas dеfin d е f i n i t е l ys p а n n i n gt h а t s thе mагinе or сontinеnta doubrful strаtigrаpЬiсаtt haЬitat dеsignations.Thе organismsis еqual to thе m а х i m u m m е а s u r е sh, o w tаха Ьесausеfamiliеs wit] oссur in Ьoth marinе аnd сontinеntal.Stratigrаphr Centlzоiс;Pс' Prесаmbгtа
Pаlеontologу аnd tbe Historу of l-ifе rеprеsеnts thе Ьеhaviorof thе tlrrеееvolutionaryfaunas:Сambгian, Pаlеozoiс, аnd Мodеrn. Thе rеplaсing furunasarе said to hаvе Ьееn сhаraсtеrizеd Ьy thе aЬilityto pеnеtratееvеr widег sеts of niсhеs and hеIrсеtсl aсhiеvе highеr divеrsitiеs.Thеrе is somе еvidеnсеin favor of this idеа; for ехamplе, lаtеr maritrе an. imalsсould Ьurrow dееpеr,fсlrm morе сornplеx rееfs,and сapturе prеу in еvеr morе ingеnious Ways. Thе еquiliЬrium rnodеls сould Ье intеrpгеtеd sirnply in tеrmsof largе-sсalесompеtition Ьеtwееn major сladеs' with Ьivalvеs outсompеtingЬrасhiopods,пrammаlsoutсompеtingdinosаurs,and sсl on. Dеspitе thе pоpular:rppеalof suсh suggеstions,mosr supposеdсаsеsof largе-sсаlесompеtitionсrumЬlеwhеn thе еvidеnсеis еxaminеd (е.g.,Gould and Сalloway 1980; Bеnton1987). Sеpkoski (1996) attriЬutеdthе pattегnsof waхing and waning of сladеs to diffrrsе сOmpеtition Ьеtwееn thеm at thе spесiеs lеvеl, whеге spесiеsin onе сladе arе gеnеrally сompеtitivеly sr"rpеriorto thosе in anothеr. Howеvеr,thеrе arе four arеas of сonсеrn with еquiliЬrium modеls:
Itime 200
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i. Тhеге is no indеpеndеr-rt еvidеnсе for еquiliЬria, that is' for fiхеd саrrу.ing сapaсitiеson thе еarth today. In еvolutionary tеrms еquiliЬrium divеrsitiеsimply that all availaЬlе rеsourсеsarе in usе and all есospaсе i s f i l l е d .I f a n е w s p е с i е sо r i g i n а t е s ,i t m u s t d i s p l a с еa p г е е х i s t i n go n е . Howеvеr, oЬsеrvаtionsof сasеs whеrе prеviously isolаtеd floras and faunasсomе into сontaсt suggеstthat spесiеsarе just as likеly to insinrratе(еntеrnеw niсhеs) аnd not сausе еxtinсtion of othеr taХa' 2. Мultiplе logistiс mоdе[s imply prеdiсtаЬlе outсomеs of intеraсtiorrs Ьеtц,ееnmеmЬеrsof thе diffеrеnt faunas. that is. that nrеmЬеrsof onе .!Иherе gгoup will gеnеrallysuссееdwhеrе thosе of аrrothеrwill fail. majоr Ьiotiс rеplасеmеntshаvе Ьееrrinvеstigirtеd,onе group is moге likеly to disappеar Ьесausеof an ехtinсtion еvеnt (Bеnton 1987) than а s а r е s u l to f i n t е r a с t i o n s .
r lt i m e 200
'r00
Jur Сret
Figurе З. Pattеrns of thе divеrsifiсation oi lifе thrсlugh timе in tсrms of сhangеs in numЬеrs of fаmiliеs ехtant реr strаtigraphiс stagе, plоttеd for all organisms (A), сontinеntal orgаnisms (B), аnd marinе organisms (С). In еaсh grаph a mаximunr аnd а minimum arе slrown, Ьasеd on a сot-r-rЬination of strаtigraPhiс and haЬitаt.prеfеrеnсеinforn-ratiоn.Thе minimum mеasurе inсludеs or-rlу familiеsrесordеd as dеfinitеly prеsеnt within еaсh stratigrаphiс stagе or as definitеlyspаnning tЬat stagе, and only fаmiliеs dеsignatеd as rеstriсtеd solеly to thе marinе or сontiDеlltаl rеаlm. Thе mахiInr.rmmеasllrе inсludеs trlso all douЬtfLrlstratigraphiс attriЬutions of familiеs and аll еquivoсal аnd sharеd haЬitatdеsignations.Thе sum of minimum mеasurеs fоr сontinеntal аnd rnaгinе organismsis еqual to thе minimllm mеasllге for all taxa togеthеr. Thе sum of mахimuпr гIlеasllrеs'h
9]
e2 Раlеoпtrllog1'апd thе L{istorуof Lifе 3. Thе dir.еrsifiсationof thе Mtrdеrn fаunа sееnrsmorе prol()ngеdand slorvеrthan prеdiсtеd Ьy a ltlgistiс mtlr']еl.Thе rising phirsеof thе logistiс сuгvе has lastес]for 2.50 million vеars,with somе еvidеnсеof a slowdown toward thе pгеsеnt.If thеге is no сшrrеntplatеau,thеn it would Sееmthat in thе sесond half of thе Phanеrozoiс,thе Ьеst-known part ()f t[rеfossil rесord, thе logistiс rulеs lr:rvеЬееn forgсlttеn. 4 . T h е с l а s s i сl o g i s t i сс u r v е sо i S е p k o s k i( 1 9 8 4 , l 9 9 6 ) m a v Ь е a r r i f a с t so f thе lеvеl of analysis.Тlrе сurvеs arе plt>ttеdat thе lеvеl of fanriliеs. \iИhеnthеsе arе translatеdto thе gеnеriс lеvеl, thе logistiс pаttеrns Ьеgin to Ьrеak down, and at spесiеslеvеl thе pаttеrn сoulс1Ье ехponеlltiai (Bеnton 1997). Thе shapе of thе сurvеs switсhеs Ьесausе еaсh gеr-rr.rs сontains manУ spесiеs,and еaсh fаmily many gеnеra.In an еvoltrtiсlnаrytrее thе spесiеsarе thе tir-rlrl twigs, whilе gеnеra ехtеnd dееpегinto thе trее, аnd fаmiliеs dееpеr still. So, althouglr thе numЬеr of familiеs might Ье dеfinеd аt a сonstant lеvеl, thе nr-rmЬеrof spесiсs in еeсh сould Ье ехpandirrgехponеntiall},. Thе аltеrrrltivе to еquiliЬгiurrris ехpс|t1sioп. Arе tlrе ill]glеeаtеPattеrns,oI at lеast stlll-lесlf tlrеm (FigLrгеs2 and 3), tЬе rеsult of unсotrstrainеdехpansiorr? Сеrtailrly, somе сlаdеs (suсh as insесts,angiospеrms,Ьiгds, and mаmnrals) sееm tсl сontinuе rаdiating linеarly or ехponеntially for many tеns or h u n d r е d s t l f r n i l l i o r r so f y е a r s . S u с h е v е r - е x p a n d i n gp a t t е r n s i m p l y t h a t t h е s е g r < l u p sa r е h i g h l y s u с с е s s f L ral n d a d а p t : r Ь l е Т . h е o v е r а l l p : 1 t t е r n so f divеrsifiсation (Figurе З) iпссlrporatеthе n[tllеr()usсonstitllеnt сladеs, sotте ехpanding' tltЬеrs diminishirlg, аnd othеrs rеrnainingat сonstilnt divеrsity аt any Partiсul:rrtimе. From an ехpensionist viеwpoint, thеrе is no prеdiсtion of how thе individual сladеs irffесt еaсh othеr. Nеw gloЬа1 divеrsity lеvеls mаy Ье aсhiеr,еdЬy сomЬinatithе numЬеrs of familiеs or othеr taхa that сan inhaЬit thе еllrth at any timе: suсh a limit rvould Ье сausеd not lеast Ьy thе аmount сlf srаndirrg room on thе ark. If a limit of living spl1сеWсrе aPprсlaсhеd'еvеr smallеr tlrganisnrswсluld prеsuпraЬlvЬе fаvorеd Ьv sеlесtion. Еquallr., аs Ьirs happеnеd llrlrny tinlеs сlrrringеvtllr'rtion,trrgelnismswould takе unехpесtеdmеasurеsto survivе, for ехirnrplс,Ьy oссupying thе аir' Ьurrсlwing into sеdimеnts,and, ill thе сasе of sonrе Ьaсtеria,living dееp within thе еarth's сrllst. With sizе rеduсtion, thе ultimatе linrit to thе divеrsifiсation of lifе might thеn Ьес
Е Q U l L | B R l U l " 1o F
It is hard to sеlесt bеtwi til rесеntly, еquiliЬrium gists, just as thеy hаvе с есologists arе now quеst сеptеdin the 1960s and versifiсation might havе Thе еquiliЬrium mod, aссommodatе only сеrt; саpaсity is rеaсhеd, nеt no sцсh assumрtion аn with no ultimаtе limit iп PalеoЬiologists havе < rесt. Реrhaps all lifе has еxpansion modеl (Stanlс fiеd in diffеrеnt wаys. I lеvеl of staЬilitу, and pz whilе lifе on land lnay and arthropods сrеpt с: еquiliЬrium and еxpans p а l е o Ь i o l o g i s t s ,Ь u t Г o r statе of gloЬal Ьiodivеrs
Spесiation
Тhе еffort to undеrstаnd is at thе uppеr еnd of thе еnd thе important сross< studiеs is spесiаtioп (see
tion'' Ьy Маrgarеt B. Pt mation of nеw spесiеs b' PаlеoЬiologists сlеаrlу сannot tеst whеthеr any thеy sееk to apply thе r distinguishеd Ьy diffеrеr a wеak suЬstitutе,Ьut th ulаtional thinking, sееk t tistiсаl studiеs of lаrgе invoIvеs morphologiсаl tion. In pгaсtiсе' this is п atists of modегn oгgаn from morphology, and I lеss studу. Systеmatistsr
Pаlеontologу апd thе Нistorу of Lifе la sееmsmоге prolongеd and dеl. Thе rising phasе of thе n Yеars'with somе еvidеnсеof t.t is no сurrеntplatеatr,сhеn it thе Phanеroztliс' thе Ьеst-known lеs havе Ьееrrforgсlгtеn' ( | 9 8 4 , 1 9 9 6 )n r a y Ь е a r t i f a с t so f эttеdat thс iеvеl of fаnriliеs. iс lеvеl, thе logistiс pitttеrns vеl thе pаttеrnсoulс]Ье of thе сurvеsswitсhеsЬесausе l еaсh familv many gеnеra.In arr rаl twigs,whilе gеnеrаехtеnd jr still. So, although thе numЬеr ant lеvel' thе nuпrЬеrrlf spесiсs r Il1'. oп. Аrе thе aggrеgatеpattеrns' or l е г е s u l to f u п с o n s t r a i n е dе х p a n rs, angiospеrms,Ьirds, and nr:rm_ )r еxponеntiallyfor many tеns or г-ехpanding pаttеrns imply thаt laptаЬlе.Thе ovеrаll pаttеrrrsof umеrousсonstituеntсladеs, somе rеrnaining at сonstant сlivеrsity аt viеwpoint, thеrе is rro prеdiсtion lthеr. Nеw gloЬal divеrsity lеvеls rdaptations,haЬitat сhangеs,arrd 'еагs thе dil,еrsifiсatiсlnof lifе has rrsоf сеrtair.r сlаdеs Ьoth in thе sеa (insесts, on land ar;rсhnids,anеvidеnсеthаt thеsе rnlrjсlrсladеs : ; l t еt h a t t h с v w i I I n o t с О n t i n U еt o livегsifiсatioI.r wotrld lаst forеvеr. of famiiiеsor othеr tахa that саn would Ье сausеd not lеast Ьy thе a limit of living spaсr Wеrе apеsumaЬlyЬе favorеd Ьy sеlесti
Е Q U I L l B R I U Мo R Е Х P A N S | o N ? It is hard to sеlесtЬеtwееnthе two modеls for tЬе divеrsifiсationof lifе. Until rесеntly,еquilibrium modеls havе dominatеd thе thoughts of palеoЬiologists'just as thеy havе dominatеd thе minds of есologists.Howеvеr, just as есologistsаrе now quеstioningthе ovеrsimplistiсеquiliЬritlпrmodеls thеy aссеptеdirr thе 1960s and 1970s, so palеoЬiologistsаrе rесonsidеrirrghow divеrsifiсationmight havе happеnеd in thе longеr tеrm. Thе еqrrilibriummodеl аssumеs that spесifiс nrajor есologiсal realms саn aссommodatеorrly сеrtain numЬеrs of spесiеs,аnd th:rt whеn thе саrrying сapaсityis rеaсhеd, nеt divеrsifiсation сеasеs.Thе ехpansion modеl makеs no suсh assumptioп and allows for сontinuing, if еpisodiс, divеrsifiсation with no ultimatе lirnit in sight. Palеobiologistshavе dеЬаtеd arrd сontinue to dеЬatе whiсh modеl is сorrесt.Pеrhaps all lifе has divеrsifiеd aссording tсl еithеr an еquiliЬrir.rmor an ехpansionmodеl (Stаnlеv 2007). Or pеrlrapsdiftЪrеntsесtors of lifе divеrsifiеd in diffеrеnt Ways. Еvolution in thе sеa mаy havе rеsultеd in a grеatеr lеvеlof staЬility, and pattеrns of inсrеasе may havе gеnеrally Ьееn logistiс, whilе lifе on land may havе divеrsifiеd ехponеrrtially sinсе thе first plants and arthгopods сrеpt сautiously out of thе watеr. Thе impliсations of thе еquiliЬriumand ехpansion modеls arе profoundly diffеrеnt, not mеrеly for palеoЬiologists,Ьut for еvеryonе сonсеrnеd aЬout thе presеnt and futurе s t a t еo f g l o Ь a |Ь i o d i v е r s i 1 1 ' .
Spесiation Thе еffort to undегstand how lifе diversrfiеd fron-lits oгigir-rto thе prеsеnt day is at thе uppеr еrrd of thе speсtгuпr of studiеs ilt lпаcroеuolutiсэll.At thе lowеr еnd thе important сrossovеr ЬеtwееnpalеoЬiology and nrodеrn еvolutionary studiеsis spеciаtirln(sееthе main еssay ..Thе Pattеrn and Proсеss of Spесiаtion'' Ьy lvlargаrеtB. Ptасеk аnd Shаlа J. Нankison tn this volumе), thе formation of nеw spесiеsЬy thе splitting of liпeаgеs(еvolutionarylinеs). PalеoЬiologistsсlеarly сannot usе thе biologiсаl speсiеsсoпсept sinсе thеy сannottеstwhеthеr аny two fossil spесimеnsarе сapaЬlе of intеrЬгееding,so thеy sееk to apply tЬe mсlrphologiсаl spесiеs сoпсept, in whiсh spесlеs arе distinguishеdЬy diffеrеnсеsin thеir phеnotypеs'This may at first sееm to Ье a wеak suЬstitutе,Ьut thеrе :rrеshaгеd assumptiOns:palеobiologistsusе populationalthinking, sееk to сhаraсtеrizеspесiеsboundariеs on thе Ьаsis of statistiсal studiеs of largе samplеs of spесimеns' and assumе that spесiation invоlvеs morphologiсal diffеrеntiаtion assoсiatеd with rеproduсtivе isolаtion.In pгaсtiсе,this is not vеry diffеrеntfrom thе approaсh of many systеmatistsof modеrn organisms-spесiеs of mollusks are gеnеrally dеtеrmined from moгphologу, and fossil and ехtant matеriаl may form parts of a sеam. lеssstLrdy.Systеrnаtistsrarеly саrry out itltеrЬrееdingtriаls.
9З
Pаleoпtologу апd thе Histor1,of Lifе Until 1970 most еvolutionists assumеd tlrаt fossils с
|\,4oгphoIo9y
F-igurе4. Соntrastingеxpесtatiorrs of spесiеs.lеvеl еr.сllutionill thе с[lsьiс plrylеtiс-grасlr'talisn-r modеl (A) and tl-rеpunсtuаtеd-еquiliЬгiuш modеl 1B). Dеgrееof nltlrphologiсalсlrаngеis indiсаtесlon thс х-ахis, tit-t.lс thе 1,-1y1,. t.lt.t
Thе punсtuatеd-еq 1970s and 1980s was tagonists kеpt shifting Ь a s е do n t h е i d е a s i п еrаl supportегs of pun. idеa of speсies sеlесtio and' in somе modеls, ordеr сharaсtеrs. Spе< and еvеn in oppositio idеa of an ..ехpansior (Gould 1990), with h Darwinian viеw. Suсh most еnthusiasts, and natural sеlесtion duriп ally сonsidеrеd to Ье t, to rеsult in signifiсant tion of individuals. Hс dеnсе pointеd to its irп to еxplain it (Landе 19 A plеthora of сasе |99О that purpoгtеd еquiliЬriumviеws.Е.ar not provide еnough еv of migrаtionsof tаxа i whаt was a graduаl i stеppеd, punсtuationa 1981; Shеldon 1987) t intеnsе foсus on finе-sс thеy wеrе still suЬjесt triloЬitеs showеd a grе agеs just did not spес mеntеd a numЬеr of pu intеrprеtеd as morе lik nonBеnеtiс сhangе in sl Тhе fossil rесord dеr and Anstеy (1995) sur tегns in thе fossil rес. гangеd from radiolаriа stratigraphiс agеs rang iority сonсеntrating in of thе еarth. of thе .5 with anagеnеsis (15 с 6 3 % ) . I t s е е m sс l е a г , t and it had not Ьееn prе Whаt thеn of thе pr Ьatе? As еvеr. thе Drс
Pаleoпtologуаnd thе Historу of Lifе ] thirt fossils сould say vеry littlе а n d G o u i d \ \ 9 7 2 ) с h a l l е n g е dt h е )y punсtuatеdеquiliЬria. Еldrеdgе ft pЬ1,lеtiсgrсtduаlisnt.It assumеd ariaЬlеratеs (Figurе 4A) Ьut wеrе иestЗ/.SpесiationWas sееn as a Ьynеs liпеад1еs had Ьесomе so diffеrrd еvolvеd into a nеw spесiеs (thе .ting (сlаdogezesls/сould aisсl haplstеr than noгmal ratеs of linеagе pиltсtuаtеdеquilibriа (Figurе 48), е at сladogеnеsis,rilthеr th:rn аnaThе normal statе Of a linеagе was ;pесi:rtionш.tluldhappеn. Ьut suсh 'nary. Thе punсtuatеd-еquilibrium rgе along a linеagеаге punсttlatеd' ;pесiаtionеvеnts.Тlrе latrеr сlaim r rеgaгdеdаs thе kеу' dеfinir.rg еlеt Ьy its supportеrs. ldеl on trд,ooЬsеrvatioпs: F o s s i l sс l n г е n l а i nС t r t l 5 1 д1n',' еdir-t-rеr-rt (i.е., tlrotlslrrrdsсlr g sееmsto сhangе. tо Мayr's аllopаtriс (gеograрhiс. a s a r a p i d с v е n ti n thе fossil rgеnсеof two isolatеdpopulations
l\,4orphology
-lеvеlеvolutionirrthе сlаssiс u а t е d - е q u i l i Ь r i rm rm o d е l( B 1 . t l r lt h ех - а х i s .t i m еt r nt h е y - . r х l s .
Thе punсtuatеd-еquiliЬгium vеrsus pЬylеtiс-gгаdualism dеЬatе of thе |970s and 1980s was hugе fun for all сonсеrnеd' nоt lеast Ьесausеthе protagonistskеpt shifting ground and rеvising thеir сlaims. Thе first phasе wаs Ьasеdon thе idеas in Еldгеdgе and Gould's еssays' From 1975 onward sеvеralsupportеrsof punсtuatеdеquiliЬria еxtеndеdthе modеl to еspousеa nеw idеa of spесiеssеlесtion, a highеr_ordеr proсеss in whiсh spесiеs wеrе sortеd and' in somе modеls, сould evеn undеrgo sеlесtion of ..emеrgеnt'' highеrordеr сharaсtеrs. Spесiеs sеlесtion сould, in thеory, oссur indеpеndеnt of, and еvеn in opposition to' natural sеlесtion (Stanlеy 1975). This lеd to thе idеa of an ..ехpаnsion'' of еvolr.rtionarythеory to many hiеrarсhiсal lеvеls (Gould \990), with hints of an apparеnt rеjесtiоn of aspесts of thе nеoDarwinian viеw. Suсh еxtrеmе positions wеге aЬаndonеd fairly rapidly Ьy most еnthusiasts,and palеoЬiologistsсontinuеd thеir staunсh adhегеnсеto naturalsеlесtionduring thе latе 1980s and 1990s. Spесiеssеlесtion is gеnеrally сonsidеrеdto Ье thеoгеtiсallуpossiЬlе Ьut ехtrеmеly fееЬlе and unlikеly to rеsult in signifiсant adaptations of thе typе that oссur in thе natural sеlесdon of individuals. Нowеvеr, thе notion of stasis stuсk: too muсh fossil еvidеnсеpointеd to its imp
95
Pаleoпtologу аnd the Ilistorу of Lifе uЬiquity of thеir modеl, and yеt сommon sеnsеSuggеststhat thеrе arе сlеar Ьiologiсal rеasons that еaсh modеl prеvails undеr pаrtiсulaг сirсumstanсеs. Bеnton and Pеarson (2001) notеd that spесiation is a сonsеquеnсеofrеproduсtivе isolation, and hеnсе thе frеquеnсy of spесiation in a grсlup is likеly to bе rеlatеd to thе еasе with whiсh rеpгoduсtivе Ьarriеrs аppеаr. At onе ехtrеmе thеrе arе organisms suсh as planktoniс protists that livе in hugе pсlpulations that sеldom еnсountеr Ьarriеrs to dispеrsal, and that do not possеss сomplеx bеhaviors assoсiatedwith rеproduсtion. For thеsе,gеnеtiс isolation of populations is a rarе еvеnt, and spесiation,whiсh pеrhaps oссLlrsrarеly' is probaЬly gеnеrally long tеrm and gradual, lasting pеrhaps half а million yеars. At thе othеr еxtrеmе arе organisms suсh as frеshwatеr fishеs that livе in spatially struсturеd and oftеn-transiеntеnvironmеnts. Неrе spесiation might bе so сommon that еvеry lakе and rivеr has its own rеproduсtivеly isolatеd population of a partiсular typе
Rhizosolenia (p|anktoniсdiatom)
5.0 4.0 3.0 2.O
2.8
fТr |
"GAUss
t\
Figurе 5. Grаdual spесi morph
ассount thе gеnеtiсs z rеlatеd еxtant spесiеsа p h o l o g i с а| d i f f е r е n t i a dolоs sееms гo havе Ь was еspесially гapid fr< pеaring in that timе, а agе. Нowеvеr, thе intе Ьy information from ] thеrе arе quеstions ovе vаl. thе oгigins of thе arе more сonfidеntly d Thе pluгality of еvс ism plus stasis, punсtu vironmеntal сontrols l ( | 9 9 6 | p г o p o s е dt h а г ; е n v i г o n m е n r sa n d с h a
Pаlеoпtologу апd the Historу of Life sеnsеsuggеststhat thеrе aге сlеar s undеr paгtiсular сirсumstаnсеs. :iation is a сonsеquеnсеof rеprolf spесiationin a grоup is likеly to 'сtivе barriеrs appеar. At onе ехriс protiststhat livе in hugе popuiispеrsal,and that do not possеss rсtion.For thеsе,gеnеtiс isolation 'n, whiсh pеrhapsoссurs rarеly, is ,l' lasting pеrhaps half a million suсh as frеshwatеr fishеs that livе vironmеnts.Hеrе spесiation might ls its own rеproduсtivеlyisolatеd hesepopulationsmight nеithеr Ье еn might liе thе majority of invеrх h i Ь i r i n gs t a s i sb u t f r o m t i m е t r l ' rеsultof a major pеrturЬation in
Rhizosolenia (p|anktoniс diatom)
rсing animаls that livе in variеd е с i а t i o n .М е l r а r а b d o t o si s a n a s lrеsеntеdtoday in thе СariЬЬеаn iniсan RеpuЬliс and еlsеwhеrеin )n yеars of sеdimеntationin shalf this Ьryozoan.Тhе fossils show from 8 to 4 million yеars aЕ]o' h had diеd out Ьy thе Quatеrnary ln (1995)havе еstaЬlishеda varivtthin Меtr аrаbdotсls, taking into
R. bergonii
l
R. prаebergonii
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protist is sееn in Rbizosoleпiа, a ;еaЬundanсеin thе еquatorial Pavalvеsof this gеnushavе aссumu. d thеy hаvе Ьееnsamplеd Ьaсk to mplеs of thе valvеs сan Ье takеn pilе, and thеsесan Ье datеd aссuosoleniаliving sidе Ьy sidе in thе nd thеsесan Ье traсkеd Ьaсk for l 3.1 million yеars ago' thе morfusе,and thеrе is apparеntly only ). This splitting еvеnt is rеported morphologiсal divеrgеnсеoссurs ,аs еvidеntlynot a loсal еvеnt Ьut iс. Diatoms gеnеrаlly rеproduсе lхual offspring. Pеrhaps thе сomе modе and thе ЬarriеrlеssPaсifiс d phylеtiсally and сlvеr a span of
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"MAТUYA|\ЛA,
Magnetoсhron
Figurе.5.Grаdual spесiationin thе diatom Rhizosolеniа.Onе of sеvеral morphologiсalсhаraсtеrs,thе Ьеightof thе hyalinеаrеa' that diffеrеntiatеthе two living spесiеsR. bergoпii and R. prаеbеrgonii.This plot' from onе of еight saшplingstationson thе floor of thе Paсifiс Oсеan, shows a long-tеrm Ьеtwееnthе two spесiеsfrom 3.1 to 2.6 million yеars ago, as the divеrgеnсе Thе sеdimеntaryrесord is сontinuous,and it populationsslowly diffеrеntiatеd. indiсatedin thе сan Ье datеdЬy fossilsand Ьy magnеtiсrеvеrsalmеasuгеmеnts, masnеtoсhronsсalеat thе Ьottom.
ассount thе gеnеtiсs and thе amount of morphologiсal diffеrеntiation of rеlatеdеxtant spесiеsand thеn еxtеnding сomparaЬlе statistiсaltеstsof morphologiсal diffеrеntiation to thе fossil forms. Linеagе splitting jn Меtrаrаbdolсls sееms to havе Ьееn rapid and punсtuational in сharaсtеr. Spесiаtion was еspесiallyrapid from 8 to 7 million yеars ago' with ninе nеw spесiеsappеaring in that timе, although sampling may Ье a proЬlеm in roсks of this agе.Howеvеr, thе intеrval from 8 to 4 million yеars ago' rеprеsеntеd largеly by information from Dominiсa, has Ьееn intеnsеly samplеd. So, although thеrеarе quеstions ovеr thе origins of thе ninе Ьasal spесiеs within this intеrval, thе origins of thе rеmainder (teпие,nеw spесiеs 10, and nеw spесiеs 8) arе morе сonfidеntly doсumеntеd аs Ьеing punсtuational. Thе plurality of еvolutionary modеs (gradualism without stasis, gradualism plus stasis,punсtuation plus stаsis)might Ье rеal, and thеrе might Ье еnvironmеntal сontrols that work in a somеwhat unеxpесtеd way. Shеldon (I996) proposеd that gradualism might сhаraсtеrizеtaхa that livе in staЬlе еnvironmеnts and сhangе in linе with slow еnvironmеntal сhangеs, whеrеas
97
98
Pаlеontologуапd thеНistorу of Lifе tenuе 9roup г-----.--.--
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Figurе 6. Punсtuational spесiаtionin thе ЬrусlzoanМetrаrаbdo,os' Thе thrеe living spесiеsаrе doсumеntеdЬy fossils,Ьut a furthеrnine spесiеsarе еxtinсt. Intensесollесtingthroughoutthе СariЬЬеanhas rеvеalеdthе pattеrnof spесiation.Samplingin thе timе from 25 to 8 rnillionyеarsago is sporadiс,Ьut thе timе from 8 to 4 million yеars ago, thе Dominiсan Sampling Intеrval (DSI), is еxtremеly wеll known' Ьasеd on a finе and сontinuous fossil rесord on thе island of Dominiсa. Spесiеsdistinсtionsаrе Ьasеdon a сomЬinаtionof morphologiсaland gеnеtiсstudiеs.
stasis might bе a fеaturе of taxa that oссupy unstaЬlе еnvironmеnts' whiсh сan vary rapidly and dramatiсally, Ьut thosе taхa do not еvolvе in linе with е v е r y е n v i г o n m е n t a fIlu с t u a t i o n '
Quality Thе quality of thе fossil rесoгd has oЬsеssеdand сontinuеs to oЬsеsspalеoЬiol. ogists. Еvеr sinсе Dаrwin (1859, 279) considеrеdthе ..impеrfесtionof thе gеo. logiсal rесord,'' palеobiologists and othеrs havе osсillatеd in thеiг сonfidеnсе. Somе havе сlaimеd, pеrhaps rathеr wildly, thаt еvеrything thе fossil rесord says is сorrесt, whilе othеrs, pеrhaps еqually wildly, havе rеiесtеd thе fossil rесord as bеing nеxt to usеlеss.Thе truth prеsumaЬly liеs somеwhеrе Ьеtwееn' and most pеoplе taсitly vееr to thе positivе еnd of thе spесtrum. A numbеr of ma. jor сhallеngеs havе arisеn rесеntiy' howеvеr, and I shall touсh on thеsе briеfly.
A quаlitativе аrgun nothing Inuсh nеw hа was Stillin 1859 аrgu urian rеptilеs and Dе. rеturn to еarth. DarW сollгsе' аnd hе knеw а vonian, amphiЬians ir in thе Тriassiс, zrnd m. 1 8 5 9 , a n d d е s p i t еt h е havе simply adjustеd has Ьееn pushеd Ьасl phibians from thе еar rеptilеs fгorn tlrе еаrl of mаmmals frorrr tht has rеmainеd unсhan lеssly unrеprеsеntativ to timе. Thе notion of a got by Мaхwеll arrd Bеntr of thе mаrinе animal l knсlwledgе from 1890 Ьoth сasеs thе sum tot Ь l i n g i n 1 0 0 y е a r s ,Ь u to timе, and sсl thе rеmainеd unaffесtеd. whеthег nеw fossil dis Thеу found thе formс thе сomplеtеness of tl morе oftеn thаn сrеet Тhеге havе Ьееn tw sampling еffесts zrrrdl thаt thе fossil rесord а light thе faсt thаt thе wеll known it is, thе { Ьodiеd oгgarrisrnsadе h z r p sl i v i n g i n u n u s u а l Thе сritiсisms of sa (2001,2007) arguеd гoсk rесord, whiсh itl posеd ехtinсtion еvеl thеrе is a major rеgrеs parеntly disappеar frt Ьut it is mегеly а sеdir еvеr, that thе divеrsifil is pгoЬaЬly rеal Ьесar v е r s i t yi s n o t d r i v е n Ь
Pаlеoпtologуапd tbе Histсlrу of Life
unguiculaturn group
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юzoanМеtrаrаbdotos.Thе thrее a furthеrninе spесiеsаге ехtinсt. has rеvеalеdthе pattегnof 8 million yеarsago is sporadiс,Ьut )ominiсanSamplingIntеrval(DSI), l сontinuousfossil rесord on thе Ьasеdon a сomЬinаtionof
upy unstaЬlееnvirоnmеnts,whiсh osе taхa do not еvolvе in linе with
l аnd сontinuеsto oЬsеsspaleoЬiolidеrеdthе ..imperfесtionof гhе gеohavе osсillatеd in thеir сonfidеnсе. hat еvеrythingthе fossil rесord says ldly, havе rеiесtеdthе fossii rесord rably liеs somеwhеrе Ьеtwееn, and of thе spесtгum.A numЬеr оf maг' and I shall touсh on thеsе bгiеfly.
A qualitativеaгgumеntfirst, in favor of thе fossil rесord, is thаt sinсе 1859 nothingtnuсlrnеw has сlrifеrous. rеptilеs in thе Pеrmiаn, dinosauгs in thе Triassiс,аnd maпrtnaisand Ьirds in thе Jurzrssiс.In thе 150 yеars sitrсе 1859,and dеspitеthе input of millions of hours of sеarсhing,palеontologists havеsimply adjustеdthе rrrid-Viсtorianpiсturе: thе origin of agnаthan fishеs has Ьееrrpushеd Ьасk from thе Silurian to thе СаmЬrian, thе origin of amphiЬiansfrom thе еarly СarЬonifеrous to thе latеst Dеvonian, thе origin of rеptilеsfronr tlrе еarlу Реrmian to thе rrrid-СarЬonifеrous, arrd thе origin of mammals from thе mid.Jurassiс to tlrе latе Triassiс. Thе origin of Ьirds .!7еrе hаs rеmаinеd unсhangеd in thе latеst Juгаssiс. thе fossil rесord hopе. r-rеwfinds should providе mаjor surprisеs from timе lеsslyr.rrrrеprеsеtltativе' to timе. Thе notiсln of a gotrd fossil rесoгd was сonfirmеd in quantitativе analysеs Ьy Мaхwеll and Bеnton (|990) сlf thе vеrtеЬratеrесord arrd Sеpkoski (199З) оf thе milrinе аnimal rесord. Thе first authors lookеd at thе aссumulation of knowlеdgеfrtlm ] .990 to 1987, thе sесond аt сhаngеs from 1982 to |992. In Ьothсasеsthе sum totals of divеrsity through timе inсrеasеd,еssеntiаllydouЬling in 100 yеars, Ьut thе inсrеаsеswеrе randomly distriЬutеd with rеspесt to til1-lе,and stl thе ovеrаll pаttеrns of divеrsifiсations and ехtinсtions rеmainеd unаffесtеd. In a furthеr study Bеnton and Storrs (1994) tеstеd rvhеthеrrrеw fossil disсovеriеstеnd to fill prеdiсtеd gaps or сrеatе nеW gaps' Thе,vfound thе formеr: in 25 yеaгs of study, nеw fossil finds haсl improvеd thе сomplеtеnеssof thе tеtrapod fossil rесord Ьy somе 5% Ьу plugging gаps morе oftегtthаn сrеating llеw saps. Тhеrе havе bееn two rnajor сhallеngеsto this somеwhat сomplасеnt viеw: sampiingеffесtsand mоlесular phylogеniеs.In both саsеs thе сritiсs aссеpt that tlrе fossil rесnеvеnts аrе nothing morе thаn сlrengеs сrf еnvironmеnt. If thеrеis a mаjor rеgrеssiсln(rеtrеаtof thе sеa),sh:rllowmаrinе organisms аpparеntlydisappеar from sесtions. This сould Ье rесordеd аs an еxtinсtion' but ir is mеrеIyа sеdinlеntаryаrtifaсt. Snrith (200t ,2007I poirrtеdout' howеvеf'that thе divеrsifiсationof lifе in thе sеa durirrgthе last 250 million yеars is proЬablv rеal bесаusеsеa lеvеls wеrе falling duгing this timе: thе risе in divеrsit1, is ntrt drivеn Ьy a гisе in sеa lеvеl.
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1 0 0 Pаleontologу апd the Historу of I,ifе Pеtегsand Footе (2001,2002) wеnt onе stеp furthеr, arguing that virtually all thе fossil rесoгd is сlosеly dеpеndеnton thе sеdimеntaryrесord. Supposеd rxtinсtions' divеrsifiсations,and otlrеr Ьiolсlgiсalpattеrns arе аl1 apparеntly drivеn Ьy thе volumе of pгеsеrvеdroсk. Thеsе authors found that thе divеrsity of lifе apparеntly matсhеs thе numЬеr оf namеd roсk formations in North Amеriсa. So, thеy arguеd, whеn lifе аppеаrs to Ье divеrsifying, it is simply bесausеthеrе is morе sеdiпrеntaryroсk and lrеnсеmore fossils.IWhеn a mass еxtinсtion is idеntifiеd' it is nothing morе than a loss of apprtlpriаtе roсks in whiсh to prеsегvеfossils. Thеsе viеws hаvе Ьееn sееn as pеrhaps rаthеr еХtrеmе (Bеnton 2003; Pеtеrs 2005). Thе сorrеlation of numbеrs of namеd formations and divегsityof lifе rеpoгtеd Ьy Pеtеrs and Footе (2001,2002) сould Ье rеvеrsеd:it is just аs likеly that whеn lifе is divеrsе аnd fossils aге aЬundirnt' gеologistsrесognizе and namе morе formations. In gеnеral' of сoursе, as wе always tеасh oLlr stu. dеnts, сorrеlatioп does not imply сausatiotl.Furthеr, assurningthat roсk volumе, or somе proхy for roсk volumе, is purе еrror in our undеrstandingof thе fossil rесord and should thеn bе applied as a сOrrесtion fасtor is hеavy handеd-maior Ьiologiсal еvеnts suсh as divеrsifiсatiсlnsand mass ехtinсtions arе rеmovеd at a strokе. As Pеtеrs (2005) pointеd out' thеге ls no rеa. son to rеjесt thе proposal that mаrinе roсk volumе and marinе divеrsity might vary in сonсеrt with a third faсtor, suсh as sеa-levеlсlrаngе.AЬundant marinе roсks аnd aЬundant marinе fossils might aсtually rеflесt high sеa lеvеls and aЬundant marinе lifе: in suсh a сasе' to dividе thе pеak in mаrinе divеrsity Ьy thе pеak in marinе roсk voluпе would еffесtivеly rеmovе that (truе) Ьiologiсal signal. Muсh morе work is rеquirеd to invеstigatеfurthеr why thе marinе roсk and fossil rесords arе с
а p p r o a с h е s :f o s s i I d а t t first fossil of a group). dаtеs tend to Ье too o| spеaking froпr thе mol molесular agе douЬlin г h е i гp o s i t i o n . o n h а l l а d е v а s t а t i n gе х p o s u r l Ьееn shown to rеst on D o г h е s еd е Ь а t е sj u е v е r Ь r i d g еt h е g a p Ь е t to Ье good) and thе pr Ье donе to soпlе ехtеn Novaсеk 1l992) rеа|i sourсеs of data on th( logеny. By fossils thеy in thе roсks. Сlaсiistiсs n е W а p p r o а с h е st o d r l phologiсal oг molесulz Norеll аnd Novaсеk сomparеd for ссrngгuе thе fossils or thе trееs сhinе, oг omnisсiеnсе f o s s i l s е q u е n с е se n d t l . gruеnt' thеn proЬaЬly h i s r o г yo f l i f е . L a с k o f i s w r o n g o r t h е t r е е sa l and thеy show good с< vасеk l 992; Bеnton ar сatе thаt all grоups е. rесord' that thеrе is no fossil rесords,аnd thl r r е е sp l O r t е da g а i t l s ts t
Conсlusion
Palеontolоgy is an aп tееnth сеnturiеs. Тo m happеnеd sinсе Ьеyon poгtеdwееkly in Sсiеп аnd thе faсt that (dеs
ing is strong еvidеnсе thе history of lifе. But thе history of li а n o t h е г .g r o u p A g i v l r n a r r a t i v еi s i m p o r t а t l t
Pаlaoпtrllogуапd tbе Нistсtу' of Lifе еp furthег,arguing that virtuаlly tе sеdimеntaryrесord. Supposеd giсal pattеrnsarе aIl apparеntly sе authors found tlrat thе divеr. of namеd roсk formations in аppеaгsto Ье divеrsifying, it is ".kand hеnсе morе fossils. Whеn morеthаn а loss of аppropriatе Lthеrехtrеmе (Bеnton 2003; Pе.mеdformationsand divеrsity of 2 ) с o u l d Ь е г е v е r s е di:t i s j u s t a s е aЬundant,gеologistsrесognizе urse' аs wе always tеaсlr our stuFurthеr'assumingthat roсk volге егror in our undегstandingof J as a сorrесtion faсtor is hеаvy i v е г s i f i с a r i o nasn d m a s s е х t i n с 0 5 ) p о i n t е dО u t ' t h е r е i s n o r е а ;k volumе and marinе divеrsity ;h as sеa-lеvеlсhаngе,AЬundant rightaсtually rеflесthigh sеa lеv;е' to dividе гhе pеаk in marinе rе would еffесtivеly rепrovе that s rеquirеd to invеstigatе fuгthеr orrеlatеd,Ьut thе tеrrеstrialroсk
02).
:hе informativеnеss оf thе fossil ЬatеsaЬout thе timing of origins plaсеthе oгigins of Меtаzoa (anrd nrodеrlr oгdеrs of Ьirds ar-rd oldеstгеpгеsеntativе fossils (е.g., Kumaг and Hеdgеs 1998; Wray е of molесular еstimatеsfor thе s ago' with most еstimatеsсlosеr l ago. Thе rangеof molесulаr еsplaсеntalmammals and modеrn with morе еstimatеsnеarеr 120 э, rеspесtivеly,trom around 600 t molесulаr datеs сould indiсate ta or Ьoth. Мany сonrmеntators l Kumаr 2004) hаvе arguеd that аnd thаt thе mоlесr-llardаtеs arе )9; Bromham and Неndy 2000; potеntiаl proЬlеms with Ьoth
approaсhеs: fossil с.latеsarе always to() young, of сoursе (onе nеvеr finds thе firstfossil of a gror.rp),Ьut not outragеously too young' whilе thе molесulаr datеstеnd tсl Ье too old, somеtiпlеsЬy a long way. Graur and Martirr (2004), spеakingfronr thе rl-rolесular sidе, prеsеnt a roЬust attaсk on thе еvidеnсеfor just molесuiirragе douЬlirrg notеd, whilе Неdgеs and Kuпrar (2004| dеfеnd thеirposition.orl balаrrсе,howеvеr, thе nrolесular lindings that sееnlеdlikе a dеr,astаting eХp()surеof thе frаiltiеs of thе fossil rесord in 1996 havе norv bееnshorvnto rеst on fаr wеаkег grouтld thаn was first assеrtеd. Do thеsе dеЬatеs just rеduсе to irssеrtiсlnand с()untеrassегtion?Сan wе еvеrЬridgеthе gap Ьеtwееnknowlеdgе of thе fossil rесord (whiсh is aссеptеd t o Ь е g o o d )а n d t h е p r o Ь l е m o f u n p r е s е r v e dl i f е o f t h е p a s t ? P е r h a p st h i s с a n bе donе to somе ехtеnt. ln a Ьrilliаnt ехamplе of latеral thinkrng, Norеll and Novaсеk (|992\ rеalizеd that еvolutiolristsuniquеlv had thrее indеpеndеnt sourсеsof dаta on thе history оf lifе: fossils, сladistiсs, aпd rnolесular phylogеny.By fossils thеy mеant thе stratigrаphiс сlrdеr of oссurrеt-tсе of fossils irrthе roсks. Сlaсiistiсsand nroiесular phylogеn1'rесOnstruсtiotrlrе rеlativеly nеWapproaсhеsto drаwing еvolшtiol-rary trееs' rvlrеtlrеron thе Ьasis of lrr
Сonсlusion Palеontologyis an аnсiеnt suЬjесt, dating Ьaсk tсl thе siхtееnтh or sеvеntееnthсеntttriеs.To п]any' it had its hеyday in Viсtorian timеs, and littlе has happеnеdsinсе Ьеyond thе disсovеriеs of nеw dilrosаurs and lronrinids rе. portеd wееklу l'nSсiепсе aг'd Nаtltrе' In a sеnsе,as I havе ilrgttеd, thаt is trr.tе, аnd thе faсt that (dеspitеtlrе сlain-rs)thеsе t-tеwdisсtlvеriеsaге rtrrеly slroсk. ing is stгоngеvidеrrсеthat tlrе fossil rесord tеlls us solnеthinЕ]truthfr.llirlrtlut tlrе histсtгyof Iifе. But thе histoгy of lifе is morе than just а nаrrativе of first onе fossil, thеn anothеr'group A givillg Wav to grсltrpB' and so On through to mankind. Thе narrativеis important for what it tеlls us aЬout thе аstonishin!]invеntivеnеss
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1 0 2 Pаlеoпtologу апd thе Нistorу of Lifе .$Иhiсh of lifе, its aЬility to еvolvе and do unprеdiсtаЬlеthings. Dеvonian oЬsеrvеrwould havе prеdiсtеd that thе multilimЬеd insесtsthat сrеpt round thе watеrsidе plants would onе day takе to tlrе air? \Whiсh Jurassiс oЬsеrvеr would havе guеssеdthat thе insесts shе saw flitting and danсing in tl-rеsunlight around thе muddy lеgs of thе dinosaцrs would еvolvе soсiality ilrrd thеrr drivе thеir Ьiodivеrsityand gloЬal Ьiomass t<> untold lеvеls?Сurrеt-ttЬiodivеrsity is highеr thаn it еvеr has Ьееn.!Иhеrе пlight lifе еvolvе nехt? Thеrе аrе intimаtions of miсroЬеs that livе in iсе and iп boiling Watеrs, and soпrе that livе pегhaps thrее kilomеtеrs down within thе roсks Ьеnеath thе sеa floor. Thеsе ехamplеs strain сrеdulity, but thеy havе happеned and arе happеning. Thеrе is morе to thе study of thе history of lifе, though, than mеrе doсumеntation of fossils. Fossils rеprеsеnt ехtinсt groups. Dinosаuгs сannot Ье prеdiсtеd from molесulеs, bшt thеy ехistеd arrd show us organisms tlrat did what no living animal doеs. Somе dinosаLlrswеrе 10 timеs thе nrass of thе lаrgеst living maпrrlals. Somе ptеrosaurs Ьad wingspans thrее or four гimеs thosе оf thе largеst Ьirds today. Somе ехtinсr arthropods wеrе largеr than any alivе today. Thеsе organisms arе all truly wondеrful, and thеy posе intеrеstingproЬlеms fсlr Ьiomесhaniсistsand physiologists. Divеrsifiсations and mаss ехtinсtions саn Ье prеdiсtеd (rеtrodiсtеd?)from studiеs of modеrn phylogеniеs,Ьut thе dеtails lravе always rеmainеd mystеrious. Palеontologists havе tlrе grеat plеаsurе of Ьеirrg aЬlе to dissесr suсh еvеnts in finе dеtаil, and as fossil-сollесtingtесhniquеs'thе prесisiorrof dating, and еnvironnrеntalanalytiсal tоols iпrprоvе, thе lеvеl of undеrsranding will inсrеasе. Spесiation сan Ье studiеd in thе laЬoratory and in long.tеrm studiеs in thе fiеld, Ьut thеrе is always a timе limit. Now' with improvеd сollесting and dating tесhniquеs,palеonrologiсal studiеs of spесiеsеvolution and spесiеssplitting сan Ье tiеd sеamlеsslyto thе prеsеntdаy, :rrrdwe arе Ьеginningto sее for thе first timе maсroеvolutiorrir.raсtion. Nеw finds сapturе thе hеadlinеs, Ьut nеw insights into Ьioгnесhaniсs, largе-sсаlееvеnts,and maсroеvolution arе еvеn morе imprеssivе.Tlrе study of thе history of litЪ has nеvеr Ьееn morе ехсiting than it is now. в|BLIoGRAPHY Bеnton,M. J. 1985.Маss ехrinсtiоnanlOngnоn-nrаrinе tеtrаpods. Nаturе3|6: 811-814. 1987.Progrеssаnd сompеtitionin llrirсroеvolutitл. Bhklgiсаl Rс,t,iсtlls 62-: 3 0 5 - 3 38 . 1995.Divеrsi{iсation аnd ехtinсtionin thе historyof |tfe.Sсieпсе268: 52-s8. 1997.Modеls {or thе divеrsifiсаtiono| \ifе.Тrепdsiп Есologу апd Еuс.llutioп|2: 490-495' |999' Еar|уоriginsof modеrnЬirdsand пrапrmals: Мolесulеsvs. mоrphоlogy.BlсlЕss.:1's 21: 1043-1051. 2003.Thе qualitvof thе fossilrесord.lп P. C.-. .}.Donoghuеаnd М. P. Sпrith,еds.,TеIliпgthе Еuоlutioпаrу-Тiпtе:МtэIесulаrСbсks апd t|lе Fсlssil Reссlrd,66-90. Boсa Raton,FL: СRС |)геss.
Bеntоn'N4.J.' and F. J B е n t o n 'М . J . , a n d D . l.ongman. 2О08.Iпtrodu Blaсkwеll. Bеntorr'М. l., аnd P. l
L|сrllсlgуаltd Еuol Bеntсln, М. J., anсl G. Palеontоlоgiсal kr Bеnt
Pаlеoпtologу аnd thе Historу of Life
:taЬlеthings.Whiсh Dеvoniаn oЬ. limЬеdinsесtsthat сrеpt round thе thе air? \Иhiсh Jurassiс oЬsеrvеr rw flitting and danсing in thе sunrrs would еvolvе soсiality and thеn to untold lеvеls?Сurrеnt Ьiodivеrnight lifе еvolvе nеxt? Thеrе аrе inLЬoiling Watеrs' and somе thаt livе roсks bеnеath thе sеa floor. Thеsе p p е n е da n d a r е h a p p е n i n g . y of lifе, though, than mеrе doсuinсt groups. Dinosaurs сannot Ье l and show us оrganisms that did LrrsWеrе 10 timеs thе mass of thе rad wingspansthrее or four timеs tinсt arthropоds wеrе largеr than r u | y w o n d е r f u l .a n d r h е y p o s е i n lphysiologists. n Ье prеdiсtеd(rеtrodiсtеd?)from ails havе always rеmainеd mystеriurе of Ьеing aЬlе to dissесt suсh g tесhniquеs'thе prесision of datlprovе' thе lеvеl of undеrstanding lry and in long-tеrmstudiеs in thе with improvеdсollесtingаnd dat;pесiеsеvolution and spесiеssplitry, and Wе arе Ьеginningto sее for nеw insights into Ьiomесhaniсs, ) еvеn morе imprеssivе.Thе study lхсiting than it is now.
n-marinеtеtrapods.Nаturе З16: :roеvolution'B iologiсаl Rеuiеtas 62: thе history of |i|e,Sсiеnсе 268: |lfe' Тrепds iп Есoklgу апd d mammals:Мolесulеs vs. tn P. С. J. Donoghuе аnd М. P. : МоIесulаr СIсlcks апd thе Fossil is.
Bеnton,M. J., and F. |. Ayalа. 2003. Dating thе trее of |ife.Sсiепсе30О: 1698_\70О. Bеnton,N,I.J., and D. A. T. Нarpеr. 1997. tsаsiсPаlеспtologу. Нarlow, Еssех' U.K.: l,ongmаn. 2008. Iпtrodl|сtioп to Pаlсobiсiogу апd thе Historу of Life, Oxford: Blaсkwеll. Bеnton' M. J., and P. N. Pеarson ' 2001 , Spесiation in thе fossil rесord. Тrепds iп F'сologу апd Еurllиtklп 16: 4О 5-41 1'. .W. Stоrrs. 1994. Tеsting thе quality of thе fossil rесord: Bеnton,М. J., and G. Pаlеontologiсаlknowlеdgе is improving. Geologу 22z |t|_1\4' Bеnttln,М.J., М. A. Wills, аnd R. Hitсhin. 2000. Quality of thе fossil rесord through ttmе.Nаturе 4ОЗ: 5З4_5З7. Brоmham, [-.D., and М. D. Hеndy. 2000. Сan fаst еarly ratеs rесonсilе molесular dаtеs tсl thе СamЬrian ехplosiоn? Proсееdiпgs сlf thе Roуаl Soсiеtу of Loпdoп, Sеriеs B 267: "l'041-|047 .
Сhееtham'A. H., and J. B. с.Jaсksоn. 1995. Proсеss {rom pattеrn:Tеsts for sеlесtiоnvеrsus random сhаngе in punсtuatеd Ьryozoan spесiation.In D. H. Еrwir"rand R' I,. Anstеy, еds.' Neи, Аp1lrоасhеs to Spеciаtkп iп thе Fossil Rессlrd,\84_207. Nеw York: СoluIтЬia Univеrsity Prеss. Соnway Мorris, s. 2003. Lifе's Solutioп: Iпеuitаblе Hиmапs iп а Loпеlу Uпiuеrse. СаmЬridgе: СаmЬridgе Univеrsity Prеss. Соopеr, A., аnd D. Pеnny. 1997. \4ass survival of Ьirds aсross thе СrеtaсеousMolесulаr еvidеnсе.Sсieпсe275: 1109-1'113. Tеrtiаrу Ьor-rndaтy: Darrvin, с. 1tls9' Оп thе Оrigiп of Spесles.London: John Мurray. Еastеal,S. 1999. iVlolесulаrеvidеnсеfor thе еarly divеrgеnсеof plaсеntal mammals. Bbl.ssays 21 :'l 0.52-10-58. Еldrеdgе'N., and S. J. Gould. 1972. PunсtuatеdеquiliЬria: An altеrnativеto phylеtiс grаdualism.In T..|. M. Sсhopf, еd.,МodеIs iп Pаleobiology, 82_115. San Franсisсo:Frееman, Сoopеr. Еrwin, D. Н., and R. L. Anstеy. 1995. Spесiation in thе fossil rесord. In D. H. Еrwin аnd R. I-. Anstеy, еds., Nси Аpрrсlасhеs fu Spесiаtiсlп iп tbе Fossil Rеcord' 11_28. Nеw York: Сolumbiа Univеrsitу Prеss. Fаrа, F].2002. Sеa lеvеl variations аnd thе quality of thе сontinеntal fossil rесord. ]сlttrпаIof the С}еologicаlSсlсiеtу, Lсlпdoп 159:489491'. Gould, S. .|. 1990.Is а nеw and gеnеral thеory of еvolution еmеrging?Pаleobiologу
6 : 1I 9 - 1 3 0 . Gould, S.J., and С. B. Сalloway. 1980. Сlаms and Ьraсhiopods-ships that pass in thе night. PаIеobiologу6: З8З-396. Graur, D.' and \й/.Martin. 2004' Rеading thе еntrails of сhiсkеns: Мolесulаr timеsсаlеs of еvolution and thе illusiоn of рrесision. Trепds iп Gепеtiсs 20: 80-86. Неdgеs'S. B., and S. Кumar.2004. Prесision of molесular timе еstimаtеs.Trеndsin Gепеtiсs 2О: 242-247. Hеwzulla, D., М. с. Boultеr, М. J. Bеnton, and J. M. Hallеy. 1999. Еvolutionary pattеrnsfrom mass originatiоns and mass ехtinсtions. Philosophiсаl Trапsасtioпsof thе fuцаl Soсiеtу,SеriеsB З54:46З-469. Kumar, S., аnd S. B. Hеdgеs' 1998. A molесulаr timеsсaiе{or vеrtеЬratееvolution. Nаtиrе 392 917_920. LaЬandеira'C. С., and J. J. Sеpkoski lr. 1993. Insесt divеrsity in thе fossil rесord. S с i е п с е2 6 1 : 3 1 0 - 3 1 5 Lаndе, R. 19B6. Thе dynamiсs of pеak shifts and thе pаttеrn of morphologiсal еvolution. Pаlеobiologу |2: З4З_3 54. Mахwеll' W. D., and М. J. Bеnton. 1990. Historiсal tеstsof thе absolutе сomplсtеnеssof thе fossil rесord of tеtrаpods.Pаlеobiologу 16:322-3З5. May' R. \4. 1994. Соnсеptual аspесts сlf thе quantifiсation of thе ехtеnt of Ьiologiсal divеrsity. l,hilсlsophiсаl Тrапsасtit-lпsсlf thе Roуаl Soсietу, Sеriеs B 345:13-2О.
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Pаleontologу апd the Historу of Life Мaynard Smith,J., аnd Е. Szаthmirу. 1995.Thе Маior Trапsitionsiп Еuolцtioп. Oxford:.W.H. FrееmanSpеktrurn. Niklas, K.J., B. Н. Tiffnеy,and A. H. Knoll. 1983.Pattеrnsin vasсularland plant divеrsifiсation . Nаturе3О3:6\4-616. Norеll' М. A., and М. J. Novасеk.|992. Thе tЪssiIrесordаnd еvoluriоn: Сomparing сladistiсand palеontologiсеvidеnсеfor vеrtеbratеhistory.Sсieпcе 255 1690-1.693. histoгyof mаrinе Pеtеrs,S. Е. 2005. Gеologiссonstrаints on thе maсroеvоlutionаry animаls.Proсeеdingsof thе Natioпаl Асаdemу of SсiеttсеsUSА 102: |2З26_1'23зI. in thе Phanеrozoiс: A rеintеrprеtation. Pеtеrs,S. Е., and М. Footе.2001.Biodivеrsity Pаlеobio logу'27: 5 83-6О1. 2002. Dеtеrminantsof ехtinсtionin thе fossilrесord.Nаtиre 416:420424. Sеpkоski,J.J.' Jr. 1'984.А kinеtiсmodеlof Phanеrozoiсtaхonomiсdivеrsity.III. Post-Palеozoiсfamiliеsаnd masseхtinсtions.Pаleobiologv\О: 246_267. |992'Phу|ogenеtiсand есologiсpаttеrnsin thе Phапеrozoiсhistoryof mаrinе Ьiodivеrsity.In N. Еldrеdgе,еd.,Sуstеmаtiсs,Еcologу,апd thе BiodiuеrsitуСrisеs,77-100. Nеw York: Сolumbia UnivеrsityPrеss. 1993.Tеn yеarsin thе librarу:How сhangеsin taхonomiсdataЬasеsaffесt pеrсеptionof maсroеvоlutionarypattеrn.Pаlеobiologу|9: 4З_5|. Thе douЬlеwеdgеrеvisitеd.In D. 1996.Сompеtitionin maсroеvolution: D. Н. еds', ЕuolutklпаrуPаlеobiologу, Н. Еrwin, and Lipps, J. Jablonski, 211-255.Сhiсаgo:Univеrsitvof СhiсagoPrеss. еvolutionof ordoviсiantrilobitеs.Nаtцrе Shеldon,P. R. 1987.Parаllеlgradualistiс 330:561-563. 1996.Plus ga сhаngе-A mоdеlfor stasisand еvolutionin diffеrеnt Pаlеoсlinшtologу,Pаlесlесologу127:209-227. Pаlеogесlgrаpllу, еnvironrnеnts. for hеtеrogеnеity of thе fossilrесord:Impliсations Smith,A. B.200 l. Largе-sсalе Phanеrozoiсbiodivеrsitystudiеs.PhilosophicаlTrапsасtiсlnsof tbе Roуаl Societу,SeriеsB 356: 1-|7. PrоЬlеmsаnd prospесts. 2007. Магinе divеrsitythroughthе Phаnеrоzoiс: lournаl of thе GeologiсаlSociеtу164:731_745. Sorhannus, U., Е.J. Fеnstеr'L. Н. Burсklе,and A. Нoffman' 1998.Сladogеnеtiс aпd anagеnеtiссhаngеsin thе morphologyof Rhizсlsolепiаprаеbеrgoпii Мцkhina. HistoricаlBiologу 1: 185-205 Stanlеy,S. М. 1975. A thеoryof еvolutionaЬоvеthе spесiеs|eуe|.Proсееdiпgsof thе Nаtioпаl Асаdemу of SсiеnсеsUSА 72: 646-650. 2007. Аn analysisof thе historyof marinеаnimаl divегsity.Pаlеobiolog,Меmoirs4. Pаlеobiology 33 (Suppl.):1-55. doсumеntation of spесiationin Сеnоzoiс Williamson'P. G. 1981.Palеontologiсаl mollusсsfroпrthе Turkana Basin. Nаture 29З: 4З744З. \йИrаy, G. A.2001. DatingЬranсhеson thеTrееof Lifе usingDNА. GeпomeBiсllogу 3:
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Adaptr
JosеphT
What Is Adaptа
Тlrе fеаturеs ()f org lifеstylеs. ln soпtе . Ьrown, mottlеd m( fusеlу shаdеd Ьrov that ссlmЬinе tO pе ing Ьird еggs hаv( s n a k е s ) ,l l o u t h s w ] Ьraе Ьеhind thе nt еmpty shеlls for е: fundaпrеntа1oЬsег how rlrеsеmatсhеs gists want to solvе Thе еаrliеst sсiе tеstеd with oЬsеr еmеrgеd through : wеrе сrеatеd Witl.l priatе f()r thеir ра Wеnt ехtinсt, lеtrv stanсеs. This thсo or ехtinсtion tlf v. loсations (е.g.,Тo n 6 n d е z I s l а n d :Е i s апd it sееmеd rеаs othеrs through tl that naturе сOuld Тhе tlrеorу of a thе ссlnviсtiorrthс intеrvеnеd throuр thе fеilturеs of Pl. and pеts Ьorе аm
,he Маjor Trапsitiсlпs iп Еuolutiсlп. 983. Pattеrnsin vasсulаr land plant Ъssil rесord aпd еvolutioп: dеnсе for vеrtеЬratеhistory. Sсiепсе maсгoеvolutionary history of marinе lеmу oi Sсiепсеs IJSА |О2: n tЬе Phanеrozoiс:А rеintегprеtаtion. е fossil rесord. Nаture 416 420424. anегozoiэtаxonomiс divеrsity. III. ns. Pаlеobiologу 10: 246-267. n s i n r h е P h l n е r o z o i сh i s t o r yo f уstemаtiсs,Ессllogу, апd thе olumЬia UnivеrsityPrеss. angеs in taxonomiс datа Ьasеs аffесt Pаleobiologу 19: 4З_5 1. Thе douЬlе rvеdgеrеvisitеd. In D. Js., Еuolutio паrу Pаl аl b iologу, Prеss. tion of ordoviсian triloЬitеs.Nаtиrе sis аnd еvolution in diffеrеnr ftologу, Pаleoесologу 127 : 2О9-227. .thе fossil rесord: Impliсаtions foг biсаl Trапsасtioпs of thе Roуаl anеrozoiс: ProЬlеms and prospесts. -745. lA. Hoffmаn' l998. Сlаdоgеnеtiс ' of Rhizosolепiа prаеbеrgoпii vе thе spесiеs|eve|.Pr
Adaptation JosеphTrаuisапd DаuidN. Rezniсk
What Is Adaptation? Thе fеarurеstlf orgzrnisпlsarе wondеrfully suitеd to thеir еnvironmеnts and lifеstylеs.In sonlе сasеs thе mаtсlr of fеaturе аnd еnvironmеnt is simplе: a browтr,mсlttlес]moth is сryptiс to its prеdators whеn it is rеsting on a diffusеly slradеd Ьг
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Adаptаtiсlп fеaturе of a plant or animal. But thеrе wеrе oЬvious limits to mallеaЬilityсhiсkеns саnnot bе Ьrеd to lаy two еggs pеr day evеry day of tlrеir livеs-and naturе sееmеdaЬlе to distingurshonly suЬstantialdiffеrепсеsamong spесiеs or stoсks (Provinе 1971; Rusе 1979)' Thеsе substantial diffеrеnсеssееmеd сapaЬlе of Ьеing produсеd only Ьy sеlесtivеЬrееdingof faгm stoсk (if naturе Was sorting among variеtiеs of donrеstiс goats introduсеd to an isl:rnd) or original сrеation (if naturе was sorting among spесiеs). This еxplanation of adaptiltion Ьесamе inсrеasingly сumЬеrsome аs morе and morе fossil organisms wеl.еdisсovеrеd.Foг onе thing, layеrs of roсk that inсludеd fossilizеd spесiеs did not inсludе fossilizеd matеrial from еxtant spесiеs;if naturе wеrе mеrеly filtеring spесiеs'whеrе Wаs thе еvidеnсе that еxtant spесiеs had еvеr сoехistеd with ехtinсt onеs? For anothеr' although many fossil organisms Ьorе limlе rеsепrblanсеto еxtant onеs (е.g.'dirrosaurs), othеrs sееmеdvеry similar to еxtant spесiеs(е.g.'fossil floundеrs).It was unсlеar why onе spесiеsshould havе gonе еxtinсt wlrilе anothеr with vегy simi. lar fеaturеsshould pеrsist. Thе sсiеntifiс rеvolution in thе studу of adаptation is thе idеa of natural sеlесtion' as suggеstеdЬy Сharlеs Darwin and Alfrеd Russеl wallaсе. Although both mеn offегеd thе idеa, it wаs Dагwin who artiсulatеd it пrorе сomplеtеly and intеgratеd it morе thoroughly into a largеr thеory of Ьiologiсal еvolution. As a rеsult, wе usе thе tеrm Dаrшiпiап еuolutiсlп to rеfеr to thе proсеss through whiсh adaptations еmеrgе'a proсеssalso саllеd еuolutioп bу паtиrаl selесtiotl or аdаptiue euolutiсlп. In Darwinian еvolution, natural sеlесtion, соuplеd with inhеritanсе of small trаit diffеrеnсеs'is thе аgеnt of adаptation. Natuгal sеlесtionis a statistiсal filtеring Proсеss; individuals with partiсular сharaсtеristiсs аrе morе likеly to survivе or produсе morе offspring than individuals with othеr сharaсtеristiсs.A morе formal dеfinition of natural sеlесtionis thе сausal аssoсiation of a fеaturе or trait with fitnеss. Bу fitпеss wе mеan thе numЬеr of offspring that an individual lеavеsЬеhind; individuals that diе without rеproduсing havе zеro fitnеss. The саusаl аssoсiаtioп of а feаture or trаit tuith fitness mеans' opеrationally, that a fеaturе or vаluе of а rrait is dirесtly rеsponsiЬlе for whеthеr an individuаl livеs or diеs or why somе irrdividuals lеavе morе offspring than othеrs. For еxamplе' many frogs brееd in tеmpоrary pсlnds thаt hold watеr for a Ьriеf pеriod and dry еvеry sеason.Thе tadpоlеs in thеsеponds must сoпrplеtе thеir dеvеlopmеnt into juvеnilе frogs Ьеforе thе pond driеs and thеy arе killеd. Tadpolеs with vеry slow ratеs of dеvеlopmеntdiе Ьесausеthеy сannot сomplеtе mеtamогphosisЬеforе thе pond driеs. Nаtural sеlесtiоnfiltеrs individuals with diffеrеnt ratеs of dеvеlopmеnt so that only thosе with morе rapid dеvеlopmеnt еmеrgе from thе pond. This filtеring would havе no lasting effесt if irrdividuals who dеvеlopеd rapidly wеrе not gеnеtiсally distinсt from thosе that dеvеloped slowly. Thе еffесtivеnеss of natural sеlесtion еmегgеs from thе hеritaЬlе naturе of trait variation; in thе nехt gеnеration thе gеnеtiс variаnts rеsponsiЬlеfor thе favoraЬlе trzritvaluеs will inсrеasе in rеlativе aЬundanсе. In tlrе frog ехaпrplе,
thе gеnеs rеsponsiЬlе fo thеy wеrе in thе prеviotr dеvеlopmеnt diеd with . quеnсy of thе favorеd gt lесtion to inсrеasе;morе avеragе thе nехt gеnеrаt
lесtion oссurs сonsistеnt Ьеing sеlесtеd сh:rngеsu tiotr aсts on тгаit vаriаt g r е a t е rг h е с u m r r l e t i v ес An аdaptation is any nеtiс rеsрonsе to а spесi plе' wе сall rаpir'1dеvеlo tеmporary ponds. Adap Ьесausе it еxplаins thе п v o k i n g p u r p t l s е f u ld е s i g mеnt for how nеw spе populаtions down divе1 Ьесomе so ехtеnsivеthа
Sеparlrtеspесiеs. Darwin's сritiсal argt сould irrdееd disringurs t r a v е l s h е h a d s е е n 't l п tions of thе samе plan сasеs thеsе diffеrеnсеsr Arсlripеlago; in othегs l i n t h е s a m е Ь i r t ls p е с i е madе rhеsе kinds of oЬ Hе saw all thеsе с1iffеr n а t u г с a s f i I t е r i l l gе х i s t individuаl diffеrеnсеs t
suЬstаntiаlсuпlulаtiv a m o n g p o p u l a t i o n s .Т } tion of whеthеr natural whethеr trait diffеrеnс and ultirnatеly whеtЬ i n t h е i r s е | е с t i r 'rее g i m a half.
Еvidеnсе for Adap
Biologists hirvе сonttn mеnt and havе ехtеnс lеvеl. Thеy havе alsс mаkе sсiеntifiс еxpla
АdаDtаtioп е obvious limits to mallеaЬilitydаy еvеry day of thеir livеs-and ;tantialdiffеrеnсеsamong spесiеs sе substantial diffеrеnсеs sееmеd Ьrееdingof farm stoсk (if naturе ;oatsintroduсеd to an island) or ,ngspесiеs). nсrеasinglyсumЬеrsomе as morе For onе thing' layеrs of roсk that : fossilizеd matеrial from еxrant :iеs,whеrе was thе еvidеnсе that inсt onсs? For anothеr, although :еto еxtantonеs (е.g.,dinosaurs), (е.g.,fossil floundеrs).It was unn с r w h i I еa n o t h е гw i t h v е r y s i m i laptationis thе idеa of natural sе.!7allaсе. Alfrеd Russеl Although ho аrtiсulatеd it morе сomplеtеly argеr thеory of Ьiologiсal еvolul еuolution to rеfеr to thе proсеss ;s also сallеd еuolиtioп bу паturаl эn, сouplеd with inhеritanсе of . t i o n .N a t u r а l s е l е с t i o ni s а s t a t i s rtiсulаr сharaсtеristiсsаrе morе than individuals with othеr сharrral sеlесtionis thе сausal аssoсifitпеss we mеan thе numЬеr of rdividualsthat diе without rеprotion of а feаture сlr trаit tuitb fitor valuе of a trait is dirесtly or diеs or why somе individuals rary ponds that hold watеr for a llеs in thеseponds must сomplеtе 'rе thе pоnd driеs and thеy arе :lopmеntdiе Ьесausеthеy сannot :iеs.Natural sеlесtion filtеrs indirt so that only thosе with morе :сt if individuals who dеvеlopеd hosе that dеvеlopеd slowly. Thе гom thе hеritablе naturе of trаit с variаnts rеsponsiЬlе for thе faaЬundanсе.In thе frog ехamplе,
thе gеnеsrеsponsiЬlе for morе rapid dеvеlopmеnt arе morе сommon than thеywеrе in thе prеvious gеnеrationЬесausеthе gеnеsrеsponsiЬlеfor slowеr dеvеlopmеntdiеd with thе tadpolеs that сarriеd thеm. Thе inсrеasе irr frеquеnсyof thе favсlrеdgеnеsсausеs thе avеragеvaluеs of thе traits r.rndеrsеlесtionto inсrеasе;morе сopiеs of gеnеsfor rapid dеvеlopmеntmеan that on .Whеn nаtural sеavеragеthе nеxt gеnеrаtionof tadpolеs will dеvеlop fastеr. lесtionoссurs сonsistеntlyovеr timе, thе avеragеvaluеs of thе traits that arе bеing sеlесtеdсhangе suЬstantiаlly.Thе longег and morе сonsistеntlу sеlес. tion aсts or-rtrait variаtion and thе morе gеnеtiс vaгiаtior-rin thе trait, thе grеatеrthе сumulativе сhangе in trait valuеs. An adaptation is any fеaturе of an organism that has еvtllvеd through gеnеtiсrеsponsеto a spесifiсесologiсal agеnt of natural sеlесtiсln.ln our ехаm. plе' wе сall rapid dеvеlopmеntratе an adaptation to thе risk of dеsiссаtionin tеmporaryponds. Adaptation is сеntral to Darwin's argumеnt for еvolution bесausеit ехplаins thе matсhеs Ьеtwееnfеaturеand еnvironmеnt withоut in. voking purposеful dеsign or spесial сrеation. It also providеs thе vital argumеnt for how nеw spесiеs arisе; whеn adaptivе еvolution takеs diffеrеnt populationsdown divеrgеntpaths, thе diffеrеnсеsЬеtwееnthosе populations Ьесomеso ехtеnsivеthat thеy no longеr сan intеrЬrееd,and еaсh Ьесomеs a sеparatеspес1еs. Darwin's сritiсal ergumеnt Was that naturе's filtеr, his natuгаl sеlесtion, сould indееd distinguish srтall diffеrеnсеs among individuals. Dr"rringhis trаvеls hе had sееn, timе and again, diffеrеnсеs in fеatuгеs аmong populations of thе sаmе plant or animаl spесiеs in diffеrеnt loсirtions. ln somс сasеsthеsе diffеrеnсеswеrе largе and dramatiс, as hе sаw in thе Galipagos Arсhipеlago; in сlthеrsthеy wеrе smallеr and morе suЬtlе, аs in diffеrеnсеs in thе samе Ьird spесiеsin diffеrеnt loсations in South Amеriсa. С)thеrshad madе thеsе kinds of oЬsеrvations, Ьut Darwin intеrprеtеd thеm diffеrеntly. Не saw all thеsе diffеrеnсеsas points along a сontinuum; rathеr than sееrng naturе as filtеring еxisting largе diffеrеnсеs,hе saw naturе аs filtеring small individual diffеrеnсеs that, ссluplеd with inhеritanсе and timе, produсеd suЬstantial сumulativе сhangеs in fеаturеs and suЬstarrtiаl divеrgеnсс a m o n g p о p u l a t i o n s .T h е t е s t i n g o f D a r w i n ' s a f ! ] u m е n t ,t h a t i s , t h е г е s o l u . tion of whеthеr natural sеlесtion сould Ье as powеrful as artifiсial sеiесti
Еvidеnсеfor Adaptation through Sеlесtion Biologists havе сontinuеd to dеsсriЬе thе matсh of tlrganism to еnvlronmеnt and hаvе ехtеndеd our knowlеdgе of that matсh to thе molесulаг l е v е l .T h е y h a v е a l s o u n с o v е r е d s t r i k i n g p a t t е r n s i n t h o s е m a t с h е s t h а t makе sсiеntifiс еxplanations tlthег than l)arwinian еvolution untеnilЬlе.
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1 0 8 Adаptаtiotl And through oЬsегvаtionaland еxpеrimеntal str-rdiеs thеy lravе providеd thе answеrs to quеstionsthat Darwin and his pееrs сould сlnly pondеr. v A R | Е т |E s o F A D A P т A т I o N Naturе prеsеnts a widе variеty of adaptations. Сarnivorotts plаnts oссur in nutrl.еnt-poorsoil and usе thеir aЬility to сapturе and digеst insесtsto oЬtain thе nitrogеn that otlrеr plants aЬsorb through thеir roots. Сеrtаin fish and сrustaсeans that oссur in tеmporary ponds and floodplаins havе еggs that сan tolеratе соп-rplеtеdrving аnd сan rеst in thе soil until floodwatеrs Ьrеak thе animals' еstivation and induсе hаtсhing. Sеvеral spесiеsof fish livе in polar wаtегs that would fгееzеothеr irnimаls solid' rеlying on a spесializеd аntifrееzе protеin that tnhiЬits iсе-сrystal formation within thеir bodiеs (Hосhaсlrka arrd Somеro 2002). Adaptаrions also сomе in lеss dramаtiс vаriеtiеs.Damsеlfly spесiеs in thе genas Еnаllаgп1|l tь'at еnсountеr dragonfliеs as thеir primary prеdators havе diffеrеnt pattеrns of movеmеnt and ЬеЬavioг than spесiеs that oссur with fish as thе primary prеdator. Thе Ьеhaviсlrsthаt protесt against dragonfly prеdation fасilitatе fish prеdation аnd viсе vегsa' so thе Ьеhaviors arе wеll matсhеd to thе prеvailing prеdator (МсPееk 7995). Thе fungal pathogеn Сollеtotrichиm liпdemцthiапttm grows on two сlosеly rеlatеd spесiеsof Ьеan plants oftеrrfoul-rdin thе szrmеloсаtions, Phаseolus tlltlgаris and P' сocciпus, and produсеs thе samе lеsions аnd sсarrirrgon еaсh spесiеs. But thе fungal srrains on thе two htlst plants arе spесializеd at surmounting еaсh host plant's сhеmiсal dеfеnsеs,just аs diffеrеnt spесiеs of damsеlfliеs arе spесiаrlizеdat ovеrсoming diffеrеnt prеdators (Siсard еt аl' 2007). Populations of thе fish Fuпdulus heterсlclitцs from morе northегn li.rtitudеs havе diffегеnt forms оf the еnzymе laсtatе dеhydrogеnasеthan populations from morе southеrly latitr.rdеs. Thе struсturе and thе rеgulаtion of еxpгеssion of еaсh form is tunеd to thе prеvailing thеrmаl rеgimеs to produсе sirnilar rеaсtion rаtеs асross widеly diffегеnt tеmpеraturеs,whiсh allows thе spесiеs to thrivе aсross а widе rangе of thеrmal еnvironmеnts (Sсhultе
2001).
Bioсhеmiсal adaptаtions сan Ье partiсularly striking Ьесzrusеrhеy oftеn involvе thе produсtion of diffегеt-ltmolесulеs Ьy thе samе individual at diffеrеnt stаgеsof its lifе, suсh as thе еxprеssiоrrof hеmoglobin in frogs. Irr most vеrtеЬratеsthе hеmoglobin molесulе in thе Ьlood that сarriеs oxygеn to сеlls is lеss ablе to hold oxygеn undеr aсidiс сonditions. This propеrty еnlranсеs its funсtion; сеlls that arе starvеd fоr oхygеn arе aсidiс еnvironmеnts,and hеmogloЬin will rеadily gir,е up irs oxygеrr to thosе сеils. But many tadpolеs that livе in warm, shallow ponds havе a hеmogloЬin molесulе with thе rе. vеrsеpropеrty: it holds tightly to oхygеn undеr morе aсidiс сonditiorrs.Thеsе :rnimalslivе in vегy aсidiс watеrs, and this hеmogloЬin faсilitatеsthеir aЬility to еxtraсt oxygеn from thе Watеr еvеn whеn thеrе is littlе сlf it availaЬlе. Thеiг сеlls aге lеss aсidiс thаn thе \^ratеr' so oхYgеn is rеadily rеlеasеdwhеrе it is nееdеd.Upon mrtamorphosis thе adult frogs, whiсh Ьrеathеair' ехprеss
a diffеrеnt hеrnoglobin mogloЬin (Fеdеr and B Somе of thе nrost st parallеl adaptation. Сo is found in unrеlatеd ol ganisms display thе sa сasеs adaptations rеflес еxamplе, two unrеlаtес сonditions on two dii Amеriсa and Сh i rсlmоt; rathеr than trrеa, as do onе-twеntiеth of thе v adzrptivеsolution to thе A drirmatiс ехamplе h i s г o г i е so f g u p p i е s [ г r thаt is rеpеatеd in sеv. aсross thе island. Gup; maturе at latеr agеs aI tions' and upstrеam ft Thеsе diffеrеnсеs arе п guppiеssufiсг muсh hi1 and, in gеnеrirl,must с. from diffеrеnt drainag. downstrеam guppiеs ln Ьеtwееrrthе upstrеam a g a i n ( R е z r r i с ka n d T г а DЕMoNsтRAт|с
N{any biology tеxtЬook d u s t r i a l m е l a n i s mt o i l l 2005). As trее trunks oration of thе pеppеrе Ьlaсk
Аdаptаtioп rtal studiеsthеy havе providеd thе pееrsсould оnly pondеr.
:ions.Сarnivorous plants oссur in :apturеand digеstinsесtsto оbtain ough thеir rtlots. Сеrtain fish and ds and floodplains Ьavе еggs that in thе soil until floodwatеrs Ьreаk . Sеvеralspесiеsof fish livе in polar i, rеlying on a spесializеdantifrееzе ':ithinthеir Ьodiеs (Нoсhaсhka апd vаriеtiеs.Dаmsеlfly spесiеsin thе rfliеs as tlrеir prinrary prеdators Ьеhavior than spесiеs that oссur haviors that protесt against dragld viсе vеrsa' so thе Ьеhaviors arе or (MсPееk 1995I' Thе fungal m grows on two сlosеly rеlаtеd amе loсations, Phаseolиs uиlgаris ;ions and sсirrringon еaсh spесiеs. 1 t sa г е s p е с i а l i z е d. l t s u r l . I 1 о [ l n t i n g as diffеrеnt spесiеsof damsеlfliеs ' е d a t o r s( S i с a r d еt al. 2007). Popzs from morе northеrn latitudеs : dehydrogеnasеthan populations ,uге:rnd thе rеgulation of ехprеsg thеrmal rеgimеsto produсе simt tеmpеraturеs'whiсh allows thе f thеrmаl еnvironmеnts (Sсhultе rrly striking Ьесausеthеy oftеn ins Ьy thе sarrrеindividual at diffеr. n of hеmogloЬinin frogs. In most : Ьlood that сarriеsoхygеn to сеlls lnditions. This propеrty еnlranсеs n arе aсidiс еnvironmеnts,and hеto thosе сеlls. But mаny tadpolеs rеmogloЬirrmolесulе with thе rеtdеr morе aсidiс сonditions.Thеsе hеmogloЬinfaсilitatеsthеir аЬility 'hеn thеrе is littlе of it availaЬlе. ) oхygеn is геadilyrеlеasеdwhеrе r f r o g s ,w h i с h Ь r е . r t h еа l r , е x p r е s s
a diffеrеnthеmogloЬin gеnе whosе protеin Ьеhavеslikе most vеrtеЬratеhеnroglobirr(Fеdеr and Brrrggгеn 1992). Somе оf thе most striking patсеrns of adaptation involvе сonvеrgеnt or parallеladaptation.Сonvеrgеnt aс1aptationoссurs whеn thе samе adaptation parallеl adaptation oссurs whеn rеlatеd oris found in unrеlаtеdorganisп-rs; ganismsdisplay thе samе adaptatiоn through indеpеndеnt origins. In Ьoth сasеsadaptationsrеflесtrеpеataЬlеmatсhеs of оrg:rnismto еnvironmеnt.For еxamplе,two unrеlatеd frogs that livе undеr similaгly dеrrrandinghot dеsеrt сonditions on two diffеrеnt сontinеnts' Phуllсlmеdиsа sаuuаgii in South Amеriса aлd Сbirсlmаntisхеrаmpiliпа in South Afriсa еaсh eхсrеtе uriс aсid гathеrthan urеa' as do othеr adLrltfrogs; uriс aсid еxсrеtion rеqr-rirеsaЬout onе-twеntiеthof thе watеr rеquirеd for urеa ехсrеtion and rеprеsеnts an adaptivеsolution tо thе nееd for wаtеr сonsеrvation (Sсhmidt-Niеlsеn1990). A drаmatiс ехarтplе of parallеl adaptation is thе сontrast Ьеtwееn thе lifе historiеsof guppiеs from upstrеam and downstrеam loсations in Trinidad that is rеpеatеdin sеvеrаl drairrаgеsfrom onе mоuntаitl гangе to anothеr aсrossthе island. Guppiеs from upstrеam loсations Ьесomе rеproduсtivеly maturе at latеr agеs аnd largеr sizеs than guppiеs from downstrеаm loсaproduсе fеwеr, largеr ЬaЬiеs in еaсh Ьrood. tions, аlnd upstrеam fеr-rralеs Thеsе diffеrеnсеs arе matсhеd to thеir diffеrеnt еnvironmеnts; downstrеam guppiеssuffеr muсЬ highег prеdation ratеs, havе lowеr poprrlation dеnsities, and, in gеnеral,must сomplеtе thеir lifе сyсlе quiсkly or not аt all. Guppiеs from diffеrеnt drainagеs arе muсh lеss сlosеly rеlatеd than upstrеam and downstrеаmguppiеs in tlrе sanrе гivеr, rvhiсlr indiсatеs that thе distinсtions Ьеtwееnthе upstrеam arrd downstrеam populаtions havе еvolvеd timе and again (Rеzniсk and Trаvis 1996). DЕМoNsтRAт|oNs oF NAтURAL sЕLЕст|oN Мany Ьiology tехtЬooks still епrploy н. B. D. Kеttlеwеll's сlassiс study of in. dustrialmеlanism to illustratе thе powеr of natural sеlесtion (е.g.,Futuyma 2005). As trее trunks in Britain turnеd dark fror-nаir pollrrtion, thе сol. oration of thе pеppеrеd moth' Bistсlп bеtulаriа, сhangеd from mottlеd to Ьlaсk ovеr a largе arеa. Thе tехtЬooks usuаlly dеsсriЬеKеttlеwеll's oЬsеrvаtions of prеdation on tеthеrеd moths of diffеrеnt сolors on diffеrеnt Ьaсk_ grounds;prеdatогsfound it еasy to dеtесtnrottlеd moths сln dark trее trunks and Ьlaсk moths on liсhеn-ссllorес] trunks in unpollutеd forеsts.Although thе valuе of thе oЬsеrvationson tеtlrеrеdпroths has Ьееn quеstionеd Ьy сritiсs' thosе oЬsеrvations Wеге not thе сritiсirl еvidеnсе. Thе сonvinсing data еmеrgеd from Kеttlеwеll's mеtiсulous mark-аnd-rесapturе studiеs; hе markеd largе numЬегs of moths of diffеrеnt с
10')
1 1 0 Аdаptаtiсlп Thеrе arе thсlusandsof dеmсlnstrаtionsof rratural sеlесtion in aсtion. A widе variеty of есologiсal forсеs сrеаtе diffеrеnсеsin mortality ratеs or lеvеls of rеproduсtivе suссеssamong individuals with diffеrеnt trait valuеs or diffеrеnt сomЬinations of fеaturеs.Frсlm prеdators and pаthogеnstсl сold strеss and drought' frсrm studiеs of snаils in British fсlrеststo Darwin's finсhеs in thе Gal6pagos' thеrе is no room to quеstion thе rеality of natural sеlесtion (Hеrеford еt al. 2004). That natural sеlесtionoссurs is сlеar, Ьut сan it Ье a сlriving forсе of еvolution? Thеrе arе twtl quеstionsaЬout natural sеlесtionthаt arе сruсiаl to еstaЬlishing thе validity of Darwiniаn еvolution. First' сan sеlесtion among individuals Ье suffiсiеntly strong and сonsistеnt to mоld thе fеаtr.rrеs of organisms? Sесond, is thеrе еnough gеnеtiс vаriation f()Гtraits undеr sеlесtion to produсе suЬstantial сhangеs in thosе fеaturеs?Two linеs of еvidеnсе answеr Ьoth quеstioтlsin thе affirmativе. Thе first linе of еvidеnсесapitalizеson еnvirсlnmеntalаltеrationsmadе Ьy humans and thе rеsponsеsof organisrnsto thosе altеrаtions.Thе dеvеlopmеnt of antiЬiotiсs in thе 1940s and 19.!0s allowеd humans to сrеatе novеl еnvironmеnts for Ьaсtеrialpathogеns.To a Ьaсtеrium' an аntiЬiotiс is а toхin; to survivе,it must sеquеstеrthе ttlxin Ьеforеit pсlisonsthе сеll сlr dеnaturеit and rеndеr it harmlеss.This situаtion сrеаtеsа powerful sеlесtivеforсе fсlr altеrnativе bioсhеmiсal pathwаys within thе сеll; individuаls thаt сould dеlay or stymiе thе toxin's еffесt would dividе аnd rеproduсе morе oftеn than thosе that сould not. Slowly at first, Ьut at an aссеlеratingpaсе, spесiеsaftеr spесiеs of Ьaсtеrial pathоgеn еvolvеd fеatuгеsthat еnaЬlеd thеm to takе onе or anothеr path towаrd surviving in thе prеsеnсеof antiЬiotiсs.Although thе сеlls of Strеptсlссlсcиs|ook thе samе as thеy did in thе -l930s, thеir Ьiсlсhеmistry аnd сеllular mеtaЬolism arе vеry diffеrеnt (Dzidiс еt al.2008). SuЬstantial Ьioсhеmiсal еvolutitln in rеsptlnsеto mсrdеrnсhеmistгy is not сonfinеd to Ьасtеria. ovеr 1,000 spесiеsof insесts havе еvolvеd Ьioсhеmiсal rеsponsеsto insесtiсidе(Roush and МсKеnzie 1987) аnd wееdy plant spесiеs havе rapidly еvсllvеdrеsistаnсеto hеrЬiсidеs,еvеn glyphosatе'thе .,onсеin a сеntury'' hеrЬiсidе (Powlеs 2008). Many aquatiс organisms hаvе еvсllvеd adaptаtions to anthropogеniсаlly produсеd hеavy mеtals in wаtеr (Klеrks and \й/еis1987) ald many spесiеs of plants havе undеrgone ехtеnsivе Ьio. сhеmiсal and morphologiсal еvolution in rеsponsеto thе prеsеnсеof hеavy mеtals in thе soil produсеd Ьy thе еffесtsof rr-rining, lеаdеd gаsolinе,and еvеn thе zinс in galvаnizеd fеnсing (MaсNаir 7987I. In thе sесond linе of еvidеnсе,Ьiоlogists havе studiеd hundrеds tlf сasеs in whiсh individuals оf thе saпrеspесiеsfrom diffеrеnt ltlсations ехhiЬit rеаdily oЬsеrvаЬlе diffеrеnсеsin сoloratior.r,m
In thе most thoroug l u t i o n a r y t r а j е с t o г yo f thе most thoroughlу st lеss of strеam or mou havе fеwеr' largеr offs a t i v е s d o w n s t г е а m .Т r in upstrеam loсations than half as many offs nеwЬorns that аrе 50piеs.Thеrе arе a num in whiсh guppiеs arе opportunity Ьy introt t i o n s , i n е f f е с tr е p l i с a hаbitat (Rеzniсk еt al. aгy Path that in lеss thosе sееn in natural strеam еnvironmеnt, а d i f f е г е n с е sа m o n g i n moldеd nеw populаti еxpегimеnt that Darrд
How Do Wе Rесl
A l t h o u g h s t u d i е so f s t lution oссurs' thе full arе joinеd with pains ogy. of сoursе,thе [ not studiеd еvеry stril m o s t s с r u t i n i z е dс a s е T h е f е a t u r е st h а t d tiсularly strong ехalx sеquеnсе of fеaturе a rеduсtion of toеs, an thе molars. Biomесhz p а r t i с u l а г f е a t u r е s ;е l riods, and highеr mс vеgеtation likе grass. mаtе аnd thе еmеrgr lutionary pаthWay t family of grazing dеs risk from а vаriеty сl Suсh a rесonstruс еlongаtionof thе lim
aге dеvеlopmеntаlly vеlopmеntal mесhan
Аdаptаtiolt ns of naturаl sеlесtion in асtion. A iffегеnсеsin л-rortalit1, rаtеs oг lеvеls rls with ditlЪrеnttr:lit valuеs tlr difеdatorsand pathogеtlsto сolсi strеss ,ririslrforеsts to DilrwinЪ 6r"rсhеsirr ition thе rеality of natural sеlесti
9871.
; h a v еs r u d i с dh u r r . l r е dtsl i с a s е si n r diffеrеntlсlсationsехhiЬit rеadily lhologУ,lifе history, oг fеаturеsof rpаЬlеof intеrЬrеес1ing. Thеv havе and, through a variеty of ехpеriing iлdividuаIs ЬеtrvееnJoсatior.rs), ,n in thе diffеrеnt loсаtions is rе_ ; ( R е z n i с ka n d T r а v i s l 9 9 6 ; T r a v i s r r2 0 0 1 ) .
In thе most thorough studiеs Ьiologists havе rе-сrеatеdthе prеsumеd еvolutionarytrajесtory of thе diffеrеnсеs.Thе Trinidаdian guppiеs offег onе of thе most thoroughly studiеd еxarnplеs.Rесall that upstrеаm guppiеs, rеgardlеssof strеam or mountаin rangе, livе lсlngеr,maturе lаtеr and largеr, and havеfеwеr' largеr offspring at еaсh Ьor-rtof rеproduсtiorrthan thеiг сlosе rеl_ ativеsdownstrеam. Thе magnitudе of thеsе diffеrеnсеs is not trivial; fеmalеs in upstгеam loсations сar-rЬе morе than 20"Ь |argеr at mаturity, havе fеwеr than half as many offspring as downstrеam guppiеs, and produсе individual nеwЬornsthat arе 50_75% largеr than tЬosе produсеd Ьy downstrеam guppiеs' Thеге arе a numЬеr of upstrеam loсations aЬovе suЬstantial watеrfalls in whiсh guppiеs arе aЬsеnt.Jolrn Еndlеr аnd Dаvid Rеzniсk ехploitеd this opportunity by introduсing downstrеam guppiеs into somе of thеsе loсa. tions,in еffесtrеpliсаtingtlrе likеly сoursе of guppy сolonizаtion of upstrеam habitat(Rеzniсk et a|.1.997).Thе introduсеd guppiеs followеd an еvolutionary path thаt in lеss than siх yеars produсеd trait valuеs сomparaЬlе with thosе sееn in naturаl upstrеarn populаtions. Natural sеlесtiorrin thе upstrеаmеnvironпrеnt' aсting on thе gеnеtiс variation that was produсing small diffеrеnсеsamoпg individual downstrеam guppiеs trаnsplantеd upstrеam' moldеd nеw populations of upstrеam gtrppiеsirr vеry short ordеr. [t was thе ехpеrimеntthat Darwin would havе likеd to do.
How Dо.Wе RесonstruсtAdaptivе Еvolution? Although studiеs of sеlесtion and rеsponsе dеmonstratе that Darwintаn еvolution oссurs,thе full piсturе of adaptation еmеrgеswhеn stцdiеsof sеlесtion arе joinеd with painstaking work in gеrrеtiсs,dеvеlopmеnt, arrd pаlеontol. ogy. of сoursе' the piсturе is nеithеr сomplеtе nor pеrfесt; Ьiologists havе not studiеdеvеrv striking fеaturеof еvеry organism, and еvеn for somе of thе most sсrutinizеdсasеs' thеrе is still muсh to lеarn. Thе tеaturеsthat dеfinе thе modеrn еquids, horsеs and zеbras, offеr a partiсulаrly strong ехаmple (MасFaddеn 1992). Palеontology has rеvеаlеd thе sеquеnсеof fеaturе appеaranсе from thе еlongation of thе lowеr limЬs, thе rеduсtion of toеs, and thе еmеrgеnсеof hoovеs to thе inсrеasing hеight of thе rnolars.BionrесhаniсaIstudiеs havе pоinted to thе аdvаntagеsoffеrеd Ьy partiсularfеaturеs;еlongatеd limЬs faсilitatе rapid running for еxtеndеd pеriods, and highеr molars arе Ьепеfiсial for grazing touglr, siliсa-сontaining vеgеtationlikе grass. Plaсing thеsе сhangеs in thе сontеХt of a сhanging сli_ matе and thе еmеrgеnсеof savatrnasand plains, wе сan rесonstruсtthе еvolutionary pathwаy through whiсh small anсеstгal Ьrowsеrs produсеd а family of graztng dеsсеndants mtlldеd Ьy living irr opеn сOuntry аnd Ьеing at risk from a variеty оf largе prеdators. Suсh а гесonstruсtionpгеsumеstlrat thе transitionswе rесonstruсt,likе thе еlоngationof thе limЬ and thе rеduсtion in thе numЬеr of digits in thе foot, arе dеvеlоpmеntallypossiЬlе.That is, thе rесtlnstruсtionPrеsumеs that a dеvеlopmеntainrесhanisп-rftlr produсing suсh сhаngеs саn Ье dеsсriЬеd, and
111
1 1 2 Аdаptаtiсlп thаг thе gеnеtiс vаri:rtions in tlrе еlеrnеntsсhrсlr-rglr wlriсh thаr mесhаtlism сtltrld асt r'"'tluldhаvе Ьееn rеadily аvailaЬlе. Although Wе сanllor tеst thеsе prеsumptionsirr схtinсt spесiеs,W-ссilIl асquirе insights frtlm str-rdiсs of ехisting spссiеs. A4сlsttеrrеstrialvеrtеЬrаtеshavе fil,е digits сln thе fосlt at tlrе еnd of еaсh limb, Ьut thе position of thosе digits on thе foс.tt,thеir геlativеsizе, and еvеn thеir nr-шnЬеr с,.1nvаiv. Stuс1iсsсlf ftlсltand сligit dеvеltlpr-nеrrt il] traсtaЬlе ехpеrimеnt:rlаnimals likе salamandеrsаnd сhiсkеns havе shown that thе numЬсr, sizе, and position of digits arе dсtеrminеdЬ},molесtrlаrsigr-rals ехсharrgеd (ShtrЬin2002)' Rеlativеly Ь1,еmЬryoniс сеlls с]urirrgеaгl,vlimЬ dеvеlсritiсizс'tЬе gеnеrality rlf сonсlrrsionsаilсlut ada1rtatiсlndегivеd frсlпl а study on a snrall sсаrlе,suсh as thе сasе tlf industrial шеlаnisrn. Тсl a сritiс, thе rарid сlrаIrgеin thе frеquеnсr,of altегrrativеforms of :r singlе gеnе ftlг ссllсlratiсlnis lraгdly еvidеnсе thаt naturi-llsеlесtiсlt-l сan dгivе profound transformаtionsin orgаnismiс fе:lturеs-сl(lсharrgingсolсlr pаttеrnsin moths tеll rrs еntluglr tсl undеrstand h
quеstions has inspirеd ian еvolution' еvеn aп
сontrovеrsiеs in l
|s тHE RAW м READILY AVAII
At first glanсе thе ans' tаtion is rеаdily availа guppiеs offеrs сompt sцЬstantial adaptivе е е x с е p t i o n a l с а s е :h u п .
сellular сonсеntrаtio h i n d l i m Ь l е n g t ho f t r found apprесiaЬlе lеv viduals within a singl B u г t h е е х i s r е n с еo l that natural sеlесtiоn sharе dеvеlopmеntal valuеs to Ье inhеritеd to sеlесtion. In sеvеr liеs, swordtails, and п an еndoсrinе pathwа1 opmеnt (Kаllmаnl9t soсiаtion bеtwееn r.t Т h i s a s s o с i a t i o nп r е a largеr Ьody sizеs at п If slowеr maturation l solution; tlrе gеnеtiс maturation is not imr Thе kеy point геv Straint hold in thе lо suffiсiеntly long, wor thеsе traits? If sеlес m u t а t i o n s f а с i l i t a t еt
and rapid maturatio though it пay wеll h mау arisе, it is imp wоцld favor suсh а п T h е p o s s i Ь i l i t yo f . of adaptationsthat ;
еxamplе' most сasеS Ь е h a v е si n a p a r t i с u sumе a partiсular pО сoloration arе fаilrr
Аdаptаtiсlп ts througlr whiсh that mесhanism llе. Although Wе сannot tеst thеsе qLrirеinsightsfronl str-tdiеs сrtе-хisгgits on thе foot at thе еnd оf еaсh tе foot, tlrеirгеlirtivеsizе' and еvеn i digit dеvеloрmеntin traсtaЬlе ех:hiсkеnshar'сshсlwnthаt tlrе numlеd Ьy mtllесrrlаrsignаlsехсlrаngеd l t l p m е n t( S h u Ь i n2 o o 2 I . R е l a t i v е l y , :rnd pattеrning сlf thtlsе sigI-rals .еlopmеtrt.Dеlays in signalirrgr,l.ill аnd fifth digits, and if thеy do dе)еlаys irr signaiing, сouplеd u,ith tion of digits on tlrе foot. Thus alэpmеntirlpath that lеd to a hoof in -rrodеl through ц,lriсh сumulativе :ould havе trаnsfсlrmесlа fivе-toеd еvеlopmеntаIеlеmеnts havе Ьееrr -rdiеsof rеlativеhindlimЬ lеngth in . lеngth of tlrе hirldliпrЬ соmparеd i n d l i m Ь ss u Ь s t a n t i i r l livo n g е гt Ь a г ) d h i n d l i m Ь sa r е r a r е l y m o r е t h a n :latеdspесiеslikе thе Ьarking trее т LjnitеdStatеsсan hаvе sLlЬstаlr.hеsе diffеrеnсеsагisе from diffеrnd tlrс rаtе tlf linrЬ_Ьшdgrowth in tion for tlrе rеlativе lеrrgthof tЬе n singlе frсlg populаtions (Blouin rаtеriаl ftlr hirrdiimЬ еvоllrtion irr on to find in thе past lrnd, Ьy ехt h е ra n i m a l s . adaptation iп hoгsеs rvhtlsе prеrimеntalstudiеson Ьirds or frogs. y rvhеnWе attеmptto rесoпstruсt Ье fсlundin thе ftlssil rесorс]'It is l u s i o n sa Ь o u t а d a p t a t i o nd е г i v е d саsе of industrial mеlаnisnl. Tсl a altеrnativеftlrms of а singlе gеnе rral sеlесtionсan drivе prсlfound сhаrrgingсolсlrpаttеrllsin moths n пrolds fish musсlеs irrto еlесtriс ps foг сatсhing аnd digеsting irrn Ье aсlriеr,еdехpеrinrеrrtallyаt thе most importаnt еvolutionarv
quеstionshas inspirеd and sustainеdсonsidеraЬlесontrovеrsyаЬout Darwinian еvolution' еvеn among sсiеntistswho study it.
Сontrovеrsiеsin thе Study of Adaptation |s тHЕ RAW MAтЕRIAL FoR ADAPтAт|oN RЕADlLY AVAlLAвLЕ? At first glаnсе thе answеr to thе quеstion whеthеr thе rаw nrаtеriаl for аdаp. tation is rеadily availaЬlе would sееm oЬvious. Thе study оf thе transplantеd guppiеs offеrs сompеlling еvidеnсе that thе gеrrегiсvariation rеquirеd for suЬstantiаladaptivе еvolution wаs avаilaЬlе. This doеs not appеar to Ье an ехсеptionalсasе;hundrеds of studiеsof a variеty of сharaсtеrs,ranging from сеllular сonсеntrations of alсohol dеhydrogеnasе in fliеs and thе rеlativе hindlimЬ lеngth of fгogs to thе сolor of swallowtail Ьuttеrfly pupaе, havе found apprесiaЬlеlеvеls of gеnеtiсvariation for individual traits among indi. viduаlswithin a singlе population. But thе ехistеnсеof hеritaЬlе variation in singlе сhaгaсtегsdoеs not imply that natural sеlесtionсan mold fеatцrеsarЬitrarily. Diffеrеnt сharaсtеrs сan sharе dеvеlopmеr.rtal pathways that сausе partiсulаr сomЬinаtions of trait vаluеsto Ье inhеritеd togеthеrand thеrеЬy сonstrain thе immеdiatе rеsponsе to sеlесtion.In sеvеral spесiеsof pсlесiliid fish-thе fаmily of guppiеs, rnoliies,swordtails' arrd mosquito fish-thе proсеss of mаturation is govегnеd Ьy an еndoсrinеpathwаy that rеduсеsgrowth ratе as it aссеlеratеssехual dеvеlopmеnt (Kallman 1989). Thе gеnеtiсvariation in this pathway сrеatеsan assoсiation Ьеtwееn rapid nraturation ratе anс] sm:rll Ьody sizе at mаturity. This assoсiation mеans that thе rеsponsе to a sеlесtion pfеssurе that favors largеr Ьody sizеs at maturity will inеvitаЬly inсludе slowеr maturation rаtеs. If slowеr maturation ratеs arе dеtrimеntal for anу rеason' thеrе is no oЬvious sоlution; thе gеnеtiс variation for thе сomЬination of largе sizе and rapid maturation is not inrrnеdiаtеlyаvailaЬlе. Thе kеy point rеvolvеs around thе word immediаtе'lу; doеs suсЬ a сonstraint hold in thе long run? Ч/еrе wе to watсh suffiсiеr-rtlyсlosеly and wait suffiсiеntlylong, would Wе sеe mtltаtioпs in individual gеnеs that dissoсiаtе thеsеtraits? If sеlесtion aсtеd with suffiсiеnt сOnsistеnсy'would thеsе nеW mutations faсilitatе thе еvеntual еmеrgеnсе of thе сornЬinatiorr of largе sizе .Wе and rapid maturаtion? hаvе no simplе answеrs to thеsе quеstions; although it may wеll Ье that givеn еnough timе, a mutation of thе right kind may arisе, it is impossiЬlе to prеdiсt if thе есologiсal сirсumstanсеs that would favor suсЬ a mutation would still prеvаil whеn it finally arosе. Thе possiЬility of сonstrainеd gеnеtiсvariation provokеs a rесonsidеration of adaptations that aге Ьuilt on assoсi:rtionsЬеtwееn individLrаl trаits. For еxamplе,most сasеs of сryptiс сoloratiсln in animals work only if thе animal bеhavеsin a partiсular fashion, wlrеthеr it is to геmain motionlеss or to assumе а partiсulaг posturе or огiеntatioп.Мisrnatсhеs Ьеtwееn bеhаvior and сoloration arе failurеs. TЬе aгdеnt advoсatе of Darп,inian еvolution might
r1)
1 1 4 Аdаptаtioп arguе that natural sеlесtion hаs assеmЬlеdthе сomponеllts of suсh adapta. tions via mеtiсulous molding of individual fеi1turеsuntil thе Ьеst сomЬination еmеrgеd from all thе possiЬilitiеs.At thе othеr ехtrепlе оnе rтiglrt агguе that thе сonсегtеd inhеritanсе tlf thе сonrponеntsoffеrеd natural sеlесtiona limitеd rаngе of rarv mаtеrial frorr-rwlriсh only a fеw good matсhеs ttr сirсumstanсеswеrе pоssiЬlе. Ьy сonsidеring thе еvolution of аny Thе samе argumеnt саn Ье prov<>kеd putаtivе rldapt:rtionthat involr.еs пrultiplе сharaсtеrs, Ье it ;l Ьioсhеmiсаl patЬWay or a suitе of assoсiatеdЬеhavitlrs.Thе сontrovеrsy is not Whеthеr suсh fеаturеs rеprеsеnt adаptlltiсrns;thе сontrovсrsу is оvеr гhе еxtеnt tо whiсh adaptаtion is сonstrainеd Ьy thе naturе of thе аvailaЬlе raw matеrial. This is L.lеinglrpproасlrеd frоп-l sеvегal pеrspесtivеs, froпr ехапrinirrg thе naturе of nеW mutations for kеy сharaсtеrsto dissесtingthе аssoсietionsamong individual fеaturеsof an adaptation inttl thеir gеnеtiссontrсrland sЬarеd dе. vеlоpmеntal pаthwavs. ls ADAPтATIoN PЕRFЕст? Thе rrrarvеlousmatсhеs of orgаnisrrrto еnvirtlnmеnt offеr a strong tеп]ptation to сonсludе that adаptation is pеrfесt. Indееd, whеn сontеmplаting intriсatе adaptatiоns likе agе-spесifiсhеmogloЬin gеnе ехprеssion,thе amаzеd sсiеntist is rr
possiblе solution сontl Ь е s t i l l u s t r а t i o n so f t h i fеrеnt poptrlаtiоns of t есologiсal сhallеngе. сidеs; diffеrеnt populс Ь i o с h е m i с а lа n d p h y s (Мatsumurа and Voss еlесtriс fishеs сo-оptес o г g а n s ( B е n n е t t1 9 7 1 ) Thе othеr part о{ th ural sеlесti
organ and suЬsеquеnt tion. An еasiеr аnd bt not through thе rеtinа Thеrе is anothеr Wi
еrеd by еvolutionary fеaturеs of organisms pеrforrn a spесifiс funt that сapturе and foсus molесular signаls intt bееn сonsidеrеd ехam of thеsе сomplеx trait of Darwiniirn еvo|uti еvеry thеmе in thе stu
сAN DARWlNI ЕxPLA|N сoM
Darwin himsеlf appl dilеmma is thаt all sr boliс pathway likе tht pоsitе оf пrany indil propеrly intеgratеd fс Ьring so пlany things nаtural thеologian's z samе position tirkеn l tеnt thеsis offеrеd Ьy thе еyе or thе KrеЬs l lесtitln. Chаnging thс аnothеr (Aуala 2006
Аdаptаtion d thе сomp
пvironmеntoffеr а strong tеmptаt. Indееd,whеn сontеmplatirrgin;loЬingеnеехprеssion,thе аmazеd awеstruсk pоеt or thе inspiгеd this qr-rеstionas а tеstаЬlе idеa. Lwе might usе thе rcrm pеrfeсt; it аn orgаnism has adrrptivеsignifitisnr to еnvir
possiЬlеsolution сontingеnt on thе rаw matеriаl providеd Ьy mutation. Thе Ьеstillustratiоnsof this соntingеnсy oссur whеn diffеrеnt spесiеsor еvеn diffеrеntpopulatiсlns of thе sarrrеspесiеs rеsponс.lidiоsynсrаtiсally to tlrе sаmе есologiсalсhallеngе. This has oссurrеd in еvolution of rеsistanсе to pеstiсidеs; diffеrеnt population of thе two-spottеd spidег mitе еvolvеd diffеrеnt to сopе witЬ thе samе pеstiсidе Ьioсhепriсalаnd plrysiologiсal mесhar-rsims (Маtsr.rmuraanсl Voss 1964| and, on a largеr sсalе' whеrr diffеrеnt spесiеs of еlесtriс fishеs сo.optеd diffеrеnt musсlеs for transformation into thе еlесtriс organs(Bеnnеtt1971). Thе othеr part of thе аnswеr is morе suЬtlе: adaptatiоn is historiсal. Naturаl sеlесtion filtеrs variation in fеaturеs that arе thеrnsеlvеs produсts of prior еvolution' As a rеsult, thеrе is a signaturе of history on еvеry adapta_ tion, zrndhistor,vсаn gеnеratеfеaturеsand ссlrnЬinationsof fеaturеsthat arе proЬaЬly not wlrаt an intеlligent dеsignеr would produсе if thе orgаnism wеrе Ьеing dеsignеddе novo. For ехamplе, thе huпran еyе has a suЬstantial Ьlind spot саusеd Ьy thе thrеаding of Ьlood vеssеlsthrough thе rеtina. This inеffiсiеntstruсtllrеis a historiсal artifaсt of tlrе еyе'sorigin as a light-sеnsing еlаЬoration of thе rеtina as a Sсrееnfor imagе rеsoluorgan and suЬsес1uеnt tion. An еasiеr and Ьеttеr dеsign would wind thе Ьlood vеssеlsaround and not through thе rеtina. Thеrе is anothеr way in wЬlcЬ perfесtioп iп adaptation has Ьееn сonsidеrеd Ьy еvolutionary Ьiсrlogistsаnd сritiсs alikе. Сomplех adaptationsfеaturеsof orgarrismsth:1tarе ЬuiIt fгom maпy сharaсtеrs thаt сombinе tсl pеrform a spесifiсfunсtion' likе thе vеrtеЬratееyе, with suЬsеtsof сharaсtеrs that саpturеand foсus light, that dеtесt Ьrightnеssаnd сolor, and that rеsolvе molесulаr signurlsinto an aссuratе iпrаgе of rhе ехtеrnal world-havе long ..pеrfесtion.''Еxplaining thе еvolution Ьееnсonsidеrеdехamplеs of naturе's of thеsесomplеx traits has always Ьееn a сеntrаl сhallеngеfor thе сhampions of Dагwiniаn еvolution, anс] thе answеrs to th;rt сhallеngе illustratе nеarly еvеrythеmе in tl.rеstudy of adaptation. сAN DARW|N|AN ЕvoLUтloN ЕХPLA|N сoMPLЕx тRAlтs?
RЕALLY
Darwin himsеlf apprесiatеd thе сh;rllеngе posеd Ьy сomplех traits. Thе dilеrrrrnаis tlrаt all suсlr fеaturеs,whеthеr аn organ likе thе еyе оr а mеta. Ьoliс pathway likе thе Krеbs сyсlе usеd Ьy сеlls to produсе еnеrgy' arе a сompositе of many individual adaptations' all of whiсh n-rustЬе pгеsеnt and propеrly intе€ ] гatеdfor thе adaptatiоn to funсtiorr.Нow саl-lnatural sеlесtion Ьring sо many things togеthеrall at onсе and makе thеrn work propеrly? Thе natural thеologian'sanswеr in thе ninеtееnthсеntury was that it сannot' thе samеposition takеr-rЬy moс1еrnproponеnts of IntеlligеntDеsign' Thе сonsisnow, is tlrat thе ссlrnplеxity of tеnt thеsis offеrеd Ьy Darwin's сritiсs, thеn аr-rс1 thе еyе or thе KrеЬs сyсlе is too grеat to havе Ьееn Ьuilt by mutation аnd sеlесtion.Сhanging thе сolrrr of moths is onе thir-rg.Ьut Ьuilding аn е}.еis quitе anothеr(Ayala 2006).
, t.)
I16
Аdаptаtit'lп But is it? Dаrwin arguеd that ni]turalsеleсtiolrсoulс1produсе сtlrrrplехadaptations if thеy еvolvеd through a sеriеs of srтall stеps, еilсh of whiсh had sоmе аdaptivе advantagе ovег its prеdесеssor.Thе еvnaryPathway to thе Oсtoplls еyе has long sinсе Ьееn lost. ]Wеwould hаvе t-to bеttеr luсk traсir-rgthе pаthwirv to tlrе vеrtеЬrаtее1'е;nаtшrеnсlrv tlffеrs а largе group of organismstlrat all lravеwеll-dеvеlopеdеyеsехсеpt foг thosе living in vеry dаrk еnvir
hagfish). A sесond intеr ians, rеptilеs, аnd Ьirds t fish, and thе аdditiсlrra from Ьonеs assoсiatеdW Thеsе would Ье rеmark; tion drovе thе wholеsalс shapеs and сrеаting еntl
z0o7l .
But thе diffеrеnсеs rn Ьеst. Gill arсhеs arе a с( аs a Ьеllows. Fish usе t сavity. .Whеn a fish opеl oral сavity inсrеasеs,an' bеllows сontrасts and r( watеr through thе gill sl сеstors of all iawеd vеrl tеrЬorne pаrtiсlеs into t in thе oral саvity, whiс also funсtions as a rеsp wеll suppliеd with blo thеm, and thе thin tissu from thе watеr into thе dеrivеd from thе gill a gгasp and proсеss foоd е n h a n с е st h е t r а n s m i s s on thе outеr surfaсе of 1
gion of our skulls' Нow сan suсh divеrs Ьratеs, Ье еvolutionaril fish arе pаrt Of a rеpеа musсlеs that opеn arrd that ехpand and сontra arсhеshavе thе funсrio grasping and grinding t h е t r a r l s f o r m a t i o nf г o so dramatiс as to sее
сhangеs. Thе trаnsformation ] is lеss dramаtiс than it spесiеs.Thе fossil rесo isms that rеprеsеnta tl thе rеptilеs tl-ratаppес сompositе of sеvеn Ьol skull was formеd by t Ьonе on thе skull (Figr dеntary, and artiсula
Аdаptаtion есtion сould produсе сonrplех adap;rnallstеps,еасh t>fwhiсh hаd sсllr.rе rе еvolutionof thе еyе сould only Ье ]quеnсесlf rhеsеsmtrll сhаnges, аlrd t doеs rеquirеsan undеrstandingof Dереw2004)' To thе modегn еvrllu. .hесtlrrtingеrrt and lristoriсаl naturеs аfgumеntsft,г IntеlligеntDеsign' еyе Ьy pointing ollt thе divеrsity сlf - . i е so f g а s t r o p o d s( s n a i l s 'm u s s е l s , angе from сlustеrsоf сеlls in somе ht аnd dаrk to thе sоpЬistiсаtеd, n g е o f p h o r o ь е n s i t i voеr g l r n sс l i i n argued Ьy analog1',assегtinЕ]thаt rgans in gаstгop()dsillustratеs thе tor to dеsсеndanttо Ьuild thе most еyе, rvith a сompаrrаЬlеpossiЬiliгy .gumеntsrnall сhаrrgеsagainst thс. аn aссumulаtе ir-rtoa rеmarkаrЬlе 3rеaгknowlеdgеof aninrzrldivеrsity nvinсе thе сritiсs and, in faсt' doеs rrаlysis.Thе spесiеs irrvсllvеdin tlrе nothеrfor skеptiсaItastеs;thе fossil е nrtllесulаrdаtа sr-Iggеst thаt it hаs эf thеm shaгеd a сommoп anсеstor l thе idеa сlf еl.oltrtitln). Thе еvolug sinсe Ьееnlost. !Ие would havе no 'Ьrаtееl.е;nаttlrе nсlu,offегs a laгgе iopеdеyеsехсеpt1Ъгthosе living in ' sессlndariiyеvolvесlrеduсed еyеs. iinrplе to сornplех с.yеsoссurrеd in 'vеr400 million yеarsi1go. lluti
hagfish).A sесond infеrеnсе is that thе singlе middlе-еar ossiсlе of amphiЬians' геptilеs,аnd Ьirds rvas dеrir,еdtrom an еlеmеntof thе jaw suspеnsionof fish, and thе additional twtl middlе-еar ossiсlеs of mammals wеrе dеrivеd fronrЬonеsаssoсiаtеdwith thе |aw joint of tЬеir rеptilian anсеstors(F-igurеl )' Тhеsеwould Ье rеmarkaЬlе еvolцtionary еvеntsin whiсh mutation and sеlесtion drovе thе wlrolеsalеtransformation of сharaсtеrs' molding еntirеly nеw shapеsand сrеating еntirеly nеw funсtions (!7akе 1979; Radinsky 1987; Luo
2007\.
But thе diffеrеnсеs in funсtion rrrakе sцсh a progrеssion sееm fаnсiful at Ьеst.Gill aгсhеsarе а сompositе of Ьonеs, musсlеs, and nеrvеs that funсtion as a Ьеllows. Fish usе thеm to еxpand and сontraсt thе volumе of thе oral .!7hеn саvity. a fish opеns its mouth, thе Ьеllows еxpands, thе volumе of thе oral саvity inсrеasеs,and watег is drawn irr. !7hеn a fish сloses its rrrouth,thе bеllowsсontraсts and rеduсеsthе volumе of thе oral сavity as thе fish ехpеls Wаtеrthrough tlrе gill slits. ln living iawlеss fishеs(and prеsumaЬly in thе аnсеstorsof all jawеd vеrtеЬratеs),this pump is a fееding dеviсе' drаwing watеrЬornеpartiсlеsinto thе mouth that adhеrе to a stiсky suЬstanсеproduсеd in thе oral сavity, whiсh is thеn сonvеyеd to thе gut. Thе еntirе apparatus also funсtions аs a rеspiratory orgаn. Thе tissuеsthat linе thе gill aгсhеs arе wеll suppliеd with Ьlood; thе pump passеs frеsh, oxygеnаtеd watеr ovеr thеm,and thе tlrin tissцеstlrаt linе thе arсlrеsallоw oхygеn to Ье trаrrsportеd from thе watеr into thе Ьlood vеssеls.By сontrast, thе struсturеssupposеdly dеrivеd froпl thе gill аrсhеs lravе mrrrе сiгсumsсriЬеd funсtions. Thе jaws grasp and proсеss food. Thе first rniddlе-еarossiсlе in tеrrеstrialvеrtеЬratеs еnhanсеsthе transmission of thе еnеrgy in sound wavеs fronr thе еardrum, on thе outеr surfaсеof thе Ьody, to thе innеr еar, whiсh is in thе tеmporal rеgionof our skulls. L{ow сan suсh divеrsе struсturеs'not all of whiсh arе prеsеnt in all vеrtеЬratеs,Ье еvolutionarily linkеd to ol1еanothеr? Thе iaws in thе еaгly jawеd fish arе pаrt of a rеpеatеd sеriеs of Ьonеs that inсludеs thе gill arсhеs. Thе rnusсlеsthat opеn and сlosе thе jaws funсtion in a similar fashitln to thosе that ехpand and сontraсt thе gill arсhеs.In somе living spесiеsof fish, thе gill arсhеshavе thе funсtiollal еquivalеlrtof tееth and funсtion as do our jaws Ьy grаspingand grinding food. Givеrr thе pattеrns of musсlе аnd innеrvаrion, thе transformationfrom gill arсh tO jaW suggеstеdЬy thе fossil rесord is not so dramаtiс as to sееm an unlikеly сurrrulativееffесt of small, attain:rЬlе сhangеs. Thе transformation from jаw support in rеptilеsto еаr ossiсiе in maпrп.rals is iеss dramatiс than it might appеаr from соmparisorrsof only thе ехisting spесiеs.Тhе fossil rесord offеrs striking pattеrns of сlrаngе aсross thе organisms that rеprеsеnta transition Ьеtwееn rеptilеs and mammals (Figurе 1). In thе rеptilеs that appеar to Ье anсеstrаl to пrammals' tlrе lowеr jаw wаs a сompositеof sеvеn Ьonеs and thе artiсulation Ьеtwееnthе lowеr jaw and thе skull was formеd by thе artiсular bonе on thе lowеr jaw and thе quаdrаtе Ьonеon thе skull (Figurе 1A). In mammals thе lowеr jaw is a singlе bоnе, thе dеntary, arrd аrtiсulation of thе jаи. tlsеs thе dеntary Ьonе itsеlf аnd thе
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Figr-rrе1. This figurе, modifiеd from Luo 2007, illustratеs thе еvolution tlf thе manrmаlian jaw, сlегivесlfrom :r sеriеs of ftlssils in thе synаpsid linеagе (thе linеagе irl wЪiсh mаmm:rls сmеrgсd) аnd froп.l thе еmЬryсlniс dеvеltlpmеnt of tЬе living maЬrтals. Thе сlrawings on tl-rсlеft (A-D) rергсsеnt thс l
sqrramosal Ьonе on thе sids (thе sсiеntifiс tеrm jaw hingеs that сonsist thе lowеr jaw and thе q 1B_Е). This dual artiсu fеaturеs of thе skеlеton, rеptilеs and mammals. I and squamosal Ьonеs fil rеplaсеd thе artiсular ar onсе thе artiсular an of jaw and skull, thеy v fossils аnd from thе еml mals indiсatеs that thе and oriеntation' and с
(С) Brаsilith еriиm rep Triassiс through thе latе Pаchуgеnеlus (B) but rеt (D) Sinocoпсldon was ' from thе еarly Jurassiс,tl though thе individualЬo GI (Lеft) Мorgапuсoс late Triassiс thrоugh thе a 8 r е a t l yr е d u с е dp а r t i с To thе right of еaсh ol thаt thе stapеdialproсеs proсеssаrtiсulatеswith t ( Е ) ( R i g h t ) T h i si s a v с Мorgапucodoz, illustrаt sеriеsof Ьonеs inсluding bonеs havе a diffеrеntеn animals and thеy сan аls есtotympaniсis a ring o1 Ьеtwееn thе outsidе wor (F) Thеsе arе adult an О rnitb orhупchus. |n tЬe mеdial surfaсеоf thе lov есtotympaniс,mallеus'а сonfiguration sееn in thе (G) Thе lowеr drawin adult jaw of Yапсlсoпod Thе сondition of thе Ме duсk-Ьillеd platypus. (H) Thе lowеr drаwin oPossum' Мoпсl delph us еmЬryoniс jаw is vеry sr Yаnoсonсldoz, with thе thе lowеr jaw, whilе thе Месkеl еlеmеntsЬеingс
Аdаptаtioп squаmosalЬonе on thе skull. Somе of thе advаnсеd nonmammalian Synapsids (thе sсiеntifiс tеrm for thе ехtinсt group of mammal-likе rеptilеs) havе jaw hingеsthat сonsist of a сomЬination of thе dеntary and thе artiсular on thе lowеr jaw and thе quadratе and thе squamosal on thе uppеr jaw (Figurе 1B-Е). This dual artiсulаtion of thе jaw, in сomЬination with many othеr fеaturеsof thе skеlеton' indiсatеsthat thеsеanimals formеd a Ьridgе Ьеtwееn rеptilеsand mammals. In thе сasе of thе jaw joint, it appеars that thе dеntary and squamosalЬоnеs first wеrе inсludеd in thе jaw joint and thеn сomplеtеly rеplaсеdthе artiсular and quadratе Ьonеs as thе jaw joint. onсе thе artiсular and quadrаtе Ьonеs wеrе rеdundant in thе artiсulation of jaw and skull, thеy wеrе availaЬlе for othеr purposеs. Thе еvidеnсе from fossilsand from thе еmЬryoniс dеvеlopmеnt of thе most anсiеnt living mammals indiсatеs that thеsе Ьonеs Ьесamе rеduсеd in sizе' altеrеd in position and oriеntation, and сonvеrtеd into thе middlе-еar ossiсlеs, thе artiсular
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lustrаtеsthе еvolutiсln of thе n thе synаpsid lirrеagе(thе linеаgе in Liс dеvеltlpmеnt
(С) Brаsilithеrium rеptеsentsa third linеagеof Synapsids' found from thе latе Triassiсthroughthе latе Сrеtaсеous'that had thе samеdual artiсulationas (B) Ьut rеtainеda quadratojugai. Pасhуgеnelиs (D\ Sinoсoпсldonwas a mеmЬеr of a fourth Synapsid linеagе,known only from thе еarly Jurassiс,tЬat had a dual artiсulation likе thаt of Pаnуgeпеluseven thoughthе individual Ьonеshаd diffеrеntsizеsаnd shapеsthan in Pапуgеnelus. (Е\ (Lеft) Мorgаnucodoп rеPrеsеntsa fifth Synapsid linеagе,known from thе latеTгiassiсthroughthе mid-Jurassiс,that also had a duаl artiсulation,Ьut with ..inсus''and no jugаl. a grеatlyrеduсеdpartiсipationof thе ..inсus.''Notе To thе right сlf еaсh of thеsеfigurеsis a dеtailеddiagramof thе thatthе stapеdialproсеssis prеsеntin (C) and (Е) Ьut aЬsеntin thе othеrs.This proсеssartiсulatеswith thе stapеs'whiсh is thе third middlе еar ossiсlе. (BI вigha TЬis is a vеntraland latеralviеw of thе lowеr jaw of ..Mесkеl'sеlеmеnt,''whiсh is assосiatеdwith a Мorgапuсodoz,illustrаting sеriеsof Ьonеsinсludingthе есtotympaniс,thе mallеus,and thе inсus.Thеsе Ьonеshavе a diffеrеnt еmЬryoniс origin from thе othеr jawЬonеs in living animalsand thеy сan also Ье сlеarlyrесognizеdin somе fossils.Thе есtotympaniсis a ring of Ьonе that suppqrtsthе еardrum,whiсh is thе intеrfaсе Ьеtwееnthе outsidеworld аnd thе middlе еar ossiсlеs. (F)Thеsearе adult and еmЬryсlniсjaws of thе duсk.billеdplatypus'gеnus ornithorhупсhus.Inthе еmЬryo,thе Месkеl еlеmеntsarе attaсhеdto thе mеdialsurfaсеof thе lowеr jaw' as in Мorganuсodon.Latеr in dеvеlopmеntthе malleus,аnd inсus sеparаtеfrom thе lowеr jaw and produсеthе eсtotympaniс, сonfigurаtionsееnin thе middlе еar of thе аdult. (G) Thе lowеr drawing is a vеntralviеw, thе upPеr onе a mеdial viеw of thе adultjaw of Yапoсoпodon,an еаrly mammal that datеsto thе еarly Сrеtaсеous. aге similar to thosесlf an еmbryonlс Thе сonditionof thе Месkеl еlеmеrrts duсk-billеdplatypus. (H) Thе lowеr drаwing is thе mеdial viеw of thе еmЬryсlniсlowеr jaw of thе opossum'Мсlпodelphus,whilе thе uppеr drawing is thе adult jaw. Тhе emЬryоniсjaw is vеry similаr to thе adult jаw сlf Мorgапuсodon and Yапoсoпodoп,with thе Месkеl еlеmеntsЬеingattaсhеdto thе mеdiаl surfaсеof thеlowеr jaw, whilе thе adult сondition is typiсal of living mammals' with thе МесkеlеlеmеntsЬеingсomplеtеlydеtaсhеdfrom thе lowеr jaw.
119
1 2 0 АdаptаtЙlп into what is now сallеd thе rтallеus and thе quadratе into what is rrow сallеd thе inсus. Thе drivеr for this transformation would havе Ьееn natural sеlесtiсln'sfavoring еnhanсеdaЬility to dеtесtviЬrations. Rеsеarсhsuggеststhat thе jaw in thеsе transitionai animals transmittеd viЬrations from thе ground to thе mid. dlе еar, as it doеs in somе modеrn snakеs-think of a small, nсlсturnalanimal that piсkеd up viЬrations Ьy touсhing its jaw to thе ground and transmitting viЬrations from thе jaw to thе stapеs.Thеsе viЬrations would havе travеlеd through thе artiсular (mallеus) and quadratе (inсus) Ьonеs to thе stapеs.In two linеagеs of nonmammalian Synapsids, nеithеr of whiсh is anсеstral ttl mammals, thе inсus has an outgrowth сallеd a stapеdial proсеss' whiсh is a lеvеr arm that transmits thе forсе of thе sound wavеs from thе inсus to thе stapеs. Its prеsеnсе in thеsе two linеagеs stlggеststhat Ьoth of thеm wеrе еvolving an еnhanсеd саpaсity to transmit sound from thе jaw to thе stapеs and thеn to thе innеr еar. Thе arrangеmеnt of btlnеs in thе linеagе that inсludеs mamrnals is diffеrеnt than in thеsе othеr linеagеs Ьut doеs inсludе аn inсus with a stapеdial proсеss.Tlrе final stagеof сoursе is thе sеparationof thе ossiсIеsfrom thе jaw itsеlf. \й/hеnthе ossiсlеs Ьесamе sеparatеdfrom thе jaw' thеy сould transmit sound viЬгations еffiсiеntly from thе еaгdrum to thе middlе еar. Thе сomplеtе fossil rесord rеvеаls that, rathеr than thеrе Ьеing a dirесt transformation from the primitivе synapsid ссlndition to thе mammal сondition, thеrе was a divеrsity of arrangеmеnts сlf Ьоnеs in thе jaw-еar rеgion and a divеrsity of rеarrangеmеntsovеr timе. Thе anatomy оf living rеptilеs аnd mammals rеprеsеnts two еndpoints of а transformation that followеd divеrsе paths in Ьеtwееn,with most of thе variants having gonе ехtlnсt. Although thе fossils Suggеstthе progrеssionof fеaturеsin this transformation, dеvеlopmеntal Ьiology offеrs us twсl important additional lirrеs of еvidеnсе. First, whеn thе ossiсlеsfirst аppеar in mammalian еmЬryсls,thеy arе part of thе jaw assеmЬly.During dеvеlopmеnt'thеy sеparatеand f
m u s с l е s a s s o с i а t е dw i г dеrivеd from what is nеrvеs that sеrvе thеsе nеrvеs. All thеsе oЬsеrvation а r с h е sa n d t h а t t h е m l mutation irnd sеlесtion ponеnts. But hоw аnd \|977) onсс dеsсriЬе nееring; a tinkеr usеs v tions, whilе an еnginе that adaptаtion is a hrs s t г u с t u r е sf o r n е w f t l n (еffiсiеnt feеding) and fl into largеr, morе aсtiv tant funсtion of thе ph a n a s s o с i а r i o nw i t h f с . pharyngеal pump hav сlosе thе jаws, so thеy funсtion. Although thе transit dеrstand, thе assoсiatt tratе.Stiсk your fillgег will sее thаt thе jaw jо you сan fееl thе joint r
v е r t е Ь r а t е s .i n с | u d i n g: арpеаг гtlpiсk up viЬг and thеn to transmit th snakеs and small mamr t i o n s a r е n o с t u r n а |, r n е m е n г so f t h е j а w s t o l l a r g е l ye с o n s е q u е n с thе prior rоlе thаt thе j vironmеnt to thе innеr
Ехаrпple 2: FIorаI еul our sесond ехamplе, v nеtiс analysеs сontribu t a t i O n s( S с h е m s k еа n d wе foсus on shаpе and еrs fсlr thеir Ьеauty аn< rеproduсtivе struсturе pollеn (thе malе gamе malе gamеtе). Thе llowеrs that insp animal pollinаtors likr
Аdаptаtion hе quadratеinto what is now сallеd rld hаvе Ьееn naturаl sеleсtion,sfa. ns. Rеsеarсhsuggеststhat thе jaw in rаtionsfrom thе ground to thе mid-think of a small, noсturnal animal j а w t o t h е g г o u n de n d r г e n s m i г t i n g rеsеviЬratiorrswould havе trаvеlеd lratе (inсus)Ьonеs ttl thе stapеs.In Js, nеithеr of whiсh is anсеstral to Lllеda stapеdialproсеss,whiсh is a sound-лavеsfrom thе inсus to thе s suggеststhat bсlth оf thеm wеrе it sound from thе jaw to thе srapеs э that inсludеsmammals is diffеrеnt ludе аn inсus with a stapеdial proation of thе ossiсlеsfrom thе jaw itfrom thе jaw, thеy сould transmit drum to thе middlе еar. Thе сomln thеre Ьеing a dirесt transformа)n to thе mammal сondition, thеrе n thе jaw.еarrеgion and a divеrsity ny of living rеptilеs and mammals Ltionthat followеd divеrsе paths in ] gonе еxtinсt. ;sionof fеаturеsin this transformal important additionаl linеs of еvir in mammaliаn еrтЬryos,thеy arе nеnt'thеy sеparateand form thе fае 1F_H). \Whilеthе notion that an еvolutionaryhistory has Ьееn dis. :h dеvеlopmеnt offеrs a сluе to an lеaЬlеin thе fossils. сlеs havе a сritiсal rеlationship to thеr fеaturеsof thе skull. Thе vеrеrеnt layеrs of tissuе' thе есtodеrеndodеrmal (innеr) layеrs. Thеsе onе anothеr еarly in dеvеlopmеnt : Ьody as dеvеlopmеntprogrеssеs. l from thе middlе, or mеsodеrmal, iatеd with thе gill arсhеs, jaw' and lеlopmеntal origin diffеrеnt from Lrеdеrivеdfrom spесializеdсеlls of Likеwisе' thе musсlеs and nеrvеs :o onе anothеr in thеir origin; thе
m u s с l е sa s s o с i a t е dw i t h t h е g i l l a r с h е s ' j a w s , a n d m i d d l е - е a ro s s i с l е sа r е a l l dеrivеdfrom what is сallеd tЬe brапсhiomеric sеriеs of musсlеs, and thе nеrvеsthat sеrvе thеsе musсlеs all dеvеlop from thе samе group of сranial nеrvеs. All thеsеoЬsеrvationssupport thе аrgumеnt thаt jaws arе dеrivеd from gill аrсhеsand that thе middlе-еar ossiсlеs arе dеrivеd from jaws, and thus thаt mutationаnd sеlесtionсan indееd m
121
122 Аdаptаtitlп сomplех сomЬinations of сharaсtеrsthat togеthеr arе an adaptation for dispеrsing and сollесting pollеn. Flowеrs pollinatеd Ьy animals are сomparativеly largе' сolorful, and shapеd in ways that faсilitatеthе transfеr of pollеn. Somе flowеrs arе highly spесializеd to attraсt spесifiс pollinators, usually Ьy a сolor and/or fragranсе that аrе partiсularly attraсtivе to a pollinator. Thе sugary nесtar is thе rеwаrd offеrеd Ьy thе flowеr to thе pollinat,or, a rеward that draws thе pollinator's intеrеstto thе insidе of thе flowеr and sеtsthе pollinator in plaсе to piсk up and dеposit pollеn. Мany flоwеrs havе mаrkings that diгесt thе visitor toward thе nесtar,somе of whiсh aге visiЬlе only to animals likе insесts that sее in thе ultraviolеt (Ьlaсk-light)frеquеnсiеs.othеrs havе modifiеd pеtals or sеpals thаt sеrvе as a soft of landing strip on whiсh thе pollinator сan геst' аnd somе spесiеshаvе spесializеdstruсturеsto attaсh thе pollеn to thе pollinator. Two сlosеly rеlatеd spесiеs of monkеy flowеrs, Мimulus letaisii and М. саrdiпаlis, oссur along riparian hаЬitats in thе wеstеrn Unitеd Statеs (Figurе 2). Thеy sеgrеgаtе Ьy еlеvation, with М. lеtuisii oссurring at highеr еlеvations, and thеrе is а narrow rangе of еlеvation in whiсh thе spесiеs ovеrlap. Gеnеtiс analysеs show that еaсh spесiesis morе сlosеly rеlatеd to thе othеr than еithеr is to any othеr spесiеs of monkеy flowеr, so any diffеrеnсеs Ьetwееn thеm еvolvеd aftеr thеy last shаrеd a сommon anсеstor. Thе two spесies havе quitе diffеrеnt flowеrs. Thе spесiеs at thе highеr еlеvations' М. lешisii, is pollinatеd primarily Ьy Ьееs. It has pink flowеrs that arе rеlativеly widе and whosе pеtals form а horizontal landing strip; yеllow struсturеson thе landing strip appеar to guidе Ьееsto thе appropriatе part of
Figurе 2. Studiеsof thе сolor, sizе,shapе,and fеaturеsof thе flowеrsof two сlosеlyrеlatеdspесiеsof Мimulus hаvе illustratеdthе gеnеtiссоntrol of ссrmplехadаptations.Lеft: TЬe Ьluе flowег of М. letuisii,whiсh fеаturеsa ..landing plаtform'' for thе insесtsthаt transfеr pollеn Ьеtwееnflowеrs and ..guidеs,' that dirесt thе insесtstoward thе nесtarand thе rеproduсtivе struсturеsof thе flowеr. Right:Thе rеd flowеr ot М. саrdiпаlis,whiсh is a long, narrow' tuЬular flowеr with nесtaгаt thе Ьasе,rеaсhaЬlеЬy thе tonguеsof thе hummingЬirdsthаt sеrvеas thе pollinators.
the flowеr. Thе flowеrs produсtivе organs сonta thеy arе еnсountеrеd Ьy of thе insidе of thе flow flowеrs that laсk thе hol Ьy hummingЬirds, whiсl duсе largе quillltitiеs Of аnthеrs (mаlе org:rns)t that pollеn is dеpositеd. stamеns (fеmalе ()rgan
t h е r nn s r h е Ь i r d f е е d r . Еaсh flowег is wеll m: diffеrеnсеs Ьеtwееn tlrе plех aсlаptations for pс matсh of florvеr tсl polli Organs' and nесtar proс and sеlесtion сould hаv a сOmmon аnсеstor. O] сussеd еarliеr thаt gеnе diffеrеnсеs rеprеsеntth( сhаraсtеrs. lf this wеrе ехplаinеd vеry simply Ь аtе thе two flowеrs; shi nario, not srrЬstantially mottlеd to Ьlaсk. At tЬ matiс diffеrеnсеsarе Ьa еaсh of whiсh has vеry l or lеngth of thе anthеr Ь е е n v е г y m е t i с u l o u sa l thе floral traits. Of сor trеmе vlеWs. O u r k r l o w l е d g ео f p l p е t i n g h y p o t h е s е s .A l t t of sеpals, pеtals, st:rm g е n е s 'i t i s u n с l е a rh o w of thе rеproduсtivе str doсtion ratе. Thе routе to thе ans аnd thеir сollеaguеs Ьy lесular mеthods (Sсhе 2 0 0 3 ) . S с h е m s k еa n d i usеd Ь,v Mеndеl whеn l tееnth сеntury. Thеy pr Ьrids rarеly oссur in n: arе quitе hardy in grее lеaguеs nехt сrсlssеd h
lza
Adа|ltаtiсlп sесond gеnеration of so-сallеd Ьасkсrossеd plants with a variаЬlе mix of gеnеsfrom еaсh original spесiеs.Thеy thеn turnеd to molесular Ьiology' еmploying molесular markеrs thаt enaЬlеd thеm to аssoсiatеpагtiсular variations in floral сlraraсtеrsas sееn in thе vаrious сornЬinations of plants with diffеrеnсеsin molесular maгkегs on spесifiс loсаtions of сhromosomеs. Thе diffеrеnсеson thе сhromosomеs rеflесtthе loсations of gеnеsthat сontriЬutе to thе vагiаtion in thе flowеrs' Twеlvе individual сharaсtеrswеrе idеntifiеdarrd studiеd with this mеthod, whiсh rеvеalеd that thе truth rvas indееd somеrvlrеrе Ьеtwееn thе гwo еxtrеmе idеаs :rЬout gеnеtiс сontrol. A singlе gеrrе dеtеrminеd whеthеr thе flowеr was геd or pink. By plaсing f.lowеringhyЬrids and Ьaсkсrossеsin naturе, Sсhеmskе and сollеaguеsfound that thе сolor diffеrеnсеаlonе had an еnormous impaсt on whеthеr thе flowеr would Ье visitеd Ьy a Ьее or a hum-I.hе mingЬird. sсiеntists also found that whilе anothеr singlе gеnе madе a largе сontгiЬr.rtionto thе diffеrеnсеsin 9 of thе 12 floral traits, thеrе wеrе many gеnеs tlrаt madе smаllеr сontributions to onе or a small suЬsеt of thе traits. From thеsеrеsultsWе сan offеr somе plausiЬlе rесonstruсtionsof this сomplех adaptation. Thе еffесt of flowеr сo1or oп visitations suggеststhat a сhangе in a singlе 8еnе' that fоr сolor, сould initiatе thе еvolution of a spесialized flowеr. Diffеrеnt pollirrators attraсtеd to thе diffеrеnt сolors would ехеrt diffеrеnt sеlесtionpressurеson thе rеmainirrgtrzrits.Although it is unсlеar whеtlrеr thе largе sirrglе-gеnеeffесt on ninе traits prесеdеdoг followеd thе сhangеs in thе many othеr gеnеs that affесtеd onе or a fеw traits' thе ovеrall piсturе is of a singlе, simplе gеnеtiс сhangе (сolor) initiаting a stеpwisе proсеss of modifiсation and rеfinеmеnt whosе еnd produсts arе thе two сomplеx adаptations that wе now sее.Thе matсh of fеaturе to сirсumstanсе was not built qrritеas еasily as сhanging thе сoloration of moths Ьut did not rеquiге so mеtiсulous a molding as to strain сгеduliry' A finаl notе аЬout thе historiсal naturе of irdaptаtion is that it doеs not sееm pоssiЬlе that thе сhangеs in floral shаpе and rеpгoduсtivе сharaсtеrs .!Иithout сould havе prесеdеd thе сolor сhangе. variation in сolor аnd thе rеsultant diffеrеnсеin spесiеsof pollinators, thеrе would havе Ьеen no сonsistеnt sеlесtion prеssurеto mold divеrgеnt vаluеs of thе othеr сhагасtеrs.But onсе thе сolor diffеrеnсеSаppеarеd,tlrе divеrgеnt foraging of Ьееs and hum_ mingЬirds proЬaЬly сata|уzeda rаpid divеrgеnсе'This ехamplе illustratеsthе сontingеnсy inhеrеnt in thе еvolution of сomplеx fеaturеs in whiсЬ a singlе сhangе in a fеaturе сan promotе а сasсadе of suЬsеquеnt сhangеs that rеfinе its adaptation to nеw сirсumstanсеs.To rеturn to thе сritiquе bf Intеlligеnt Dеsign, wiсhout apprесiatingthе rolе of history, wе would Ье hаrd prеssеdto ехplain how аnс{why thеsе flowеrs divеrgеd so sulrstаntially. W H A т с A N I N D l V | D U A Ls Е L Е с т | o N N o т Е X P L A | N ? Our disсussion of adaptation hаs еmphasizеdhow thе fеаturеsof individr'rals arе moidеd Ьy thе aсtion of sеlесtion on thе avirilaЬlе gеnеtiс V;rrii1tion.
A fundamеntal tеnеt of I tеrs that еnhanсе thе fitnс wеll-Ьеing of а spесiеs.I: in pаrtiсul:rr for thе gughthis may ехplanatiоt-rfor all fеatu dividual sеlесtiсlnсomеs m i t е s ,i n w h i с l r n е a r l ya l | It is diffiсult to гесonstгu individuа| with :r fitnеss.
not геproсluсе. Thе kеy to rеsolving th that thе сol
Аdаptаtioп еd plants with a variaЬlе mix of l turnеdto molесular Ьiology, еmhеm to assoсiatеpartiсular variarious сomЬinаtionsof plants with fiс loсationsof сhromosomеs. Thе : ioсationsоf gеnеsthat сontriЬutе ifiеdand studiеdwith this mеthod' somеwhеrе Ьеtwееn tlrе two ехglе gеnе dеtеrminеd whethеr thе n g h у Ь г i d sа n d Ь а с k с r o s s е si n n а thе сolor differеnсеalonе had an 'ould Ье visitеd Ьy a Ьее or a humwhilе anothеr singlе gеIrеmadе a of thе 12 florаl traits, thеrе wеrе |nsto onе or a small suЬset of thе usiЬlеrесonstruсtionsof this сomlor olr visitatirlns suggеsts that a uld initiаtе thе еvoiutiсrnоf a spе_ сtеd to thе diffеrеnt сolors would еmainingtraits. Although it is un,n ninе traits prесеdеd or fсl]lowеd ' affесtеd onе oг a fеw traits, thе i с с h n n g е( с o I o г )i n i t i a t i n gа s t е p rt whosе еrrd pгоduсts irrе thе two : matсh оf fеaturе to сirсumstanсе lе сoloration of moths Ьut did not n сгеdulity. , of adaptation is that it doеs not hapе and rеpгoduсtivесharaсtеrs horrt vaгiation irr сolor аnd thе rеthеrс would hаvе Ьееn no сonsis,aluеsof thе otlrеr сhaгaсtеrs.But иеrgеntforаging of Ьееs аrrd humgеnсе.This ехamplе illustratеsthе omplеx fеaturеs in whiсh a singlе of suЬsеquеntсhangеsthаt rеfinе эturn to thе сritiquе оf Intеlligеnt ;tory' Wе would Ье hard гlrеssеdto .d so suЬstаntirrlly. oN Noт ЕХPLAIN? еd how thе fеаturеsof individuаls l t h е a v a i l a Ь | еg е n е t i с v а r i a t i o n .
A fundаmеntаltеnеt of Dагwinian еvtllution is that sеlесtion favors сharaсtеrsthаt еnhanсеthе fitrrеssof individuais; it doеs not nесеssarilуеnhanсе thе wеll-Ьеingof a spесiеs.Indееd,thе notion thilt еvolution hаs driеs, аnсl гhе сritiсzrlissuе in nlodеrn еvolrrtionaryЬiology is to diаgrrosеhow
I !.\
1 2 6 АdаDtаtiсlп parаsitе еvolutiot-t''in this volumе); a pathogеn tlrat nrultipliеs too quiсkly аnd kills its lrost tсlo quiсklу Ьеforе it сan bе trаr-rsmittеdto аnothеr host losеs out Ьесausе sеlесtion among familiеs Or groups (rеprеsеntеdЬy thе pathogen populаtiorr within an individual host) ovеrwlrеlms sеlесtion a m o n g i n d i v i d u a l s ( г е p r е s е n t е dЬ y t h е s t r u g g l еf o r p r o l i f е r i r t i o nw i t h i n а n individual host). ARЕ sтUDlЕs oF MlсRoЕVoLUтloN RЕLEVANт тo U N D Е R s т A N D IN G M A с R o Е v o L U т | o N A R Y P A т т Е R N s ? [t is сonvеniеnt to сharасtеrizеthе produсts of evolution as еithеr mlсroеvolution or maсroеvсrlutirln.МiсroeuoLutioll rеfеrs ttl small-sсirlесhangеs that arе dirесtly oЬsегvaЬlе, likе many o{ thosе disсtrssеdеагliеr (mеlanism irr moths, disеasе rеsistanсеin Ьaсtеriа, or insесtiсidеrеsistanсе).As wе havе disсussеd, miсroеvolution has Ьееn vеry thorouglrly doсurтеntеd and has Ьееn studiеd irr ways thаt mееt any tеst of sсiеntifiсrigi
sее that thеrе arе long not at аll, thеn Ьriеf in drеdgе dеsсriЬеd thе l< short intегvals as ptrnсl аssoсiаtion Ьеtwееn pu thе tеrm ptlпсtuаted еq Gotrld аrgrrеd that Ьot with nаturаl sеlесtiona on thе prеmisе that if sс
a prеd
First, neturаl sеlесtion isms to small-sсalесhar tlran natural sеleсtion quеnt assoсiation Ьеtw suggеststo Gould and phеnomеna, Ьut thеy h d u r i n g t h е 3 6 - y е a rh i s t
Thе сountеrargrrmе hаs thrее parts. First, v tion Ьy nаtural sеlесtr thаn thе ratеs i]ssoсlat Gа16pagоs finсhеs сan i n a p с l p u l а t i o ni n а s i r fall. In dгought yеаrrs sееdswith thiсk sеесlс< fесtivе at harvеsting su Bесausе tlrеrе is a gеn( finсhеs еxhiЬits largеr, to put this ratе of еvol sil rесоrd' it is l0,000 tегprеt as punсtuation inсonsistеnt witlr tlrе r tion' [f anything,wе r
fossil rесord. S е с o n d , s е l е с t i o l li s This, of сottrsе, is tlr.э Ьut hеrе it is importan tion сan onlу makе fi tаnсе to сhangе, mltst Darwin's linеs of argu саtе that domеstiс dtlg
Аdаptаtklп 1 o g е nt h a t m u l t i p l i е s t o o q u i с k l y r Ье transпrittеdto аnothеr host ]s or groups (rеprеsеntеdby thе ual host) ovеrwhеlms sеlесtion ugglе for prolifегаtiсlnwithin an
oN RЕLЕVANт тo г|oNARY PAттЕRNs? s of еvolutionas еithеr miсroevorеfеrsto smirll-sсalесhangеs that ;е disсussеdеаrliеr (mеlanism in .sесtiсidеrеsistanсе).As wе havе :horoughlydoсumеntеd and has :iеntifiсrigor' As а rеsшlt,it is not l сritiсsof evolution (sееthе rnain spесt and Рrospесt'' Ьy Еugеniе еvеntsthat wе аttriЬutеto еvoluliffегеntialpг
sееthat thеrе arе long intегvals whеn thе tгait in quеstion сhangеs littlе or not at all' thеn Ьriеf intеrvаls wlrеn thе tr:lit еvolvеs rapidlv. Gсlr-rldапd ЕldrеdgеdеsсriЬеdthе long, staЬlе intеrvals as stasis or еquiliЬrium and thе short intеrr.irisas punсtuаtions. Thеv also pointеd out that tlrеrе is oftеn an assoсiatiоrrЬеtwееnpunсtцations :rnd thе сlrigin of nеw spесiеs and сoinеd thе tеrm punctuаted equilibrium to dеsсriЬе thе еntirе pattеrn. Еldrеdgе and Gould aгguеd that Ьoth phasеs of pr'rnсtuatеdеquiliЬrium arе inсons,istеnt rvithnaturаl sеlесtionas a singlе urrdеrlyingсausе.Тhеir argtlmеntи,аs Ьasеd on thе prеmisеthat if sеlесtionwеrе suсh а unifying сausе' wе should oЬsеrvе a prеdominаrltPаttеГnof graduаI.сotrtinuousсhangе in сhагaсtеrs.Stаsis in сharaсtеrssuggеstsrеsistanсеto сhangе. Thе disсontinuity of punсtuations suggеstеd to thеm that somеthinghappеnеdto Ьrеak this rеsistanсеand сausе а suЬsеquеntpulsе сlf aссеlегatеdеvolutiorr. AlthougЬ Gould аnd Еldгеdgе'sargumеntshаvе еvolvеd during thе dеЬаtе rhatеnsuеdeftеr thеir first с.ssay,thеir argumеntshavе two unifying fеaturеs. First,natшralsеlесtionis pсlsitеdаs Ьеing еffесtivеonly in fir-rе_tuning organisп-rs to smirll-sсalесhangеsin thеir еrrvironmеnt.Sесоnd' somе proсеss othеr thаn naturirl sеlесtion must сomе into plaу to сausе punсtlliltions. Thе frе_ quеnt assoсiаtion Ьеtwееrrpunсtuirtionsarrd thе appеaranсе of nеw spесiеs suggеststo Gоuld and Еldrеdgе thаt this proсеss' whаtеvеr it is' сausеs Ьoth plrеnomеna,Ьut rhеy lravе аltеrеd tlrеiг prtlpоsеd mесhаnism tor this proсеss during thе 36-yеar history of punсtuatеd еquiliЬrium as an idеa. Thе сountеrargumеntin favor of natural sеlесtiсrnas a unifying Proсеss has thrееparсs.First, wе hаvе еmpiriсal еstimatеsсlf сhе r:rtеat whiсh еvoiution Ьy natural sеlесtionсаn oссur' and wе know that it сarr Ье muсh fastеr thаn thе ratеs assoсilltеdwith punсtllаtions irr thе fossil rесord' For ехamplе, Gal6pagosfinсhеsсan еvolvе a |0"Ь сhangе in avеragеЬody sizе or Ьill sizе in a populartionin a singlе vеar in rеsponsеto еithеr droughts or hеаvy rainfall. In drought yеlrrs ftlod avаilaЬility is low' thе Ьiгds mrrst rеly orr largе sееdswith thiсk sееdсoats and individuals rvith widе, hеavy Ьills arе morе еffесtivеat harvеstingsuсh sееdsand arе morе likеly to survivе and rеproduсе. Bесausеrhегеis ir gеrrеtiсЬаsis t
127
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Аdаptаtioп of yеars ago. Thе fiгst appеaranсеof morphologiсally distinсt domеstiс dogs datеs to around 10,000 yеаrs аgO (Savolainеnеt al. 2002). Еrom suсh rесеnt Ьеginningswе havе Ьrееdsthat rangе in sizе from thе Сhihuahua to thе mastiff аnd in shapе from thе Pеkinеsе to thе lгislr wolfhound. If wе foсus on Ьody wеight alonе' thе rangе of avеragеwеights аmong Ьrееds is fгom around 1 kilogram for Сhihuahuas to 80 kilograms for mastiffs. This rangе еХсееds thе еntirе rangе of Ьody sizеs оf othеr spесiеsin thе family Сanidaе' whiсh inсludеs dogs, wсllvеs, foхеs, and othеr doglikе сarnivorеs (Finarеlli and Flynn 2006). It talls slroгt of wh:rt wе sее in thе ordеr Сaгnivora, whiсh inсludеs thе family Сanidaе along with othеrs' suсh as thе Fеlidaе (сats)or Ursidaе (Ьеars). Tеn thousand yеaгs of artifiсial sеlесtion havе thus Ьееn suffiсiеnt to gеnеratе a rangе сlf morphologiсal variation that is еquivalеnt to thе rangе wе Sееwlrеn wе loоk thrее or fottr stеps up thе tirхonomiс hiеrarсhy (spесiеs'gеnus' family, ordеr, сlass' phylunr, kingdom). Third, wе must сoIlsidег whеthеr thе prеsеnсеof stаsis' or long intеrvals сlf littlе or no сhangе, сan Lrеехplainеd Ьy natural sеlесtion.Thе Gal6pagos finсhеs again providе a good ссlnсеptual altеrnativе to ехplain why thеrе might bе long intеrv:rls of no apparеnt сhangе in thе fossil rесord. In drought yеars thеrе is intеnsе sеlесtion for inсrеasеd Ьill and Ьody sizе. In thе гаiny yеars that aссompаnv Еl Nino еvеnts' thе rеsourсе Ьаsе сhаngеs Ьесausе thеrе is an аЬundanсе of small, thin-shеllеd sеeds from diffеrеnt spесiеs of plants. Sеlесtion now favors smаllеr individuals with narrowег, morе forсеps-likе Ьills. This mеans that pеriods of sеlесtion for inсrеasеd Ьill sizе altеrnatе with pеriods of sеlесtion for dесrеasеd Ьill sizе, and in somе yеars thеге is in faсt nсl sеlесtion at all (GibЬs аnd Grzrnt 1987). ovеr thе nеarly thrее dесadеs in whiсh thеsе Ьirds hаvе Ьееn studiеd, thеrе has Ьееn no nеt сhangе in thе Ьill sizе of thе populaгion in spitе of strong еvi_ dеnсе for intеnse sеlесtion and rapid еvolution on a yеar-to.yеаr Ьasis (sее .!Иеinеr 1994 for а nontесhniсаl rеviеw of studiеs of Dаrwin's finсlrеs).Thе fossil rесord сould rеprеsеrrta frаgmеntеd,long-tеrm history of suсh shorttегm fluсtuating sеlесtion. Thе fossil rесord doеs nсrt rеpгеsеnt еaсh аnd еvеry yеar' and, in faсt, a dеfinесl pеriod in thе fossil rесord will rеprеsеnt a random rniхturе of thеsе diffеrеnt еpisodеs of sеlесtion.TЬе aсtual rаtе of еvolution that wе sее in thе fossil rесord is a long-tеrm avеragе of thе inсrеasеs and dесrеasеs and will inеvitaЬly undеrеstimatе thе true rаtе at whiсh orgаnisms сan еvolvе. A fоssil rесord of thе Gal6pagоs finсhеs may w е | |l o o k l i k е s t a s i s . In tlrе final аnalysis thеrе is nothing in thе fossil rесord that inhеrеntlyсon. tradiсts Dаrwin's daring idеa that natural sеlесtion is thе unifying mесhаnism. Organisms сап еvolve muсh morе гapidly tlran tlrеy appеar to еvolvе during punсtuations,and thе сapaсity of organismsto сhangе undеr sеlесtion far еxсееds thе сonstraints that arе apparеnt during stasis. Thе aЬsегrсеof сhangе during stasis пlay instеad Ье a statistiсalartifaсt of flrtсtuatingеvolution thаt traсks a fluсtuating еnvironnlеnt. But our argrrmеntsdo not provе that maсroеvolution is miсroеvolution writ largе;thеy mеrеly support thе viaЬility of naturаl sеlесtion as a singlе, ovеri1rсhingехplаnation. Thе rоot of
thе сontr
Horizons in thе Stuс
Adаprirtion is Ьеing sttrd of adaptation is еvidсnt, аrе ЬеginniIrgto dissесttl .!Ие havе а f аdaptations.
Ьut rr.е саllnot сonсlr'lt1 found arе gеnеrlll. Gеn() s е а r с l r а, n d e v с г s i . l t.ll f t v е r y с l if f е r е n tс ( ) n с | u 5 i O on thе Thе с
individual gеnеsth21tPro that tlrеу arе inl,rеritеdar p | а u s i Ь l еr ( )p o s i tе х t е n s in fасt thеге:rгеa fеrvstu ..Еvollttt thе пririn еssay rah Сharlеswoгth and th suggеststhаt thе !]еn()m not mеrеly a сoDstralllt. important quеstion thilt our сollесtivе viеr'vo1 it has сhangеd rnaгkесl11
portаnt for undеrstаnd this aгеir is lеаding to [а thе еvсllutitln mеntl оf thе сеll thе еvolr-rtiсln tivе аrеas of rеsеaгсh l
rеvсlllttion hаs еrraЬlеd n е W ( ) n е st o Ь е a s k е d . . and tlrс diffiсrrlty сlf aр thаt hilppеnеd ovеr a l otl-rеrttlpiсs, Ьut irr a dr o u r l p р r е с i e t i < l on Г t n t vеrr, diffс-rеntthan thеу Т h е s t t r d yс l f D а r ц ' i n аftеr (Jll Ibс Оrigitt ,
Аdа7ltаtiсlп lhologiсallydistirrсtdomеstiс dogs nеn еt al. 2002). From suсh reсеnt ze from thе Сhihuаhua to thе masе Irish wolfhound. If wе foсus on lightsamong Ьrееdsis from around ns for mаstiffs. This rangе еxсееds :сiеsin thе family Сanidaе, whiсh doglikе саrtrivorеs(Finarеlli and in thе order Cагnivora, whiсh inгs,suсh аs thе Fеlidaе (сats)or Urгtifiсial sеlесtion havе thus Ьееn 4iсalva;:iаtionthаt is еquivalеnt to )ur stеpsup thе taхonomiс hiеrar_ rylum,kingdom). rеsеnсеof stasis,or lorrg intеrvais nаtural sеlесtion.Thе Gal6pagos аltегnativеto ехplain why thеrе сhangе in thе fossil rесord. In 'r inсrеasеdbill and Ьody sizе. In эvеnts'tlrе rеsourсе Ьasе сhangеs thin-shеllеdsееds from diffеrent nаllеr individuаls with narrowеr' эеriods of sеlесtion for inсrеasеd ln for dесrеasеdЬill sizе, and in l l l ( G i b b sа n d G r a n t 1 9 8 7 ) .o v е r irds havе Ьееn studiеd, thеrе has p o p u l а t i o ni n s p i t е o f s t r о n g е v i ution on a yеar-to-yеarЬasis (sеe studiеsof Darwin's finсhеs).Thе , long-tеrmhistory of suсh shortlrd doеs not rеprеsеnt еaсh and r thе fossil гесord will rеpгеsеnra :s of sеlесtion.Thе aсtual ratе of is а long-tегm аvегagеof thе in. . undеrеstimatе thе truе ratе at rd of thе Galdpagos finсhеs may : fossil rесoгdthat inhеrеntlyсonsеlесtion is thе rrnifyirrg mесhaLpidlythan thеy appеar to еvolvе чanismsto сhangеundеr sеlесtion rnt during stasis.Тhе aЬsеnсе of ltiсal artifaсt of fluсtuating еvoluBut our аrgumеntsdo not provе largе;thеy mеrеly Support thе viаrсhing еxplаnаtion.Thе root of
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thесontrovегsyrеrnainstlrе difIiсulty of rесonсiling wlrat Wе сan study in thе shorttеrm rvith thе еnormously сliffеrеnttirтеsсalеof thе miri
Hоrizonsin thе Study of Adaptation Adaptаtion is Ьеing stuсliеdаt lеast as intеnsеly as еvеr. Althtlugh thе rеality fi1сg15 of adaptatiolris е','idеnt,trrtrn1, of it rеrnain unсlеаr. Foг схittт1llе,rr,е arеЬеginnirrgto dissесtthе gеnеtiсЬasis of аdаptatiоns' ;lartiсularlv сorrrplех adaptatiоns..й/е hlrr,еа fец.сlassiс studiеs likе tlrosе ()n thе mоnkеy flоwеrs, Ьut wе сannot ссlr-rсludе whеthеr thе pi-lttсrnsthat Sсlrеrnskеаnd сollеagr'rеs found arе gеnеral.Gеnomiс and protеomiс nrеtl-rods arе aссеlегatingthis rс_ sеarсh,and a vеrsion of tlris еsslr1. wгittсt-ra dссаdе frсttltnorr,rrrаyсlffсгsorrrс vеrv diffеrеntсtlnсlusiсlnsaЬout this tсlpiс. Tlrе сtlnstгаrints on thе raw mаtеriаl f
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Adаptаtiсlп argumеnt in Ьroad outlinе, it fеll to his suссеssors to disсovеr whiсh еlеmеnts of his argumеnt Wеrе possiЬlе in thеory, whiсh wеrе dеmonstraЬlе in praсtiсе, and whiсh wеrе roЬust to variаtions among spесiеs and сirсumstanсеs. T'hat so muсh of his original аrgumеnt геmains standing is a triЬutе to his gеnius; that so muсh rеmains to Ье disсovеrеd is a triЬutе to thе mаrvеls that adaptation offеrs and thе divеrsity of naturе th:rt it has сatzrlyzеd.
в|вLIoGRAPl{Y Ayala, F. J. 2006. Dаrшiп ttпd lпtеlligепt Dеsigп.lvIinnеapolis:FсlrtrеssPrеss. Bеnnеtt,М. V. L. 197l. Еlесtriс organs. In \W.S' Hoar and D. J. Randall' еds.' ЛisЙ Phуsiologу, voll. 5, З47_492. Nеw York: Aсadеmiс Prеss. Blouin, M. S. 1991. Proximatе dеvеlopmеntal сausеs of limЬ lеngth variаtion bеtwееn Hуlа сiпerеа and I7уkt grаtklsа (Anr'rra:Hylidае). .|ourпаl o|.Мorphobgl'209: 3 0 5 - 3 10 . 1992. Genettс сorrеlations among morphоmеtгiс traits аnd ratеs of growth and diffеrеntiation in thе grееn trее frоg, Hуlа сiпerеа. Еuolutioп 46:735-744' Brаdshaw, H. D., Jr., and D. \W' Sсhеmskе.2003. Allеlе suЬstitutionаt а flowеr сolour loсus рroduсеs a pollinatoг shift in monkе,vflowеrs,N,ltнrе 426: 776-178. Dаrwin, с. 1859. On thе origiп of Spесies.London: Iohn Murray. Dzidiс, S.,J. Suskoviс,and B. Kos. 2008. AntiЬiotiс rеsistanсеmесhanismsin bасtеria: Bioсhеmiсаl and gеnеtiс aspесts. Food Тechпolog1'апd Biote сhпсlklgу 46: 11'_21, Еldrеdgе, N., and S. J. Gоlrld. 1972. РunсtrratеdеquiliЬria:An altеrnativеto phylеtiс gradualism. In T' J. M. Sсhopf, ed., Мodеls iп Pаlеobiolсlgv,82-115. San Franсisсo: Frееman, Ссlopеr. Еisеlеy, L. 1958. Dаrtt,iп's Сепturу: Еuсllцtioп аnd thе Меп.V/h
МaсFаddеn, B. J. |992. l"rl the Fаmilу Еquidаc. N N{асNair,М. R. 1987.Hеa sуstеm' ТrепtJs ilt Есtll Маtsurnura, I]', and G. Vоss i n г h е r r , r ' t l - s p о t t еsJp i t Епtomtllogу 57: 9| |-9 N,lсPееk,М. ,\. l99.5. Мor1 damsеlfliсs сrf tw
сontеmP()гJг1.rd.rрt.rr t h e t p r о I n r t t еa r l a p т i е r Rеzniсk, D. N.' F. H. Shaw rаtе ()f еr,сllutionin nlt 275: |9З4-19З7. R е z n i с k . D . . . r n d. l . T r : l r i ' . G. [,atrdеr,еds.,Аdаpt' York: Aсаdеmiс Prеss. Roush, R. T., :rr-rd J. A. МсI асtrriсidеrеsistаnсе';ll, Rusе, М. |L):9.тhс Dапt,i Сhiс:rgo: Univеrsity of Sirvolаtnеn, P.' Y. P. Zhang. еvidеnсе foг an Еast i\s S с h е m s k е 'D . W ' , a n d H ' D е v о | u t i t l nс l f f l o r а l t г r i r Nаtioпаl Аcаdеmу o| S S с h m i d t - N i е l s е n 'K . | 9 9 О . l Сan-rЬгidgе:Сambгidgс S с h u l r е ,Р . ] \ l . 2 ( ) 0| . l . , l rirr t еvсllutiоlt.С| |mРаrсt! i I, S h u Ь i n ,N . Н . 2 0 0 2 . o r i g i r r of М
АJаptаlit lп
lссеssorsto disсovеr whiсh еlеmеnts , whiсh wеrе dеmonstraЬlеin praсs among spесiеsand сirсumstanсes. mains stаndingis a tributе to his gе_ еrеd is a triblltе to thе marvеls that -urеthat it has сirtаlyzеd.
;lgr. Мinnеаpolis:FоrтrеssPrеss. /' S. Hoar аnd D. J. Randаll, еds., FlsЙ Aсаdеrг'iсPrеss. саusеsof lirnb lеngth vаriаtion Ьеtwееrr Hylidaе)..|ourпаltl| Мсlrphohgу 2О9: эrphomеtriс trаits arrd rаtеs of growth ' HуIа сinerеа.Еuolиtioп 46:7З5-744. 003. Allеlе substitutionat a flowеr n monkеyflowers. Nаtltrе 426: -ondon:Jоhn Murray. lliсltiсrеsisтanсеmесhanisп-tsin balсtеriа: chnologу апd Biottlсhпologу 46: ||-21. tеd еquiliЬria:An irltеrnаtivеto phylеtiс bls iп Pаleсlbiolog1',82_115. San п апd thе Меп \WЬoDisсouerеd It. '. Епuiroпmепtаl Phуsiоlogу of thе :ago Prеss. aI statеrесonstruсtionof body sizе in Thе еffесtsсlf inсorрoгаting dаtа from
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МA: SinauеrAssoсiасеs. ng sеlесtionon Darrvin's finсhеs. Nаtиre tеd еquiliЬria:Thе tеmpo and modе of 115-151. 04. Compаring strеngths of dirесtional эп 58:21'З3.214З. B ioсhеmiсаl Аdаptаt itlп: М есh апism Nеw York: oxfоrd UrrivегsityPrеss. n с е1 9 6 : 1 \ 6 | - | | 6 6 . at maturity in Xiphсl1lhorиs. In G. K. у апd Еuolutioп o| Liuеbеаriпg Fishеs s, NJ: Prеntiсе Hall' rdаpratiоn t о h е a v y . m е г а |i ns a q u a t i с llutioп 45: 173_205, 1006.Gеnomiсsand thе irrеduсiЬlе 0 11 - 1 0 1 4 . ifiсationin thе еarly mаmmаliаn
Мaсtаddеn, B. '|. 1992. Frlssi!Нrуsеs: Sуstеmаtiсs, I,аlесlbkllogу,апd Еuolutioп of Nсw Yсlrk: Сambridgе LIrlivеrsityPrеss. the Fаmilу Р-t,1uidае. МасNair, М. R. l9[l7. Hеavy.lllеtаl lсsistаnсе in plirrrts-ir rт
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P U r p Ibeа с t e г i а
Molесular Еvolution FrаnсisсoJ. Aуаlа
Сyаnobасteriа Flavobaсtеria Thermotogа |es
Molесular biology hаs madе it possiЬlе to rесonstruсtthе сontinuity of suссеssion from thе original form of lifе, anсеstral to all living organlsms' to еvеry spесiеsnow living on еarth. Thе univеrsal trее of life, whiсh еmЬrасеs all known sorts of organisms, inсludеs thrее sеts of Ьranсhеs' Baсtегia, Ar. сhaеa' and Еukarya' whiсh all еmеrgеd from onе form of lifе, LUСA (Last Univеrsal Сommon Anсеstor; Figurе l). Al1 living organisms arе rеlatеd Ьy сommon dеsсеnt from a singlе form of lifе, rеprеsеrrtеdЬy thе trее trunk in thе figurе. Lifе may havе originatеd morе than onсе on our planеt-wе prеsеntly do not know-Ьut only onе form of lifе prospеrеd and lеft dеsсеndants, thе organisms that nоw populatе thе еarth. Baсtеria and Arсhaеa arе prokaryotiс miсrosсopiс сlrganisms.Еukarya arе organisms with сomplеx сеlls that сontаin sеvеral orgаnеllеs,onе of whiсh' thе nuсlеus, inсludеs thе hеrеditаry DNA. Most еukaryotiс organisms аrе singlе сеllеd and miсrosсopiс. Animals, plants, and fungi arе multiсеllular organisms, thrее of thе many Ьrаnсhеsof thе Еukaryа sеt. Тhе main Ьranсhеs of thе univеrsаl trее of lifе from LUсA, sеvеral Ьillion yеars ago' to thе prеsеnt havе Ьееn rесonstruсtеdon thе wholе and in many dеtails. Morе dеtails аЬout morе and morе Ьranсhеsarе puЬlishеd in sсorеs of sсiеntifiсartiсlеs еvеry month. Thе virtually unlimitеd еvolutionary infor. mation еnсodеd in thе DNA sеquеnсеof living organisms allows еvolutionists to rесonstruсtany еvolutionary rеlationshipsthat havе lеd to prеsеnt-day organisms, or among thеm, with as muсh dеtail as wаntеd. Invеst thе nесеssary rеsouгсеs(timе and lаЬoratory ехpеnsеs),and you сan hаvе thе answеr to any quеry with as muсh prесision as you want.
Мolесular Еvolution: Uniformity and Divеrsity In its unvеiling of thе naturе of DNA and thе workings сlf organisms at thе lеvеl of еnzymеs and othеr protеin molесulеs, molесular Ьiology hаs shown thе unity of lifе. Мorеovеr, molесular Ьiology has shown that thеsе molесulеs, DNA and protеins, hold informаtion aЬout an organism's anсеstry. t.)z
Figurе 1. Thе univеrsaltrее Baсtеria,Arсhaеa, and Еuk oгganismsarе rеlatеdЬy сo Ьy thе trее's..trurrk''(thеst using slоw-еvolvingriЬсlso
This has madе it possiЬlе l ously unknown and to сor Thе prесision with whiсh l еvidеnсе from molесular b Тhе molесular с
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to rесonstruсtthе сontinuity tlf suса n с е s t r a tl o a I I I i v i n g o r g a n i s m s ,r o tnivеrsaltrеe of lifе, whiсh еmЬraсеs thrее SеtSof Ьranсhеs,Baсtегia, Arfrom onе fоrrn сlf lifе, LUСA (Last . All living organisms arе rеlatеd Ьy lifе, rеprеsеntеdЬy thе trее trunk in norе than onсе on our planеt-wе lrm of lifе prospеrеdand lеft dеsсеnthе еarth. miсrosсopiсorganisms.Еukarya arе ain sеvеralorganеllеs,onе of whiсh, tJA. Мost еukaryotiс organisms arе llants, and fungi arе multiсеllulаr orthе Еukarya sеt. ее of lifе from LUCA, sеvеral Ьillion 'nstruсtеdon thе wholе and in many orе Ьranсhеsarе puЬlishеd in sсorеs rtually unlimitеd еvolutionary infor. lf living organismsallows еvolution'ionshipsthat havе lеd to presеnt-day :h dеtail as wantеd. Invеst thе nесеsеnsеs)'and you сan havе thе аnswеr you want.
'y and Divеrsity nd thе wоrkings of organisms at thе есulеs'molесular Ьiology has shown Ьiology has shown that thеsе molеation aЬout an оrganism's anсеstry.
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Figure1. Thе univеrsaltrее of lifе. Тhе thrееmajor groups of organisms, Baсtеria, Arсhaеa,and Еukarya' arе rеprеsеntеdЬy thе thrееmаin Ьranсhеs.All organismsarе rеlatеd Ьy сommon dеsсеntfrom a singlе fоrm of lifе, rеprеsеntеd by thеtrее's..trunk''(thеstraight.uplinе аt Ьottom).This trее was сonstruсtеd .Woеsе 1998.) usingslow-еvolving riЬosomalRNA gеnеs.(Adaptеdfrom
This has madе it possiЬlе to rесonstruсtеvolutionary еvеnts that wеrе prеviously unknown and to сonfirm and adjust thе viеw of еvеnts alrеady known. Тhе prесisionwith whiсh thеsееvеntsсan Ье rесonstruсtеdis onе rеason thе еvidеnсеfrom molесular biology is so сompеlling. Thе molесular сomponеnts of organisms arе rеmarkaЬly uniform in thе naturеof thе сomponеnts' as wеll as in thе ways in whiсh thеy arе assеmЬlеd and usеd.In all Ьaсtеria' arсhaеa' plants, animals, аnd humans' thе DNA сonsistsof a diffеrеnt sеquеnсе of thе samе four сomponеnt nuсlеotidеs (rеprеsеntеdаs A, с' G, and T; Figurе 2). Thе gеnеtiссodе, Ьy whiсh thе information сontainеdin thе DNA of thе сеll nuсlеus is passеd on to protеins' is virtually thе samе in all organisms (Figurе 3). Thе еnormously divегsе protеins in all sortsof organisms arе synthеsizеdfrom diffеrеnt сomЬinations, in sеquеnсеsof variaЬlеlеngth, of thе samе 20 amino aсids (listеd in Figurе З), although sеvеralhundrеdothеr amino aсids еxist. Similar mеtаЬoliс pathways-sеquеnсеs of Ьioсhеmiсalrеaсtions-aге usеd Ьy thе most divеrsе organisms to produсе еnеrgyand to makе up thе сеll сomponеnts. This unity rеvеals thе gеnеtiс сontinuity and сommon anсеstry of all organisms.Thеrе is no othеr rational Way to aссount for thеir molесular uniformity whеn numегous altеrnativе struсturеs arе in prinсiplе еqually likеly.Thе gеnеtiс сodе sеrvеs as an еxamplе. Еaсh partiсular sеquеnсе of thrееnuсlеotidеsin thе nuсlеar DNA aсts as a pattегn for thе produсtion of еxaсtlythе samе amino aсid in all organisms. This is no moге nесеssary than it is for a languagе to rrsеa partiсular сomЬinаtion of lеttеrs to rеprеsent a partiсular oЬjeсt. If it is found that сеrtаin sеquеnсеs of lеttеrsplanеt,trее' Woman-arе usеd with idеntiсаl mеanings in a numЬеr of diffеrеntЬooks, onе сan Ье surе that thе lаnguagеs usеd in thosе Ьooks arе of сommon origin.
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Gеnеs аnd protеins arе long molесulеs that сontаin information in thе sеquеnсе of thеir сolтponеnts in muсh thе samе way in whiсh sеntеnсеsof thе Еnglish languagе соntain information in thе sеquеnсе of thеir lеttеrs аnd words. Thе sеquеnсеsthаt makе up thе gеnеsarе passеd on from parеnts to offspring and arе idеntiсal from gеnеration to gеnеrаtion' еxсеpt for oсса. sionаl сhangеs introduсеd Ьy mutations. Сlosеly rеlatеd spесies havе vеry similar DNA sеquеnсеs;thе fеw diffеrеnсеsrеflесt mutations thаt oссurrеd sinсе thеir last ссlmmon аnсеstor. Spесiеsthat arе lеss сlosеly rеlatеd to onе anothеr ехhiЬit morе diffеrеnсеsin thеir DNA than thosе morе сlosеly rеlatеd Ьесausеmorе timе has еlapsеd sinсе thеir last соmmсln аnсеstor.This is
Figurе 3. The gеnеtiссodе:. mеssеngеrRNA and thе am nitrogеn Ьasе thyminе doеs thе othеr thrее nitrogеn Ьas adеninе (A)' сytosine (С), aI protеins (with thе thrее-lеt (Ala, A), argininе (Arg, R), ' (Сys, С), glyсinе (Gly' G), g ( H i s , H ) ' i s o l е u с i n е( I l е ,I ) ,l М)' phеnylalaninе(Phе,F), tyrosinе (Tyr' Y), tryptophа
thе rationalе for thе rесor аnd outсomеswiIl Ье rеvi As an illustгation, lеt ul Ьooks are 2oo pagеs long ехamination rеvеals that t for word, еxсерt that an r two Ьooks сannot havе l
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thаt сontain information in thе sе_ samеWay in whiсh sеntеnсеsof thе l thе sеquеnсеof thеir lеttеrs and ]еnеsarе passеd on from parеnts to ion to gеnеration, еxсеpt for oссa. Сlosеly rеlatеd spесiеs hаvе vеry rсеsrеflесt mutations thаt oссr.rrгеd i that arе lеssсlosеlv rеlatес{to o1-lе г DNA than thosе moге сlosеly rе. : thеir last сommon anсеstor.This is
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Figurе3. Thе gеnеtiссodе:сorrеspondenсеЬеtwееnthе 64 possiЬlесodons in messеngеr RNA аnd thе amino aсids (оr tеrminаtionsignals,..stop'').Thе nitrogenЬasеthyminеdoеs not ехist in RNA, whеrе urасil (U) tаkes its plaсе; тhеothеrthгееnitrogen Ьasеsin mеssеngеrRNA arе thе sаmе аs in DNA: adеninе(A), сytosine(С), and guaninе(G). Thе 20 amino aсids that makе up protеins(with thе thrее-lеttеrand onе-lеttеrstandard aЬЬrеviations)arе alaninе (Ala,A), argininе(Arg, R), asparagine(Asn, N), aspartiсaсid (Asp, D), сystеinе (Сys,С), glyсinе(Gly, G), glutamiсaсid (Glu, Е)' glutaminе(Gln. Q), histidinе (His,H), isolеuсinе(Ilе,I), lеuсinе(Lеu, [-)'lysinе (Lys' K), mеthioninе(Меt' (Phе,F)' prоlinе (Pro, P), sеrinе(Sеr'S), thгеoninе(Thr' Т), М), phеnylalaninе ryrosinе(Тyr, Y), tryptophаn(Trp' W), аnd vzrlinе(Val' V).
thе rаtionalе foг thе rесonstruсtion of еvolutionary history, whosе mеthods and outсomеs will Ье rеviеwеd latеr. As an illustrасion,lеt us assumе that wе arе сomparing two Ьooks. Both Ьooksarе 200 pagеs lorrg and сontain tlrе samе numЬег of сhaptеrs. Closеr ехaminationrеvеais thаt thе two Ьooks arе idеntiсal pagе for pagе and word for word, еxсеpt thаt an oссasional word-say, 1 in 100-is diffеrеnt. Thе two Ьooks сannot havе Ьееn writtеn indеpеndеntly: еithеr onе has bееn
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N\сllесulаrЕtlolt.ttion сopiеd froпr thе othеr, сlr Ь
InformationalМaсromolесulеs Nuсlеiс aсids and prorеins havе Ьееn сa||ed iп|'ormаtioпаl пшсromolесtllеs Ьесaцsе thеy arе long linеar molесulеs madе up tlf sеquеnсеs of unitsnuсlеotidеsin thе сasе of nuсlеiс aсids, amino асids in thе саsе сlf prсltеins_ tirat rеtаin сoirsidеr.rЬlеаmoLlnts of еvolutionary itrfсlrmirtion.Сomparisor-l of thе sеqцеnсе of thе сomponеnts in two mасгomolесulеs еstaЬlishеsthе numЬеrs that arе diffеrеnt.Bесausееvolution usually oссuгs Ьy сhanging onе unit at a tiпlе' thе numЬеr of diffеrеr-rсеs is an ir-rdiсationof tlrе rесеnсy of сoшmon аnсеstгy. Thе dеgrее of similarity in thе sеquеnсеof nшсlеotidеsor tlf amino асids сan Ье prесisеly quantifiеd. For ехamplе, in humans and сlriшpanzееsthе protеin molесulе сallеd сytoсhromе_с.whiсh sеrvеsа vitаl funсtion in rеspir a t i o n w i t h i n с е l l s ' с o n s i s t so f t h е s a m е ] 0 4 а m i n o а с i d s i n е х a с t l vt h е s a m е ordеr. It сliffеrs, horvеvеr, frоm thе сytoсhroп-tе_сof rlrеsr.rsrnonkе1.s Ьy 1 amino aсid, from that of horsеs Ьy 11 additiоnаl amino aсids, and from that of tuna Ьy 21 additional amino lrсiсls. Thе dеgrееof similaritу rеflесtsthе гесеnсyсlf сommon аnсеstгy.Thus infеrеnсеsfrom сomp.rгiltivеenаtопrr'аnd othеr сlisсiplinеsссlnсеrtlir-rg еvсllu. tionary history сan Ье tеstеd in molесular studiеs of DNA аnd protеins by еxamining thеir sеquеnсеsof nuсlеrltidеsand aminо aсids. TЬе authority of of gеnеs irnd thorrthis kind of test is ovеrwlrеlming:еirсl-rof thе thor"rsands sаnds of protеins сontаinеd in an orgаnism pгоvidеs an indеpеndеrrttеst of that organism's еvolutionary histor1'. Molесular еvolutionаrystudiеshavе thrее notaЬlе advаntagеsovеГсompariltivе anatoпly and thе tltlrеrсlassiсal сlisсiplinеs.onе is that thе informаtion is morе rеadily quаntifiaЬlе.Thе nr-rrrrЬеr of Lrnitsthаt arе diftЪrеlltis rеаdilу
еstaЬlishеd whеn thе sеqut diffеrеnt organisms. Thе s еvеn Ьеtwееn vегy diffеrеr parаtivе anatomy' for еха pinе trееs, and humаn Ьеiг protеin sеquеnсеs that сar multipliсity. Еaсh oгganis all rеflесt thе samе evoluti gеne or protеin does not si a sеt of spесiеs, additionа mattеr has Ьееn sеttlеd to Мoгеovег, thе widеly d opеn up thе opportunity с еnt dеgrееs of rеsolution il еvolving gеnеS to reсonst fastеr-еvolvin$ $еnеs to rе divеrgеd oгganisms. Gеnеs that еnсodе thе l еvolving gеnеS.Thеy havе ships among groups of or among Ьасtеria, аrсhаеa,; ing world), whiсh divеrgе among thе miсrosсopiс pl сomparеd with plants and of orgаnisms that divегgе tionеd еaгliеr, whiсh еvolv gеnеs' is usеd to dесiphеr l suсh as among humans, fi thе fiЬгinopеptidеs involvс ing thе еvolution of сlos maсaquеs' сhimpanzееs,a
Мolесular Phylogеni
DNA and protеins providt agеs from сommon nПCeS nеtiс сhangе that hаs oсс sееm at first that quantifyi Ье impossiЬIе Ьесausеit w isms that livеd in thе pаrst past arе somеtimes prеsе largеly disintеgratеd. Nev vidе informatiоn about aп As a spесifiс ехamplе' сhromе-с, whiсh is involvе
Мolесulаr Еuolution сopiеd' dirесtly or indirесtly, from ,, if еaсh сomponеnt nuсlеotidе of rplеtеsеquеnсеof nr-lсlеotidеs in thе э sеvеralhundrеd Ьooks, еaсh with .Whеn rd lеttеrs on еасh pagе. thе . . Ь o o k s ' (' g е n o m е s ) 'hеsе arе ехam. hе ,.lеttеrs''(nuсlеotidеs)givеs unargumеntsfor еvolution, Ьasеd on еt analogy, thе first аrgumеnt says : (thеsamе hеrеditarymolесuiе, thе lеs,аnd thе sanrе20 amino aсids in rary (thеsamеgеnеtiссodе), сannot ul-nеntсonсеrns similarity in thе sеhus thе sеquеnсеof amino aсids in similar tехts сannot Ье of indеpеn-
||ed iпformаtioпаl mасromolесulеs madе up of sеqшеnсеsof unitsnino асids in thе саsе of protеinsutiсlnary infornration. Ссlmpаrisсln Wo maсromolесulеsеstaЬlishеsthе tion usually OссursЬy сhanging onе ; is an indiсirtion of thе rесеnсy of ; е o f n u с l е o t i d е so r o f a m i n o a с i d s з, in humans and сhimpanzееs thе l i с h s е r v е sа v i г а |f u n с r i о ni n г е s p i 04 amino aсids in ехaсtly thе samе toсhromе-сof rhеsus monkеys Ьy additional аmino aсids, and from i.
еnсy of сommon anсеstry.Thus inothеr disсiplinеsссlnсеrningеvolulr studiеsof DNA and protеins Ьy and amino aсids. Thе authority of f thе thousandsof gеnеs and thousm providеsаn indеpеndеnttеst of :ееnotaЬlе advantagеsovеr сompar:iplinеs.onе is that thе informatiоn of units that arе diffеrеnt is rеadily
еstaЬlishеdwhеn thе sеquеnсеof units is known for a givеn maсromolесulе in diffеrеntorganisms. Thе sесond advantagе is that сomparisons сan Ье madе еvеnЬеtwееnvеry diffеrеnt sorts of organisms. Thеrе is vеry littlе that сomparativеanatomy, for еxamplе, сan say whеn organisms as divеrsе as yеasts' pinеtrееs,and human Ьеings arе сomparеd, Ьut thеrе arе numеrous DNA and protеin sеquеnсеsthat саn Ье сomparеd in all thrее. Thе third advantagе is multipliсity.Еaсh organism possеssеsthousands of gеnеs and prоtеins, whiсh all rеflесtthе samе еvolutionary history. If thе invеstigation of onе partiсular gеnеor protеin doеs not satisfaсtorily rеsolvе thе еvolutionary rеlationship of a sеt of spесiеs, additional gеnеs and protеins сan Ье invеstigatеd until thе mattеrhas Ьееn sеttlеd to thе satisfaсtion of thе invеstigator. Мorеovеr, thе widеly diffеrеnt ratеs of еvolution of diffеrеnt sеts of gеnеs opеn up thе opportunity of invеstigating diffеrеnt gеnеs for aсhiеving diffеrеnt dеgrееsof rеsolution in the trее of еvolution. Еvolutionists rеly on slowly еvolving gеnеs to rесonstruсt rеmotе еvolutionary еvеnts but inсrеasingly fastеr-еvolvinggеnеs to rесonstruсt thе еvolutionary history of morе rесеntly divеrgеdorganisms. Gеnеs that еnсodе thе riЬosomal RNA molесulеs arе among thе slowеstеvolvinggеnеs.Thеy havе Ьееn usеd to rесonstrцсt thе еvolutionary rеlationships among groups of organisms thаt divеrgеd vеry long ago: for еxamplе, among Ьaсtеria, arсhaеa, and еukaryotеs (thе thrее major divisions of thе liv. ingworld), whiсh divеrgеd morе tЬan2 Ьillion yеars ago (sее Figurе 1); or among thе miсrosсopiс protozoa (e.g., Plаsmodiиm, wЬiсh сausеs malaria) сomparеd with plants and animals, thе thrее of whiсh arе еukaryotiс groups of organisms that divеrgеd aЬout 1 Ьillion yеars ago. Сytoсhromе-с' mеn. tionеd еarliеr' whiсh еvolvеs slowly, Ьut not as slowly as thе riЬosomal RNA gеnеs,is usеd to dесiphеr thе rеlationships within largе groups of organisms, suсh as among humans' fishеs, and insесts. Fаst-еvolving molесulеs, suсh as thе fiЬrinopеptidеs involvеd in Ьlood сlotting, arе appropriatе for invеstigating thе еvolution of сlosеly rеlatеd animals, for еxamplе, thе primatеs: maсaquеs'сhimpanzееs, and humans.
Мolесular Phylogеniеsof organisms DNA and protеins providе information not only aЬout thе Ьranсhing of linеagеsfrom сommon anсеstors (сladogеnеsis)Ьut also about thе amount of gеnеtiс сhangе that has oссurrеd in any givеn linеagе (anagеnеsis).It might sееmat first that quantifying anagеnеsis for protеins and nuсlеiс aсids would Ье impossiЬlе Ьесausе it would rеquirе сomparison of molесulеs from organismsthat livеd in thе past with thosе from living organisms. Organisms of thе past arе somеtimеs prеsеrvеd as fossils, bцt thеir DNA and protеins havе largеlydisintеgratеd. Nеvеrthеlеss, сomparisons Ьеtwееn living spесiеs prov i d еi n f o г m a t i o na Ь o u t a n а g е n е s i s . As a spесifiс ехamplе, сonsidеr thе prеviously mеntionеd protеin сytoсhromе-с,whiсh is involvеd in сеll rеspiration. Thе sеquеnсеof amino aсids in
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Мoleсulаr Еuolution this protеin is krrown for many оrganisms, fгom Ьасtеria and yеаsts to insесts and hunrans;in animals' сytoсhromе_ссollsistsof 104 amiпo aсids. Whеn thе amino aсid sеquеnсеsof humans and rhеsus monkеys arе сomparеd' thеy arе found to Ье diffеrent at position 58 (isolеuсinе in humans' thrеoninе in rhеsus monkеys), Ьut idеntiсal at thе othеr 103 positions. Whеn humаns arе сompared with horsеs, 12 amino aсid diffеrеnсеSare found, and whеn horsеs arе сomparеd with rhеsusmonkеys, thеrеarе 11 amino aсid differеnсеs(Figuге4). Еvеn without knowing anything еlsе aЬout thе еvolutionary history of mammals, onе would сonсludе that the linеagеs of humans and rhеsus monkеys divergеd from еaсh othеr muсh morе rесеntly than they divеrgеd fгom thе horsе linеagе. Мorеovеr, it сan Ье сonсludеd that thе amino aсid diffеrеnсе Ьеtwееn humans and rhеsus monkеys mr-rsthavе oссurгеd in thе human linеаgе aftеr its sеparation fгom thе rhеsrrsmonkеy linеagе (sееFigurе 5).
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пUman Monkeу Horse пumаn Monkey Horsе
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5 5 6 0 6 5 7 0 1 5 8 0 8 5 9 0 9 5 10 0 1 0 4 KNKGIlWGЕDТLMЕYLENPKKYIP6TKMI FVGIKKKEЕRADLlAYLKKATN Е .....7
Figurе 4. Amino aсid sеquеnсеof сytoсhrоmе-сprotеinsin humans,rhеsus monkеys,and horses.Thе sеquеnсесonsistsof 104 amino aсids,еaсh rеprеsеntеdby a lеttеr.A dot indiсatеsthе samеamino асid as in humаns.Sее Fisurе 3 for thе namеsof thе аminо aсids.
Еvolutionary trееs aI еvolutionary histoгy of as gеnеra' familiеs, or t kinds of information rе nеsis. Figurе 5 illustratе thе rеlаtivе rеlationshiр of thе figurе, humans al to еасh othеr than еith shorvs that thе last сoп motе past than the last Еvolutionary trееs m; еaсh linеagе' or аnagеl last сommon аnсеstoг с h a n g е d i n t h е l i n е a g еt t o r h е s u s m o n k е y s .T h i that at position 58' п Figurе 4) havе thе sаnrс ,h е n t o n е ( i s o l е u с i n е )w aftеr it sеparatеd fгom 1
Мolесular Rесonst Sеvеral mеthods ехist f opеd for intеrprеtirrg п data; somе сan Ье usеd usеd in molесulaг еvol maхimum likеlihood. D|sтANсЕ MЕт|
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Figurе 5. Thе еvolutionоf сytoсlrromе-сamong hurnans,monkеys,and horsеs. Thе numbегsindiсаtеthе аmino :rсidrеplaсеmеnts that havе tаkеn pl:rсеin еасh Ьranсh of thе phylogеny.
A ..distanсе'' is thе num diffеrеnсеs arе mеаsurс data) or to сеrtаin maсI protеins or thе sеquеnс in Figurе 5 was oЬtain amino aсid diffеrеnсеs protеin. Thе amino aсid is rеflесtеdin thе numЬ геplaсеmеnt of onе am сlеotidе substitution in сasеs it rеquirеs at lеast numbеr of nuсlеotidе di еssary to aссount foг th( lutionary trее basеd on nuсlеotidе сhаngеs in еz
Мolеculаr Еuolution from Ьaсtеriaand yеasts to insесts Lsistsof 104 amino aсids' Whеn thе us monkеys arе сomparеd, thеy arе сinе in humans,thгеoninеin rhеsus .Wlrеn positions. humаns arе сom. ]еs arе found, and whеn horsеs arе 1 amino aсid diffеrеnсеs(F-igurе4). t thе еvolutionary history of mam_ of humans and rhеsus monkеys diy than thеy divеrgеd from thе horsе t thе amino aсid diffеrеnсе Ьеtwееn ;urrеd iir thе human linеasе аftеr its l (sееFigurе.5).
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nе-сprotеinsin humatrs,rhеsus ; of 104 aminсraсids,еaсh ;аmеamino aсid as in huI-rrans. Sее
Еvolutionary trееs arе modеls or hypothеsеs that sееk to rесonstruсt thе еvolutionaryhistory of taxa (i.е.,spесiеsor othеr groups of organisms, suсh as gеnеra'familiеs, oг ordеrs).As pointеd out е:lrliеr' thе trееs еmЬгaсе two kindsof information rеlatеd to еvolutionary сlrangе'сladogеnеsisand anаgеnеsis.Figurе .5illustratеsboth. Thе Ьrarrсhiпgгеlаtionshipsof thе trееs геflесt thе rеlativеrеlationshipsof anсеstry, or сlаdogеnеsis.Thus in thе right sidе of thе figurе,hunrаns and rhеsus monkеys 21геsееn to Ье morе сlosеly геlatеd to еaсh othеr than еithеr one is to thе horsе. Statеd anothеr way' this trее showsthat thе last сommon anсеstor to аll thrее spесiеslivеd in a morе rеmotеpast than thе last сommon anсеstor to humans and monkеys. Еvolutionarytrееs may also indiсаtе thе сhangеs that havе oссurrеd along еaсhlinеagе,or anagеnеsis.Thus in thе еvolution of сytoсhromе-с siпсе thе lаst сomnron zlnсеstor of humans and rlrеsus monkеys, сlr-rеarтino aсid сhangеdin thе linеagеthat Wеnt to httmаns Ьut none in thе linеаgе thaс Wеnt to rhеsusmonkеys' This ссlnсlusionis drаwn from thе oЬsеrvation (Figurе 4) that at positiоn 58, monkеys and horsеs (as wеll аs othеr animals; sее Figurе4) havе thе samе amino aсid (thrеoninе)'whilе humans havе a diffеrеntonе (isolеuсinе),whiсh thеrеforеmust hirvесhangеd in thе human linеagе aftеrit sеparatеd frolrl thе monkеy linеagе.
МolесularRесonstruсtionof Еvоlutionary History Sеvеralmеthods еxist for сonstruсting еvolutionary tгееs.Somе wеrе dеvеlopеd for intеrprеtingmorphologiсal data, othеrs for interprеting rnolесular datа;somе сan Ье usеd with еithеr kind of data. Thе main mеthods сurrеntly usеd in molесulaг еvolution arе сallеd distапсе. maхimum parsimony. and m a x i m u ml i k е l i h o o d ' DlsтANсЕ МЕтнoDs
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A ..distanсе''is thе numЬеr of diffеrеnсеsЬеtwееntwo kinds сlf organisms. Thе diffеrеnсеsarе mеasurеd with rеspесt to сеrtain traits (e.g., morphologiсal data)or to сеrtain maсromolесulеs (primarily thе sеquеnсе of amino aсids in protеinsor thе sеqttеnсеof nuсlеotidеs in DNA or RNA). Thе trее illustratеd in Figurе 5 was oЬtainеd Ьy taking into aссount thе distanсе, or numЬеr of amino aсid diffегеnсеs,among thrее orgагlisms with rеspесt to а Pаrtiсular protеin.Thе аmino aсid sеquеnсеof a protеin сontаins morе intЪrmаtionthаn is rеflесtеdin tlrе numЬеr of аmino aсid diffегеnсеsЬесausе in somе сasеs thе rеplaсеmеntoi onе amino aсid Ьy anothег rеquirеs no morе thurn onе nuсlеotidеsuЬstitution in thе DNA that сodеs for thе protеin, whеrеas in othеr сasеsit rеquirеs at lеast two nuсlеotidе сhangеs. TaЬlе 1 shows thе minimum numЬеrof nuсlеotidе diffегеnсеsin thе gеnеsof 20 sеparatеspесiesthat is nесеssaryto ассount for thе amino aсid diffеrеnсеsin thеir сytoсhromе-с. An еvolutionarytrее Ьasеdon tlrе data in TaЬle 1, shorvirrgthе minimum nuшЬегs of nuсlеotidе сhangеsin еасh Ьranсh, is illLrstгatеd in Figurе 6.
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The rеlationships Ьеtwееn spесiеs as shown in Figurе 6 сorrеspond fair|у wеll to thе rеlationships dеtеrminеd from othеr sourсеs' sllсh as thе fossil rесord.Aссording to thе figurе,сhiсkеns arе lеss сlosеly rеlаtеd to duсks and pigеonsthan to pеnguins, and humans and monkеys divеrgеd from thе othег mammalsЬеforеthе marsupial kаngaroo sеparatеdtrom thе nonprimаtе plaсеntals.Although thеsе еxamplеs аrе known to Ье еrronеous rеlationships, thе powеr of thе mеthod is apparent in that a singlе protеin yiеlds a fair|у aссuratеreсonstruсtionof thе еvolutionary history of 20 organisms that startеd to divеrgеmorе than 1 Ьillion yеars ago. Thе most сommon proсеdurе to transform a distanсе matrix into a phylogеnyis сallеd сlustеr analysis. Thе distanсе matrix is sсannеd for thе
141
1 4 2 Мoleсulаr Еuolutirlп smallеst distanсе еlеmеnt,and tlrе two taхa involvеd (say, human and monkеy in TaЬlе 1) arе joinесlat an intеrnal nodе, or Ьranсhing point. Thе matriх is sсannеd аgain fоr thе nехt-smаllеstdistirnсе,аnd thе two nеlv tахa (sаy' horsе zrnd donkеy) arе сlustеrеd. Thе proсеdurе is сontinuеd until аll taxa .!fhеn havе Ьееn joinес1. a distanсе involvеs a taxon thаt is alrеady }rertof a pгеviсlusсlustеr, thе avегagеdist:inсеis oЬtаiirесlЬеtwееnthе nеш'tахon irnсl thе prееxisting сlustеr (say, thе avеragе сlistanсеЬеtwееn humurnand horsе and monkеy anсl horsе).This simplе prtlсеdurеаssllmеsthаt thе ratе of еvo. lution is uniforrn alorrg :rll Ьranсl.rеs. Othеr distanсе mеthods (inсluding thе onе usеd ttl сonstruсt tlrе trее in Figurе 6) rеlax thе сondition of r"rniformrаtе and illlow for rrnеquаlratеs of еvolr.rtionalсlng thе brirnсhеs.or-rеof thе most ехtеnsivеl1,usеd ll-rеthodsсlf this kirrd is сallеd nеighЬor-joining.Thе шеthod starts' as Ьеforе,Ьy idеntifying thе smallеst distanсе in thе mаtrix and linking thе two tахa involvеd. Thе nехt stеp is to геmovе thеsе two tахa аnd сalсul:ltеa nеw mаtri-х in whiсh thеir distanсеs to othеr taхa arе rеplaсеd Ьy thе distanсе Ьеtwееn thе nodе that links thе tw.o taxa and all otlrеr taхa' Thе smallеst distаnсе in this nеw matrix is usеd for making thе nехt сonnесtion' rvhiсh will Ье Ьеtwееn trvсl othеr taхa or bеtwееn thе prеvious nodе and a nеW taхon. Thе proсеdurе is геpеаtеduntil all taxа havе Ьееn сonnесtес]with Ollе an()thегЬy intсгvеning nodеs. l oNY MЕтнoDs М A x l M U r . 4 . P A R sМ Мaхimum-parsimony mеthods sееk to rесonstruсtthе trее that rеqrrirеsthе fеwеst(i.е.,most parsimorrious)numЬеr of сhаngеsstlnrmеdltlongаll Ьгаrrсhеs. This is а rеasorraЬlеassumption Ьесausеit usually will Ье tlrе rnost Iikеly. But еvolution may not nесеssarilyhavе oссurrеd follorving a minimum path, Ьесаusе thе sarnе сlrangе irrstеadnray havе
from thе linеagеs that . vorеs' fоr examplе' dol gеthеr Ьесausе they pol сommon anсеstor bran( and сoyotеs.
MAХ|МUМ-LlKЕL
Мaximum-likеlihood mt availaЬlе data. Thеy rе< would makе it possiblеt. сhangе. For ехamplе, as morе likеly than transv proЬaЬility must Ье assl p г o Ь а Ь i l i t i е sf o r е a с h i n с trее is thе onе with thе I all possiblе trееs' Мaximum-likеlihood numЬеr of taхa is largе whiсh thе proЬability m of taхa. With 10 taхa, taxa, tЬе numЬеr of pos Еvеn with powеrful сoг h i Ь i t i v е i f t h е n u m Ь е ro t t i m е r е q u i r е d .H е u г i s t i с siЬlе tгееs is еxаminеd, а sтAт|sтlсAL
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Thе statistiсal dеgrее o1 and maximum-likеlihoо strapping. It сonsists of data point at random aг random sampling proсе Ьootstrap valuе for еaсl all spесiеs dеrivеd from bootstrap valuеs aЬovе thosе with Ьootstrap val
lVlolесular Phylogе
Thе mеthоds for oЬtai mously improvеd in rес. gеnеs havе bееn sеquеnс has Ьееn sеquenсеdin r
МoleсulаrЕuolцtion < ai n v o l v е d( s a y ,h u m а n а n d m o t r dе, сlr Ьranсhingpoint. Тhе matriх tanсе,and thе two nеw tаха (say' lсеdurе is сontinuеd until all tахa 3s а taхon tlrat is аlгеirdypart of a ltainеdЬеtwеегtthе nеw taxon arrd istanсеЬеtwееnhuman аrndhoгsе зduгеassutt-tеs thаt tl-rеrаtе of еvoonе usеd to сonstruсt thе trее in .atе i1ndallor,vfoг ltllс'qual ratеs сlf most ехtеnsivеlyusеd mеthods of еthod starts,аs Ьеforе,Ьy idеntifylirrkirrgrhе rrvo taха irr'',olvеd.Tlrе j с a l с u l а t еa n е w m а t r i х i n w h i с h Ьy thе distirnсеЬеtwеегtthе nodе . Tlrе srnallеstdistarrсе in this rrеw эсtiorr,whiсh will Ье Ьеtwееn trvo rnd a nеw taх()n.Thе proсеdurе is . J ц ' i г h ( ) n е : l I 1 ( ) t h е rl ) \ . i l . l г с г V е l l i l l g
s сonstruсtthе trее that rеquirеs tЬе :hаngеssummеdalong аll Ьrarrсhеs. u s u а l l yw i l l Ь е t h е r т o s t l i k е l y . B u t " е df o l l o w i n gа m i n i m u m p a t h ' Ь е oссuгrеd indеpеlrdеrrtli,along diflve involvеd intеrmеdiatеstеps. е thаt involvе a singlе stеp, may Ье : forrr nuсlеotidе Ьasеs in DNA, с1.. ; of a family of rеlatеd molесulеs rnd guaninе (G) Ьеlong to a family rithin а DNA sеqrrеnсefrom oпе е purinе to anothеr (A.'G), сallеd с h а n g , fеr с l mа p u r i n е t t l а p y r i m i , сallеd а transvеrsion.Parsimon1, labrlittеsof сlссurrеnсеif thеy irrе tеd to сladistiсs'a vеrУ formalistiс ехtеnsivеiyusеd with nloгphologifеaturеin сladistiсsis tlrе idеntifi. lomorphiс trаits.A synapomorpЬiс lrs Ьесausеtlrе formеr inhеritеd it hе tгait аftеr its linеagе sеpагatеd
from thе linеages that wеnt to thе othеr taхa. In thе еvolution of сarnivorеs,for ехamplе, domеstiс сats' tigеrs' and lеopards arе сlustеrеd togеthеrЬесausе they possеss rеtraсtaЬlе сlaws' a trait aсquirеd aftеr thеir сommon anсеstoг Ьranсhеd off from thе linеagе that lеd to dogs, wolvеs, аnd сoyotеs. MAxlMUM-L|KЕL|HooD МЕтHoDs Mахimum-likеlihood mеthods sееk to idеntify thе most likеly trее, givеn thе avаilaЬlе data. Thеy rеquirе that an еvolutionary modеl Ье idеntifiеd that would makе it possiЬ1еto еstimatеthе pгoЬabiiity of еaсh possiblе individual сhangе.For еxamplе, as is mеntionеd in thе prесеding sесtion' transitions arе morе likеly than transvегsions among DNA nuсlеotidеs, Ьut a partiсular proЬaЬilitymust Ье assignеd to еaсh. Ali possiblе trееs arе сonsidеrеd. Thе proЬaЬilitiеsfor еaсh individual сhangе arе multipliеd for еaсh trее. Thе Ьеst trееis thе onе with thе highеst probaЬility (or maхimum likеlihood) аmong all possiЬlеtrееs. Мaхimum-iikelihood mеthods arе сomputationally ехpеnsivе whеn thе numЬеr of taхa is largе Ьесausе thе numЬеr of possiЬlе trееs (for еaсh of whiсh thе proЬаЬility mцst Ье сalсulated)grows faсtorially with thе nцmbеr .!7ith of taхa. 10 taхa, thеrе arе aЬout 3.6 million possiЬlе trееs; with 20 taхa' thе numЬеr of possiЬlе trееs is aЬout 2 followеd Ьy 18 zeгos (2х1018). Еvеn with powегful сomрцtеrs' mаximum-likеlihood mеthods сan bе prohiЬitivе if thе numЬеr of tахa is largе, Ьесausе of thе сonsidеrаЬlе сompцtеr timе геquirеd.Hеuristiс mеthods еxist in whiсh only a suЬsamplе of all possiЬlеtrееsis еxаminеd, аnd thus an еxhaшstivеsеarсh is avoidеd. sтAтIsт|сAL APPRAIsAL oF ЕVoLUт|oNARY тRЕЕs Thе statistiсаl dеgrее of сonfidеnсе of a trее сan Ье еstimatеd for distanсе and maхimцm-likеlihood trееs. Thе most сommon mеthod is сallеd Ьootstrapping.It сonsists of taking samplеs of thе data Ьy геmoving at lеast onе data point at random and thеn сonstruсting a trее for thе nеw data sеt. This random sampling proсеss is rеpеatеd hundrеds or thousands of timеs. Thе bootstrap valuе for еaсh nodе is dеfinеd Ьy thе pеrсеntagе of саsеs in whiсh all spесiеsdеrivеd from that nodе appеar togеthеr in thе trееs. Nodеs with Ьootstrap valuеs aЬoуe 90oЬ arе rеgardеd as stаtistiсally strongly rеliaЬlе; thosеwith bootstrap vаluеs Ьelow 70oЬ arе сonsidеrеd unrеliаblе.
Мolесular Phylogеny of Gеnеs Thе mеthods foг oЬtaining thе nuсlеotidе sеquеnсеs of DNA havе еnormouslyimprovеd in rесеnt yеars аnd havе Ьесomе laгgеly аutomatеd. Many gеnеshavе Ьееn sеquеnсеd in numеrous organisms' and thе сomplеtе gеnomе has bееn sеquеnсеdin many spесiеs,ranging from humans to Ьaсtеria. Thе
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144
Мoleculаr Еuolиtion usе of DNA sеquеnсеs has Ьееn partiсularly rеwarding in thе study of gеnе dupliсations. Thе gеnеs that сodе for thе hеmсlgloЬins in humans and сlthеr mammals providе a good еxamplе. Knowlеdgе of thе amino aсid sеquеnсеs of thе hеmogloЬin сhains and of myogloЬin, a сlosеly rеlatеd protеin, has madе it possiЬlе to rесonstruсt thе еvolutionary history of thе dupliсations thаt gavе risе to thе сorrеsponding gеnеs. But dirесt еxamination of thе nuсlеotidе sеquеnсеs in thе gеnеs that сodе for thеsе protеins has shоwn that thе situation is moге сompleх, and also morе intеrеsting,than it appеars from thе protеin sеquеnсеs. DNA sеquеnсеstudiеs on human hеmogloЬin gеneshavе shown that thеir numЬеr is grеater than prеviously thought. Hеmoglobin molесulеs arе tеtramеrs (molесulеsmadе of four suЬunits)that сonsist of two polypеptidеs (rеlativеly short protеin сhаins) of onе kind and two of anothеr kind. In еmЬryoniс hеmogloЬin Е, onе of thе two kinds of polypеptidе is dеsignatеd с; in fеtal hеmoglogin F, tt ls Т; in adult hеmogloЬin A, it is F; and in adult hеmogloЬin A,, it is 6(hеmogloЬin A makеs up аЬout 98"Ь of humаn adult hеmoglobin, and hеmogloЬin A, aЬout 2"Ь|. Thе othеr kind of polypеptidе in еmЬryoniс hеmogloЬin is (; in Ьoth fеtal and adult hеmogloЬin, it is a. Thе gеnеS that сodе for thе first group of polypеptidеs (е, y, 0, and ф аге loсatеd on сhromosomе 11; thе gеnеsthat сodе for thе sесond group of polypеptidеs (( and a) arе loсatеd on сhromosomе 16. Thеrе arе additional сomplехitiеs.Two y gеnеseхist (known аs G,and A/' as do two 0 gеnеs (сt' and a,). Furthеrmorе, thеrе arе two B psеudogеnеs (уB, and VF,) and two gpsеudogеnеs (уa,and {{х,),as wеll as a (psеudogеnе. Thеsе psеudogеnеsarе vеry similаr in nuсlеotidеsеquеnсеto thе сorrеsponding funсtional gеnеs, Ьut thеy inсludе tеrminating сodons and othеr mutations that makе it impossiЬlе for thеm to yiеld funсtional hеmogloЬins. Thе similarity in thе nuсlеotidе sеquеnсеsof thе polypеptidе gеnеs and pseudogеnеs of Ьoth thе a and B gene familiеs indiсatеs that thеy arе all homologous-that is' that thеy havе arisеn through various dupliсations and suЬsеquеnt еvolution from a gеnе аnсеstral to all. Morеovеr, homology also ехists Ьеtwееn thе nuсlеotidе sеquеnсеsthat sеparatе onе 8еnе from anothеr. Thе еvolutionary history of thе gеnеs for hеmogloЬin and myogloЬln is sum.
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Figurе 7. Еvolutionaryh whiсh аnсеstralgеnеsdt а p p r o x i m a t еt i m е sw h е y е a г s( М Y 1 a g o .T h с t i n unсеrtаin.
сytoсhromе-с сonsists of only 104 аmino aсids, еnсodеd Ьy 312 nuсlеotidеs. N е v е г t h е l е s st, h i s s h o r t p r o t е i n s t o r е s е n o г m o u s е v о l u t i o n a r yi n f o r m a t i o n ' whiсh madе possiЬlе thе fairly good approхimation' shown in Figurе 6, to thе еvolutionary history of 20 verу divеrsе spесiеs ovеr a pеriod longеr than 1 Ьillion yеars. Сytoсhromе-с is a slowly еvolving protein. Widеly diffеrеnt spесiеs havе in сommon a largе proportion of thе amino асids in thеir сytoсhromе.с, whiсh makеs possiblе thе study of gеnеtiс diffеrеnсеs Ьеtwееn organisms only rеmotеly rеlatеd. Foг thе samе rеason, howеvеr, соmparison
of сytoсhromе-с molес twееn сlosеly rеlatеd сytoсhromе-с in humz vеrgеd 6_8 million yеa divеrgеd from thеir сol only onе amino aсid rе
marizеd in Figurе 7.
Мolесulаr Еuolutioп rly rеwarding in thе study of gеnе hеmogloЬinsin humans and othеr
gеnеs hemoglobin gеnеs myogIobin
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s of thе hеmogloЬin сhains and of nadе it possiЬlеto rесonstruсt thе hat gavе risе to thе сorrеsponding еotidе sеquеnсеsin thе gеnеs that rе situation is moге сomplех, and r thе protеin sеquеnсеs. globin gеnеshavе shown that thеir шght. HеmogloЬin molесulеs arе :s)that сonsistof two polypеptidеs Ldand two of anothеr kind. In еmls of polypеptidе is dеsignatеd s,.in loЬin A, it is B; and in adult hеmoaЬout 98% of human adult hеmoThе othеr kind of polypеptidе in and adult hеmogloЬin,it is a. Thе pеptidеs(е, Ъ 0, and ф arе loсatеd ,r thе sесondgroup of polypеptidеs r genеsехist (known as G,and A/, lorе' thеrе arе two B psеudogеnеs х, and уа,\, as wеll as a (psеudon nuсlеotidе sеquеnсеto thе сorrе_ rdе tегminatingсodons and othеr n to yiеld funсtional hеmogloЬins. rсеs of thе polypеptidе gеnеs and amiliеs indiсatеs that thеy arе all n through various dupliсations and al to all. Morеovеr, homology also tatsеparatеonе gеnе from anothеr. rеmogloЬinand myogloЬin is sum-
)rty асids,еnсodеd Ьу З1'2nuсlеotidеs. iormous еvolutionary information, rохimation, shown in Figurе 6, tсl е spесiеsovеr a pеriod longеr than еvolving protеin. \Х/idеly diffеrеnt rtion of thе amino aсids in thеir tudy of gеnеtiсdiffеrеnсеs Ьеtwееn s a m ег е a s o n h. o w е v е r ,с o m p a r i s o n
1,100N/Y Figurе7. Еvolutionaryhistory of thе glоЬin gеnеs.Thе forks indiсatеpoints at whiсhanсеstralgеnеsdupliсаtеd,giving risе to nеWgеnеlinеagеs.Thе timеs whеn thеsеdupliсations oссurrеd arе indiсatеd in millions of appr.oхimatе yеars(МY) ago.Thе timе whеn thе dupliсationof с' and сr, oссurrеdis unсеrtaln.
of сytoсhrome-с molесulеs сannot dеtеrminе еvolutionary rеlationships bеtwееn сlosеly rеlatеd spесiеs. Fоr ехamplе, thе amino aсid sеquеnсе of сytoсhromе-с in humans and сhimpanzееs is idеntiсal, although thеy divеrgеd6_8 million yеars ago; Ьеtwееn humans and rhеsus monkеys, whiсh divегgеdfrom thеir сommon anсеstor З5_40 million yеars ago' it diffеrs Ьy only onе amino aсid rеplaсеmеnt.
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Мoleculаr Еuolutioп Protеins that еvolvе morе rapidly than сytoсhromе-с сan Ье str'rdiеdin or. dеr to еstaЬlish phylogеnеtiс rеlationships Ьеtwееn сlosеly rеlatеd spесiеs. Somе protеins еvolvе vеry fast; thе fiЬrinopеptidеs-small protеins that arе involvеd in thе Ьlood-сlotting proсеss-arе suitaЬlе for rесonstruсting thе phylogеny of rесеntly еvolvеd spесiеs' sцсh as сlosеly rеlatеd mammals. othеr protеins еvolvе at intеrmеdiatе ratеs; thе hemogloЬins, for еxamplе' сan Ье usеd to rесonstruсt еvolutionary history ovеr a fairly Ьroad rangе of timе (sееFigurе 8). Onе grеat advantagе of molесulаr еvolution is its multipliсity, as notеd
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O n е с l l n s p i с u o t ' tаs t t r i h o m < l I o g o um s olесul plе. pгopoгtionsоf nL е v o l u t i o n a r yс h a n g ес t o D N A o r p r o г е i n st h tion. Studiеs of mсllе maсromсrlесulеsmay s It wаs first oЬsеrvе еnсеs Ьеtwееnhomolt n е a r l y p r o p с l r t i o n a lt t r o r . I f r h е г a t е o f е rt sаmеin thс еvoIuгiо D N A s е q u е n с е sW o u q u е n с е sс o u l d r h е n h е ing еvеnts of a phyl oссurrеd. Сonsidеr, for ехam gеnе сoding for сytoс} с o u l d d е t е r m i n еt h е t simply Ьy ехamining Ь r а n с h .o n е w o u I dn е sourсе' suсh as thе tt t i m е r h a t е l а p s е di n а r T h е m o l е с u l а rе v o сloсk, likе a watсh с
Мolесиlаr Еuolutioп сytoсhromе-ссan Ье studiеd in orps bеtwееnсlosеly rеlatеd spесiеs. ropеptidеs_small protеins that arе -аrе suitaЬlе for rесonstruсting thе suсh as сlosеly rеlаtеd mammals. ttеs;thе hеmogloЬins,for ехamplе, histoгy ovеr a fairly Ьroad rangе o{ olution is its multipliсity, as notеd
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еaгliеr.Within еaсh organism afе tЬousands of gеnеs and protеins; thеsе еvolvеat diffеrеnt rаtеs, Ьut еvеry onе of thеrrrrеflесtsthе sаnrееvolutionary е\.еnts.Sсiеntistsсan oЬtain grеatеr and grеatеr aссuraсy in rесonstruсting thе еvolutionary phylogеny of any group of organisms Ьy inсrеasing thе numЬеrof gеnеsinvеstigatеd.Thе rangе of diffеrеnсеsin thе ratеs of еvolution ЬеtwееnЕ]еI.lеs opеns up thе opportunity of invеstigatingdiffеrеr-rt sеts of gеnеsfoг aсhiеvil-lgdiffеrеnt dеgгееsof rеsсllutiorrin thе trее of litЪ; slowly еvolvingЕ]еnеsсаn bе usеd to study rеmotе еvolutionary еvеllts. Еvеn gеnеs thatеnсоdеslorvly еvоlving protеins сan Ье usеful for rесonstruсtingthе еvolutionaryrеlationshipsЬеtwееnсlosеly rеlatеd spесiеsЬy ехaminаtion of thе геdundantсodon suЬstitutions (nr.rсlеotidе suЬstitr'rtions that do not сhangе thе еnсodеd аmino aсids), thе intrоns (nonсoding DNA sеgmеnts intеrspеrsеdamong thе sеgmеrrtstlrirtсodе foг аmino асids), or othеr nonсoding sеgmеntsof tlrе gеnеs (suсh as rlrе sеquеnсеsthat prесеdе and tollow thе еn. сoding portions сlf gеnеs);thеsе gеnеrally еvolvе muсh fastеr than thе nuсlеotidеsthat spесify thе amino aсids.
Thе Мolесular Сloсk of Еvolution
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147
148
Мoleculаr Еuolutioп stoсhastiс сloсk' likе radioaсtivе dесay. In a stoсhastiссloсk thе proЬaЬility of a сеrtain amount of сhangе is сonstant (for еxаmplе, a givеn quantity of atoms of radium.226 is еxpесtеd' through dесay, to Ье rеduсеd Ьy half in 1',62Оуears), although somе variation oссurs in thе aсtual amount of сhangе. Ovеr fairly long pеriods of timе a stoсhastiс сloсk is quitе aссuratе. Thе еnormous potеntial of thе molесular еvolutionary сloсk liеs in thе faсt that ..tiсks', еaсh gеnе or protеin is a sеpаrаtе сloсk. Еaсh сloсk at a diffеrеnt ratе-thе ratе of еvolution сharaсtеristiс of a pаrtiсular gеnе or protеin-Ьut еaсh of thе thousands and thousаnds of gеnes or protеins providеs an indеpеndеnt mеasurе of thе samе еvolutionary еvеnts. Еvolutionists havе found that thе amount of variation obsеrvеd in thе еvo. lution of DNA аnd protеins is grеаtеr than is ехpесtеd from a stoсhastiс ..ovеrdispеrsеd,'' or somеwhat еrratiс. сloсk-in othеr words, thе сloсk is Тhе disсrеpanсiеs in еvolutionary ratеs along diffеrеnt linеagеs arе not ехсеs. sivеly largе, howеvеr. So it is possiЬlе, in prinсiplе, to timе phylogеnеtiс еvеnts with as muсh aссuraсy as may Ье dеsirеd,Ьut morе gеnеs or protеins (aЬout two to four timеs as many) must Ье еxaminеd than would Ье rеquirеd if thе сloсk wеrе stoсhastiсally сonstant. Thе avеragе ratеs oЬtainеd for sеvеral protеins takеn togеthеr Ьесomе a fair|у prесisе сloсk, partiсularly whеn many spесiеs arе studiеd and thе еvolutiоnary еvеnts involvе long timе pеri. ods (on thе ordеr of 50 million yеars or longеr). This сonсlusion is illustratеd in Figurе 9, whiсh plots thе сumulativе nцmЬеr of nuсlеotidе сhangеs in sеvеn protеins against thе dаtеs of divеrgеnсе of 17 spесiеsof mammals (16 pairings) as dеtеrminеd from thе fossil rесord. Thе ovеrall ratе of nuсlеotidе suЬstitution is fairly uniform. Somе primatе spесiеs (rеprеsеntеdЬy thе points bеlow thе linе at thе lowеr lеft of Figurе 9) appеar to havе еvolvеd at a slowеr ratе than thе avеragе for thе rеst of thе spесiеs.This anomaly oссurs Ьесausеthе morе rесеnt thе divеrgеnсе of any two spесiеs,thе morе likеly it is that thе сhangеs oЬsеrvеd will dеpart from thе avеragе еvolutionary ratе. As thе lеngth of timе inсrеasеs, pеriods of rapid and slow еvolution in any linеagе arе likеly to сanсеl onе anothеr out. Еvolutionists havе disсovеrеd, howеvег, that molесular timе еstimatеs tеnd to bе systеmatiсally oldеr than еstimatеs Ьasеd on othеr mеthods and' in. dееd, to Ье oldеr than thе aсtual datеs.This is a сonsеquеnсеof thе statistiсal propеrties of molесular еstimatеs' whiсh arе asymmеtriсally distriЬutеd. Bесausе of сhanсе, thе numbеr of molесular diffеrеnсеs Ьеtwееn two spесiеs may Ье largеr or smallеr than еxpесtеd. But ovеrеstimation еrrors arе unЬoundеd, whеrеas undеrеstimation еrrors arе Ьoundеd, sinсе thеy сannot Ье smallеr than zеro. Сonsеquеntly, a graph of a typiсal distriЬution of еstimatеs of thе agе whеn two spесiеs divеrgеd, gathеrеd from a numЬеr of diffеrеnt gеnеs' is skеwеd from thе normal Ьеll shapе, with a largе numЬеr of еstimatеs of youngеr agе сlustеrеd togеthеr at Onе еnd and a long tail of oldеr-agе еstimatеs trailing away toward thе othеr еnd. Thе avеragе of thе еstimatеd timеs thus will сonsistеntly ovеrеstimatе thе truе datе (Figurе 10). Thе ovеrеstimation Ьiаs Ьесotnеs grеatеr whеn thе ratе of molесular
3so z
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Figurе 9. Ratе of nuсlе 15 dots marks thе timе anсеstor (horizсlпtаIsс protеin сhangеs,that h solid linе drаwn from t suЬstitution.(Aftеr Fit<
еvolution is slowеr, t} сrеasingly rеmotе.
Сonсlusion
N4olесular Ьiology еrп thе 1953 disсovеry с сhеmiсal. N4olесular еvolution and makеs muсh dеtail and prесi N4olесular Ьiology unity of lifе in thе nat of еnzymеs and othеr lutionists, Ьy making that wеrе prеviously tionary relationships organisms. As pointеd out еar samе Ьasiс сomponеn
Мolесtt|аr Еuolиtitlп
n a stoсhastiссloсk thе proЬaЬility rt (for ехamplе, a givеn quantity o{ gh dесay' to Ье rеduсеd Ьy half in :urs in thе aсtual amount of сhangе. hastiс сloсk is quitе aссuratе. Thе lutionary сloсk liеs in thе faсt that . Еaсh сloсk ..tiсks'' at a difjеrеnt cf a partiсular gеnе or protеin-Ьut gеnеsor protеins providеs an indе_ y еvents. rnt of vаriation oЬsеrvеd in thе еvo:han is ехpесtеd from a stoсhastiс еrdispеrsеd''' or somеwhat еrratiс. ong diffеrеnt linеagеs arе not еХсеsin prinсiplе, to timе phylogеnеtiс d е s i r е dЬ , u r m o r е g е n е so r p r o t е i n s е еxaminеd than would Ье requirеd Thе avеragеratеs oЬtainеd for sеvrly prесisе сloсk' partiсularly whеn ) n a r yе v е n t si n v t r l v еl o n g t i m е p е r i эngеr). Lrе 9, whiсh plots thе сumulativе rrotеins against thе datеs of divеr_ ings) as dеtеrminеdfrom thе fossil rЬstitutionis fairly uniform. Somе s Ьеlow thе linе at thе lowеr lеft of owеr ratе than thе avеragе for thе Ьесausеthе morе rесеnt thе diverit is that thе сhangеsoЬsеrvеd will г е .A s t h е l е n g t ho f t i m е i n с r е a s е s , ny linеagеarе likеly to сanсеl onе , that molесular timе еstimatеs tеnd i Ьasеd on othеr mеthods and, inris is a сonsеquеnсеof thе statistiсal arе asymmеtriсally distriЬutеd. Bеar diffеrеnсеsbеtwееn two spесiеs But ovеrеstimation еrrors arе un. ; arе boundеd' sinсе thеy сannot Ье h of a typiсal distriЬution of еstiеd, gathеrеdfrom a numЬеr of difЬеll shapе,with a largе numЬеr of hеr at onе еnd and a long tail of thе othеr еnd. Thе avеragе of thе )vеrеstimatеthе truе datе (Figurе rеatеr whеn thе ratе of molесular
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-125
Figurе 9. Ratе сlf nuсiеotidе suЬstitution ovеr palеontologiсal timе. Еaсh сlf thе ]5 dots marks thе timе аt whiсh a pair оf spесiеs divеrgеd from а сOmmon anсеstor (horizoпtаl scаle) and thе numЬеr оf nuсlеotidе suЬstitutions, or protеin сhangеs' that havе oссurrеd sinсе thе divеrgеnсе (uertiсаl sсаlе).Thе solid linе drаwn from thе origin to thе ()utеrmost dot givеs thе avеragе ratе of suЬstitution.(Aftеr Fitсh 1976.)
еvolutionis slowеr, thе sеquеnсеsusеd arе shortеr, and thе timе Ьесomеs inсrеasingiyrеmotе.
Conсlusion Мolесular Ьiology еmеrgеdas a disсiplinе 100 yеars аftеr Darwin' following thе 1953 disсovеry of thе douЬlе-hеliх struсturе of DNA' thе hеrеditary сhеmiсal.Molесular Ьiology providеs thе strongеst еvidеnсе of Ьiologiсal еvolutionand makеs it possiЬlе to rесonstruсt еvolutionary history with as muсh dеtail and prесision as anyonе might want. Molесular Ьiology provеs еvolution in two ways: first, Ьy showing thе unity of lifе in thе naturе of DNA and thе workings of organisms at thе lеvеl of еnzymеsand othеr protеin molесulеs;sесond,and most importаnt for еvolutionists' Ьy making it possiЬlе to rесonstruсt еvolutionary rеlationships that wеrе prеviously unknown, and to сonfirm, rеfinе, and timе all еvolutionary rеlationships from thе univеrsal сommon anсеstor up to all living organisms. As pоintеd out еarliеr in this сhaptеr, all organisms arе madе up of thе samеЬasiс сomponеnts,whiсh, morеovеr' are similarly assеmЬlеdand usеd.
119
150
Мoleсulаr Еuolиtiсln
't8
organisms, from baсtеr now Ье rесonstruсtеd w Ьiology. Darwin сould r
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B
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Divergenсetime(x100MY) Figurе 10. Skеwingand agе Ьias in еstimatingmolесulardatеs.Тhе insеtshows thе trее topology for linеagеsA, B, and С; t.. and tт rеprеsеnt'rеspесtivеly' сaliЬrationand targеttimеs.Thе mаin panеl shows a fгеquеnсydistriЬutionof 1,000 еstimatеsof thе divеrgеnсеtimе ЬеtwееnlinеagеsС and AB in thе insеt' sеt to havе oссurrеd3 billion yеars ago and оЬtainеdwith thе usе of a short (7.5 rеsiduеs),slow.еvоlving(onеrеplасеmеntpеr sitе pеr 1010yеars)protеin and with thе usе of thе split ЬеtwееnA and B, sеt to 300 million yеarsago' as a сaliЬratiсlnpoint. T and M rеprеsеntaсtual (3 Ьillion yеars)and еstimаtеdmеan (4'084 Ьillion yеars)timеs.(Мodifiеd from Rоdriguеz-Trеllеs еt a|.2002.|
In all organisms' from Ьaсtеria to humans, thе instruсtionsthat guidе thе dеvеlopmеnt and funсtioning of organisms arе еnсasеd in thе samе hеrеditary matеrial, DNA, whiсh providеs thе instruсtions for thе synthеsis of protеins. Thе thousands of divеrsе protеins that еxist in organisms сonsist of thе samе 20 amino aсids in all organisms, from Ьaсtеria to plants and to animals. Thе gеnеtiс сodе, Ьy whiсh thе information сontainеd in thе DNA of thе сеll nuсlеus is passеd on to protеins, is sharеd Ьy all sorts of organisms. All organisms usе similar mеtaЬoliс pathways-sеquеnсеs of Ьioсhеmiсal rеaсtions-to produсе еnеrgy and to makе up thе сеll сomponеnts.Thе unity of lifе rеvеals thе gеnеtiс сontinuity and сommon anсеstry of all organisms. Thе dеgrее of similarity in thе sеquеnсеof nuсlеotidеs in thе DNA (and thus thе sеquеnсеof amino aсids in thе еnсodеd protеins) makеs it possiЬlе to rесonstrцсtеvolutionary history. Еaсh of thе thousands of gеnеsand thousands of protеins prеsеnt in аn organism providеs an indеpеndеnttеst of thе organism's evolutionary history. Thе еvolutiоnary геlationships among all
Avisе,J. С.2004. Мolесu Sundеrland,МA: Sinа A y a l а ,F . J . , е d .1 9 7 6 .М o l B a k е r ,A . J . ' е d .2 0 0 0 .М o Сarroll, S. B. 2О06.Тhе М Rеаlrd of Еuсllutiсlп D i с k е r s o nR , . Е . 1 9 7 1 .T h еvolution.lourпаl of 1 Fеlsеnstеin, l. 2О04.lпfer Fеnсhеl,т. 2002. Thе Оri1 UnivеrsityPrеss. Fitсh,.W.x4. 1976.Molес Еuolutioп,160-.l78. l Fitсh, \V. N4.,and Е. Мarg I55 279-284. Grаur, D., аnd \7.-Н. Li. 2 Sundеrland,MA: Sinа Hаll' B. G.2004. Phуlogе Assосiatеs. Hazеn, R. М. 2005.geи.e DС: JosеphНеnry Prt Lynсh.M. 2007. Тhе orig Assoсiatеs. Nеi, \4.,and S.Kumar.2 Oxford UnivеrsityPrс Rоdriguеz_Trеllеs' F., R. T toward оvеrеstimatio Nаtir.lпаlАсаdеmуof .Woеsе, C. R. 1998.Thе ur SсiепсеsUSА 95: 68.5
МoIеculаr Еuolutioп organisms'froпr baсtеria and protozoа to plаnts, anirnals, and humans сan now bе rесollstruсtеdwith as muсh dеtail as wantеd Ьy mеans of molесular Ьiology.Darwin сould not havе hopеd for morе.
-+
tт tс
115
BIвLIoGRAPHY
1з5
,l 55
175
,l 95
215
ime(xl00MY) ng mсllесulardatеs.Thе insеtshows .. and t, rеPrеsеnt'rеspесtivеlv' :Ishowsа frеquеnсydistriЬutionof ,ееnlinеа8еsС and AB irr thе insеt, obtainеdwith thе usе of а short (75 еr sitеpеr 10l0yеars)protеin and еt to 300 million yеarsago' as a (3 Ьillionyеars)and еstimatеdmеаn Rodriguеz-Trеllеs еt al. 2О02'|
s' thе instruсtionsthat guidе thе dеarе еnсasеd in thе samе hеrеditary lсtions for thе synthеsis of protеins. ist iп organismsсonsist of the samе сtегiato plirntsand to animals' Thе ontаinеdin thе DNA of thе сеll nury all sorts of organisrns.All organuеnсеsof Ьioсhеmiсal rеасrtons-ro omponеnts.Thе unity of lifе rеvеals ;tгyof all organisms. се of nuсlеotidеsin thе DNA (and эnсodеdpгotеins)mаkеs it possiЬlе of thе thousandsof gеnеsаnd thoшprovidеsan indеpеndеnttеst of thе olutionary rеlationships among all
Avisе,.|. с. 2004.МolеснlаrМаrkеrs,Nаturаl Нistorу,апd Еuolutiсlп'2nd ed. Sundеrland' N{A:SinаuеrAssoсi21tеs. Ayala,}-.l., еd.|976, МolесиlаrЕuolt,ttirlп, Sundеrland'MA: SinаuеrAssoсiatеs. Bakеr,A. J., еd.2000.МolесulаrМеtЬrldsiп Ессllogу.Oхford: Blaсkwеll. Сarroll,S. B. 2006. Thе Маhiпg of the Fittеst:DNА апd thе UltimаtеForeпslс .!?...W. Rесordof Еuсllutiсlп.Nеw York: Norton. Diсkеrsоn, R. L. 1971.Thе struсturеof сytoсhromес and thе ratеsof molесular еvolution. Jtluпlаlof МolесulаrЕuolutioп|: 2645. MA: SinauеrAssoсiatеs. Fеlsеnstеin, Sundеrland, J.2004, IпfеrriпgPhуlogеniеs, Fеnсhеl,Т.2002, TЬе origitl аnd Еаrlу ЕL,lllutitlпof Lifе, oхford: Oхford Prеss. Univеrsit,v Fitсh,W. I\4.1976.Мolесulаrеvolutiorrary сlсlсks.In F. J. Ayаla.еd.,Мolесulаr Еuolutkln,|60_178, Sundеrland,]r,1A:SinauеrAssoсiatеs. Fitсh,W. М., and Е. Margoliash.1967.Сonstruсtionof phylogеnetiс trееs.Sсiеnсe 155:279-284. of МoleсulаrЕuolutiсtп.2ndеd. Graur,D.' аnd \W.-H.Li. 2000.Fuпdаmeпtсlls }vIA:SinauеrAssoсiatеs. Sundеrlаnd, МA: Sinauеr Hаll,B. G. 2004.PhllogепеtiсТreesМаdе Еilsу.2ndеd. Sundеrland, Assoсi.rtеs. Hazеn,R. N{.2005. gепoеosis:Тhе Sсiепti|icQuest for Li|е's Оrigiп. Washington' DС: Josеphl{еnryPrеss. Lynсh,M. 2ОО7,Thе Оrigiпs of Cепomе Аrchitесturе.Sundеrland,MA: Sinauеr Assoсiatеs. Nеi, М., and S. Krrmar.2000. Мoleсulаr Еuoltltionапd Phуlogепсriсs.oxford: oхford UnivеrsityPrеss. Ьias Rodriguеz-Tтеllеs, F', R, Tarrio,and F. .].Avala.2002.A mеthodologiсal timе sсalеs.Proсееdiпgs of the towardovеrсstimatiоn of molесulаrеvolutionary NаtioпаIАсаdеmуof SсiепсеsUSA 99: 8112-8l15. .!Иoеsе, С. R. l998. Thе univеrsalanсеstor.Proсееdingsof the Nаtiс-lпаlAсаdemу oi USА 95: 6854_6859. Sсiеnсеs
i ),
Еvolution of thе Gеnomе Briаn Сh аrlesluorth аnd Dеborаh СhаrlesшОrth
Сhangеs in thе gеnеtiс information storеd in thе gеnomе arе thе ultimatе Ьasis of еvolution. Мuсh of еvolцtionary Ьiology involvеs studiеs of thе oЬsеrvaЬlе сharaсtеristiсs of organisms and thе hеritaЬlе сhangеs on whiсh thеir еvolution dеpеnds. But gеnomеs thеmsеlvеsalso еvolvе. Thе gеnomеs of сontеmporary spесiеs rеflесt Ьillions of yеars of еvolution, and thеy arе still еvolving, oftеn surprisingly rapidly. Data on gеnomе organization havе Ьееn aссumulating sinсе thе еra of сlassiсal gеnеtiсs, starting with thе disсovеry that gеnеs are сarriеd in thе сhromosomеs of сеlls and сan Ье mappеd gеnеtiсallyand physiсally to spесifiс loсations in thе сhromosomеs. Thе latеr disсovеry that сhromosomеs arе madе of nuсlеiс aсids has lеd to inсrеasingly finе.sсalе physiсal maps of gеnomеs' most rесеntly thе сomplеtе sеquеnсеsof (parts of thе) gеnomеs of (singlе individuals from) inсrеasing numЬеrs of spесiеs, now inсluding sеvеral spесiеs of animals (e.g', С. еlegапs Genomе Sеquеnсing Projесt 1'9991International Human Gеnomе Sеquеnсing Сonsortium 2001; Мousе Gеnomе Sеquеnсing Projeсt 2002; Drosopbilа 12 Gеnomеs Сonsortium 2007) and plants (е.g.,Thе AraЬidop. sis Gеnomе Initiative 2001), as wеll as ovеr 80 Ьaсtеrial spесiеs (Sharp еt al. 2005). Gеnomеs of many morе spесiеs will сеrtainly Ье sеquеnсеd in thе nехt fеw yеars, givеn thе rapid advanсеs Ьеing madе in sеquеnсing tесhnology. This information has gеnеratеd rеnеwеd inrеrеst in gеnomе еvolution, whiсh сan now bе dеsсriЬеd in unprесеdеntеd dеtail, and two major Ьoоks havе rесеntly Ьееn dеvotеd to it (Burt and Trivеrs 20О6;LуnсЬ 2007). !иith suсh еxtеnsivе data in hand, Wе сan hopе to idеntify somе of thе main pro. сеssеs involvеd in gеnomе еvolцtion. Modеls of many of thеsе proсеssеs ехist, and somе gеnеral thеmеs arе сlеar. Gеnomе еvolution oftеn involvеs various opposing forсеs, So that thе organization of thе gеnomе of a givеn spесiеs, or of a givеn gеnomiс rеgion, may dеpеnd оn situations that wеakеn or strеngthеn onе forсе or anothеr. Partiсularly intеrеsting situations arisе whеn thе еvolutionary intеrеsts of individual gеnomе fеaturеs сonfliсt with sеlесtion that асts on thе organisms thеmsеlvеs. Bесausе of thе сomplех IJZ
intегplay of diffеrеnt сrеasе in gеnomе stzе As with othеr typе thе typеs of сh:rrrgе within individuals (rт
matеrial of еvolution сan sprеad through t[ of thе spесiеs.Thеrе l lutionary proсеssеs.I may сausеindividual agе; as wе shall sее,s als is not thе only dе is thе random proсеs nеnts of gеntlmеs thl tions аrе finitе in siz dеtеrministiс fсlrсеs r ovеr gеnеrations, sor taЬlishеd (fixеd)in al trollеd Ьy thе еffесti thе numЬеr of Ьrееd rious variantsсan bе ordеr of thе rесiproс Thе rеlativе nragnitu dirесtion and spееd Ьееn strongly еmphа (2007). Bеforе dеsсriЬing r important fеaturеso tionary faсtors that r
Thе Compositio
тHЕ GЕNЕт|с
Тhе сhеmiсal Ьаsis о is a long strand tlf р linkеd Ьy sugar and 2008). Irr all сеllul сlеotidе is douЬlе-st may Ье douЬlе-stran strandеd DNA (suс fluеnza virus). Thс сoпrplеmеrrtary:wht ninе, thе othеr straг thе сomplеmеntary l thus Ье dеsсriЬеd ir
Еuolиtion of thе Cenomе
Gеnomе d 1
in thе gеnomеarе thе ultimatе Ьaiology involvеs studiеs of thе oЬl thе hеritaЬlе сhangеs on whiсh msе]vеsalso еvolvе. Thе gеnomеs f yеars of еvolution, and thеy arе )ata on gеnomе organization havе сal gеnеtiсs' starting with thе dislromosomеs of сеlls and сan Ье ifiс loсations in thе сhromosomеs. е madе of nuсlеiс aсids has lеd to nomеs' most гесеntly thе сomplеtе i n g l е i n d i v i d u a l sf r o m ) i n с r е a s i n g rl spесiеsof animals (e'g., С. еle.ntеrnational Нuman Gеnomе Sе:nomе Sеquеnсing Projесt 2002; 7) and plants (е.g.,Thе AraЬidop:r 80 Ьaсtеrialspесiеs(Sharp еt al. мill сеrtainly Ье sеquеnсеd in thе ; bеing madе in sеquеnсing tесh' .еd intеrеst in gеnomе еvolution' :ntеddеtail, and two major Ьooks Trivеrs 2006;Lупсh 2007). \Хlith t o i d е n t i f ys o m е o f t h е m a i n p r o Lеlsof mаny of thеsеproсеssеsехGеnomе еvolution oftеn involvеs nization of thе gеnomе of a givеn dеpеnd on situations that wеakеn сularly intеrеsting situations arisе lual gеnomе fеaturеs сonfliсt with msеlvеs.Bесausе of thе сomplеx
intеrplayof diffеrеnt forсеs' сhangеs oftеn oссur in onе dirесtion (е.g.,аn inсrеasеin Е]еnomеsizе) and thеn latеr rеvеrse. As with othеr typеs of еvolutionary сhangе, wе nееd to undеrstand Ьoth thе typеs of сhangеs in gеnomе оrgаnization and сomposition thаt arisе within individuals (mutations and othеr molесular сhangеs that arе thе raw matеrialof еvolution) and alsсl how a trait сarriеd initially Ьy onе individuаl сan sprеadthrough thе wholе population, lеading to еvolution of thе gеnomе of thе spесiеs.Thеrе arе tWO main сausеsof this sprеаd, just as for othеr еvolutionaryproсеssеs.First, dеtеrnrinistiсforсеs, partiсularly natural sеlесtion, may сausе individuals with a givеn trаit to lеavе morе dеsсеndantsthan avеrаgе;as wе shаll sее,suсh Daгwinian natuгal sеlесtionat thе lеvеl of individuals is not thе only dеtеrministiсforсе that aсts on gеnomеs.A sесond faсtor is thе random proсеss of gепеtiс drift, wЬicЬ is еspесially rеlеvant for сomponеnts of gеn()mеsthat do not affесt orgаnismal funсtions. Bесausе populations arе finitе in sizе, gеnеtiс variants that arе suЬjесt to suffiсiеntlywеak dеtеrministiсforсеs will ехpеriеnсе random fluсtuations in thеir frеquеnсiеs ovеr gеnеrations,somеtimеs сausing an initially rarе vаriant to Ьесomе еstaЬlishеd(fiхеd)in all individuals of a spесiеs.Thе ratе of gеnеtiсdrift is сontroliеd Ьy thе еffесtiuе poplilаtioп siee, whiсh is usually muсh smallеr than thе nunrЬеrof Ьrееding individuals in a spесiеs(Kimura 1983). Еvеn dеlеtе. rious variаnts сan Ьесomе fiхеd Ьy drift if thе intеnsity of sеlесtion is of thе ordеr of thе rесi;lrсlсalof tЬе еffесtivеpopulation sizе or lеss (Kimura 1983). Тhе rеlativеmagnitudеsof drift and dеtеrministiсforсеs thеrеforесontrol thе dirесtion and spееd of еvolutionary сhangеs irr gеnomеs; this hаs rесеntly Ьееn strongly еmphasizеd as а сausal faсtor in gеnomе еvolution Ьy l,ynсh
(2007).
Bеforе dеsсriЬing ехamplеs of hypothеsеsаnd tеsts,wе first outlinе somе important fеaturеstlf gеnolте orgаnization аnd sizе and thеn disсuss еvolutionary faсtors that may havе sЬapеd thеsеpropеrtiеs.
Thе Сomposition and Sizе of thе Gеnomе тHЕ GЕNЕт|с MAтЕR|AL Thе сhеmiсal Ьasis
15З
154
Еuolutioп of thе Geпomе (A, T' G, and С), whilе that of thе douЬlе strцсfurе is spесifiеd Ьy thе frе. quеnсiеs of the Ьasе pairs AТ and GС. RNA is gеnеrally single strandеd, with a diffеrеnt sugar rеsiduе from that in DNA and with uraсil Ьasеs instеad of thyminеs' Although thе origins of thе gеnеtiс сodе arе unknown' sеlf-rеpliсatirrg RNA molесulеs may havе Ьееn thе еarliеst form of ..lifе,'' Ьut thе transition to gеnomеs that usеd thе muсh morе stablе DNA oссurrеd long ago (Joyсе 1989). DoцЬlе-strandеdDNA also allows damagе to Ье сoгrесtеdЬy сopying from thе undamagеd сomplеmеntаry strand. Sinсе DNA largеly laсks RNAs ability to aсt as a сatalyst, this сhangе must havе gonе along with thе еvolution of a mеans of transсriЬing onе stгand of a gеnе's DNA into RNA. In prеsеnt-dayorganisms thе sеquеnсеof basеs in thе ..mеssеngеr''RNA tгansсriЬеd from a gеnе dеtеrminеsthе sеquеnсеof thе amino aсids in thе protеin сhain еnсodеd Ьy thе gеnе (Figurе 1). Thеrе arе also many RNA molесulеsof dirесt funсtional signifiсanсе, whiсh аrе transсriЬеd (сopiеd) frоm DNA Ьut not translatеd into an аmino-aсid sеquеnсе.
vlгus gеnomеs arе usuz fluеnza) paсkagе sеvеrс into tlrе samе viгus pal have diffеrеnt RNAs pa thus сomЬinе diffеrеnt ing multiplе infесtions, F{uпrаns and otlrеr а isms Ьеlong to thе еuki DNA organizеd into l сеlls (Figurе I). Тhе с dеal with thе proЬlеm с сulеs, and сепtromеrеs sion to thе daugЬtеr се еukaryotеs, suсh as thе gеnoп1е,with just onе с matе' thеге is а Ьriеf d еaсh mating partrrеr.Tl
oRGANlzAт|oN oF тHЕ GЕNЕт|с MAтЕR|AL Мany prokaryotеs' gеnomеs (Ьaсtегia and virusеs) сonsist of just a singlе DNA or RNA n-rolесulе,oftеn сirсtrlar (TaЬlе 1). Somе Ьaсtеriа (suсh as Borelliа, thе сausе of Lymе disеasе)lravе sеvеral sеParatе molесulеs; although
Сhromosome
Genes messenger RNA intron
telomerе
а.
f"
I сenтromere
telomere
Ц г F FI
t
'i',,
spIiсеd MRNA
+lЕ
Protein
trans|аtion
-+
T а Ь l е l . G е n о m еs i z е s orgаnism Virusеs Plаnt viroids Influегlzavirus Rеovirus Phagе tpX174 SV4O Vaссitriavirus Baсtеria Е. сoli Му сo1llаsmа gепitаlium
intron i
i ntron
+#
Figurе 1' Chromosomеs,showingthеir major fеаturеsand thе Ьandingpаttеrns that сan Ье sееnwith stаiningmеthods.Thе figurеаlso shows a sсhеmatiсof a rеgion of thе сhromosomе сontaining thrее gеnеs'thе mеssеngеrRNA produсеd Ьy thеm, and thе individuaIprotеinsеnсodеdby thе mеssеngеrRNA.
Nuсlеurrgеnomеsоf еtrk Y east (Sаcchаro|l,t)) L:еsсе Nеmatodе (Саепorhаbd Fruit fly (Drosophilа mе Ftsh (Fugu rubripеs) Sаlаmandеr Mat-lrmal (Homo sа|liеп Сress (Arаbido1l sis thаlit Mаizе (Zeа mауs) Fritillа11'p ritillаriа,lssу
Ntlrс: AЬЬrеviаtions:Ьp kiloЬаsеs;МЬ, mеgаЬasеs ? mеаns thаt thе gеnеnu ? ? t h . r ri t i s b а s е do т l i n . lаr
Еuolutiсlпof tbе Gепome эlе stгuсturе is spесifiеd Ьy thе frе,IA is gеnеrallysirrglеstrandеd,with 'trAand with uraсil Ьasеs instеad of ]odе arе unknown, sеlf-rеpliсating :st form of ..lifе,'' Ьut thе transition Ьlе DNA oссurrеd long ago (Joyсе i damagеto Ье сorrесtеdЬy сoрying nd. Sinсе DNA largely laсks RNA's Jst havе gonе along with thе еvolund of a gеnе's DNA into RNA. In lsеs in fhе ..mеssеngеr''RNA tranrсеof thе amino aсids in thе protеin rе arе also many RNA molесulеs of ransсribеd(сopied)from DNA Ьut эе.
virus gеnomеs aге trsually singlе nrolесulеs,somе RNA virusеs (suсlr as influеnza)paсkagе sеvеrаl diffеrеrrtRNA rrrolесulеsthat саrц, diffегеIltgеnеs into thе samе virus partiсlе. Otlrеr RNA virusеs (е.g.,alfalfa rr-rosaiсvirus) havеdiffеrеntRNAs paсkagеd into sеparatеvirus partiсlеs.Thеsе virusеsсan thus сomЬinе diffеrеnt portions of thеir gеnomе from diffеrеnt parеnts during multiplе infесtions,a primitivе typе of sеxualitY. Humans and othеr аnimals, plants, fungi, and man,v singlе_сеllеdor!]anisms Ьеlong to гhе еukaryotе division of lifе' whiсh is dеfinеd Ьv hаving thе DNA organizеd into linеar сhromosomеs сarriеd within thе rrLrсlеiinsidе сеlls (F.igurе1). Thе сhromos
lс мAтЕRIAL nd virusеs)сonsist of just a singlе (TaЬlе 1). Somе baсtеria (suсh as lеvеralsеpаratеmolесulеs; although
spIiсed MRNA
Protein
translation
.+|Е
+
+# lr fеaturеsand thе Ьanding pattеrns figurеalso shows a sсhеmаtiсof a gеnеs'the mеssеngеr RNA produсеd d Ьy thе mеssеr-rgеr RNA.
TaЬlе1. Gеnorrrеsizеs Organism Virusеs Plant viroiсls Influеnzavirus Rеovirus Phagе
Gеnomе
Gеnе numЬеr
('еnomе sizе
0 12 22 11 6 .100
З00Ьp l 3 . . 5k Ь 2зkb 5 . 4k Ь
Vaссiniaviгus
ssRNA ssRNA dsRNA ssDNA dsDNA dsDNA
Baсtеria Е, сoli МусoplаsmаgепitаIium
dsDNA dsDNA
4,400 500
4 . 6М Ь 0 . 6М Ь
sv40
Nuсlеаrgеnomеsof еukaryotеs Y еast(Sассbаro1п)| сеs cеrеuisiае) Nеmаtodе1Саепсlrhаhditisеlеgап,s) Fruit fly (Drosrlph ilа melапсlgаstеr) FisЬ (Fugи rubripes) Salamandеr Mammal (Homсl sаpiеns) Сr ess(Аrаb i dopsi s th аliапа) Мaizе (Zеа lttаvs) Fritillary (F ritil lаriа аs sуriаcа)
6,000 19,000 14,000 22,000(?) 3 0 , 0 0 0( ? ? ) 2 0 , 0 0 0( ? ) 27,000 .r0,000(??) 2 7 , 0 0 0( ? ? l
)
Кl]
187kЬ
12Мb 100МЬ 1 4 0М Ь 400MЬ 90,000МЬ 3,000МЬ 1 0 0М b .i,000МЬ MЬ L20,000
Nofe: AЬЬrеviations:bp, basеpаirs;ss, singlestrаndеd;ds, douЬlс strаndеd;kb, kilоbasеs; МЬ' mеgаЬasеs. ? mеаnsthаt thе gеnе numbеr is сlnll' аpproximatеlyknоlvn froпr thе gсnolrrеsеqllеnсс' gсlltlt-t-tеs ?? that it is Ьasеdoгrinсompletссvidеrrсеor analсlgуrvitЬ sеquеnсесl
].i.i
1.'6
Еuolutirп of tbе Gепomе to rеstorе thе haploid statе.In this division' gеl1еsfrom thе Parеntal сеlls аrе rесOmЬinеdthrough rесiproсal еxсhangеsof poгtions of thеir сhromosomеs (crossiпg ouеr: SеeLеwin 2008 аnd Figurе 2). In animаls and highеr plants thе diploid stagеprеdominatеs,аnd thе haploid sti.ltеis oftеn just a Ьriеf part oI rhе rеprсlduсtivеproсеss' Chromosomе numЬеrs in thе haploid sеt vary widеly among diffеrеnt spесiеs:16 in thе сasе of Сhlаmуdomoпаs,5 in Drosophilа,2З in humans, but somеtimеs just a singlе сhromosomе (in a spесiеsof ant and an Аsссtris roundworm). Сharrgеs Ьеtwееn spесiеs in сhгomosomal stгuсturе arе сommon, involvtng dtlpliсаtion.sаnd dеIеtit.llts of gеnetiс matеrial, inuеrsioпsof parts of сhromosomеs (Figurе 3), and trапslocаtiсlпs(ехсhangеsof matеrial Ьеtwееn diffеrеnt сhromosomеs). Сhromosomе rеarrangеmеnts oссur infrеquеntly in еvolution (roughly onе pеr gеnomе pеr 10 million yеars in mammals, although somе gгoups, suсh аs rodеnts, havе rаtеs 10 timеs highеr: Еiсhlеr and Sаr-rkoff2003). Ovеr еvolutionary timе) tlrе rlrdеr of gеnеswithin a сhromosomе gradually Ьесomеs sсramblеd Ьy suссеssivе invегsions. Sеvеrаl human сhromosotnеs sееm to havе rеmainеd unсhanяеd in gеrrе сontеnt
Сrossingover
f
\
Figurе 3. A сlrromсlsomt сhromosomе, and thе aр Ьееn rеаrrangеdso that othеr way аrttund from
ABсD
PаrentaI сhromosome
(though not ordеr) ovе m a d е u p < l fs е p a r a r еЬ l
сoD|NG AND N
U n e q u a |с ro s s ingo v еr bet wеendup|iсated or rеpeatedgеnеs
I
Y
Figurе 2. Тop: Сrossing ovеr in a rеgion of a сhгomosomе сontaining fivе gеnеs, A to Е, shсlwing thе rеsulting rесomЬinant сombinations of thе gеnеs (indiсatеd Ьy uppеr. and lowеrсasе lеttеrs аnd аlso Ьy Ьlасk аrrd grаy linеs for tlrе twсl diffеrеnr parеlrtal сЬromosonrеs). Bottom: Сrсlssing ovеr in a геgion rrf сhromosomе сontaining two dupliсatеd gеnеs that аrе similar еnor.rghthat thеy may mispair, lеading тo unеqual сrossing ovеr.
Gеnomе sizе is dеfinе loid gеnomе. A gеnom а r е t r а n s с r i Ь е di n r o m t quеnсеs (Lеwin 2008 qиепсes ar'd iпtroпs.h transсriЬеd but arе rеr latеd; in еukаryotеs,ir |л as thе spliсе
Еuolutioп of tbe Genomе )n' gеllеsfrom thе paгеntal сеlls arе s of portions of thеir сhromosоmеs r e 2 ) . I n a n i m a l sa n d h i g h е r p l a n t s aploid statеis oftеn just a Ьriеf part
I Ц
invertеd rеgion
l-
l sеt vary widеly among diffеrеnt зs, .5in Drosopbilа,23 in humans, (in a spесiеsof ant and an Аsсаris n сhromosomal struсturе arе сomls of gеnеtiс matеriаl, iпuеrsiсlпs of lпsloсаtioпs(ехсhangеsof matеria] osomе fеarrangеmеnts oссur infrе-
I
nе pеr 10 miiliorr уеaгs in mamrnals, havе гаtеs 10 tiпrеs highеr: Еiсhlеr lе' thе ordеr of gеnеswithin a сhroЬy suссеssivеinvеrsions. Sеvеral rainеd unсhangеd in Е]enесontеnt
lr
!
I
I
non-invertеdregion
-
l. ffi
!
,l
Figurе 3. A сhrtlnlosomе invеrsion. Thе diagram shorvs thе Ьаnding pattеrn of a сhromosomе, and tЬе appеaranсе whеn thе top pаrt of thе сhromosomе has Ьеегlrеarrangеd so that part Of thе gеtrorте in thе гight-hand сhromosomе is thе othеr Way around from thе orсlеr in thе lеft сlnе.
\ \
ff,H,i;:il' t:i
I
ParentаI сhromosome
_/
(thoughnot ordеr) ovег thе сoursе of somе 70 million yеars, Ьut othеrs arе madе up of sеparatеЬloсks dеrivеd from diffеrеnt atrсеstralсhromosomеs. сoDING AND NoNсoDING sЕauЕNсЕs
up|iсated or repеatedgenes -
Wж3Е-
жWE
сlrromosomе сontaining fivе gеnеs, lmbinations of thе gеnеs (indiсatеd llaсk and gray linеs f
Gеnomе sizе is dеfinеd as thе numЬеr of Ьasеs in a singlе strand of thе haploid gеnomе.A gеnomе has two main сomponеnts:сoding sеquеnсеs(whiсh arе transсriЬеdinto mеssеngеrRNA and еnсodе protеins) and nonсoding sеquеnсеs (Lеwin 2008). Nonсodirrg sеquеnсеs inсludе Ьoth intеrgеllic sе. quеnсes and iпtrсlпs' Introns arе sеgmеnts of sеquеnсеswithin gеnеs that arе transсriЬеd Ьut aге rеmovеd Ьу spliсiпg Ьеforе tlrе mеssеngеr RNA is translatеd;in еukaryotеs,intron spliсing involvеs a protеin.RNA maсhinе known as tЬe splicеosorпе' Intеrgеniс sеqllеnсеs and somе introns inсludе rеgions thаt aге rеsponsiblеfor сontrolling gе11е еxpгеssionby dеtеrmining thе lеvеls rrrеssеngеr produсtion timing of RNA fronr rrеarbygеnеs.Thеsе arе nonаnd с o d i n gЬ u t f u r l с t i o n a lp a r r s o [ g е n о m е s . Еvеn with сomplеtе gеnomе sеquеnсеs'it is diffiсult to сount a gеnomе's gеnеsЬесausесoding sеquеnсеsarе almost indistinguishaЬlеfrom othеr sеproЬlепr Ьесausеof thе low proquеnсеs.Thе task is a nееdlе-in-tЬе-haystaсk poгtiоn сlf сoding sеquеnсеsin thе gеnomеsof man1.nrultiсеllr"rlаr orgаnisms
157
158
Еuolutiсlltrlf thе Сепolltt, (еstimаtеd to Ье aЬout 1.5% of hunran DNA; sее Intег11i1tional Human Gеnomе Sеquеnсing Сonsortium 2001). Thе triplеt gеnеtiс сodе usеd Ьу mеssеngеrRNA, ilr whiсЬ thгее ad jaсеnt nuсlесrtidеs(сodoпs)сorrеspond to еaсh amino rrсid of thе prсltеirr еnсodеd' and сеrtain triplеts-rhе sfoдr сodсlпs-stgnify tЬе еrrd of traIlslation,сan sllggеstсandidаtеsfor sеquеtlсеs thаt еnссldеamino асid sеquеrrсеs.Thе rrrrсlеotidеsin thе third pсlsitionsof many сodons do not аffесt thе aпrino aсid еnсodеd, sitrсе sеvеral diffеrеnt сodons сihatеroсЬromаtiп'tlrе Ьloсks ot unrtsuallу dееply staining matеriаl visiЬlе in dividing сеlls' сhromosomеst usually сonсеntratеd nеar thеir сеntl:olтlеrеsаnсl (in somе spесiеs)tеlomегеs (Jtlhn and Мiklos 1988; Еlgin and Grеwаl 200з). Tlrеy сltn rnakе up astonishirrg amounts of thе DNA o[ somе
thе fruit fLуDrosсlphilа mеL tеrminаtion) has aЬout 20 r thеm сomposеd of a bloсl.
sparsеr in hеtеroсhromatin Thе amount and sеquеnсе among diffеrеnt spесiеs.Fo madе up of fouг short sa1 thosе оf its distant rеlаtivе, gеnomе sizе (John and Mi
2007 ). Diffеrеnt kangaroo faсtor of 1.6 |a rangе similа of diffеrеnсеs in thе alnoun V a r i a t i o n a m o n g s p е с i е si n largе diffеrеnсеs in gеnom( nttmЬеrs (С:rvaliеr-Smitlr1
Traпsposаblе elemеnts SцЬstantial proportions of p е a t s ( 2 0 0 b а s е s - 1 0k i l o Ь a wholе gеnomе than sаtеlli ttble еlemeпrs (TЕs)' whiсh сations in thе gеnomе (/r worm Саеnorbаbditis еle5 .s-10% of tlrе total gеnom humans thе figurе is about Сonsortium 2001)' and st aЬundanсеs (Lynсh and Сс Sеvегal nrajor typеs of T of organisms (TaЬlе 2); Within еaсh of thе nlajor сlassifiеd into diffеrеnt farт ilar. Unlikе thе othеr typе lеast somе mеmЬеrs with (
for thеir transposition' Ьu mutations in thеir sеquеn еnсе of сomplеtе еlеmеnt othеrs arе frаgtnеnts who human gеnomе is madе u; Just as with satеllitеsес latеd spесiеs сan Ье duе t
without major diffеrеnсе split from its rеlativе D. aЬout thrее timеs as man amounts of thеsе sеquеnс аnd onе diрloid riсеspесi thе nrultipliсation of a fеv
Еuolution of the cenome n DNA; sее Intеrrrаtional Нtrtnan . Thе triplеt gеnеtiс сodе usеd Ьy nuсlеotidеs(сodспs) сorrеsponсlto еd, aIrсl сеrfаin triplеts-thе srop ]n suggеstсаndidаtеsfor sеquеnсеs ruсiеotidеsin thе third pсlsitions of сid еnсodеd,sinсе sеvеral diffеrеnt id (thе сodс is dcgепеrаte)(Lvnсlr tvеngеnomеrеgion is сomparеd Ье_ lf diftЪrеnсеs at еvеry third position ng sеquеnсеsno suсh pattеrn will nutnЬеrsrеmain unсеrtain for tlrе гhеsееstimatеsarе сonstantly bеing .ganisпlsdiffеr widеly Ьoth in thе l and in thе amottnt of еасh ty-pеof tе t-tt-lntЬеrs gеrrеrllllyсorrеIatеwith amollnt of intеrgеrriсDNA (L1,nсh l gеnomеsof prokaryotеshavе vегy thеy laсk spliсеosomirlintrons' аlгеrrttptеdЬy rnсlЬilеsеquеnсеsthаt ( L е w i n2 0 0 8 ) .U n i с е l l u l а rе u k а r y ' havе gеnеswith fеw, small introns largеstgеnomеsof еukaryotеstеnd iс DNA (L1.nсhаnсl Сonеrr' ?00З;
!сoDING RЕGIoNs h as prсlmotеrsand еnhanсеrs in_ Lеwin 2008), nоnс<;dingrеgions of lеsslikеly to havе important funсypеs thаt oссur rеpе:1tеdlyin tЬе lwo 11lаl()г сomponеllts of gеrrсlt-trеs эsсriЬеothеr typеs оf rеpеats,suсh ' Сharlеsworthеt аl. |994).
rraYs of highly rеpеatеd,nontran; vaгy in lеngth frorn fivе to sеvеral . i с hi n t Ь е Ь a s е s A and T. Satеllitе roсhromаtiп,tlrе Ьl
thе fruit f|у Drosrryhilа melапogаster (thе X chromosotttе, inуolrvedin sеx dе. tеrmination)has aЬout 20 million Ьasеs (MЬ) of satеllitеDNA, aЬout half of thеm сomposеd of a bloсk of rеpеatеd 359 Ьp units. Funсtional gеnеs arе sparsеrin hеtеroсЬromatinthan in thе rеst of thе gеnonre(tЬe eиchromаtiп)' Thе amount and sеquеnсесompositiorr of satеllitе DNA may vary widеly amongdiffеrеntspесiеs.For instanсе,aЬout 4О"Ь of thе DNA of D. uirilis is mаdе up of fotrr short satеllitе sеquеnсеs'whiсh arе quitе diffеrеnt from thosеof its distant rеIativеD. mеlапogаsterzlndсontriЬutе to its muсh largеr gеnomеsizе (Jolrn and Мiklсls 1988; Drosс,rphilа12 Gеn
I5e
1 6 0 Еuolиtiсlп of t|lе Gепсппe TaЬlе 2. TЕ сontеnts оf human and Drсlso1lhlia gеr.roп.rеs TЕs in thе hurтan and D. mclашlgаstеr еuсhromatiс gсnOmсs
Typ"
NumЬсrof сoplсs
Nuп-rЬеr of familiеs
Huпrаns l-ТR еlеmеnts StNЕs LINЕs DNA еlеmеnts
443x10r 1 , 5 . 5xU 1 0 r 8 6 8x 1 0 ' 294x10t
100 3 3 60
682 486 404
49 27 20
D. mеlапogаstеr LТR еlеmеnts LINЕs DNA еlсmсnts
7. of thе gеnomе 8 l-)
z0
-)
/-.b J
0.97 0.З.'
[пtеrnаtiсlnirl Humаn GеnсlnrеSequеnсingСonstlrtium Sсlurсcs:Humаn dаt:rfrсln.r (200l); Drсlsсlphilir сlаtаirom Kaminkеr еt аl. (2002). (еlеmеntswith rеpеatеd Аbbrеuiаtiсlпs:LТIt сIсrrlсnts,[-сlngTсrmrnirl Rсpеat с|сп.rеrrts rсvеrsсtrаnsсrip. sсqLlсIlссs at сaс|-r сnd, iri thс sаrтlссlriсntatiсln, whiсh rсpliсаtсtl-rrсlrrgh tiсln intсlDNA сlf аn RNA ссlpyof thеir DNA sеquепсе); SINЕs, SЬtlrtIпtеrspеrsесi (еlеrrrеlrts<.500Ьp Nuсlе:rrЕlеt-nеrits 1ong,whiсh rеpliсаtеthrotrglrаn RNA intеrmеdiаtе Ьut lасk rеpеаts:1ndrеli, оn LINЕs to prоvidе thе еt-tzyпrе nееdеdfor thеir rеvеrsеtrаnsсгiptiоn);I-lNЁ, l-оrrglntеrspеrsеdNrrсlеarЕlеmеnts(similаrto LТR еlеmеnts,Ьut > lkb long аr-rdlaсking thе tеrnrir-rаl rеpеаts);DNA еlеmеrrts(еlеmеntsthat rеpliсatе withtlr:tusе сlf аn RNA lntеrmеdiatе, rrsuаllywith shсlrtinvеrtесlrеpеаtsat еaсh еnd).
Most TЕs arе found in intеrgеniсDNA оr (to a lеssеrеХtеnt)in introns. In stlmе rеgions of thе gеnomе' ТЕs саn Ье vеry dеnsеly paсkеd, with multiplе еlеmеnts insеrtеd witЬin onе anothеr. Thе portion of thе D. mеlапogаstеr lrеtеroсhromatinthat irdjoinsthе еuсhromatin is largеly mаdе up of matеrial dеrivеd fronr TЕs (John and Мiklos 1988); thе rеgions around thе сеntromеrеs of А. thаliап.l сhrom()somеs(!7right еt al.200З) and many intеrgеniс rеgions in maizе (SanMiguеl еt al. 1996) arе sirтilar. GЕNoМЕ ADD|т|oNs Еarly gеnornеsmust havе Ьееn vеrv small, Ьut today's organisms havе largе nunrЬеrs of gеnеs with divеrsе funсtions. An important' though infrеquеnt, proсеss is addition сlf gеnomеsor Е]еnеsfrom othеr organisms. Baсtегiа геgularly асquirе novеl gеnеs fr
(Ьluе-grееnalgaе)and pro| mitoсhondria еvolvеd mu. protеoЬaсtеria (Graу 1999 Latеr еndosymЬiont еvе zoa (ma|aria parasitеs and dеrivеd from rеd a.lgaе;prt
МеmЬеrs of thе сhrоmop} сhlоroplast, whiсh has rе сеll. As wеll as thеir plasti still havе a vеstigial nuсlеa ovеr 40O gеnеs)and thus and thе truе nuсlеar gеno
GENЕ DUPLlсAтlс
N{orе frеquеntly, inсrеas Nеw gеnеs arisе from d gеnomеs (Еiсhlеr and Sar сan oftеn Ье rесognizеd tioпs с|ose to thеir progе suсh arrays сan thеn сhal Ьеtwееn two diffеrеnt mе сopiеs of thе sеquеnсеan Somе dupliсatеd array vorеd largе amounts of l gеnеS that еnсodе thе Rl nism (riЬosomеs) and t} gеnеs (Ranson еt al. 200 vantagе' so that natural s pliсatеd gеnеs. Givеn еn< onе of thе dupliсatе gеn Onсе a dupliсatеd gеnе l it and Ье fixеd in thе pс protеin-сoding aЬility Ьу rеmnant psеudogепе'.еvt or part of it. Nеwly dt quiсkly lost from gеnoп сatеs mеans that' aftеr a tinguish from Partial du gеnomе is rесognizaЬly d s е q u е n с еd а t a t h a t p r o v i tеnt, dupliсatе rеgionsсс thе strеtсhеs havе rеturr mеnts will, howеvеr' еvс Somеtimеs, howеvеr, t Ьеforе inaсtivating mutа
Еuolutioп of the Gепome cphiIа gеnonеs .-rсhronratiс!]еn()Пlеs
Numbеr of fаmiliеs
r00 З з 60 49 27 20
,%
of tЬe gеnomе
8 13
z0
.)
2.65 0.97 0.З.'
umаn (lепсlt.t-tе Sсс1uеI-rсing Соnsсlrti um
(2002).
l l R е p е а t с I е m е n t s ( е l е п r с l r t sw i t h r е р е а t c d . w h i с h г с р | i с l r еt h r r ' u н h г ( v е r \ ( .t r ; l I t s с r i р s с q u е n с с ) ;S I N Е s ' S h t l r t I п t е r s p е r s е с l : h r е p l i с а t е t h r с l t r g hа n R N A i n t е r r r l с d i а t е thе еnz1'mе nееdеd for thеtr геvеrsс tгanl е m с n t s ( s i r n i I а rt о L T R е l е r - n е n t sl,l u t ) N A с l е m е n t s ( е | е l n е п t st l r a t г е p l i с а t с vith short invеrtсd rеpеats аt еaсh еnd).
A or (to a lеssеrехtеnt)in introns. In е vеr,vdеnsеlvpасkеd, with rnultiplе rhе portion of thе D. mеlапogаster lmatin is iargеlv mаdе up of matеrial 1 9 8 8 ) ;t h е r е g i o n s a r o u n d t h е с е n \X/rightеt al. 2003) and many intеr1 9 9 6 ) a r еs i m i l а г .
rll, but today's orgаnisms havе largе s. An irrrportant'tЬough infrеqttеnt, rom othег orgаnisms.Baсtеriirrеgu: t е r i a sl p е с i е s( o с h m а n е t a l . 2 0 0 0 ) . i-rеirown gеnoпlеs'as wе]l as thе nulgaеhаvе сhloroplasts,and геd аlgaе lls Ьoth сontаin mitoсhсlndriа (Lvnсh е of prokaryorеtlrigin :rnd arosе еarly tеriаl сеll was еngulfеd into a еukaryn еr-rdosymЬiont. sеqtlеl1сеsof gеnеs tosеof photosynthеtiссyanoЬaсtеria
(bluе.grееnalgzrе)and proЬaЬly еvolvеd around 800 million yеаrs ago, whilе mitoсhondria еvolvеd muсh еarliеr from a group of Ьaсtеria known as сprotеoЬaсtеria(Gгay 1'999). Lаtеr еndosymЬiont еvеnts havе also oссurrеd. Thе apiсomplеxan рrotozoa (malaria parasitеsand thеir rеlаtivеs)and dinоflаgеllatеsсontain plastids dеrivеdfrom rеd algaе;prеsumаЬly a protozoаn сеll еngulfеd a rеd algal сеll. МеmЬеrs of thе сhromophytе group of algaе also сontain a rеd-algal-dеrivеd сhloroplast, whiсh has rесеntly Ьееn shown to rеprеsеl.lta wholе rеd algal сеll.As wеll as thеir plastid gеnomе, mеmЬеrs of thе сryptomonаd suЬgroup still havе a vеstigial nuсlеar gеnomе dеrivеd from thе rеd algal anсеstor (with ovеr 400 gеnеs)arrd thus possеssfour gеnomеs. inсluding thе mitoсhondriа and thе truе nuсlеar gеnomе (Douglas еt аl. 2001). GENE DUPL|сAтIoN AND GЕNЕ Loss Мorе frеquеntly, inсrеasеsin gеnе numЬеrs сomе fronr gеnе dupliсations. Nеw gеnеs arisе from dupliсations of parts of thе gеnomе or of wholе gеnomеs(Еiсhlеr and Sankoff 2003; Lynсh 2007). Singlе gеnе dupliсations сan oftеn Ье rесognizеd Ьесausе thеy fгеquеntly oссur as tаndеm duplicаtioпs с|ose to thеir progеnitor gеnе (Baumgartеn еt al. 2003). Thе sizеs of suсh arrays саn thеn сhangе furthеr Ьy unеqual сrossing ovеr. An ехсhangе Ьеtwееntwo diffеrеnt rnеmЬеrs of an array сrеаtеs onе dеsсеndant with thrее сopiеsоf thе sеquеnсеand onе with a singlе сopy (sееFigurе 2). Somе dupliсatеd arrays of gеnеs proЬаbly еvolvеd undеr sеlесtion that favorеd largе amounts of thе gеnе prodttсt' for ехamplе' thе largе arrays of gеnеsthat еnсodе thе RNA сomponеnts of thе protеin translation mесhanism (riЬosomеs) and thе еxpandеd aггays of sonrе insесtiсidе-rеsistаnсе gеnеs (Ranson еt al' 2002). Oftеn, howеver, highеr gеrrе dosagе has no advantagе'so that natural sеlесtionwill not aсt to prеsеrvеthе funсtions of dupliсatеdgеnеs.Givеn еnough еvolutionary timе, an inaсtivе mutant сopy of onе of thе dupliсatе gеnеs may Ьесomе fixеd in thе spесiеs Ьy gеnеtiс drift. onсе a dupliсatеd gеnе has lost its funсtion, fLrrthеrmutations may oссuг ln it and Ье fixеd in thе population Ьy drift. Еvеntuаlly thе gеnе may losе its protеin-сodingaЬility Ьy mutations сrеating сodons' and it thеn Ьесomеs a rеmnant pseиdсlgeпе;еvеntually delеtions оf gеnеtiс nlаtеrial mаy rеnrovе all or part of it. Nеwly dupliсatеd gеnеs arе thеrеforе oftеn ехpесtеd to Ье quiсkly lost fronr gеnomеs (Walsh 1995; Lynсh 2О07). Loss of gеnе dupliсatеSmеans that' aftеr a timе' wholе gеnomе dupliсations arе diffiсult to distinguish from partial dupliсations; in еithеr situаtion only a fraсtion of thе gеnomеis rесognizаЬly dupliсatеd (IJ7onget a|.2002). \Х/ithсornplеtе gеnomе sеquеnсеdata that providе largе gеnomе strеtсhеsof сlеarly similar gеnе сon. tеnt,dupliсatе rеgions саlr Ье rесognizеd,еvеn whеn most of thе gеnеswithin thе strеtсhеs hаvе returnеd to thе singlе-сopy statе. Chromosomе геarrangеmеntswill, howеvеr, еvеntuallyеrasе all traсеs of dupliсation. Somеtimеs' howеvеr' dupliсatеd gеnеs may gain nеrv funсtions Ьy mr-rtation Ьеforе inaсtivating mutations oссur. For instаnсе, an еnzymе that сatalyzes a
161
162
Еuolиtiсllt
tlf thе (}епсllllе
givеn rеасti
Although it is not knс trollеd, sеvеral gеnomе fеi Ьination ratе. Oпе suсh a of thе frеquеnсy of GС v, man gеnomе thе mеan Gl giоnally from aЬout 30o% Сonsortium 2001).Thе (
с o n с o r d а n t l y Ь е t w е е nr е g morе AT riсh than сodin; tions (whеrе m()st mutatl latеs to somе ехtеnt with tl sеquеnсеs'suсh as psеtrdо tiсularly intеrеstingЬесau Ьесausе of thе input of nrt rhе faсt that thеrе is oftеn (Lynсh 2007\. In thе hum tеnt is highеst for suсh sitt high (lntеrnational Hurnz
and Piganеaо2О02), Anothеr сorrеlatе of rес in high-гесomЬination rе1 Human Gеnomе Sеquеnс А. thаliапа (ltltеrnаtitln \й/rightеt al. 2003) gеnе . 8апs t|7eopposirе is foulrс TransposaЬlе-еlеmеnt.
D r o sop h ilа low-rесomЬiп sеrtions than high-rесom havе a morе сomplех pat low-rесomЬination AT-ril rесomЬinаtion) rеgions (I tium 2001).
Еvolutionary Faсtorl and Organization
FAстoRs тнAт A IN A GENoМЕ
Among гelatеd spесiеs,u lifе (parasitism or intraс quirеd for survival and rl baсtеriа that nrakе thеir nrurсhsmallеr gеnе numl ехtrеmе rеduсtion lras smallеr thаn еithеr Ьaсtе
Еt,сllution of thе Geпome hwа1.mаygаiп а nеW aЬility to асt on tе a nеW prсlduсt. Sorrrеgеnеs еnсodе rnd inaсtivatingnrutations that affeсt of Ьoth dupliсаtеs,еасlr lvith just tlnе эrv 200З; Lуnсh 2007). This inсгеasеs gеnomе.F.arniliеsof gеnеs that havе nponеntsof Pеnomеs,and solnеtimеs of funсtions,suсh as nrammаls' odorrlant disеasеtrеsistanсе gеnеs (Bauml forrn Ьy fusion of parts of two gеnеs :nе is transсriЬеdЬaсk into DNA and or adjaсеnt to anothеr gеnе (Long ransрositionir-rtothе gеnomе саn аlso )Llt introns (proсеssеtl pseиdogепеs)
REGloNAL DIFFЕRЕNсЕs е pаttеrпs just dеsсriLrеdis vzrriаtiorr (сrossing ovеr) aсross thе gеrrome. in hеtеroсhromatin.RесomЬinаtiсln nаtin. RесorrrЬinatiсlnis frеquеlrtiy .hе сеntromеriс hеtеroсhromarin Ьut lf thе сhromosomе (B. Сharlеsworth Drosсlphilааnd manv plаnts, rесomсilromos
Although it is rrot knowlr how rесomЬinаtion-ratе diffеrеnсеs arе сontrollеd' sеvеralgеnomе fеаturеshavе Ьееn found to сorrеlatе with thе rесomЬination ratе. onе suсh assoсiation is Ьasе сompositiсln (ехprеssеdin tеrms of thе frеquеnсy of GС vеrsus AT Ьirsеpаirs, mеntionеd еаrliеr). In thе human gеnomе tlrе mеan GС сontеrrtis aЬout 41"Ь,Ьut thе сontеnt variеs rеgionally from about ЗО"Ь to 657" (IntеrnationаlHumаn Gеnomе Sеquеnсing Сonsoгtium 200l). Thе GС сontеnts of gеnеs and intеrgеniс sеquеnсеsvаry сonсordantly Ьеtwееn rеgions. Altlrough nonсoding DNA tеrrdsto Ье nrцсh morе AT riсh than сoding sеquеnсеs'thе GC сontеnt of third сoding positiоns (whеrе most mutations do not affесt protеin sеquеnсе)usually сorгеlatеsto somе ехtеnt with that of adjасеnt nonсoding sеquеnсеs.Nonfunсtional sеquеnсеs'suсh as psеudogеnеsand dеfесtivеtransposaЬlееlеmеnts,arе partiсularly intеrеstingЬесаusеthеy rеvеal thе GС сontеnt that will ехist purеly Ьесausеоf thе ir-rputof mutations (without rraturalsеlесtion),аnd thеy rеtlесt thе faсt that thеrе is oftеn a mutation prеssurе toward AT and away from GС (Lynсh 2007)' Iп thе human, С. еlеgапs, and Drosopbilа genomеs, GC сontent is highеst for suсh sitеs in сhromosomе rеgions whеrе сrossovеrratеs aге high (IntеrnationalHuman Gеnonrе Sеquеnсing Сonsortium 2001; Marais and Piganеau 2002). Anothеr сorrеlatе of rесomЬirrarior-ris irrtron lеrrgrh;this tеnds to Ье lowег in high-rесomЬinationrеgions (Сomеron ar-rdKrеitmаn 2000; Intеrnаtionаl Human Gеnomе SеquеnсingСonsortium 2001). In addition, in humans and А. tbаliаtzа (lntеrnational Нuman Gеnomе Sеquеnсing Сonsoгtium 2001; !Иriglit еt al. 2003) gеnе dеnsitiеs arе highеst in thеsе rеgions, Ьut tn С. еlеgаns tЬe oppositе is found (С. еlеgапs Gеnomе Sеquеnсing Projесt 1999). TransposaЬlе.еlеmеntdеnsitiеs also varу rеgionally within gеnomеs. In Drosophilа low_rесomЬinationrеgions hаvе muсh highеr numЬеrs of TЕ in. sеrtions than high-rесomЬination геgions (Kaminkеr et aL.2О02|. Humans havе a morе сomplех pattегn: LINЕ еlеmеnts (TaЬlе 2) arе assoсiatеdwith iow-rесomЬinationAТ.riсh rеgions, аnd SINЕ еlеmеntswith GС-riсh (highrесomЬination)rеgions (IntеrnаtionalНuman Gеnomе Sеquеnсing Сonsort i u m2 0 0 1 ) .
Еvolutionary Faсtors that Contrоl Gеnomе Sizе and Organization FAстoRs тHAт AFFЕст тнE NUMвER oF GЕNЕs lN A GЕNoМЕ Among rеlatеd spесiеs'unusually small gеnomеsarе assoсiatеdwith ways of lifе (parasitism or intrасеllular symЬiosis) whеrе most of thе геsourсеs rе. quirеd for survivаl arrd rеproduсtion аrе providеd Ьy thе host. Foг ехamplе, Ьaсtеria that nrаkе their living as intraсеllular symЬionts or parasitеs havе muсh smallеr 8еnе numЬеrs than frее-living rеlаtivеs (Мoran 2003). Morе ехtrеmе rеduсtion hаs oссurrеd in organеllе gеnorrrеs, whiсh arе muсh smаllеrthan еithеr Ьaсtеrialor nuсlеar gеnomеs;thеy сarry only gеnеsnееdеd
16з
164
Еuolution rэfthе Gепomе for thеir own геpliсation and prtltеin synthеsisand fсlr a fеw spесializеdorganеllar funсtions. Мany gеnеs еssеntial for organеllе fr-rnсtiсlns havе Ьееn trаnsfеrrеd to thе nuсlеus (Gray 1999). ongoing gеnе trаnsfеr hаs Ьееn dеtесtеd frorn plant organеllеgеnomеs,аs wеll as transfеrsthi1tсrеatеnonfunсtional psеudogеnеsof orgаnеllеgеnеsin thе nuсlеar gеnomеsof many spесiеs ( G r a y 1 9 9 9 ;B е n s a s s o nе t a l ' 2 0 0 1 ) . Gеnome-sizе еvolution involvеs sеvеrаl prеssurеs.Thеrе may Ье advantagеs сlf smallеr gеnomе sizе, Ьесausеir rеduсеd gеnomе саn rеpliсatе fastеr, allowing fastеr сеll division; this сarr oссLlr through dеlеtions of gеnеs that arе no longеr nееdеd, or of intеrgеniс and introniс sеquеnсеs.Thе finding that сompaсt gеnomеs oftеn havе ovеrlapping gеnеs, in whiсh thе samе strеtсh of DNA is transсriЬеd in two diffеrеnt rеading frаmеs (Douglas еt al. 2001; l,еwin 2008), suggеststhat sеlесtion fаvorеd sizе rеduсtiorr in thеsе сasеs.But loss of somе sеquеnсеsmay Ье sеlесtivеlynеutral, so that dеlеtions сan Ье fixеd Ьy gеnеtiс drift, as outlinеd еarliеr for rеdundant gеnе dupliсatеs. In nonrеpеtitivе sеquеnсеsthat arе unсonstrainеd Ьy sеlесtion, thе amount of DNA tеnds to dесrеasе ovеr timе Ьесausе rеpliсation rnistakеs sееm to сausе small dеlеtions rnorе oftеn thаn insеrtions of Ьases (Grеgory 2004; Lynсh 2007).If sеlесtivесonstraints on gеnеs эrе rеmovеd, thеy v'.ill thеn gradually dесlinе in sizе ovеr timе аs morе dеlеtionsthan insеrtions Ьесomе fiхеd Ьy gеnеtiс drift. PrtlЬaЬly Ьoth sеlесtivе and nonsеlесtivе prос е s s е sh а v е Ь е е no p е r a t i n g . MUтAт|oN RAтES AND тHЕ NUMBЕRS oF GЕNЕs Мost mutations with еffесts on an organism's funсtions rеduсе survival or fеrtility (fitnеss,for short). Unlеss sеlесtiсlnis vеry wеak, thеrе will Ье a Ьalanсе Ьеtwееnthе mutational input of nеw dеlеtеriousvariants into a populаtion and thеir еliminatiсln Ьy sеlесtion. Thе prеsеnсе of thеsе mutаtions rеduсеs avеragеfitnеss,ссlmparеdwith a mutation-frееpopulatiоn; this mutаtioпаl loаd depeпdson thе totаl numЬеr сlf nеw dеlеtеriousmutations that arisе pеr lndividual еaсh gеnеration,suсh that thе nе!]ativеof thе natural logаrithm of thе mеan fitnеssof a poprrlatiсlnis еqual to thе lоad (Сrow 199з|. For a givеn mutation ratе pеr gеnе, thеrе will thus Ье a grеatеr load if thе numЬеr of gеnеs in a gеnomе is largег. RNA gеnomеs laсk еrror-сorrесting meсhаnisms and havе ехtrеmеly high mutatiсlnrаtеs pеr gеnomе pеr rеpliсation, dеspitе thеir small gеnomе sizе: around 1 nеw mutation pеr rеpliсatiсln сyсlе for thе influеnza virus (Drakе еt al. 1998). Suсh gеnomеsсannot' thеrе. forе, havе largе numЬеrs of gеnеs, Ьесausеthеir {itnеsswoLrld Ьесtlmе vеry low. DNA-Ьasеd gеnomеs havе еrror-сorrесtingmесhanisms that givе thеm muсh lowеr, Ьut not zеro' mutаtion ratеs; theЕ. сoli !]еnomеis еstimаtеdto havе a mutation ratе of around 10_r0pеr nuсlеotidеpеr rеpliсation and a mutation rаtе pеr gеnomе of only 0.0025 (Drakе еt al. 1998). Мultiсеllular сlrganismshavе largе gеnе numЬеrs аnd many сеll divisions еaсh gеnеration.Bесausееrrоr сOrrесtionсlrn nеvеr Ьe pеrfесt,and thе mutation ratе pеr nuсlеotidе pеr сеll division is quitе similar to that in Ьaсtеria,
thе mutation ratе pеr nuсl Ьaсtеria. For ехamplе, in } drashov 2003). Givеn thе n man gеnomе, this translatе protеin sеquеnсеof aЬout tion, and around 80% of tl
nеt mutation ratе to dеlеtе largеr numЬеr of dеlеtеrro thе nonсoding portions of 1 thе еstimatе of thе human H i g h d е l е t е r i o u sm u t а t i (Crow 199З) maу limit p. Thеorеtiсal modеls of thе с сatе that mutatiоnal load 2 0 0 0 ) . H o w е v е r , t h е r еi s l mесhanisms, whiсh slow sourсеs. Thе oссurrеnсеo ratеs to zеro, Ьut in sеxua Ьеtwееn gеnеs' allеlеsthat atеd with favoraЬlе mцtat l i t t l е а d v a n t a g е .М u t а t i o r arе thus likеly to rеflесt tl rеduсing thе mutation rat load (Sniеgowski еt al. 20t I n с o n t r a s t ,i n о r g а n i s m еffесtivе gеnеtiс rесomЬ s P е с i е s .а n a l l е l еt h а t i n с г soсiatеd with any favoraЬ qЦеnсy as thе mutation s1 m u г а t i o n г a t е st h a n i n s е } iпg aпd is obsеrvеd in Ьal sеlесtion prеssurеs(Sniеg
GЕNoMЕ s|zЕ |N oF NoNсoD|NG t
Gеnomе-sizе diffеrеnсеs v o l v е l a r g е d i f f е r е n с е si r DNA, with only minor Lynсh 2007). In somе сa in lifе history and есolo havе morе satеllitе and ot onеs' suggеstingthat thе nеutral with rеspесtto sе
forсеs (likе thе balanсе liеr) providеs a plausiblе
Еuolиtioп of thе Gеnomе ynthеsisand for a fеw spесializеd orial for organеllеfunсtions havе Ьееn ). ongoing gеnе trаrlsfеr has Ьееn dе. ; rvеllirstransfеrstlrаt сгеatе nonfunс_ l thе nLrсlеarЕ]еnolllеs of mаny spесiеs еral prеssurеs.Thеrе may Ье aс.lvanr rеdrr.^еd 8еnomе сan rеpliсаtе tаstеr, lссur through dеlеtiсlnsof gеrrеsthat and intror-riсsеquеnсеs.Thе tinding еrlapping gеnеs, in whiсh thе samе iffеrеntrеadingfranrеs(Douglas еt al. сtiorr fаvorеd sizе rеduсtion irr thеsе lе sеlесtivеlyoeutfell,so that dеlеtions r е d е a r l i е rf o r r е d u n d a n tg е n е d u p l i arе unсonstrainеdЬy sеlесtitln, thе 'еr tinlе bесausеrеpliсation пristakеs геn thаn insеrtionsоf Ьаsеs (Grеgory llnts on gеnеsаrе rеmovеd' thеy vyill as morе dеlеtionsthan insеrtions ЬеЬotlr sеlесtivе:ttlс{ntlnsеlесtir,еpro-
UMBЕRs oF GЕNЕs ganisш'sfunсtions rеduсе survivаl or tion is vеry wеak, thеrе will Ье a Ьаlеw dеlеtеriousvariаl-ltsinto a ptlpr'lla. n . Т h е p r е s е n с еt l f t h е s е m u t i l t i o n s а п1l-ltation-frее population this mu. Ьеr of nеw dеlеtеriсlusmutations that :h thаt thе rrеgativеof thе naturаl logi o n i s е q u a lt o t h е l o а d ( С r o w 1 9 9 З \ ' еrе ш'ill thus Ье а grеatеr loасl if гhе . R N А g е n o m е sl a . . k е r r o r - с o r r с с t i n g lutаtion ratеspеr gеnomе pеr rеpliсa.ound 1 nеW mutаtior-r pеr rеpliсаtion t. 1998).Suсh gеrromеsсannot, thеrеausе thеir fitnеsswould bесoпrе vеry orrесtingmесhanismsthat givе thеm еs;thе Е. сoli gеn()пlеis еstimatеd to r nr.rс[еotidе pеr rеpliсаtion :rnс{а muDrakееt al. 1998). еnе numbеrs and nrany сеll divisions )n сan nеvеrЬе pеrfесt,аnd thе mlltаn is quitе similаr to thаt irr Ьirсtеria,
thе mutation rаtе pеr nuсlеotidе sitе pеr gеnеration is muсh highеr than in baсtеria.For ехamplе, in humans it is еstimatеd to Ьe aЬout 2x10 8 (Kondraslrov2003)' Givеn thе numЬеr of sitеsthat сodе for amino aсids in thе human gеnomе, this translarеsirrto a mutation гatе pег 8еnomе foг сhаngеs in protеin sеquеnсеof aЬout 0.82 nеw пltltаtions pеr individual еасh gеnеra. tion, and around 80"Ь of thеsе arе likеly to Ье slightly dеlеtеrious,yiеlding a nеt mutation ratе to dеlеtеriоusamino aсid mutations of aЬout 0.66. An еvеn largеrnumЬеr of dеlеtеriousmutаtions is likеly to Ье сilusеd by mutаtions in thе nonсoding portions of tlrе human gеnomе (Asthаna et aI.2О07),Ьringing thе еstimatеof thе human dеlеtеriousmutation ratе to wеll aЬovе 1. Нigh dеlеtегiousmutation гatеs and thе rеsulting low population fitnеssеs (Сrow 1993) may limit possiЬlе gеnomе sizеs for multiсеllular oгganisms. Thеorеtiсаlmodеls of thе еvolution of gеrrеsthat сorrtrol mutatiol-lratеs indiсatе that mutational load favors a rеduсеd mutation ratе (Sniеgowski еt al. 2 0 0 0 ) .H o w е v е r . t h е г еi s a n o p p o s i n g p r е s s u r е :t h е с o s t s o f е r r o г - с o r r е с t i n g mесhanisms,whiсh slow down DNA rеpliсation and сonsumе сеllular rеsollrсеs.Thе oссurгеnсе of irdvantagеousmutations аlso disfаv
165
l66
Еuсllutiсlttof thе Сепotпе
proсеssеstlrаt invo|vе еrr()rsin DNA rеpliсаtion irrrdrtnеqual сrossin!]ovеr саn amplitr, аrril\rsbу multiplеs сlf rvhсllеrеpеаtеd units, sо thеrе аrе forсеs thаt inсrеasе сopy numЬеr' somеtimеs adding DNA to thе gеnonrеof an individrrаl;gеnеtiсdrift сan tlrеn сausе it to sprеad to fixation (B. Сhaгlеswсlrth еt аl. ] 994;' LуncЬ 2007). Sеlесtiсln against high сopy nuпrЬеr will oftеn opposе this proсеss' Ьut suсh sеlесtion is lеast еffссtivе in spесiеswith а small еffесtivеpopulаtiсln sizе (Kimr.rrа198з). This suggеststhаt thеrе should Ье а rеlаtion Ьеtwееnthе еffесtivеsizе оf a spесiеs (whiсlr сan Ье еstimatесlfroпl its lеr.еl of DNA sеqllеnсе с.livегsity;11,nсЬ2007) and thе сontгiЬutirln oi rеpеtitivс sеquеnсеsttl its gеnomе sizе. Broаd сomparisons aсross diffегеnt taхa suPport this prеdiсtion (l-ynсh 2007). Hor'vеvеr,spесiеssuсh as D' uirilis and D. mеlапсlgаstеr diifer сonsidеrably in thеir аmount of rеpеtitivе DNA Ьuг sееm to havе similar еffесtivе рopulation sizеs (Drrlsophilа 72 Gеnomеs Сonstlrtium 20О7I. Тhis suggеsts thаt othеr faсtors must plav a гсllе. A likеli" disadvantagеof a largе anlount of sаtеllitеDNA is a slolvеr dеvеlopnlеllt timе, sinсе сеll с]ir,isionswill Ье slow lf it takеs longеr to геpliсatе gеn()mеswith largе DNA аnlсtunts(Cavaliеr-Smith1985). \Whеnrapid dеvеlopmеnt is important, thе Ьalanсе is tippеd towаrd lowеr сopy numЬеr, but i{ slow dеvеlopmеnt is not disfavorеd Ьy sеlесtion' sеlесtion against thе aссumulаtiоn of rеpеtitivеDNA ц,ill Ье wеakеr, аnd sr.rсlr sеquеnсеsсan aссLlmLll а t е ( F i g t r r е4 ) . T h u s l a r g е D N A с o n t е n t d < l е sn o t n е с е s s a r i l yi m p h , t l r а r sеlесtiotlhаs favorеd nroгеDNA (Pagеland Jсllrnsttrnе1992'B. Сhirrlеsworth еt al. 1994). Of сoursе, it might somеtilnеs Ье advantagеotlsto havе morе nonсoding DNA. For instanсе' morе DNA pеr nuсlеus might еnaЬlе organisms with largе сеlls to movе RNA morе rapidly into thе сvtoplasm (Саvaliег-Snrith 1985). Нсlш. сan onе distingtrislrЬеtwееn thеsе possiЬilitiеs? Ехpеritrrеnts thаг altеr thе i.rпrountof hеtеroсhrolnatin in D' пrclапogLlstеrhardly rrffесt viaЬilitr, сlr dеvеlopmеnt tilr-rе'suggеstingtlrat largе сhangеs in сopy numЬ е r s ( m i I l i o n s o f Ь a s е s )h а r ' е a t m o s t v е r y s l i g Ь t a d v a n t a g е so r d i s а d v a n tagеs (John and Miklos 1988). Vеry slight fitnеss diffеrеnсеsсan, howеvеr, Ье importаnt in еvсllution, so this is not сonсlusivе' In сomparativе tеsts thаt еxаnrinе dеvеlopmеnt tiпlеs and gеnomе sizеs irсross diffеrеnt spесiеs, thе bаlаnсе rrrodеlprеdiсts thilt а rеlationship will Ье fсlund еvеn аftеr st..t-..---> insеrtion5, inс|uding rереatаdditions 5ma|| sаtе|litе
insеrtiопs, |аrge iпс|uding ТЕs
small genome <<-
prеssurе undеrmUtаtiOn dеlеtions
fаvorеd sе|есtivеIy deletiоns <--UПPЧU3| сrossing ovеrwithgenetiс drifl
lаrge genome highсostsof rеplасing DNA slowgrowtfl
Figurе 4. Oppсlsing forсеs aсtir.rgOn gеnomе.sizе сvrlIution.
tistiсal сorrесtions for diff. this is not ехpесtеd if thеr. from salamarrdеrs and nе Johnstonе 1992). Сan wе sее thе footprir . sizеs, as assumеd еаrliеr? сonсеntration in rеgions o w е с a n . T h е а r g u m е n ti l r \ ' ray undеrgoеs unеqual сro pliсations). Unequal ехсhz сopiеs in thе array. Ьut it i
Ьеr is nеithеr advantagеous spесiеs to Ьесomе fixеd for rеquirеs multiplе сopiеs, a r aftеr rеmain singlе сopy (t сopiеs сan Ье lost again Ьy that affесt array sizеs, thе с a tandеm arrаy thus produ ity ovеr timе that thе pop
сially if unеqual еxсhang individuals with high аrra rеsulrs. Largе агrays aris (B. Chaгlеsworth еt a|. \99, low-rесomЬination gеnomi forсе that pushеs rеpеat n forсе that aсts in thе оppos No funсtional advanta DNA sеquеnсеs is tlrus nt thеir distributiоn within gс latеd spесiеs oftеn diffеr quеnсеs' whiсh also strong ]v{iklos 1988; Drosophilа doеs not mеan that satеlli Drosopbilа, portions of t} mosomal Ьеhаvior at lnеlo volvеd in сеntromеrе [un probaЬly did not сausе t} morе likеly, thеsе arrays v liеr and wеrе latеr сo-optе тRANsPosAвLЕ
Е
Мost typеs of transposa t h е m s е l v е si n t o n е w p o s i t nal сopy. Thеsе transpos m е n t n u m Ь е r so v е r t i m е u For ехampl e, tn D. mеIап
Еuolиtioп of the Geпomе эliсationand unеqual сrosslng ovеf з rеpеаtеdunits, so thеrе arе forсеs tding DNA to thе gеnomе of an insprеасlto fiхаtion (B. Сhаrlеswoгth lst high сopу numЬеr wil| oftеn op'ast еffесtivеin spесiеswitlr а small This suggеststhаt thеrе should Ье а lесiеs(rvhiсhсаn Ье estimatеd fгom nсh 2007) and thе сontriЬution of Broаd сompагisons ilсross diffегеnt 7).Нowеvеr, spесiеssuсlr as D. uirгaЬly iп thеiг amount of rеpеtitivе з population sizеs (l)rosг-lphilа 12 .еsts that otlrеr faсtors must plaУ t of sаtеllitеDNA is a slowеr dеvеlsiow if it t:rkеslongеr rсl repliсatе i е r - S m i t h1 9 t l 5 ) W . hеn rаpid dеvеll towirгd lou,еr сopy nun-rЬеr,lrut if эlесtion,sеlесtionagainst thе aссuэr, and suсlrsеquеnсеsсаI1aссulnult doеs not nесеssarily imply that rdJсlhrrstonе1992:B. Сhагlеswoгth ltltаgеousto hаl,е nrorе nonсoding :lеusrnight еnaЬlе organisms with n t o t Ь е с y t o p l a s m( С a v а l i е r - S m i t h ln thеsе possiЬilitiеs? Ехpеriments n in D. mеlапсlgаstarhаrdly affесt g thаt largе сhangеs in сopy num' r y s l i g h t a d v a n t а g е so r disadvаnlt fitnеssdiffеrеnсеsсan, howеvеr, t с o n с l u s i v е .l n с o l n p а r а t i v е t с s t s t o m е s i z е sа с r o s sd i f f е r е l r rs p е с i е s , nship will Ье found еvеn аftеr stadditions--------->
+ -
lаrge genome highсosts ofrеplасing DNA slowgrоwth
-sizе еvolutiоn.
tistiсalсorrесtions for diffеrеnсеs in nuсlеar volumе and сеll sizе, whеrеаs this is not expесtеd if thеrе is an advаntagе of more DNA. Сorrесtеd data from salarnandеrs and nеWts still show a signifiсant rеlation (Pagеl and Johnstonе 1992). Сan wе sее thе footprint сlf a mutational prеssurе that inсrеasеs аrray sizеs,as assumеd еarliег? Thе distriЬution of sаtеllitе DNA, with a strong сonсеntration in rеgions of infrеquеnt gеnеtiс rесomЬination, suggеsts that wе сan. Thе аrgumеnt involvеs a simplе modеl in whiсh a tandеm rеPеat array undеrg
167
168
Еurllиtiсlnof thе Gепomе nеw TЕ is addеd to a haploid еuсhromatiс gеnomе еvеry 10 gеnеrationsin laЬoratory сonditions whеrе sеlесtionis rеlaxеd (Мasidе еt al. 2000). Thеrе arе aЬout 1,000 fairly сomplеtе TЕs in thе gеnomе (Kaminkеr еt al. 2002), so thе mеan transpositiсlnrаtе pеr pсltеnгiallyaсtivе еlеmеnt is aЬout 10 a pеr gеnеration. \й/hatrеgulatеsthе aЬundanсе of TЕs in thе gеnomе? Thеrе arе two сontrasting viеws (B. Сharlеsworth еt al. 1994). First, TЕs сould Ье maintainеd Ьесausе thеy arе advantagесlusfoг thеir host organisms; for instanсе' thеy might oссasionally induсе favorаЬlе mutations Ьy insеrting into gеnеsor rеgulatory sеquеnсеs.A proЬlеm with this idеа is that insеrtions mostly сausе harmful, not advantagеous' еffесts, disrupting сoding or rеgulatory sеquеnсеs. Many known spontanеous dеlеtеrious mutations' inсluding somе human disеasе mutations' аrе duе tо insеrtions into сoding sеquеnсеs(os. tеrtag and Kazazian 2001). Suсh strongly dеlеtеriousmutations are usuallv rapidly еliminatеd from populations, and аs mеntionеd еarliеr, it is indееd oЬsеrvеd that in thе gеnomе sеquеnсеsof highеr organisms TЕs arе largеly absеnt from ссlding sеquеnсеs'indiсating that insеrtions thеrе arе harmful (Intеrnational Human Gеnomе SеquеnсirrgСonsortium 200l ; Kaminkеr еt a|.20О2; \Х/rightеt al. 2003). F.urthеrеvidеnсеthat TЕ movеmеnt is disadvantagеous to thе host is that marry spесiеs,suсh as yеast' thе mold Neиrosporсt, maizе, and Drosophilа' Ьaуe mесhаnisms that rеstriсt thе ratе of movеmеnt of TЕs (Sеlkеr2002; Aгavin et aI.2ОО7).Мorеovеr, thе viеw that TЕ insеrtions arе advаntagеousfor thеir hosts' futurе еvolution rеsts on thе idеa that thе long.tеrm survival of a spесiеsis еnhanсеd Ьy thе pгеsеnсеof TЕs, and it doеs not ехplain how TЕs Ьесomе еstaЬlishеdin thе first plaсе. Sесond, TЕs сould Ье maintainеd Ьy thеir aЬility to sprеad by sеlf-rеpliсation within thе gеnomе, сouplеd with transmissiсln of nеw ссrpiеsto thе offspring during sехual rеprоduсtion, еvеn if thеy usually havе hаrmful еffесtson thеir hosts (thе selfish DNА hypothеsis).on this viеw TЕ aЬundanсе will dеpеnd on thе Ьalanсе Ьеtwееntransposition that сausеsinсrеasеdсopy numЬеr vеrsus sеlесtion against individuals with largе сopy numbеrs (B. Сharlеsworth et a|. 7994; Lynсh 2007). This Ьalanсе impliеs thаt thе rеduсtion in fitnеss сausеd Ьy аn еlеmеnt insеrtion musr on avеragееqual thе сhanсе that an еlе. mеnt transposеs. Еstimatеs of this ratе arе around 10_apеr gеnеrаtion in Drosophilа, showing that this sеlесtionprеssurеmust Ье wеak. This hаs Ьееn tеstеd furthеr in D. mеlапogаsterЬy dеtеrminingеlеmеntpositions on thе giant сhromosomеs of larval salivary glands. Thе frеquеnсiеsof TЕ insеrtions in thе population arе nеarly always vеry low at a givеn plaсе on thе сhromosomе, again implying that insеrtionsarе disadvantagеous.Thе strеngthсlf sеlесtion сan Ье infеrrеd from thе frеquеnсiеs,аnd it agrееswith thе еstimatеd transposition ratе (B. Сharlеsworth еt аl. 1994|. \Х/hat is thе naturе of this sеlесtion? \iИеhavе alrеady disсussеd sеlесtion against largе gеnomе sizе, and harmful еffесts of transpositions on thе host. Anothеr disаdvantagе сomеs from сr:ossingovеr Ьеtwееn еlеmеnts in diffеrеnt gеnomiс loсations (ecto|liс ехсhапge), This сausеs сhromosomе invеrsions, transloсations,dеlеtions,and dupliсations(B. Сharlеsworthеt al. 1994). Somе
rеarrаngеmеnts havе fеw bесausе of gеnеtiс drift, l mosomе struсturе. BLlt n highly dеlеtеrious:many J aгrаngеmеnrs (gспсlmiс 2003). If this is an impo prеdiсts that TЕs should сomЬination ratеs,sinсе mеnts and will thеrеforе есtopiс еxсhangеs. As mе proportion сlf thе Y сhrс quеnсеs (B. Сharlеswortl planations for this pаttеr of thе gеnomе with rеdu Т Е s m а y s o m е t i m е 5i n mеnts' and sеlесtionwill TЕ-dеrivеd sеquеnсеsap or сonfеr сlthеr Ьеnеf]ts satеllitе sеquеnсеs,hоwс tion pгomotеd thе initia tory or еvеn сoding funс w е r е i n s е r t е di n t t l t h е i г1
МAsslvЕ тE Aсс sIzЕ DIFFЕRЕNс
A | t h o u g h t h е r a t е о | :i г D. mеlапсlgasler sееms l roughly еvеry 10 gеnеra tionary timеsсаlеsif no с tгansposition еstimatеd D r o sop b ilа gеnеratiOns danсes among rеlatеd s еarliеr, arе thus rеadily somеtimеs rеlaхеd. Anо whiсh аn autosomе Ьес yеаrs ago; this has sinс this gеnomе rеgion to st сur in Droso1lhilа ma|e sity of TЕ insеrtions intс somе spесiеs (е.g.,hurna (TaЬlе 2), and at many q u е n с i е s( o r е v е n i n a l l j
r n g ,w i t h t h е | o w i n s е r t i .Why arе thеrе suсh l lаrgеr amounts of intе
Еtlolutioп of thе Gепomе ltlс gеnomееvеry 10 gеr-rеrations in rеlaхеd(Мasidе еt al. 2000). Тhеге е gеnomе(Karninkеrеt al. 2002), so Llly асtivе еlеmеnt is aЬсlut 10_apеr in thе gеnomе? Thеrе i1геtwo сon. 94). First, TЕs сould Ье maintainеd . host orgarrisпrs; for instаrrсе. thеy rtiorrsЬy insеrtinginto gеnеsOr rеgidеa is tЬat insеrtions f]lostly сatlsе srllрting сoding or геgulatoгУ sе_ еtеriousmutations' inсluding somе sеrtionsinto сoding sеquеnсеs (os|y dеlеtегioLrs mutаtions аrе usuall1, d as mеntionеdеarliеr, it is indeеd эf highеr organisms TЕs arе largеly g tЬаt irrsеrtionstherе аrе harmful сing Сonsortium 2001; Kamirrkеr :vidеnсеthat TЕ movеmеnt is disadlсiеs, suсh as уеаst' rhе nrold Nсzllесhanisms th:lt rеstriсt гhе ratе of r aL.2007). Мorеovеr, tЬе viеw tЬat hosts' futr:rееl.o]utionгеsts on thе сiеs is еnhanсеdЬy thе prеsеnсе of :omе еstaЬlishedin thе Iirst plaсе. ir aЬilit1'to sprеerd Ьy sеlf-rеpliсation ssion of nеw сopiеs to thе offspring rsuallyhavе harmful еffс:сtson thеir h i s v i е r д , , T aЕ Ь u n d a n с еw i l l d е p е n d t сattsеsinсrеasеdсopy rrumЬеrvеrgе сopy numЬеrs (B. Сlrarlеsworth mpliеs that thе rеduсtion in fitnеss vеrаgееqual tl-rесhanсе thаt an еlеа r е a r o u n d l 0 - a p е r g е n е r a t i o ni n :еssurеmust Ье wеak. Thls has Ьеегr :miningеlеmеntpositions on thе gi. ls. Thе frеquеnсiеsof TЕ insеrtions oW at a givеn plaсе olr tЬе сhrt>molisadvantagеoшs. Thе strеngthof sе'еs,and it agrееswith thе еstimatеd 19941. Vе lrаvе alrеady disсussеd sеlесtion [fесtsof transpositions on thе host. g ovеr bеtwееnеlеmеnts irr diffеrent h i s с а u s е sс h r < l m о s o n tiеn v е r s i o l r s , (B. Сharlеsworthеt al. 1994). Somе
rеarrangеmеnts havе fеw or no harmful еffесts and саn sprеad in populations in сlrrobесausеof gеnеtiс drifl, thеrеЬy сorrrriЬuting to еvolutionary сh:rr-rgе mosomеstruсturе. But many rеarrangеmеnts disrupt gеnе funсtions аnd аrе highlydеlеtеrious:nrany humаn gеnеtiсdisеаsеsаrе сausеdЬy сhromosomе rеаrrangеmеnts(gепсlmiс disеclsеs),inсluding mаny саnсегs (Dеiningеr еt аl. 2003).If this is аn importalrt disаdvurntаgе tо having high TЕ aЬundanсе, it prеdiсtsthаt TЕs sЬould aссltmulatе mainly in gеntrmiс геgions rvith low гесomЬinаrtionrаtеs' sinсе tlrеy arе tlrеп lеss likеly tсl саusе harnrful rеarrangеmеntsаnd will thеrеforе not Ье rеmovеd Ьy sеlесtion against thе produсts o{ есtopiсеxсhangеs'As mеntiсltlеdеarliег, this is oftеn truе' For ехanrplе, a largе pгоportion of tlrе Y сhromсlsоmеs of many spесiеs сonsists of ТЕ-dеrivеd sе_ quеnсеs(B. Сharlеsworth еt a|. |994|. Howеvеr, thеrе arе othеr possiЬlе еxplanatiоnsfor this pattеrn' srrсhas thе геduсеd еffiсiеnсy of sеlесtiоrrin rеgitlns of thе gеrromеwitlr rеduсеd rесoпrЬinаtion(sееlаtеr disсr"rssiorr). TЕs miry somеtimеsinduсе favoraЬlеmutations or сhromosomе rеarrangеmеnts'and sеlесtionwill thеrl sprеad thеm throughout thе pсlpulation.Son-rе ТЕ-dеrivedsеquеnсеsаppе21rto rеgulаtеgеnе асtivity (Dеiningегеt аl. 200З) or сonfеr othеr Ьеnеfitson thеir hosts (Brookfiеld 2003). As wе arguеd for satеllitеsеquеnсеs'howеvеr, a prеsеnt-dayЬеnеfitdoеs not impl,v that sеlесtion prсlmotеdtlrе initial sprеаd of tlrеsеsеqtlеnсеs.lr is possiЬlе thаt rеgulа_ tory or еr,еnсodin8 funсtions havе Ьееn aсquiгеd by suсh TЕs long aftеr tlrеy wеrеinsеrtеdinto thеir Prеsеnt loсations and fiхеd in thе population. MAssIVЕ тЕ AссUМULAт|oN AND PoPULAт|oN sIzЕ DIFFЕRЕNсЕs Although thе ratе of inсrеаsе of TЕs Ьy trаnsposition in spесiеs suсh as D. melаnogаsle/sееmslow (onе nеw еlеmеnt in thе haploid gеnomе еlеmеnt гoughlvеvеry 10 gеnегations)'сopl,numbеr lvill inсгеasеrapidl,vovеr еvolutionarytimеsсalеsif no oppсlsingfoгсе opеrаtеs:for еxаlmplе,with thе ratе of transpositiсlnеstimatеd еarliеr, a tеnfold inсrеasе woLlld takе only 2з,000 Drosopbilа gеnеrirtiotls,lеss tlran 2,000 yеars. Lаrgе diffеrеnсеsin TЕ аЬLrrrdanсеsamong rеlаtеd spесiеs,аs in thе maizе and riсе ехamplеs dеsсriЬеd еarliеr,aге thus rеadily ехpliсaЬlе if sеlесtion prеssuгеs against thеm аrе sоmеtimesrеlaхеd. Arrothеr ехamplе is proviсlеd Ьу Drosсlphilа mirаndа, itl whiсh art autos()nlеЬесаmе attaсhеd to thе Y сhromosomе аЬout 1 million yrars ago; this hаs sinсе Ьееn transmittеd only from fаthеr to son, сausing this gеnomе геgion to stop rесomЬining ЬесаusеrессrmЬirrаtiondoеs not oссur in Drr,,sophilа ma|еs.Тhе rеgion has sinсе thеn aссumulatеd a high dеnsityof TЕ insеrtionsinto nonсoding sеquеnсеs(Baсhtrog 2003)' Gеnomеs of somеspесiеs(е.g.,lrumаns arrd mаizе) lrаvеa vеry higЬ ovеrаIlTЕ aЬundarrсе (Тablе2), and at many сhromosomal sitеs, TЕs may bе prеsеllt at high fгеquеnсiеs(or еvеn in all individuals) (Ostеrtag and Kazazian 2001)' сontrasting lvirh thе low insегtiсlnfrеquеnсiеsin Drosсsphilа. \fhy arе thеrе suсh largе diffеrеnсеsЬеtwееn spесiеs?Pеrhaps thе пruсh largеr аnrounts of intеrgеniс DNA and largеr introns in humans than in
1,6L)
1 7 0 Еuolutioп of tbе Geпomе Drosophilа п1еаnthat insеrtions hаvе lеss risk of сausing harmful mutations (although this would not Ье tгuе if intеrgеniсrеgions' sеquеnсеsoftеn сontrol genе aсtivity). A morе intеrеstingpossiЬility dеpеnds on thе wеaknеss of sеlесtion against еaсh nеW TЕ insеrtion. If TЕs rarеly ехсisе from a sitе, gеnеtiс drift сan somеtimеs lеad tо a sitе Ьесoming iгrеvеrsiЬlyfiхеd for an еlеmеnt. In spесiеs with low population sizеs, suсh as humans, sеlесtion against еlеmеnts is lеss еffесtivеin opposing gеnеtiс drift' and this possiЬly allows thе prеssrrrеfor еlеmеnt Ьuildup to prеdominatе (Lynсh 2007I. Nеw insеrtions into аlгеady_оссupiеdsitеs woшld flot Ье prеvеntеdЬy sеlесtion(thеrеwould Ьe no direсt hаrmful еftесts,just a slightly grеatеr risk of есtopiс еxсhangе), and so еlеmеnts сould snowЬall ovеr timе. This may aссount for thе fixеd еlеmеnts in mаnrmalian gеnomеs' Ьut rrot for thе vеry high TЕ aЬundanсе in maize, a spесiеswhosе high DNA sеquеnсеvaгlaЬility indiсatеs a largе population sizе (Tenaillon еt al. 2002I. RесomЬination in maizе may Ье largеly сonfinеd to gеnеs' so that TЕs in intегgеniс sеquеnсеs сould not Ье rеmovеd Ьy есtopiс ехсhangе. Thus еlеmеnts would Ьuild up Ьеtwееn gеnеs' as oЬ. sеrvеd (SanМiguеl еt a|. 1.996)'Нowеvеr, thе сausаtion сould Ье thе othеr way round: TЕs may simply rесomЬiпе lеss than l.lostsеquеnсеs. тHЕ ЕVoLUтIoNARY сoNsЕoUЕNсЕs oF GЕNЕтIс RЕсoMвINAт|oN AND PoPULAтloN s|zE SеlесtionagainstTЕs is only onе Way in whiсh small population sizе and laсk of rесomЬination сan Ье importаnt for gеnomе еvolution. RесomЬination rаtеs play important гolеs in numегous еvoluгionаryproсеssеs'еspесiallythе еvolutionary advantagеs and disadvantagеsof sехual rеproduсtion. Sеvеral diffеrеnсеs among gеnomе rеgions аrе сonnесtеd with rесomЬination ratе diffеrеnсеs' аnd thе еffесts of low rесonrЬination rаtеs arе similar to thosе of small еffесtivеpopulаtion sizе (Gоrdo arrd Chaгlеsworth 2001). Sеx and rесombinаtiorr аllow sеlесtion to aсt indеpеndеntly on diffеrеnt sitеs within thе gеnomе. This inсrеasеsthе еffiсiеnсy of sеlесtion.For ехample,if favorаblе mutaсions arisе indеpеndеntly, but vеry rаrеly' at two sitеs, thе populаtion will rarеly сtrntainany individualsthat сarry douЬlе mutants'еvеn if this is thе fittеst сomЬination (unlеssthе populаtion sizе is so hugе that thе sесond mutation еvеnt happеns Ьеforе sеlесtion fiхеs the first favoraЬlе mutation). Gеnеtiс rесombination allows thе douЬlе-mutant сomЬination to Ьe formеd. Whеn thеге is littlе or no eеnеtiс rесomЬination' or whеn rеproduсtion is asеxual, sеlесtioп on onе gеnе thus impеdеs sеlесtion aсting on othеr gеnеs' making fаvoraЬlе mutations lеss likеly to sprеad and dеlеtеrious mutаtions (suсh as amino aсid сhаngеs in prоtеins) moге likеly to Ье fiхеd Ьy gеnеtiс drift, paгtiсularly whеn population sizеs arе low (Gordo and Сharlеsworth 2001). This Proсеss proЬaЬly сontriЬutеs to gеnon-lеrеduсtion in symЬiotiс Ьaсtеria that livе within inseсt сеlls (rесomЬination bеtwеen Ьасtеria of thеsе spесiеs is prеvеntеd by isolаtion);thеsеrеduсеdgеnomеsalso havе fastеramino асid sеquеnсе еvolution' as prеdiсtеd givеrrthе lowеrеd aЬility of sеlесtionto еliminatе mutations with wеakly disаdv:rntagеous еffесts(Мoran 2003).
Gеnеs irr gеnonrеr.еgion similar еvolutionаry proсеs еls of adaptation. Тhis ma сomЬirring сhrotnosomal rt (pегh:rpsаlso in pаIt саLls strikingly illustrаrе thе ( D . С h а r l е s w o r t hе t a i . 2 0 С s o m е g е n е s ' Ь е t г а r ' i n gr h е paiг, Ьut tlrе Y laсks n)()st(
thе gеnеtiс informаtion onс nonrес()mЬiningсhromoso p е d е t h е i r а Ь i l i t yr o m a i n г fastеr than tЬеir Х-linkеd d i s а d v e n г а g е o u sr . e r i e r l t si gеnеs thаn likе normal gеn s е s o f s е х . l i n k е dg е n с si n ( F г i d o l i s s o nа n d Ё l l с g г е n. gеnеs addеd to thе Y сhro сonfirm гhetthis is duе tll i mutations (Bartolсlrnёand Similar Ьut mildеrеffесt gions with diffегеntrесoml сodons that еnd irr G or С сontеnt of third сoding pos oг thе аdjaсеnt r-ronсtrdi gапs, and А' thаlitlпа, tЬerс геflесts thе aсtion of sеlес fastеr аrrd/or morе aссurаt tеin sеquеirсе(AkasЬi еt al is' horvеvеr, vеr1' small сo protеin sеquеnсеs.so that prеfегrеd ovеr AТ. In an o сomPonеnt of tlrе gеllomr whеrе rесomЬination is in1 mal сodon usagе шight Ье would Ье lеss Ьiаsсdthаn o f t h е o Ь s е r r ' е r ]r е l l t i o n s сontеnt of сoding sеquеn and for thе wеakеning of tесtеd for thе gеnеs addеd and Сharlеswсlrth 2006). Horvеvеr, thе GС с()ntе С. еlеgапs also с
Еuolutklп rlf the (}uюtпе l risk of сausingharmful mutations niс rеgions'sеquеnсеsoftеn сontrol ity dеpеndson thе wеaknеss of sе.Еs raгеly еxсisе from a site, gеnеtiс rg irrеvеrsibly fiхеd for an еlеmеnt. э as humans' sеlесtion against еlе: drift, and this possiЬly allows thе laге (Lynсh 2007). Nеw insеrrions lrеvеntеdby sеlесtion (thеrе would r grеatеrrisk of есtopiс ехсhangе), . Тhis may aссOunt for thе fixеd еl[or thе vеry high TЕ aЬundanсе in эе vaгiaЬilityindiсatеsa largе popтbination ir-rrnаizе may Ье largеly iс sеquеnсеsсould not Ье rеmovеd ld Ьuild up Ьеtwееn gеnеs' as oЬ' thе сausationсould Ье thе othеr ;s thurnhost sеquеnсеs. :NсЕs oF GЕNЕт|с
.IoN sIzЕ
lriсh smali population sizе and laсk ]еnomе еvolution. RесomЬination olutionaryproсеsses,еspесially thе еs of sеxuаl rеproduсtion. Sеvеral эnnесtеd with rесomЬination rate ination ratеs arе similar to thosе of l Сhirrlеsworгlr2001 ). )aсt indеpеndеntlyon diffеrеnt sitеs :nсy of sеlесtion.For еxamplе, if favеry rагеly, at rwo sitеs, thе рopuat сarrУdouЬlе mutants' еvеn if this rtion sizе is so hugе that thе sесond es thе first favюrаЬlеmutation). Gе.utant сomЬination to Ье formеd. Ltion,or whеn геproduсtion is asехсtion асting on othеr gеnеs,making rnd dеlеtеriousmutations (suсh аs , to Ье fiхеd Ьy gеnеtiс drift, partiсгdo and Сharlеsrvorth 2001). This :duсtion in symЬiotiс Ьaсtеria that 'ееnЬасtеriаof thеsеspeсiеsis pгеalsohavеfastегаmino асid sеquеnсе l i l i t yo f s е l е с t i o n г o е l i m i n a t еm u t а Мoran 2003)'
Gеnеsin gеnomе rеЕ]ionstlrat lасk gеnеtiс rессlmЬinatiсlnshould r.rndеrgo similarеvolutionirrvproсеssеsthar iпrpеdеsеlессionаrrсllеаd tсl rеduсеd lеvеls of аdaptation.This may also сontгiЬutс to thе Ьuildup of TЕs in nonrесomЬiningсhromosomal rеgions and to thеsе rеgions' inсrеasеd intron sizеs (pеrhapsаlso irr p2rrtсausеd Ьy ТЕ-dеrivеd matсrial). Y sех сlrгomos
171
172
Еuolutiсlпrlf thе Gепome ratеs. сеrtainly, not all mutаtions oссLlr еqually frеquеntlv' As аlrеady mеntionеd, thе rеlativеly high AТ сontеnt of nonсoding DNA is сausеd by mutational biаs toward AT. A proсеss that may opposе this is biаsеd geпе сonuеrsion; Ьесausе of thе molесular mесhаnism of gеnеtiс rесomЬination' whеn onе gеnomе has GС at a sitе and thе samе sitе in thе othег has AT, rе. сomЬination сan pгoduсе a vеry slight ехсеssof GС in thе daughtеr gеnomе (Мarais 2003). This will inсгеasеGС сontеnt in Ьoth сoding and nonсoding sеquеnсеs' сausing GСs to Ье fiхеd moге frеquеntly than ATs' just as though GСs wеrе favorеd by sеlесtion.Bесausе it is paгt of thе rесomЬination proсеss, Ьiаsеd gеnе сonvеrsion is еxpесtеd to aсt mainly in rеgions with high ratеs of rесomЬination, lеading to a highеr GС frеquеnсy in suсh rеgions. Thiгd positions of сodons will havе an аdditionаl еnhanсеmеntof GС from thе еffесtsof sеlесtion for сodorr Ьias' Statistiсalanalysеsof thе GС сontеnt of thе gеnomе of D' mеlаnogаstel"supPort this hypothеsis, as do data from thе highlу rесomЬining parts of sеx сhromosomеs of nrammаls (Мarais
2 0 0 )З.
Соnсlusions Gеnomе еvolution, likе othеr еvolutionаry сhangеs, is opportunistiс. Сhangеs in gеnomе fеaturеs hzrvесonsеquеnсеsof two kinds. First, сhangе may lеad to fuгthеr сhangеs. For instanсе, сhr{rmosomеrеaгrangеmеntsaffесt rесomЬination. A gеnе сan movе into a rеgion of lowеr or highеr rесomЬination, affесt. ing thе Ьаlаnсе Ьеtwееn Ьiasеd gеnе сonvеrsion that pushеs GС сontеnt up vегsus mutation Prеssurе in thе othеr dirесtion, So that GC сontеrrt will start сhanging. If a rеarrаngеmеntrеduсеs rесomЬinаtion, as happеns whеn a сhromosomе arпr is joinсd to a Y сhromosomе, thе dесrеasеdaЬility of natrrrаl sеlесtion to еliminatе wеaklу disadvаntagеousсhangеs may ultinratеlylеad to thе loss of funсtionality' or еvеn thе physiсal prеsеnсе'of gеnеs from this сhromosomе' as indееd has hаppеnеd in D. пtirапdа (D. Сharlеsworth еt al. 2005). Sесond, еvеn whеn a gеnonlе fеaturе еr,olvеswitlrout Ьеing favorеd Ьy individual sеlесtion,thеге сan oссasionаlly Ье pоtеntially advantagеouseffесts for organismal funсtions. For ехamplе, TЕs that сontain sеquеnсеsthat сontrol thе ехprеssion of thеir own gеnеs саn аlso аffесt thе aсtivity of gеnеs сlosе to thеir insеrtion sitеs.Initially parasitiс sеlfishDNA (sprеadingpurеly as a сonsеquеnсеof sеlесtion for thе sеquеnсеs'own aЬility tо rеpliсatе)сan ..domеstiсatеd'' bесomе as a part of thе gеnomе of a spесiеs,prеsеntin all individuals аnd funсtioning in its host, rathеr likе thе organеllеs'whiсh wеrе onсе indеpеndеntorganisms (Broоkfiеld 2003). This possiЬility is often ovеrlookеd, Ьut it is important to avoid thе naivе attitudе that prеsеnt.davЬеnе. fits сan ехplain thе origin of irll gеnomе fеatuгеs. Genomе еvоlution is far morе сomplех than straightforward adaptivе еvolution Ьy natural sеlесtion,and many fеaturеsmay havе hаd a long history in gеnomеs Ьеforе аny Ьеnеfiгs t
latiol.lsizеs dесrеаsеdas п trons еxp()sеs gеnеs t() с] сhangе thе prсltеin irnd spliсir-rgmust Ье сOnsегvе Ь y s е l е с t i o nt l n l y i n s р с с i prеssurе inсrеаsеs intron pгokllry
ous tеsts of hypothеsеsthl BIвLIoGRAPнY
A k а s h i 'H . , R . l \ { .K l i m а n ,a
s е | е с t i с l r rl r n d т h е е r ' t > | t
49-60. Thе ArаЬidopsis Cеnсlmе In flсllvеring plмtt Аrаbidl, Arаvin, A. A.' G. J. Hanпtln рrovidеs an aсlirрtivеdе Asthаl-rа,S., \и. s. NoЬlе, G. St:rnll-ttovаnnсlgl
Еuolutioп сlf thе cепolпе еquаllyfrеquеntly.As alrеаdy mеnnonсodingDNA is саusеd Ьy mutа: mаy opposе this is biаsеd gепe :сhanismof gеnеtiс rесomЬination, 1е samе sitе in thе othеr has AT, rе:сеssof GС in thе daughtеr gеnomе ltеnt in Ьoth соding and nonсoding tiеquеntly than AЪ, just аs though it is part оf thе rесomЬination proto aсt mainly ir-rrеgions with high hеr GС frequеnсy in suсh rеgions. dditionalеnhanсеmеntof GС 1rom .ltistiсаlanalysеsof thе GС сontеnt 'rt this hypothеsis,as do data from lromosomеs of mammals (Мarais
, сhаngеs'is opportunistiс. Сhangеs wo kinds. First, сlrangе may lеad tо lе rеaгrangеmеntsaffесt rесomЬinavеr or highеr rесomЬination, affесtvеrsion thаt pushеs GC сontеnt up сtion' so that GС сontеnt will start lЬination, as happеnswhеn a сhгol, thе dесrеasеdability of naсural sе)us сhangеs may ultimatеly lеad tо al prеsеnсе,of gеnеsfrom this сhro,апdа(D, Сharlеsworth еt аl. 2005). ,.olvеswithout Ьеing firvorеd Ьy inЬе potеntially advantаgеous еffесts Еs that сontain sеquеnсestЬаt сontn аlso affесt thе aсtivity of gеnеs sitiс sеlfishDNA (sprеadingpurеly еnсеs'own aЬility to rеpliсatе) сan nomе of a spесiеs'prеsеnt in all inrеr likе thе оrganеllеs, whiсh wеrе 003).This possiЬility is oftеn ovеr'ivе аttitudеthat prеsеnt-dayЬеnеaturеs. гhanstгaightforwаrd adaptivе еvolrеsmay havе had a long history in аnism еvolvеd. Iг hаs еvеn Ьееn эrеadwithin gеnomеswhеn popu.
lаtionsizеsdесгеаsеdаs rrruIriсеllrrlаг orgаnisпrsеvolvеd.Thе prеsеlrсеof introns ехposеs gеnеs to ехtrа hаrmful mutations in addition to thosе that сhangеthе pгotеir-rand ссlrrtгollirrgsеquеnсеs (Ьgсдu5gsiгеs rеquirеd for spliсingmust Ье сonsеrvеd).It is ptlssiЬlеthаt thеir prеsеnсесan Ье rеsistеd Ь,vsеlесtiononly irr spесiеsrvith vеry l:rrgеpсlpulations.IГ somе rlrutational prеssurеinсrеirsеsintron nunlbеrs. this соuld aссOllnt for introns' rarity in рrokaryotеsand prеsеrrсеin multiсеlltrlar еuk:rryotеs(Lynсh and Сonеry 2003;Lynсh 2007). SеIесtionmау аlstl firvoг small рrokarvotе gеllomе slzе for othеrrеasons' llut in prinсiplе all rrpposingforсеs must Play somе rolе. Again, horvеvеr,it sеепrs unlikеly tlrаt n.rutirtiсlпаl prеssllrе ехplains thе prеsеnсеof аll intгons in gеnеs of living multiсеllular еukaryсltеs,еspесially Ьесausеintron sizе and nunlЬеrs сan dесrеаsе,аs wеll as itrсrеasе(this has happеnеd.frrr instаnсе,in thе smаll gеnomе of thе plant А. tbаliапа;.Wright еtal.2002). \й/hаtеvеrthе сausеsof thеir initial origins, introns havе еvolvеd to Ьессlt-l-tе dоrnеstiсаtеdаnd l-rаvеасqrrirеd сеllulаr funсtiсrns' as wе lrevе suggеstеd for othеr gеn()mеfеaturеs,and thеrе is inсrеasing еvidеnсе for sеlесtivесonstrail-tгs tltr intгtln аrrd lr in Drosоphila.cепеtiса1'О2.. 49-60. ThеAгаЬidopsis GеnоmеInitiativе. 200.l. Аnаlysisof thе gеnomеsеqr.rеnсе of thе florvеringplantArаbidсlpsisthсtli.lпа.Nаturе 40B:796_8l.5. Aгavirr, A. A.' G..J.Fiаnnoп,аnd'|.Brеr-rnесkе. 2007.Тhе Piwi-piRNA раthwav providеs an adaptivес1еfеnsс it.rthе trаrlspоsоll ]rп1sraсе.SсicttсеЗ18 76|-764, , . S u n v a е ra, ,n d . l .A ' A s t h a n аS.. , . WS' . N о Ь l е ,G . K r у . L r k oСv ., Е . ( ] r а n t S Stamato1'аnnoроulos. 2007. WidеlydistriЬutеd nоrtсodirrg puгifvingsеlесti
17.1
174
Еuolutiсlп of the Gепome Barnеs, T. М., Y. Кohara, A. Сoulson, аnd S. Неkim|. 1995. Меiсltiс rесomЬination, nonсoding DNA and gеnоmiс organizаtion tn Саеnorhаbditis еlеgапs' Gепetiсs 147: I59-179. Bartolomё, С., and B. Сharlеsworth. 2006. Еvolution of аminсl.асidseс1uеnсеs and ссldon usаgе on thе DrOsOpЬilа mirапdа nеo-sеx сhromosomеs . (]епеtiсs 174:
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Baumgartеn,A., S. Сannon, R. Spаnglеr' and G. Мay. 2003. Gеnоmе-lеvеl еvolution of rеsistanсе gеnеs in Arаbidopsis thаliапа. Geпеtics 165 ЗО9_319. Bеnsasson,D., D. х. ZЬang, D. L. Hartl, ar-rdG. М. Неwitt. 2001. Мitoсhondrial psеudogеnеs:Еvolution's misplaсеd witnеssеs. Trепds iп Ессllogу апd Еuoluthn 16:314-321. Brookfiеld, J. F. Y. 2003. МoЬilе DNAs: Thе poaсhеr turnеd gаmеk eеpеr.Сurrепt Biologу 13: R846-R847. Bruggmann' R., A. K. Bharti, H. Gundlaсh, J. S. Lаi, S. Young, A. С. Роntaroli, F..S. \Wеi,G. НaЬеrеr, G. Fuks, С. G. Du, С. Rаymond, М. С. Еstеp, R. Y. Liu,.|' L. Bеnnеtzеn'A. P. Сhan' P. D. Rabinowiсz, J. QuaсkеnЬush, W. B. BаrЬazuk, R. A. Wing' B. Biггеn' С. NusЬaum' S. Rounslеy, K. F' Х. Мayеr' and J. Меssing. 2006. Unеvеn сhromosomе сontraсtion and ехpаnsion ir"rthе mаizе gеnomе. Gепome Resеаrсh 16: 124,|_1251. Burt, A., and R. L. Trivеrs. 2ОО6. Geпеs iп Сoпfliсt: Thе Biolсlgу of Sеlfisb Gепеtiс Еlеmепts. СamЬridgе, МA: Harvard Univеrsity Prеss. Сavaliеr.Smith, Т. 1985. Тhе Еuolutioп of Gеnсlme Slzс. Сhiсhеstеr,U.K.:.|ohn !(iilеy. С. еlеgапs Gеnomе Sеquеnсing Prсljесt. 1999. How thе woгtт was Won. Trепds iп Gепetiсs 15: 51-58. Сharlеsworth' B., P. Sniеgowski,and W. Stеphan. 1994.The еvolutiоnary dynamiсs of rеpеtitivеDNA in еukaryotеs.Nаturе З71:215-220. Сharlеsworth, D., B. Сharlеsworth, and G. Мarais. 2005. Stеps in thе еvolution of hеtеromorphiс sех сhromosomes. Неrеditу 95| 118*128. Сomеron' J. M.' and M. Krеitman. 2000. Thе сorrеlation Ьеtwееnintron lеngth аnd rесombinаtion in Drosophilа: ЕquiliЬrium Ьеtwееnmutational and sеlесtivе forсеs. c eпеtiсs 1 5 6: 1 77 5-|190. Сrow, J. F. |993. Mutation, mеan fitnеss, and gеnеtiс load. Охford Suruеуs of Еurllutioпаrу Biologу 9 : 3-42. Dеiningеr, P. L.' J. V. Moran, М. A. Batzеr, and Н. H.Kaz'azlan.2003. Mоbilе еlеmеnts and mammalian gеnomе еvolution. Сurrепt Оpiпioп iп Gепеtiсs апd D euelсlpmепt13: 65 1_658. Douglas, S., S. Zаunеr, М. Fraunholz, М. Bеaton, S. Pеnny, Х. N. \йИu,М. Rеith' T. Сavаliеr-Smith' аnd U. G. Maiеr. 200l . Тhе Ьighly rеduсеd gеnomе of an еnslavеdaigal nuсlеus.Nаturе 4I0: 1О91-J'096. D r a k e , J . W . ' B . С h a r l е s w o r t h ,D . С h a r l е s w o r t h 'а n d J . F . С r o w . l 9 9 8 . R а t е s o f spontanеousmutation. Gепеtiсs 148l.1667-1686. Drosсlphilа 12 Gеnomеs Сonsortium. 2007. Еvolution of gеnеs and gеnсlmеsоn thе Drosophila phylogеny' Nаturе 4.50:203_21 8. Еiсhlеr, Е. Е., and D. Sankoff. 2003. Struсtural dynаrniсsof еukaryotiс сhromosomе еvolution. Sсiспсе 3О|: a93_797. Еlgin' S. С. R., and S. I. S. Grеwal. 200З. Hеtеroсhromatin:Silеnсеis gоldеn. Сurreпt Biologу 13: R895_R898. Fridolfsson, A., and H. Еllеgrеrr.2000. Мolесulаr еvolution of thе aviаn СHD l gеnеson the Z and.W sеx сhrоmosomеs. Gепеtiсs 15.5:1903-1912. Gеrrаrd, D. T., and D. A. Filatov. 2005. Positivе irnd nеgativеsеlесtionon mammalian Y сhromosom еs' Мсlleсulаr Biolсlgу апd Еurllutioп 22: 142З-1432, Gordo, I., and B. Charlеsworth.2001. Gеnеtiс linkаsе аnd molесulаr еvolution. Сurreпt Biologу 11: R684_R686.
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Еuolutioп tf thе Gепomе ]ekimi' 199.5.Меiotiс гесombination' l in (,аепorhаbditiselеgапs. Gепеtiсs llution of amino-асid sеquеnсеsand еo-sехсhrсlп-lоsot-t-tеs. Gсиel iсs 17 4: -i.Мay. 200.]' Gеnоmе-lеvеl is thаliаnа, Gепetiсs 165 ЗО9-З]-9. ] . М . Н е w i t t . 2 0 0 1 .М i t o с h o r r d r i а l ;ses.Trепds iп Есtllogу апd Еuolutioп oасhеrturnеd gamеkееpеr.Сurrепt i. Lаi, S. Yоung, A. С. Pontaroli, F. s. rymond, Nl. С. Еstеp, R. Y. Liu, J. L. J. QuасkеnЬush,!и. B. BarЬаzuk, unslеv,K. F. Х. Мayеr, and J. raсtionand ехpansiсlnin thе mаizе 1. nfliсt:Tbе Bioklgl' of Sеlfish Gепetiс сrsity Prеss. юmе Sizе.Сhiсhеstеr,U.K.: John How thе Worm Wаs won, Trеnds iп, an. 1994.Thе еvсllutior-rаry dynamiсs 712215-220. rrais'2005. Stеpsin thе еvolution of y 95:I 18-128. сorrеlationbеtwееnintrоn lеngth аnd bеtwееnmutаtiоnаl аnd sеlесtive gеnеtiс load. oхford Sиrueуs сlf d H. H. Kazazian.2003. MoЬilе n. Сurrепt Opinioп iп Gеnеtiсs апd on, S. Pеnny,Х. N. Wu, М. Rеith, ' Тhе highly rеduсеdgеnomе of an 1096. h, and J' F. Crow. 1998. Rаtеs of 7-1686. ,olutionof gеnеsirnd gеnоmеs on thе :i8. dynаmiсsof еukaryotiссhromosomе гoсhromatin:Silеnсеis goldеn. lar еvolutionof thе аvian СHD 1 Эепetiсs15 5 : 19ОЗ_|9 |2. ,'еand nеgativеsеlесtionon iologl апd Еuolиtioп 22: 1423_|432. linkagеand molесulаr еvolution.
Grаv,М. !и. 1999. Еvolutiorr оf organеllar gеnomеs.Сurraпt Оpiпioп iп Сепеtiсs апd Dеuеkl1lmепt9: 678_687, Grеgоry,T' R' 2004. Ir.rsегtion.с]еlеtitln Ьiasеsаnd thе еvсllutionof gеnоmе sizе. Cutе 32.4:|-31. Hаlligan,D. L., and P. D. Kеightlеу.2006. UЬiquitous sеlссtivесonstraints in thе DrсlsophilаgетromеrеvеаlеdЬy а gеnomе-widеsеquсrrсесompаrison. Сепfgеnе loss in oЬligatе Ьасtеriаl symbionts.СьtrrепtOpiпfutt iп Мiсrobiolсlgy 6: 512_.518. N{ousе(iеrrсlrnеSеquеnсirrgСoпsorrium. 2002. Irritialsес1Llеnсing аnd сonlрarаrivе analysisof thе morrsеgсnomе. Nаtttrе 420 520-562, ,N{vеrs, S., L. BоttсlIo' С. Еrееmагr,(i. MсVеаn, аrrd P. I)сlI-rrrеtty. 200.5. A firrе-sсаlе nrap of lссоmЬinatiоn rаtеs and hotspots асross thе huпlan !]еnomе.Sоепсс Jl0:ЗI2_з21. oсhmаn. H., J' G. Lаwrеnсе' аnd Е. A. Groismlln. 2000. Lаtеrаl gеnе trаnsfеr аlld thе niltrrrесlf Ьtсtеriаl innсlvаtiсln.NLlturе405:299-.]04. ostеrtag,Е' M.' аnd H. H. Kazаzian. 2001. Biology оf mаn.rmаliаnL.l rетrоtfilnsposotls. Аttпuаl Ilеuiеtuof Сепеtiсs.].5:.501_5З8.
17-\
1 7 6 Еuolutiсln of thе Gепome Pagеl, М., and R. A. Jсlhnstonе. 1992.Уariation aсross spесiеs in thе sizе of thе nuсlеar gеnomе suрports thе junk-DNA ехplanation for thе C-valuе paradoх. Proсеediпgsof thе Roуаl Soсiеtу of Londoп, Sеriеs B 249:119-124, Piеgu, B., R. Guyot, N. Piсault, A. Roulin, A. Saniyal, H. Kim, K. Сollura, D. S. Brar, S. Jaсkson, R. A. !Иing, and o. Panaud. 2006. Doubling gеnomе slzе without polyplоidization: Dynamiсs of rеtrotransposition-drivеngеnomiс еxpansions in Оrуzа аиstrаliеnsis, a wild rеlativе of riсе. Geпome Resеаrch 16 1262-\269. Ranson, H.' С. Сlaudianos' F. Ortеlli, С. AЬgrall, J. HеmingwaУ' М. y. Sharakhova, M. F. Ungеr, F. H. Сollins, and R. Fеyеrеisеn. 2002. Еvolution of suреrgеnеfamiliеs assoсiаtеdwith insесtiсidеrеsistanсе.Sсieпсе 298: \79-|81. SanМiguеl' P., A. Tikhonov, N. Jin, N. Мotсhulskaia, А', Zakharov, A. МеlakеЬеrhan, P. S. Springеr' К. J. Еdwards, М. Lее, Z. tvramova, and J. L. Bеnnеtzеn. 1996. Nеstеd rеtrotransposons in thе intеrgеniс rеgions of thе maizе gеnomе. Sсiепсe273: 7 65-7 69. Sеlkеr, Е. U. 2002. Rеpеat.induсеd gеnе silеnсing in fungi. Аduапсеs in Сепetiсs 46: 439450. Sharp, P. М.' Е. Bailеs, R. J. Groсoсk,J. F..Pеdеn, and R. Е. Soсkеtt.2005. Vаriatiоn in thе strеngth of sеlесtеd сodon usagе Ьias among Ьaсtеriа. Nuclеiс А с i d s R е s е а r с hЗ З : 1 | 4 1 _ | | 5 З . Sniеgowski, P. D., P. J. Gеrrish' T. Johnson, and A. Shavеr.2000. Thе еvolutiоn of mutation ratеs:Sеparаtingсаusеsfrom сonsеquеnсеs.Blo-Еssауs22: 1057_\О66. Suilivan' B. A., М. D. Blowеr' and G. H. Karpеn. 2001. Dеtеrmining сеntromеrе idеntity: Сyсliсal storiеs аnd forking patЬs' Nаturе Rеuiеt'usGепеtiсs 2: 584-596. Теnaillon, М. I., M. С. Sawkins, L. K. Andеrson' S. M. Staсk, J. F. DoеЬlеy, and B. S. Gaut. 2002. Pаttеrnsof divеrsity and rесomЬinatiоn along сhrоmosomе 1 of maizе (Zеа mауs ssp.m[lуs L.|. Gепеtiсs 1'62:1401_1'41З. Viеira, С., С. Nardоn, С. Arpin, D. Lеpеtit' and С. Bi6mont.20О2. Еvolution of gеnomе sizе in Drosophila: Is thе invadеr's gеnomе Ьеing invadеd Ьy transposaЬlе еlеmеnts? Мo Ieсu lаr B i o l ogу аn d Еu o lиt klп 1'9: 1 1'5 4_1'1'6I. 'Wаlsh' B. 1995. Нow oftеn do dupliсatеd gеnеs еvolvе nеw funсtions? Geпеtics J. 1.39:421.-428. .Wong, S., G. Butlеr, and K. H. !Иolfе. 2002. Gеnе ordеr еvolution and palеopolyploidy in hеmiasсomyсеtе уeasts. Proсееdings of thе Nаtioпаl Аcаdеmу сlf Sсiеnces USA 99 9272_9277. .lfright, S. I., N. Agrawal, and T. Е. Burеau.2003. Еffесts of rесomЬination ratе аnd gеnе dеnsity on transposaЬlе еlеmеnt distriЬutions in Аrаbidopsis thоliапа. Geпomе Resеаrсh 13: 1897-1903. .!7right, S. I., B. Lauga, and D. Сharlеsworth. 2002. Ratеs and pattеrns of molесular еvoiution in inbrеd and outЬrеd AraЬidopsis. Мoleculаr Biologу аnd Еuolиtioп 1'9:'1'4О7-1'42О. ZЬang, x. H.-F., and L. A. Сhasin 2006. Сomparison of multiplе vеrtеЬratе gеnomеs rеvеals thе Ьirth and еvolution of humаn ехons. Proceеdiпgs of the NаtioпаI Асаdemу of Sсieпсes USА 103: 13427-|з4з2.
Thе Pattе of Spесia
IvLаrgаrеtB. 1
Thе еssсntial Ьit сlf сvo gin trnd n:lturе of speсl
Spесiation' thе еvolr-rtion and maintаin thеir indеpе non еvеr sinсе Darwin (1
divеrsifiеd from sharеd an ing how spесiation oссurs О с с u r r е di n г h е p e s t ' l е з v i thеir оссurrеnсе. Spесiеs,l tiсs assoсiatеd with thеir rion, thеy аlso сarrу uni oссurrеd sinсе spесiation thе spесiation proсеss fro paгtiсularly diffiсult. Sесtlnd, nеW spесiеs ar ( е . g . , n a t u r a t s е l е с t i o n ,s t thеrеforе, finding a unifyir an impossiЬlе сhallеngе.T spесiеs сharасtеristiсs anr nomiс, systеmatiс' and сo F i n a l l y .s p е с i e t i o ni 5 а .
divеrgеnсе, a middlе stag Ьy various forсеs of еvolu сomеs a сomplеtеly sеpa еvolutionary сhangе witlr tion into nеw linеagеs(FiE сontinuum tlf spесietion tionаry Ьiologists whо w this hurdlе, tЬе study сlf l
ing arеas of еvolution:rry
esin the size of the : the C-valueparadox. 19 119-124. m, K. Collura, D. S. ,ublinggenome size rn-driven genomic ;. GentnneResearch\6: 4way.M. V. sen.2002. Evolution of :. Science298 179-1'81'. rkharov,A. 1.Avramova,and J. L. ;enicregionsof the maize Adtancesin Genetics 46: ,. Sockett.2005. .mongbacteria.Nwcleic 2000.The evolution of BioEssays22: 'terminingcentfomere uiewsGenetics2: ck, J. F. Doebley,and ion alongchromosome 1 - 14 1 3 . rt. 2002. Evolution of ing invaded by ion 19: 1154-1161. ew fnnctions? Genetics ,olution and 4sof tbe National rateand of recombination Arabidopsisthaliana. a n d p a t t e r n so f m o l e c u l a r lar Biologyand Euolution nultiple vertebrate tns. Proceedingsof the )L.
The Patternand Process of Speciation Margaret B. Ptacek-dnd ShalaJ. Hank"ison Tl-reessentialbit of evolutionary theor\.which is concernedrvjth the origin and nirture of spet:iesremainsr.rtterlyrnyster',.rut. *. Batcso. (192r)
Speciation,the evolutionary processby which new and distinct lineagesarise and mirintain their independenttraiectories,has been a perplexingphenomenon ever since Dirrwin (18-59)first proposed that all living organisms have frorn sharedancestors.There are severalreasonswhy unclerstanddiver:sified i n g h o w s p e c i a t i o no c e u r si s c h e l l c n g i n g .F i r s t . m o s t s p e c i r r i o nt v c n t s h r v c occurredin the past, leaving only the end products, species,:rs a signattrreof exrant and extinct tornts, [re,rrthe cher,rctcristheir occurrence.Species,l.r
178
The Раttеrп апd Proсеss of Spесiаtioп
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Speсies
sеlесrion.gеnеtiс drrft. a gеnotypiс diffеrеnсеsbеtш how аnd why nеw spесiе in whiсh nеw spесiеs аrе primary mеans Ьy whiсh n dеnt еvoIr-rtionarypathwa hаvе Ьеgul.rto rеsсllvе thе
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Thе Naturе of Spесi
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Common Anсestor Figurе 1. Thе proсеssof speсiationis a соntinuum.InitiaIdivеrgеnсеЬеtwееn populatiоnsis followеd Ьy а pеriod of anаgеniссhangеwithin еaсh nеw linеagе whеrеin spесiеs.spесifiссharасtеristiсsarе rеfinеd Ьy various forсеs of еvolution. In somе spесiеslong pеriоdswith littlе еvolutionaryсhangе(stasis)may ()ссur. onсe formеd,spесiеsmay furtherdivеrsifyinto nеw linеagеs(сladogеnеsis) or may Ьесomе ехtinсt. Thе сhallеngеin thе study of spесiation is unсovеring whеre along this сontinuuma spесiеsaсtuallyеxists.
еvolutionary Ьiologists ovеr thе past 15 yеars has lеd to mаny ехсiting advanсеs. Thеsе inсludе thе disсovеry of sеvеral spесiаtioп gепеs that сonfеr rеproduсtivе isolation, a Ьеttеr undеrstandingof thе importanсе of sympatriс spесiation (spесiationwithоut gеographiсisolation);and a геsurrесtionof intеrеstin how natural sеlесtionсan lеad to thе formatiсlnof nеw speсiеsas Ьyproduсts of adaptivе diffеrеntiation. In this еssaywе outlinе somе of thе major сhallеngеsin undеrstandingspе. сiation and showсasееxamplеs that illustratеthе major advanсеsin thе study of thе origin and divеrsifiсation of spесiеs. wе start with thе proЬlеm of dеfining spесiеs, and how an undеrstanding of thе undеrlying meсhanisms that lеad to thе formation of nеw spесiеs may Ье the Ьеst approaсh in attеmpting to dеfinе what a spесiеsrеally is. Nехt, wе outlinе thе various rypеs o f i s o I a t i n gЬ а r r i е г st h a n с а n i n i t i а t е 'p r o m o t е .a n d с o m p l е t еt h е s p е с i a г i o n proсеss.Finally' wе disсussthе еvolutionary mесhanismsthаt drivе thе spесiation proсеss. Outlining thе rеlativе rolеs thаt natural sеlесtion, sеxual
Spесiеs сonсеpts, :r sеt ot a Ь o u n d i n t h е l i t е r a t u r е( } lсlng-standingdеЬatе enro lеm is сеntеrеd arсlund ir pаttеrn-oriеntеd
Whаt do wе do with all dеfinе spесiеs irnywаy? T
Тhc Pаttеrп апd Prсlсеssof Spесiаtiсlп 1 7 9
Speсies D
peсIes с
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sеlесtion,gеnеtiс сlrift, and mutаtion plаv in prom()titlg phеnotypiс and gеnot1,piс diffеrсnсеsЬеtwесn populations is сritiсal to our undеrstanding of how ar-rdwhy nеw spесiеsarisе. Our gсlal is not t() сovеr еvеry potеntial way in whiсIrlrеw spесiеs аrе formес.lЬшt rathеr tсl illustratе with ехаmplеs thе primarymеans Ьy whiсh nеw s1-lесiеs arе f
Thе Naturе of Spесiеs }Sтдsls
Aшдсrшвsts
)mmon nсestor гinuum.InitialdivеrgеnсеЬеtwееn ;еniссhirngеwithin eaсh nеw linеаgе 'еfinеdby variousfoгсеsof еvolr.rtion. utionaryсhangе(stasis)may oссuг. into nеw linеagеs(сladogеnеsis) сlr , u d yo f s p е с i а t i o ins u n с o v е r i n g lly еxists.
yеars lras lеd to m:rny еxсiting ad.era|spесiсttio|1 gеnrs that сonfer rеing of thе importanсе of sympatriс : isоlation);and a rеsurrесtionof inthе formation of nеw spесiеsаs Ьyjor сhаllеngеsin undегstandingspегatеthе major advirnсеsin thе study :iеs.\7е start with thе proЬlеm of ling of thе undеrlying mесhanisms ]s may Ье thе Ьеst approaсh in at. N е ч г ,W еo u t l i n еt h е v а г i o u s t y p е s )motе' and сomplеtе thе spесiation try mесhanismsthat drivе thе spесillеs thаt гtаtural sеlесtion. sеxual
SpесiеsсOnсеpts'a sеt of rulеs tlr сharасtегistiсsusеd to dеfinе a sPе1'igs' abotrndin thе litеratuге(N[ir,vdеn|997;ТaLl|e l)аnd hilr,еЬееn a srrЬjесtof long.stаndingdеЬаtеamong еvсllr"rtionary Ьiсllogists.Tlrе naturе of rhis proЬlеm is сеntеrеdarоund a disagrееnrеntЬеtwееn еv
1 8 0 Тhе Pаtterп аnd Procеss of Spесiаtiсlп Tablе 1. Spесiеsсonсеpts'thеir dеfinitions'and rеfеrеnсеs Spесiеs сonсеpt Patternoriеntеd Biologiсal
Dеfinition
D o Ь z h a n s k y1 9 3 7 ; Groups сlf intеrЬrееding natural populationsthаt Мaуr 1942,196З аrе геproduсtivеlyisolatеd from othеr suсh groups.
Сohеsion',
Thе most inсlusivеgroup of organismshаvingthе potеntialfor gеnеtiс and/ordеmogrаphiс еxсhangеаЬility. Phеnеtiс A sеt of organismsthаt look similar to еасh othеr and arе distinсtfтom othеr suсh sеts. Rесognition A sеt оf populationsthat shаrеa сOmmon fеrtilization systеm (spесifiс mJtе-rесOgn itit-ln systеm). Proсеssoгiеntеd Сohеsion'.
Rеfеrеnсеs
Thе most inсlusivе group of organisms having thе potеntial for gеnеtiс and/or dеmographiс ехсhangеaЬility.
T е m p l е t o n1 9 8 9
Sokal and Сrovеllo 1970
P a t е r s o n1 9 8 5
Tеmplеton 1989
Есologiсаl
A sеt сlf organismsаdаptеd уanУa|en 1'976 to a singlеесologiсаlniсhе, еvolving sеparatеlyfrom linеаgеsoutsidеits rаngе. Еvolutionary A singlеlrnеagе S i m p s o n1 9 61 ; (an anсеstral-dеsсеndant W i l е y - l 9 7 8 sеquеnсеof pоpulations) еvolvingsеparatеlyfrom othеrsand with uniquе еvolutionarytеndеnсiеs and its own historiсalfatе. P h y l o g е n е t i сT h е s m a l l е s t d i a g n о s a Ь l е С r a с r a f t1 9 8 3 , сlustеrof individual t989 organismswithin whiсh thегеis а parеntаlpаttеrn оf anсеstryаnd dеsсеnt. ".Pаrts оf dеfinition сonsidеr Ьoth pаttеrn and prоссss сlf spесiation.
Figurе 2. An illustrаtionof } d i f f е г е n tp o i n t s i n t h е s p е с i .Whеn divеrgеntlir into two. SpесiеsСonсеpt (ЕсSС) will rеprоduсtivеisolation (ISM1 sеparatеspесiеsundеr thе B rеPrеsеntmonоphylеtiссlad сommon anсеstor)ЬеforеЬс SpесiеsСonсеpt (PSС).
sсiеntists сall spесiеs sееm сannot sееm to agrее.Thе having somе form of dеfiт еvеn if diffеrеnt spесiеs rt ariеs. First? dеfining Ьiolog nеr in whiсh to сlassify.
Sесond, dеfining diagnosa еntitiеs that еxist in naturс spесiеs aгisе without havir plaсе. Fourth, spесiеs,as thе еvolutionary history O surеd Ьy thе numЬеr and usuallymadе at thе spес сatеgorizing and сonsеrvl
T'he Pаttcпt аrld Proсеss of SDесiаtion and rеfеrеnсеs Rеfеrеnсеs intеrbrеесling D o Ь z h a n s k y1 9 3 7 ; lulationsthat Мaуr 1942,1963 lсtivеl1, isolatеd srrсhgroups. -rсIusivе group T е m p l е t o n1 9 8 9 ls havingthе lr gеnеtiс rоgrаphiс rility.
Lr'
BSс
Sokal and Сrovеllo ;anismsthаt r to еасhothег 1970 tinсt fтom othег pulаtiоnsrhat Patеrson-l985 nmon l systеm rtе-rесogniгion nсlusivеgroup ns havingthе )I gеnеtlс rographiс rility.
Tеmplеton1989
adаptеd van Vаlеn 1976 ;arrisms есologiсаlniсhе, paratеlyfrom tsidеits rangе. Simpsоn 196 1; аl-сlеsсеndа nt Wilеy 197tl f populations) paratеlyfrom with r"rniqr-rе .y tеndеnсiеs r lristoriсalfatе. sr diаgr.rosaЬiе С г a с r а f t1 9 8 З , rdividual 1989 withinwhiсh arеntalPattеrn and dеsсеnt.
tеagе
l р r о с е ь sо f s р е с i l l т i о n
Figurе2. An illustr:rtionof lrorv diffеr:еntspесiеsсonсеpts dеfi.rеspесiеsat diffеrеntpoints in thе spесiationproсеssaftеr thе splittingof a siфlе linеаgе into two. lfhеrr divеrgеntlinеagеsdispеrsеinto diffеrеntЬaЬitats'ihе ЕсоtЬgiсal SpесiеsСсlnсеpt(ЕсSС) will dеfinе tlrеrnаs sеpаrаtеspесiеs.Thе еvolutiоn of rеproduсtivе isolation(ISM1 or ISM2) Ьеtwееnthе two linеаcеswill сlеfinе sерaratе spесiеsundеr thе BiologiсalSpесiеsСorrсеpt(BSС). iinеagеs must rерrеsеnt monсlphylеtiссiadеs(all p<rpulаtiсlr.rs irгеdt-sсеndе.i frсlm а singlе с o m m o na n с е s t о rl)r е f r l г е Ь е i n gr е с t l g r l i z еаds s p е с i е su n t l е гt h е P h y I o g е n е r i с Sресiеs Сonсеpt (PSС).
sсiеntistsсall spесiеssееm to know thеir own Ьoundariеs' еvеn if biсllоgists саnnotsееm to agrее.Thеrе arе, howеvеr' somе vеry impоrtant геаsons ftrr h a v i n gs o m е f o г m o f d е f i n i t i o nt h a t s с i е n t i s t sс а n u s е г o г е с o g n i z еs p е с i е s , еven if diffЪrеnt speсiеs rеquirе different сritеria for dеfining thеir Ьoundariеs.First, dеfining Ьiologiсal еntitiеs аs spесiеsprovidеs a svstеmatiсmannеr in whiсh to сlаssify divеrsity and is thе Ьаsis of modегn taхonomy. Sесond,dеfining diagnosaЬlе groups as spесiеs соrrеsponds to thе disсrеtе еntitiеsthat ехist in naturе. Third' onе сannot study thе proсеss of how nеw spесiеsarisе without having somе dеfinition сrf what a spесiеs is in thе fiгst plaсе. Forrгth, spесiеs, аs thе lеast inсlusivе саtеgory of сlivеrsity, rеprеsеnt thееvolutionaryhistory of organisnrs'Finаlly, Ьiodivеrsity is gеnеrally mеasurеdЬy thе numЬеr аnd kinds of living organisпrs,and thеsе еstimаtеsarе usuallymadе at thе spесiеs lеvеl. Thus for a variеtу of геasons, inсluding сatеgtlrizingand сonsеrving divеrsity, as wеlI аs undеrstanding its oгigitls'
181
182
Тhе Pаttеrп апd Prс-lсеss of S1lесiаtkп dеfining spесiеsas disсrеtе Ьiologiсal еntitiеs is еssеntialto our undеrstandirrg of thе pr
ТаЬlе 2. IsolatingЬarriе Тyp. Prеmating
Есolо
Tеmр
Рolliл
Thе Naturе of IsolatingBarriеrs Thе importanсе of isolating Ьarriеrs is nеarly univеrsal rеgardlеss of thе spесiеsсonсеpt Ьеing appliеd. Although thе link Ьеtwееnrеproduсtivе isolation and tlrе BSС, whiсh dеfinеsspесiеson thе Ьasis of Ьаrriеrs to intеrЬrееd. ing, is сlЬviсlus,isoiatirrg Ьarriеrs also providе thе mеans through whiсh pсlpulatiсlrrsЬеgin to divеrgс through dесrеasеdgеnе flow, thе first stеp in spесiation. Thus еvеn m()rе Proссss-oriеntеdсonсеpts may Ье linkеd indirесtly tO thе еffесtsof isolating Ьarriеrs Ьесausеthеsе Ьarriеrs may at somе pсlint play tr rolе in сеssationсlf gеnе flow Ьеtwееnеvolutionаry linеagеs' Thеrе аrе nuпlеrous Ways to сlassify isolating Ьагriеrs;htlwеvеr' onе of thе rnost widеly usеd divisions is Ьеtwееn prеmаting and postmating bаrriеrs. Thеsе Ьаrriеrs inсludе thosе that arе duе to ехtrinsiс faсtors, suсh as есologiсal сlr Ьеhaviоral rтесhanisms, and thosе that arе duе to intrinsiс faсtors, suсh as еgg/spеrminсompatiЬilitiеs сlr gеnеtiс inсоmpatiЬilitiеs Ьеtwееn hyЬrid gеntlmеs(TaЬlе 2). Prеnlating Ьerriегsinсludе thosе thаt prеvеnt or dесrеаsеthе likеlihood of mating Ьеtwееn taхa. In еffесt, prеmating Ьarriеrs prеvеnt taхa (or thе gamеtеs from thosе taхa) from mееting.In есologiсаl isоlation potеntial mаtеs dtl ntlt meеt Ьесausеof diffеrеnсеsin haЬitat usе. For ехamplе, many insесts arе lirnitеd to fееding, сourting, mating' and ovipоsitioning on spесifiс plant hosts. Thus diffеrеrltspесiеserе prеvеntеdfrom intеrЬrееdingЬy thе rеstriсtion of сaсh ttl а spесifiсhost plant (Futuyma et a|. 1994). Altеrnativеly,indi. viduals may Ье tеmporally isolatеd' diffеring in thеiг timing of rеproduсtion. For ехamplе, thе sympatriс сoral spесiеsМoпtаstrаеа tlппulаris, М. fаuесllаtа, and М. frапksi arе tеmpoгally isolatеd through diffеrеnсеsin pеak spawning timеs, and diffеrеnсеs сlf only 1 to 2 hours Ьеtwееn spawning еvеnts providе еnough timе to dilutе gamеtеsand prеvеnt intеrspесifiсhyЬridization (Knowlton еt al. |997).In othеr сasеsindividuals of diffеrеntspесiеsmay Ье prеsеnt at thе sаmе timе and plaсе arrd still avoid intеrЬrееding.Pollinator isolation is tlnе suсh mеthod. Сharaсtеrs suсh as flowеr shapе,rеwагd (pollеn vеrsusnесtar), and сolor attraсt diffеrеnt typеs of pollinators (е.g.,moths' bееs, hummingЬirds) that rrray prеfеrеntiallvvisit only сеrtain flowеr tуpеs, еnsuring thаt pоllеn is trarrsfеrrеdonly within а spесiеs. A {inаl typе of ехtrinsiс isсllatingЬarriеr rеliеs Ol-lЬеhavioral diffеrеnсеsas prеmаting Ьаrriеrs.Сlosеly rеlirtеdspесiеsoftеn diffеr in partiсular traits thаt funсtion as signirls in thе mating proсеss. Thr-rsеvеrrspесiеsthat ехhiЬit no
Bеha. Postmating, prеzygotlс
Месh
Еgg-s
Сonsp prесе
Postmating, postzygotiс
HyЬri HyЬri
Dесrе fitnеss
othеr pre- or postmatil Ьrееding) may avoid int ing signals that rеstriсt ЕlaЬoratе malе ornamе rеlаtеd spесiеs аrе oftе (Andеrsson 1994), Dеspitе thе inhеrеnt mating at thе outsеt' m. pеn Ьoth prе- and postz in taxa with postmatinl plaсе. For еxamplе, in
Tbе Pаttеrп аnd Рroсess of Speсiаtion :iеsis еssеntiаlto our undеrstandаttеrnsof Ьiologiсal divеrsity. No lеsеpurposеs.Еvolutionаry Ьiolohеir quеstion with rеgard to thе istoryof thеir organism of intеrеst, еstto thе sсllvingof that partiсulаr
TaЬlе2. IsolatingЬarriеrs(Ьothprе- and postmаting)
Prеmating
Typе of Ьarriеr
Dеfinition
Есologiсalisolation
Spесiеsarе sеparatеdЬy diffеrеnt hosts or miсrohaЬitats.
Tеmporal isolation
Rеprоduсtion oссurs at diffеrеnt timеs. Di ffеrеnгspесiеsаttrасt diffеrеntpollinators,or pollеn of diffеrеnt spесiеsis сarriеd on diffеrеnrЬody parts.
Pollinator isolation
nеarly univеrsal rеgardlеss of thе rе link Ьеtwееnrеproduсtivе isola. ' thе Ьаsisof Ьarriеrsto intеrЬrееdlrovidе thе mеans through whiсh :rеаsеdgеnе flow, thе first stеp in rtеd сonсеpts may Ье linkеd indilесausеthеsеЬarriеrs may at somе Ь е t w е е nе v o l u t i t l n а г yl i n е a g е s . lating Ьarriеrs;howеvеr, onе of thе rеmatingand postmating Ьarriеrs. гo ехtrinsiсfaсtors' suсh as есologе that arе duе to intrinsiс faсtors, nеtiс inсompаtiЬilitiеsЬеtwееn hyг е v е n ro г d е с r е a s еt h е l i k е L i h t l o do Г g Ьarriеrsprеvеnt taхa (Or thе ga. есologiсalisolation potеntial matеs i t a t u s е .Е o r е x a m p l е .m e n y i n s е с t s rnd ovipositioningon spесifiс plant d from intеrbrееding Ьy thе rеstriс,ma еt al. 1994).Altеrnativеly,indiing in thеiг tirning of rеproduсtion. \oпtаstrаеааnпulаris, М. fаueolаtа, rough diffеrеnсеsin pеak spawning .s Ьеtwееnspawning еvеnts providе hyЬridizаtion (Knowlt intеrspесifiс s сlf diffеrеnt spесiеsmay Ье prеsеnt intеrЬrееding.Pollinator isolation is 'еr shаpе,rеward (pollеn vеrsus nес. pollinаtors(е.g.,moths, Ьееs' humo n l у с е r t a i nf l t t w е rt y p е s ' е n s u r i n g есlеs.
:г rеliеson Ьеhavioraldiffеrеnсеsas s oftеn diffеr in partiсulaг traits that ;. Thus еvеn spесiеsthаt ехhiЬit no
Postmating, prеzygotlс
Bеhavioralisolation
Bеhaviorsusеd as mаting signalsdiffег Ьеtwееnspесiеs.
Месhaniсal isolаtion
Spеrm transfеrсannot takе plaсе Ьесausеgеnitaliaarе not сompatiЬlе(or pollen doеs not adhеrе)Ьеtwееndifferent spесiеs. Propеrtiеs of thе gamеtеs (oftеnsurfaсеproteins)are not сompatiЬlеЬеtwееn spесiеsand prеvеnt fеrtilization. Hеtеrospесifiсspеrm arе outсompеtеd Ьy сonspeсifiс s p е r m 'r е g a r d l е sosf m a t i n g ordеr.
Еgg-spеrmrесognition
Сonspесifiс spеrm prесеdеnсе
Postmating, postzy8otiс
HyЬrid inviability HyЬrid stеrility DесrеasеdhyЬrid fitnеss
H y Ь r i d sd i е Ь е f o г еr е а с h i n g sеxual maturity. HyЬrids arе inсapaЬ1еof rеproduсing. HyЬrids havе lower fitness t h a n е i t h е rp a r е n t а sl p е с i е s and аге sеlесtеdаgаinst.
othеr prе- or postmating isolating Ьarriеrs (e.g.,sympatriс or synсhronous brееding)may avoid intеrЬrееding Ьесausе of prеfеrеnсеs for partiсular mating signalsthat rеstriсt thеir mating options to mеmЬеrs of a singlе spесiеs. ЕlaЬoratеmalе ornamеnts аnd сourtship displays that diffеr Ьеtwееnсlosеly rеlatеd spесiеs arе oftеn thought to rеsult in Ьеhаvioral isolating Ьarriеrs (Andеrsson1994\. Dеspitе thе inhеrеnt appеal of Ьarriеrs that prеvent diffеrеnt taхa from matingat thе outsеt' many isolating Ьarriеrs oссur postmating and may happеnЬoth prе- and postzygotiсally. As impliеd Ьy thе nаmе' mating may Oссur in taхa with postmating, prеzygotiс Ьarriеrs, but fеrtilization doеs not takе plaсе.For ехamplе, in Ьoth plants and animаls сonspесifiс spеrm (pollеn)
18З
184
The Pаtterп апd Proсеss of Spесiаtioп prесеdеnсеis сommonly fоund, whеrе, dеspitе multiplе mаtings, thе fеmalе (or fеmalе struсturе of plаnts) only irсссpts spеrm (or pсlllеn) from сon. spесifiсs, or, altеrnativеly, сonspесifiс spеrm outсompеtеs hеtеrospесifiсspеrm for fеrtilizаtion. Anita Diaz arrd Мark Maсnair (1999| studiеd сonspесifiс pollеn prесеdеnсеin thе monkеyflowеrs Мimиlus guttсltL|sand М. паsutus. Оn М. guttаtus сonspесifiс pollеn-tuЬе growth was fastеr than hеtеrospесifiс pollеn-tuЬе growth' еnsuring сorrspесifiсfеrtilization аnd сonfеrring rеproduсtivе isolation Ьеtwееnthеsе spесiеs. Postmating' postzygotiс Ьarriеrs rеprеsеntа finiri сatеgory of isolating Ьаrriеrs. Although this is a fairly сOп1monmесhanism of rеproduсtivе isolаtion, Dаrwin Wаs сonсеrnеd with this isolating Ьirrriеr Ьесausеit is thе Ьasis for thе produсtion сlf stеrilеhyЬrids. His dilеmmа, simply statеd,was this: if two taха еvolvеd from a сommon anсеstor' how сould thе сomЬination of thеsе .Would taхa form a stеrilе hyЬrid? that not imply stеrility аt somе timе in thе еvolution of tахa anсеstralto prеsеnt-dayspесiеs?Today wе know, howеvеr, that although hyЬrid stеrility is oftеn an important isсllаtingЬarriеr, it is far frсlm thе only form of postzygotiсisolation, and a Ьеttеrundеrstandingсlf gеnеtiсs has yiеldеd a solution to Darwin's proЬlеm of stеrilе hyЬrids. As with thе study of many еvolutionary proсеssеsin Ьiology, Drosophilа spесiеs havе provеd еxtrеmеly usеful in undеrstandingpostzygotiс Ьаrriеrs. In a сlassiс study of postzygotiс Ьаrriеrs, Alfrеd sturtеvаnt (1920) showеd that сrossing D. mеlапogсlsterfеmalеs with malеs of thеir sisгеr spесiеs D. simulаns yiеldеd only fеmalе hyЬrids, witlr malеs dying at thе larval to pu. pal transition. Мorеovеr' thе rесiproсal сross gavе risе to only hyЬrid mаlеs bесausеthе fеmalеs diеd as еmЬryos. This study providеd not onlY еvidеnсе of postzygotiс barriеrs to hyЬridizаtion Ьut also еvidеnсеthat thеsе Ьarriеrs сan appеar at diffеrеnt dеvеlopmеntalstagеs,that thе dirесtion of thе hyЬrid сross сan bе influеntial, and that hyЬrid inviaЬility сan span thе rаngе from partial to сompletе (Сoynе and Orr 2004). Although thе postzygotiс Ьarriеrs just disсussеd providе еvidеnсе of thе variеty of intrinsiс postzygotiсinсompatiЬilitiеs,thеy givе us only a rudimеntary undеrstandingof thеsе Ьarriеrs аnd thеir rеlationship to spесiation;that is' thеy tеll us what might happеn' Ьut not why or how thеsе Ьаrriеrs еvolvе. For that, Wе must turn to gеnеtiс modеls of postzygotiс isolation. Darwin Was unawarе of gеnеs or gеnе intеrасtions,Ьut his сonсеrn aЬout stеrilе hyЬrids was onе that trouЬlеd еvоlutiсlnaryЬiologists for somе tiпrе. Thе quеstion of how two spесiеs сan еvolvе from а сommon anсеstor yеt' whеn matеd, form stеrilеhyЬrids without at lеast onе of thсlsеspесiеspassing through a maladaptivе form was quitе pеrplехing.A solution to this dilеmma is providеd Ьy thе DoЬzhansky-Мullеr n-rodеl(although, аs notеd Ьy orr 11996]' Batеson еssеntiаllysolvеd this samе prсlЬlеm 25 yеars еarliеr). Thе solution dеpеnds upon undеrstandingthat gеnеtiс inсompatiЬilitiеsthat lеad to unfit offspring mаy Ье amеlioratеd Ьy mr.rltiloсr.rs intеraсtions.ln thе simplеst modеl, сonsidеr two loсi, AABB (Figurе З). In сlnе spесiеs a mutation сausеsthе ..а'' allеlе to appear and Ьессlmеfiхеd, rеsr-rlting in thе аaBB gеno. typе. In thе sесond spесiеsa mutation lеads to a ,.Ь'' аllеlе (again Ьесoming
/
(speсies2) AAbI
I
AABT \
Figurе З. Thе DoЬzhansky dеmonstrаtеs how spесiat intеrmеdiatе hyЬrid stagе. that possess thе variant allr taхon rеsults in spесiatron inсompatiЬlе' mating Ьеtw inviaЬlе, or othеrwisе lеss ] gеnе intеrасtion сomеs fro
fiхеd) and thе AAЬЬ gеn with thе anсеstral allеlе (с spесiеs nееd pass througl and ..Ь', allеlеs arе inсom d i f f е г е n tl i n е a g е sm а t е 'p r еrwisе lеss fit) Ьесausе tl baсkground, arе inсompа thоugh this proсеss may s mating barriеrs among multiloсus gеnеtiс inсomр Anothеr important arеа obsеrvation Ьy J. B. S. H with two diffеrеnt sеx сhr malеs, ZW, in Ьirds) is tht aЬility. Сallеd Haldanе's rl in a variеty of taxa (Сoy еrogamеtiс. Flaldanе's ru postzygotiс isolation (Сoy
Thе Pаttеrпаnd Processof Speciаtiott 1 8 5 эitе multiplе mаtings, thе fеrrrаlе )ts spеrm (oг pollеn) from сonoutсompеtеslrеtеrospесifiсspеrm rсnair (1999) studiеd сonspесifiс шlus gltttаtusand М. nаsutцs. Ол h was fаstеr than hеterospесifiс . r t i l i z n t i о lаl n d с o n Г с r r i l ] gr е p r ( ) . t a finаl сatеgoгуof isolirtingЬarhаnism of rеproduсtivе isolation, ЬzrггiеrЬесausеit is thе Ьasis fоr та, simplv statеd,was rhis: if two л.,сould thе сomЬination of thеsе irrrрlystеriIityаt somе timе in thе pесiеs?Today wе know, howеvеr, lportаnt isolating baгriеr, it is far ' and а Ьеttеrundегstandingof gе.oЬIеrnof stеrilеhyЬrids. proсеssеsin Ьiology, Drosсl|lhilа ldеrstandiпgp()stzygotiсЬarriеrs. Alfrеd Sturtеvarrt(1920) showеd l i r h m e | е so f r h t ' i r s i s г е r s p е с i е s itlr malеsdying аt thе l:rrvalto puOssgavе risе to only hyЬrid malеs study providеd rrot only еvidеnсе rt аlso еviсiеnсеthat thеsе Ьarriеrs еs' that thе dirесtiсlnof thе h,vЬrid tviaЬilityсan spаn thе rangе from disсussеdprovidе еvidеnсе of thе ilitiеs,thе1,givеtrsrlnly a rudilrrеnttt spесiation;that rеir rеlatilvе. lf postzygotiсis
(inviable/steri le hybrid) AaBb
/
\
(speсies 2) AAbb
A A B B (speсies1)
tI
Т AABb
\
AaBB
/
AABB (аnсestrа| spесies)
Figurе3. Thе DoЬzhansky-Мullеr modеlof irrtrinsiс postmating isolation dеmonstratеs how spесiаtionсould proсееdunhindеrеdЬy a dеirimental
intегmеdiatе hyЬrid stage.Тhe anсеstralspeсiеsdivеrgеsinto two sеParatеtaxa thatpossеssthе vаriant allеlеs..a',аnd ..Ь.''Fiхation of thе nоvеl аlЬlеs in еaсh taхonrеsultsin spесiаtion(spесiеs1 and spесies2). Sinсe..a'' and ..Ь'' arе inсompatiЬlе, mating Ьеtwееnthе two spесiеsrеsultsin a hybrid tlrat is stеrilе' inviaЬlе,oг othеrwisеlеssfit thаn thе parеntalspесiеs.Support for this modеl of geneintеraсtionсomеs from str"rdiеs с>[Drosophilа (Сoynе and orr zo04).
fiхеd) аnd thе AAЬЬ gеnotypе. In еithеr саsе thе nеw allеlе is сompаtiblе with thе anсеstralallеlе (е.g.,Ьoth AaBB and AABЬ arе viaЬlе). Thus nеithеr speсiеsnееd pass through a sеlесtivеlydеtrimеntal stаgе' Howеvеr, thе..a'' and ..Ь'' allеles arе inсompatiЬlе whеn thеy сo-oссur. If individuals from thе diffеrеntlinеagеsmatе, produсing an AaBЬ hvЬrid, it сould Ье stеrilе (or oth. еrwisеlеss fit) bесausе thе..а'' and..Ь'' allеlеs, whеn in thе samе gеnеtiс baсkground' arе inсompatiЬlе and form a postmating isolating Ьarriеr. Althoughthis proсеssmаy sееm unlikеly, multiplе еxamplеs,еspесiallyin post. mating barriегs among Drosophilа spесiеs, show that thеsе typеs of multilосusgеnеtiсinсompаtibilitiеsrnаy in fасt Ье quitе сommoп (orr 1995). Anothеr important arеa of study in postzygotiс isolation has foсusеd on an oЬsеrvаtionЬy J. B. S. Нaldanе (1922) that thе hеtеrogametiсsеx (thе onе with two diffеrеnt sех сhromosomеs, suсh as mаlеs, ХY, in mammals, and fеmalеs,ZW, in Ьirds) is thе onе most OftеnaffесtеdЬy hyЬrid stегility or inviaЬility.Сallеd Haldanе's rulе, this oЬsеrvation has сonsistеntly Ьееn supportеd in a variеty of taхa (Сoynе and orr 20О4| regardlеssof whiсh sех is hеtеrogamеtiс.Haldanе's rulе appеars to funсtion еarly in thе еvolution of postzygotiсisolаtion (Сoynе and orr 2004), sinсе rеlativеly rесеntly divеrsеd
1 8 6 Тhе Pаtterп апd Рroсеss rlf Speсiаtiott taхa arе morе likеly to еxhiЬit Нaldanе's rulе; сlldеr taхa oftеn show svmmеtriс hуЬrid proЬlеrns that аffесt Ьorh sехеs. Although Haldаnе's rulе has primarilv Ьееn oЬsеrvеd to rеsult in hybrid stеrility or inviaЬility of thе hеtеrogamеtiсsеx, soпlе еvidеnсе suggеststhat hеtеrogamеtiсhyЬrids rтay suffег dесrеasесlfitnеsstlrrough a variеty of othеr mесhanismsas wеll. For ехaпrplе,Nеal Daviеs anсl ссlllеaguеsshowеd tlrаt in thе Nеotropiсаl Ьuttеrflies Aпаrtiа fаtimа and А. аmаtbеа strong assсrrtlrtivе mating оссurrеd within еaсh spесiеs'Ьur whеn thеy wеrе сrossеd artifiсiаlly, fеmalе hyЬrids showеd геduсеd tЪrtiiity,сonsistеrrtwith Наldanе's rr-rlе(tЪmalе Ьuttеrfliеs arе hеtеrogаnlеtiс;Dаviеs et aI' 1997). In addition to this morе typiсаl rеsult,howеvеr,hyЬrid fеmalеsfrom thе А. аmаtbеа (fеmalе)xА. fаtitпа (malе) сross showеd а rеdr'rсеdtеnсlеnсyto miltе (Dаviеs et a|. 1997), Тhis study providеs еvidеnсеthat Haldarrе'srulе mzryеxtеnd Ьеyond thе typiсal oЬsеrvation of hyЬrid stеrility or inviaЬility, and that hyЬrid {itnеssmay Ье dесrеasеdthrough Ьоth prеmating and postmаting Ьarriеrs' A сomplеtе gеnеtiс undеrstаndingof postzygotiс isоlating Ьаггiегsis n.rцсh mоrе сomplеx than Нaldanе's гulе alоnе impliеs. Of partiсular intеrеstis thе сonсеpt of speсiаtirл gеnеs. Speсiation gеnеs arе gеnеs that diffеr Ьеtr-l,ееn taха and саusе rеproduсtivе isolation Ьеtrvееnthеn-r.A gеnе саllеd Оd1,55g'', for ехamplе, shows еvidеnсеof rapid еvolution in sсrmеfruit fliеs,dеspitеrеlativеly slow еvolution in other organisms. This gеnе appеars tсl Ье rеsponsiЬlе for stеrility in hyЬгid malеs ЬеtrvеenD. simцlаlusаnd D. mouritiапa (Ting еt al. 1998). Likе oсlysseиsJЕ]еnеsthat ехpеriеnсеrаpid еvolшtion(аt lеilst in somе taхa) may Ье likеly to саusе gеnеtiс inсompatiЬilitiеsЬеtwееntaхa and thus Ье good сandidatеs for spесiation gеnеs.МuсЬ of thе wсrrk сln sPесlation gеnеs rеmains thеorеtiсurl; howеvеr, еvolutiоrr:rгyЬiоlogists аrе addrеssing ехсiting quеstiorrssuсh as whеthеr partiсulaг gеnеs arе gеnеrally rnorе likеly to lеad to rеproduсtivе isolation, or whеthеr gеnеsassoсiatеdwith сеrtain funсtions arе Ьеttеrсаndidatеsfor spесi:rtiоngеnеsthаn tltlrеrs.
Thе Proсеssof spесiation Еvolutionary mесharrismssuсh as natural sеlесtion,sехual sеlесtion,and gеnеtiс drift сan promotе diffеrеrrсеsЬеtwееn populations in phеnotypеs and thеir undегlying gеnotypеs'еvеl1to thе ехtеrrtthаt diffеrеnt ;lopuiatiorrsЬесomе fixеd for сontplеtеly diffеrеnt аltеrnativеs. Why, thеn, is not еvеry сlеarly diffеrеntiatеdpopulatiсln соnsidеrеd a diffегеnt spесiеs?Thе сruх of thе proЬlеm геsts on two issuеs.First' htl.,vmuсh gеnе flow сlссurs Ьеtr-l,ееn diffеrеntiасingpopulаtions? Gеnе flow :rсtsto honrоgеnizеpopulatiorrs both phеnotypiсally and gеnеtiсally;hеnсе it works against sеlесti
сomplеtе thе spесiatron ovеrlap in gеographiс rar sеrvе а5 а strong Ьaггiе whosе ranges ovеrlap (sу or whеn prеviou.slyisoll o n d а r y с o n t a с t ) 'i n t r i n s Ьrееding Ьесomе nесеs importanсе of rеproduсt of spесiation' and muсh с е n t е r е do n r h е m е с h a n i Ьеtwееn spесiеs' Сlassiс modеls of thе s bution of populations un gеographiс isolation to t} d е g г е е o f g е r t g r а p Ь i сs е р an important сontriЬutol of spесiаtion havе foсus (natural sеlесtion,sехual d i v е r s if i с а r i o n e n d s p е с i а тHЕ RoLE oF NA
Thе imрortanсе of adapt lсlgicаl spеciаtioп) Was fil in thе 1940s in dеsсriЬin liеvеd that spесiаtitlnin I divеrgеlrt physiologiсa1сr m е n t s .Е г n s г M а y r \ | 9 4 2 latеd gеnеtiс diffеrеnсеs a n d е с о | o g i с e la d e p t a г i o rеproduсtivе isolating mt duсtivе isolаtion is thе dri allopatriс spесiation (FigL Nl[orе rесеntly thе impо d u с t i v е i s o l а г i o nе i t h е ri n аn important rоlе foг natr Ьесomе сlеar. LaЬoгator1 havе сoпfirmеd tlrat есo thаr rzrisеdfruit fliеs (D. l vironmеnts (varying tеml s o m е l е v е l o f p r е n t a t i n gl in diffеrеr-rtеnvironmеnts dеpеndеnt linеs raisеd in s r г а t еh o w t h е p r r l с е s sm i In thе simplеst modеl еvolvеs Ьеtwееrr popuiati
Тhе Pаttеrn апd Рroсess of Spеciаtioп гulе;oldеr taхa oftеn show sym)ееnoЬsеrvеdto rеslllt in hyЬrid sех' somе еvidеnсе suggеststhat l fitnеssthrough a variеty of othеr liеs and сollеaguеsshowеd that in n d А . а m а t h с аs t r o n g a s s o r t а t i v е hеn thеy wеrе сrossеd artifiсiurlly, эnsistеntwith Haldanе's rulе (fееt a|. 1997). ln addition to this from thе А. аmаthеа(fеmalе)x А. еnсy to matе (Daviеs et a|. 1997). s rulе may ехtеnd Ьеyсlnd thе typЬility,and that hyЬrid fitnеssmаy эostmаtingbarriеrs. tzygotiсisolatingЬarriеrs is muсh npliеs.of partiсular intеrеstis thе nеs arе gеnеs that diffеr Ьеtwееn ееnthеm.A gеnесallеd odysseиs, tion in sоmе fruit fliеs, dеspitе rеlТ h i s g е n еa p p е а r st o Ь е r е s p o n s i simulаns and D. mаuritiапа (Тtng еriеnсеrapid еvolution (at lеast in nсompatiЬilitiеsЬеtwееntaхa and rеs.Muсh of thе work on spесiаrolutionaryЬiсllogistsarе аddrеssrrtiсulargеnеs arе gеnеrally morе whеthеrgеnеsassoсiatеdwith сеr:сiationgеnеsthan othеrs.
sеlесtion,sеxual sеlесtion,and gееn populations in phеnotypеs and tеnt that diffеrеntpopulаtions Ьегnativеs.Why, thеn, is not еvеry : d а d i f f е r е n ts p е с i е s ?Т h е с r u х o f w muсh gеnе floш,oссurs Ьеtwееn :s to homogеnizеpopulations Ьoth lorks against sеlесtion and drift in ;iation, rеspесtivеly.Sесond' how е is thorniеr and points to thе imэесiatioпproсеss.Although divеrgnsiс barriеrsto rеproduсtion, somе Ье prеsеnt to stop gеnе flow and
сomplеtеthе spесiation proсess. For allopatriс populations' whiсh do not ovеrlapin gеographiс rangе' thе physiсal distanсе imposеd Ьy gеography сan sеrvеas а strong Ьarriеr to gеnе flow. Нowevеr, for divеrging populations whosеrangеsovеrlap (sympatry)or arе adjасеnt to onе anothеr (parapatry), or whеn prеviously isolated allopatriс pоpulations сomе into сontaсt (sесondaryсontaсt),intrinsiс or ехtrinsiс Ьarriеrsto gеnе flow that prеvеnt intеrЬrееding Ьесomе nесеssary to сomplеtе thе spесiation proсеss. Thus thе importanсеof rеproduсtivе isolating Ьarriеrs has Ьееn paramount in studiеs o{ spесiation,and muсh of our undеrstandingof thе proсеss of spесiation is сеntеrеdon thе mесhanisms that favor thе еvolution of rеproduсtivе isolation bеtwееnspесiеs. Сlassiс modеls of thе spесiation proсеss foсusеd on thе gеographiс distriЬutionof pоpulations undеrgoing divеrgеnсеаnd thе rеlativе сontriЬution of gеographiсisolation to thе formation of nеw spесiеs(Figurе 4). Although the dеgrеeof geographiс sеparation Ьеtwееn divеrging populаtions is сеrtainly an important сontriЬutor to thе disruption of gеnе flow, morе rесеnt studiеs of spесiationhavе foсusеd on thе importanсе of еvolutionary mесhanisms (naturalsеlесtion,sеxual sеlесtion,gеnеtiсdrift, and mutation) in promoting divеrsifiсationand spесiationеithеr in allopatry or in sympаtry. тHЕ RoLЕ oF NAтURAL sЕLЕстIoN lN sPEс|AтloN Thе impоrtanсе of adaptivе divеrgеnсе in thе spесiation proсеss (tеrmеd eсologiсаlspесiаtioп)was fiгst notеd Ьy thе gеnеtiсistThеodosius DoЬzhansky in thе 1940s in dеsсriЬing spесiation in Drosophilа. DoЬzЬansky (1946) Ьеliеvеdthat spесiation ln Drosophila oссurrеd mаinly through thе еvolution of divеrgеntphysiologiсal сomplехеs that wеrе suссеssful in diffеrеnt еnvironmеnts.Еrnst Мaуr (1942) Was thе first to point out that many of thе ассumulatеd gеnеtiс diffеrеnсеs Ьеtwееn populations' partiсularly in physiologiсal and есologiсaladaptations to partiсular еnvironmеnts' Wеrе also potеntially rеproduсtivеisolating mесhanisms. Suсh ..Ьy-produсt'' еvolution of rеpгoduсtivеisolation is thе driving forсе Ьеhind Мayr's сlassiс modе оf viсarianсе allopatriсspесiation (Figurе 4). Morе rесеntlythе importanсе of есologiсal divеrgеnсеin promoting rеproduсtivеisolation еithеr in allopatry or in sympatry has Ьееn rесognizеd, and an importantrolе for natural sеlесtionin a variеty of routеs to spесiationhas Ьесomесlеar. LaЬoratory ехpеrimеnts (rеviеwеdin Riсе аnd Hostеrt 1993) havе сonfirmеd that есologiсal spесiation сan oссur; ехpеrimеntal studiеs that raisеd fruit fliеs (D. melаnogаstеr or D. psеudoobsсurа) in diffеrеnt еnvironmеnts(varying tеmpеraturеsor food sourсеs) havе dеmonstratеd that somе lеvеl of prеmating rеproduсtivе isolation еvolvеd Ьеtwееn linеs raisеd in diffеrеntеnvironmеnts,whilе no prеmating isolation еvolvеd Ьеtwееn indеpеndеntlinеs raisеd in thе samе еnvironmеnt. Thеsе ехpеrimеnts dеmonstratеhow thе proсеss might also work in naturе. In thе simplеst modеls of есologiсal spесiation, rеproduсtivе isolation еvolvеsЬеtwееn populations inсidеntally as a Ьy-produсt of adaptation to
187
188
Тhе Раttеrп tlпd Prсlсеssrlf Spесiаtklп
Viсаrianсe AlIopatriс
,a\
(A) \ ",." ."/
\i/
PeripheraIlsoIаtesor Founder Еffeсt
/б -*/B О\ ((\/\7
Sympatriс
altеrnativе sеlесtiоn rеgrп tivе isolation has Ьееn rе1 Thesе Ьirds arе onе of th and havе evolvеd an im1 funсtion, in ассordanсе v havе сomе to oссupy. Lo (Grant et aL. 1976) ar'd tl Darwin's finсhеs has еvo spondеnсе to сhanging ес i n t е r s p е с6i с с o m p е t i r i o n tions Ьеtwееn Ьеak morp n е n г o f m a t i n g s i g n a l si n bеhavioral rеproduсtivе i D a r w i n . s f i n с h е s .T h е p г (pitсh) and tеmporаl pr с h а n g е s i n Ь е a k g a p е ;h . vary as a funсtion of Ьеа thе struсturе of song aп finсhеs on Santa Сгuz Is Ьеaks adaptеd foг сrushiл I o w е г г a t е s o f s y l l а Ь l еr е sресiеs with smallеr Ьеak сausе song plays a сеntra this linkagе Ьеtwееn Ьеak its сonсomitant influепсе plеs of Ьy-produсt еvolut portanсe in spесiаtion of
PARALLЕL sPЕс|l oF ЕсoLoG|сAL l
I-.igr-rrе 4. Сlassiс modеls (сlr rтodеs) tlf spесiatitln аrе Ьasеd on thе dеgrее of gеographiс sеpаration аs tЬе driving foгсе of spесiation. In viсarianсе allopаtry, аnсеstrаl pоpulations of a onсе-сontinuous, largе rangе of a spесiеs аrе sеparatеd Ьy а viсаriаrrсе еvеnt (е.g.,mountains, rivег, oсеan). Diffеrсnсеs in еnvironmеntal сonditions on еithеr sidе of thе Ьarriеr to dispеrsаl pronrotе loсal adaptation and Ьy-prсlduсt rеprtlduсtivе istlliltion, 1еadingto thе formаtion сlf nсw spссiсs (Мayr 1942). Thе pеriрhеral-isolatеs or foundеr-еffесt modеl of spесiatiсln p()stulаtеsgеnеtiс drift as thе prirтаry mесhаnism that prсrmotеs divеrgеnсе аnс1spесiаtion. Pеriphеral isolatеs or foundеr сvеnts rlссur whеrt ехpirrrd Outward from thе еdgеs of thеir distriЬutions to OссuPy рсlpr.rlatiсlr.rs dispеrsе to а nеW loсatior-r nеw l-raЬitats,сrr lvhсn ir sп.ral]numЬеr of ir-rdividLrаls аnd еstаЬlish a nеw population. Мayr (1954) prtlpсlsесithat gеnеtiс сhangе
ParallеIеvolution of sim ronmеnts strongly impliс s p е с i a t i o n с а n r е s u I tf г o n produсtivе isolation that rеlatеd populations as a t
would Ье rapid in suсh fou сould rеsult in gеnеtiсrеor i s o l a t i o na n d r е s u l ri n r a p i prrpulationsthat ovеrlаprn spесiationwhеrе rеproduс not geographiсallysеparat aссompaniеd Ьy assortativ
Thе Раttеrтlапd Prсlcеssof Spесiаtion altеrnativеsеlесtionгеgimеs.A rесеnt ехamplе of suсh Ьy-produсt rеproduсtivеisolation has Ьееn rеportеd irr Darwin's finсhеs of thе Galdpagos Islands. ThеsеЬirds arе onе of thе most сеlеbratedillustrations of adaptivе radiation and havе еvolvеd an imprеssivе 21rraуof spесializations in Ьеаk form and funсtion, in aссordanсе with thе divеrsе fееding niсhеs that diffеrеnt spесiеs havесomе to oссupy. Long-tеrm fiеld studiеs Ьy Pеtеr and Rosеmary Grant (Gгаrrtеt aI. 1'976)and thеir сollеaguеs havе showrr thаt Ьеak morphology in Dаrwin's finсhеs hаs еvolvеd Ьy nrеans of natural sеlесtion in prесisе сorrеspondеnсеto сhanging есologiсal сonditions, inсluding food availaЬility and intеrspесifiссompеtition. Jеffrеy Podos (2001) tеstеd for potеntial сorrеlations bеtwееn Ьеak morphology ar-rdsong struсturе. Song is a major сomponеntof mating sigrralsin Ьirds, and diffеrеnсеsin Ьirdsong lеad to prеmаting bеhаvioralrеproduсtivе isolation in a variеty of spесiеs of Ьirds, inсluding Darwin's finсhеs. Thе produсtiоn of Ьirdsongs with variation in frеquеnсy (pitсh) and tеmporal propеrtiеs (е.g., syllаЬlе rеpеtitions) rеquirеs rapid сhangesin Ьеak gapе; hеnсе voсal pеrformanсе сapaсitiеs arе prеdiсtеd to vaгy as a funсtion of Ьеak morphology. Podos tеstеdthis idеa Ьy сompаring thе stгuсturе сlf song аnd Ьеak Inoгpholog1'in еight spесiеs of DarwinЪ finсhеson santa Сruz Island (Figurе 5). Hе found сhаt spесiеs with largе Ьеaksadaptеdfor сrushing hard sееdshаd еvolvеd songs with сomparativеly lowеr rаtеs of syllaЬlе rеpetition and narrowеr frеquеnсy rangеs than thosе speсiеswith smallеr Ьеaks еvolvеd for fееding on smallеr, softer sееds. Bесausеsong plays ir сеIrtralrolе in rеPгoduсtivе isolation in Darwin's finсhеs, this linkagе Ьеtwееn Ьеak morphоlogy sеlесtеdfor fееding pеrformanсе and its сonсomitant influеnсеon song struсturе illustrаtеs onе of the Ьеst еxamplеs of Ьy.produсt еvolution of rеproduсtivе isolation and its potеntial importanсеin spесiatiоnof Darwin's finсhеs. PARALLЕL sPЕсIAт|oN As A s|GNAтURE oF ЕсoLoGIсAL sPЕс|AтIoN
ation аrе Ьasеd on tlrе dеgrее сlf Е spесiation.In viсarianсе allopatry, larее rangе of a spесiеs arе rins, rivеr, oсеan). Diffегеnсеs rn nе bаlriег to dispеrsal pronlсrtе loсal . r г i t l п l' е l d i n g t o t h е [ o r m а t i о n o Г )lirtеsor frlundеr-еtfесtmodеl оf r.rаrymесhаnism that рromotеs 's or foundеr еvеnts oссur whеt-t ; rlf thеir distriЬutirins to oссupy dividulrlsdispеrsеto i'1llеw loсаtion 1) pг
Parallеlеvolution of similar traits in populations that inhaЬit similar еnvitonmеntsstrongly impliсatеs natural sеlесtion аs i] сausativе agеnt. Pагаllеl speсiationсan rеsult from thе paгallеl еvolution of trаits that dеtеrn-linеrеproduсtivеisolzrtionthat еvolvе геpеatеdlyin indеpеndеntlydеrivеd, сlosеly rеlatеdpopulations as a Ьy-produсt of adaptation to diffеrеnt еnvironmеnts
wouldЬе rapid irr suсh founding ptlpulatiсlnsЬесausесlf gеnеtiсdrift. This сouldrеsultin gеr-rеtiс rеoгganizаti
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Figurе 5. An illustrаtionof Ьv-produсtrеproduсtivеisolirtionas a геsultof adаptivеdivеrgеnсеin Ьеak lnсlгphologyoссurs in Dаrlvill.sfinсhеs.Bеak morphologyand rеprеsеntаtivе sound spесtгogrаmsof solrgsfror.rr еight Dilrwirr'sfiлсh spесiеsotl SantaСгrrzlslаnd (frоm пry trl btltttlllt:Gеospizа tltаgпirostris,G. iortis' (}. Iuligiпоsа, С. sсапt]еlts'Сашаrhупсhus pаruиlus' С. psittасulа, С. pаllidа' С. tlliuасеа)arе shown. Sglесtrogrаmfгеquеnсy rеsolution,98l{ц sсalеЬ.lr,0.5s.Intеrspссifiсvаrrзгiсlrlis llppэrеntin Ьoth rr.r
Figurе 6. Parallеl spесiatio d е t е r m i n еr е p r o d u с t i v iеs o adаptation to diffеrеntеnv Ьеtwееn есotypes from thе (width inсrеasеswith inсrе Ьetwееndiffеrеntесotypе
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(Sсhlutегand Nagеl 1'995).Thе Ьеst ехamplеs of parallеl spесiation сomе from sympatriс spесiation еvеnts whеrе indеpеndеntсolonizations of partiсular еnvironmеnts havе lеd to similar, rеpеatеd pattеrns of сharaсtеr divеrgеnсе in adaptivе traits assoсiatеd with diffеrеnt niсhеs and thе parallеl Ьuildup of аssortativе mating Ьy selесtivееnvironmеnt Ьasеd upon diffеrеnсеsin thosе adаptivе trаits (Figurе 6). Thе thrеespinе stiсklеЬack (Gаsterostеus асuleаtus) Ьas Ьесomе a modеl systеmfor thе study of pаrallеl spесiation. Thе anсеstral thrееspinеstiсklеЬaсk is a marinе fish found aсross a widе gеographiс distriЬution from Alaskа and British Сolumbia through lсеland, Sсotland, Norway, and Japan. This spесiеsis аnadromous, Ьеing spawnеd in frеshwatеr strеams, spеnding thе juvеnilеstagе in mаrinе еnvironmеnts,nnd migгating Ьaсk to strеaпls as adults to Ьrееd. lndеpеndеnt сolonizations of strеam еnvironmеnts havе lеd to multiple strеam-rеsidеntstiсklеЬaсk populations that no longеr migratе to thе oсеan. In addition, in British СolumЬia and Alaska indеpеndеnt сolo_ nizаtionsЬy mаrinе stiсklеЬaсksof postglaсial frеshwatеr lakеs formеd aftеr thе rеtrеat of thе glaсiеrs at thе еnd of thе Plеistoсеnе havе lеd to thе indеpеndеntеvolution of lakе forms (Ьеnthiсsаnd limnеtiсs)in multiplе fгеshwatеr lakеs.Spесiationin stiсklеЬaсkshas involvеd thе rеpеаtеdсolonization of nеw еnvironmеntsand thе aссomparryingсhangеs in adaptations, primarily Ьody.sizеdiffеrеrrсеsand numЬеr and sizе of gill rakеrs (spinеs on thе gill p|аtеsusеd to 6ltеr food paгtiсlеs),аssосiatеdwith есologiсlrl diffеrеnсеsin еaсhеnvironmеnt.Havе thеsеadaptivе сhangеs lеd to rеproduсtivе isolation Ьеtwееndiffеrеnt stiсklеЬaсk есotypеs? In a rесеntstudy Jеffrеy МсKinnon and сollеaguеs(МсKinnon еt al. 2004) found strоng еvidеnсе of assortativе mating Ьy sizе through diffеrеntial fеmalе prеfеrеnсеsfor пralе Ьody sizе in altеrnativе strеam and mаrinе еnvironmеnts.
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luсtivе isolatitln as a rеsult of пrs in Dагlvin's finсhеs. Bеak ]granls сli songs fгсlrn еight ,from top tсl bottottl: (}еospiztt ldепs, Сdmdrhу пс b u,s1lаruulu s' rvn. Spесtrogram frеquеnсy с varilrtion is apраrеnt in Ьotlr largе Ьсaks (е.g.,G. mаgnirostris) rIowеr frеquеr-rсyfangеs thаn thosе (From Pоr-lсls2001.)
Figurе6. Parallеlspесiationсtrnrеsultfrom thе parаllеlеvolutionof traits that reproduсtivеisolаtionthаt еvolvеrepеаtеdlyas a Ьy-pгoduсtof dеtегminе adaptаtionto diffеrеnt еnvir
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Thе Pаttern апd Proсess of Spесiаtioп Anadromous marinе populations arе laгgеr in Ьody sizе than strеam-rеsidеnt populations, prеsumaЬly an advantagе in thе long-distanсеmigrations that marinе populatiоns undеrgo. Mating сompаtiЬility Was morе than tr,l,otimеs highеr whеn fеmalеs Wеге pairеd with malеs from thе sаmе есotypе (from British СolцmЬia оr Japan) than whеn thеy wеrе pairеd with malеs from a diffеrеnt есotypе. To tеst thе importanсе of Ьody sizе as thе Ьasis for аssortativе mating Ьy есotypе,МсKinnon and сollеaguеs(MсKinnon еt al. 2004) rеarеd stiсklеЬaсksfrom strеam-rеsidеntand marinе populations in thе laЬoratory and manipulatеd thеir Ьody sizеs Ьy сhаnging thе lеngth of thе growing sеason. This produсеd еithеr largе-Ьodiеd or small-Ьodiеd fish of Ьoth sеxеsin Ьoth mаrinе and strеam-rеsidеntесotypеs.In mating trials with thеsе ехpеrimеntally manipulatеd fish, thеy found that malеs and fеmalеs had highеr mating сompatiЬilitiеs whеn thеy wеrе matсhеd for sizе, rеgardlеsso{ their eсotypе of origin. Thеsе rеsults dеmonstratеthе importanсе of a singlе phеnotypiс trait, Ьody sizе, in adaptivе divеrsifiсation in stiсklеЬасks and suggеst that divеrgеnt natural sеlесtion on this trait in diffеrеnt еrrvirontnеnts also makеs a primary сontriЬution to rеproduсtivе isolation that lеads to spесiаtion.
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{ тHЕ RoLЕ oF NAтURAL sЕLЕстloN lN Hosт sHIFтs AND sYMPAтR|с sPEсlAт|oN Thе oссurrеnсеof sympatriс spесiation,spесiationwith
Figurе 7. Sympatriсspес faсilitatеdЬy host or haЬ divеrging phеnotypеs.Tl rеproduсtivеisolationеv ir-rdividuals tln thе nеw hr spесiationproсеsswithtl
primary сharaсtеristiсt host shifts in Rhаgolеtis Ьrееd on thе samе host spесiеs is low. For еxam ing еggs on applе trееs oviposition sitеs.This st Ьеtwееn hawthoгn and с u m u l a t е ds i n с еt h е i n i t nology, suсh as timing a d u l t s ( е . g . ,F е d е r 1 9 9 8 natural sеlесtion as thе fruiting phеnology Ьеtш diffеrеnсеs Ьy еaсh hos thе host raсеs and аugп еnсes. Thus thе Rhаgolс
Thе Pаttеrп апd Рroсеss of Speciаtioп in Ьody sizе than strеam.rеsidеnt гhе long-distanсеmigrations that а t i Ь i l i г yW e sm о r е t h a n t w o t i m е s lеs from thе samе есotypе (from y wеrе pairеd with malеs from a f body sizе as thе Ьasis for assor. ollеaguеs(МсKinnon еt al. 2004) .d marinеpopulations in thе laЬoсhanging thе lеngth of thе growJiеd or small-Ьodiеdfish of Ьoth otypеs.In mating trials with thеsе ind thаt malеs and fеmalеs had эrе matсhеdfor sizе, rеgardlеssof nstratеthе importanсе of a singlе ivеrsifiсationin stiсklеЬaсks and . h i st r а i ri n d i f f е r е nеt n v i r o n m е n t s lroduсtivе isolаtion that lеads to
Disruptive seleсtion
Assortativеmating within phеnotypеsor habitats
oN IN Hosт 'toN есiationwithout gеographiс isolaausе thе сonditions undеr whiсh эgеnizingеffесtsof gеnе flow wеrе сirсumstanсеs.Мorе rесеntly thе r с с o m p a n i е dh у s r r o n gа s s O r t а t i V е (Figurе7) as a likеly modеl for thе iеs has сonvinсеdmany еvolution, a n i m p o r t a n tа n d е v е n p r i m a r y 1anisms.lmpliсit in thе proсеss of геproduсtivеisоlation Ьеtwееn di. эrvе as thе primary Ьarriеr tO gеnе о p u l а r i o n so. n е с o m m o l l w a y i n dly еvolvе is through host shifts Ьy с i a l i z еi n p e r r i с u l а rh o s г s p е с i е s . . х а m p l еo f a s у m p а t r i сь р е с i а t i o n l i е s ( 1 9 6 6 ,\ 9 6 9 \ o f t h е h o s t r a с е s olеtis pomonеllа).HawtЬorn tгееs rthorn rасе of R. pomсlпеllа is tЬe tggot fliеs wеrе first disсovеrеd on dson Valiеy геgiсlnof Nеw York in ravе Ьееn studying diffеrеnсеs Ьеpplе raсе sinсе thе mid-1960s and ; diffеrеnсеsin lifе history and rеr Ьеtwееnthе two host rасеs. onе
Figurе 7. Sympatriс spесiation сan Oссur whеn disruptivе natuгal sеlесtton faсilitatеd Ьy host or hаЬitat shifts is aссompaniеd Ьy assortativе mating Ьy thе divеrging phеnotypеs. Thе sympаtriс modеl сlf spесiation rеquirеs that ..likе'' rеproduсtivе isolatiсln еvсllvеsаs a rеsult of аssortativе mating оf individuаls on thс nеw host or in thе nеw hаЬitat in oгdеr to initiatе thе spесiatiсlnpr()сеsswithtlut gеogrаphiс isolation.
primary сharaсtеristiсthat promotеs sympatriс divеrgеnсе assoсiatеd with host shifts tл Rbаgolеti.sand othеr phytophagous insесts is that thеy fееd and Ьrееdon thе samе host spесiеs;thus dispеrsal Ьеtwееn diffеrеnt host plant s p е с i е iss l o w . F о r е х a m p l е .f е m a l е so f h a w t h o r no r i g i n а r е a v е r s еt o o v i p o s i t ing еggs on applе trееs, whеrеas applе-origin fеmalеs prеfеr apple trееs for ovipositionsitеs.This strong host fidеlity limits intеrhost movеmеnt of adцlts Ьеtwееnhawthоrn and applе trееs. In addition, gеnеtiс diffеrеnсеs havе aссumulatеdsinсе thе initial host switсh that promotе сhangеs in Ьrееdingphеnology, suсh as timing tlf mating, pupation and diapausе' and есlosion of adults(е.g.,Fеdеr 1998). Thеsе сhangеs arе thought to hаvе Ьееn favorеd Ьy natural sеlесtionas thе diffеrеnt host raсеs of fliеs adaptеd to diffеrеnсеsin fruiting phеnology Ьеtwееnhawthorn аnd applе hosts. Suсh loсally adaptеd diffеrеnсеsЬy еaсh host raсе сontriЬutе to rеproduсtivе isolation bеtwееn thе host raсеs аnd augmеnt host fidеlity through fеmalе oviposition prеfеrеnсеs.Thus tЬе Rhаgolеris fliеs providе а fundamеntal ехamplе of есologiсal
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Thе Pаtterп аnd Proсеss of Speсiаtioп divеrgеnсеwhеrе сomplеtе gеogrаphiс isolation is not аlways rеquirеd to initiatе spесiation. Although phytophаgous insесts offеr sеvеral wеll-doсumеntеd ехamplеs of sympatriс spесiation though host shifts, a rесеnt study providеs at lеast onе ехаmplе of thе potеntial for sympatгiс spесiation via a host shift in a vеrtе. Ьratе' Afriсan indigoЬirds (gеnus Уiduа) arе host-spесifiсЬrood parasitеs, laying thеir еggs in thе nеsts of firеfinсhеs (gеnus Lаgonostiсtа)' and diffеrеnt indigobird spесiеs spесializе in pzrrasitizingdiffеrеnt spесiеs of firеfinсhеs.IndigoЬird nеstlings arе rеarеd along with thе host young and mimiс thе mouth markings of thеir rеspесtivе hosts, thus lowеring thе proЬaЬility of Ьеing rеjесtеdЬy thеir host fostеr parеnts.In addition to this uniquе mimiсry adaptаtion Ьy young indigobiгds, as adults, malе indigoЬirds mimiс thе song that is sung Ьy thеir host spесiеssirе, and fеmаlеsrеarеd by a spесiliс host spесiеsof firеfinсh prеfеrеntially matе with malе indigoЬirds that sing thеir natаl hostspесifiс song. This faсilitatеs host-assortativе mating and lеads to rеproduс. tivе isolation among diffеrеnt spесiеs of indigoЬirds that parasitizе diffеrеnt host spесiеs of firеfirrсhеs.A rесеnt phylogеnеtiс study Ьy Мiсhaеl Sorеnson and сollеaguеs(Sorensonеt al. 2003) that сomparеd n-litoсhondrialDNA sеquеnсеs for a numЬеr of diffеrеnt spесiеsof indigoЬirds and thеir rеspесtivе firеfinсh hosts dеnronstrаtеd that diffеrеnt indigoЬird spесiеs that parasitizе diffеrеnt firеfinсh hosts arе gеnеtiсally diffеrеntiatеd from onе anothеr, a finding сonsistеntwith assortativеmating of indigoЬirds rеarеd Ьy a partiсular firеfinсh host spесiеs.Thеse rеsults suggеstthat divеrgеnсеthrough loсal adaptations in nеstling mouth markings, adult nrаlе song сopying, and fеmalе prеfеrеnсеs for host spесiеs song typе has lеd to positivе assortativе mating Ьеtwееn diffеrеnt host-spесifiс spесiеs of indigoЬirds. This pattеrn of host-spесifiс adaptations linkеd with positivе assortativе mating within a host typе is сonsistеnt with sympatriс spесiation irr Afriсan indigoЬirds through host switсhеs in thе firеfinсh spесieswhosе nеsts thеy parаsitizе. RЕPRoDUст|VЕ lsolAтloN вY NAтURAL sЕLЕст|oN
MAY BЕ RE|NFoRсЕD
Natural sеlесtionсan aсt to dirесtly inсгеasеthе аmount of prеmating isolation bеtwееn two divеrging populations by sеlесting against hyЬrids formеd Ьеtwееn thеm. This proсеss' first proposеd Ьу Thеodosius Dobzhansky (19з7) and tеrmеd rеiпforcemeпlby Frank Blair (1955 ), сan oссur in arеasof sесondary сontaсt whеn prеviously allopatriс populations сomе into сontaсt and intеrЬrееd. Whеn hyЬrids Ьеtwееn formеrlу allopatriс populations arе partially infеrtilе, rеinforсеmеnt саn сomplеtе thе spесiation proсеss. Rеinforсеmеnt was а popular сonсеpt аftеr thе modеrn synthеsis Ьесausе it allows natural sеlесtion to drivе spесiatiоn dirесtly, Ьut its еmpiriсal dеmonstration has Ьееn diffiсult, and its ехistеnсе as an important сomponеnt of есologiсal spесiationhas Ьееn сontrovеrsiаl(е.g',Noor 1999; Мarshall еt al. 2002). Most of thе еvidеnсе for rеinforсеmеntсomеs fгсlm сomparisons Ьеtwееn allopatriс and sympatriс populаtions in thе strеngth of fеnralе mating
prеfеrеnсеsfor сonspесi of D rosolt h iltt psendoоlts luсtаlnсe to matе with ht populаtions (Noor 199.5 fеrtilе, allowing fсlr gеnе onе of thе Ьеst-doсtr t h i с a n d l i m n е t i се с o t y p е Ьaсk. Нoward Rr"rrrdlе: lаЬor21toryсrossеs anсl ir Ьrids suffеr a foraging d pаrеntal еnvironmеnts.It vironnrеnt with аrmplеас parеrrtal spесiеs.Horvеvе parеr-rtаlеnvironmеnt, lit ratеs :rnd wеrе smallеr at Wеrе pooгеr at саtсhing fiеld еnvironmеnts Ьесiru In adсlitiol-l' Ьеnthiс fеп likеly to matе witlr irrtеr malеs from al|opatriс pс sults support a modеl of t h r o u g l l n а t r l r а ls е | е с t i o fitnеss in еithеr parеntlll t How impoгtant h.rs rе Т h е p г t l Ь | е mi s t h l t r с i n pattеrns of strongеr divе tions. Imaginе that two s] grее of геprсlduсtivеisrll I i k е l vс o r l t i n u еt ( )с ( ) е х i s еls of геproduсtivе isolat or thе ехtinсtion oi thе spесiеs pairs) that wе ol еvolvеd a high dеgrееof following sесondаrv сoг v o l r ' е di n m a t i l l g с l с с i s i o dеrrrrinеsthе prосеssof rt рromotе divеrgеnсеirr rn must Ье tightlv linkеd wi ity. Tlrеsе геquirеmеntsп Thеsе argumеnts do nс plеting thе spесiatiсlnprс that thе еvidеnсе for tnе '
sivе. of thе two proсеssе rr'ith ссologiсel s1rgсiд1 rеinfoгсе:tтеnt-thе first i spесiation; thе irnpoгtаn
Тhе Pаttеrn апd Рroсеss o| Spеciаtiсtп 1 9 . t lation is not always rеquirеd to ini_ ',еrаlwеll-doсumеntеdеxamplеs of rесеnt study providеs at lеast onе есiation via a host shift in a vеftеаrе host-spесifiсЬrood parasitеs, (genusLа goпОstiсtа), and diffеrеnt 3 diffеrеntspесiеs of firеfinсhеs. In. rеhost young and nrimiс thе mouth ,wеringthе proЬaЬility of Ьеing rе:ion to this uniqце mimiсry adaptaindigoЬirdsmimiс thе song that is ; rеarеd by a spесifiс host spесies of ligobirds that sing thеir natal host. tivе mating and lеads to rеproduсndigobirds that parasitizе diffеrеnt gеnеtiсstudy Ьy Мiсhaеl Sorеnson .сonrparеdmitoсhondriаl DNA sеo f i n d i g o b i r d sa n d t h е i г r е s p е с t i v е t i n d i g o Ь i r ds p е с i е st Ь a t p a r a s i t i z е liffеrеntiatеd from onе anothеr, a o f i n d i g о Ь i r d sr е a r е dЬ y а p а г t i с u ggеstthat divеrgеnсе through loсal adult malе song сopying, and fеypе hаs lеd tо positivе assortativе :сiеsof indigoЬirds.This pattеrn of 'sitivе assortativеmating within a spесiation in Afriсan indigoЬirds :iеsц.hоsеnеstsrhеy pаrаsiгizе. r вЕ RЕ|NFoRсED
asе thе amount of prеmating isolaly sеlесtingagainst hybrids formеd 'osеd Ьy Thеodosiцs Dobzhansky k Blair (1955),сan oссur in arеas of rtriс populаtionsсomе into сontaсt Ъrmеrly allopatriс populations arе rplеtеthе spесiatiоn proсеss. Rеin: modеrn synthеsisbесausе it allows tly, Ьut its еmpiriсal dеmonstration important сomponеnt of есologiсal > o r1 9 9 9 ;М a r s h a l l e t a | . 2 О 0 2 ) . t сomеs from сomparisons Ьеtwееn n thе strеngth of fеmalе mating
prеfеrеnсеsfor сoгlspесifiсs.For ехirmplе, fеmalеs dеrivеd from populations of Drosсlphilа 1lseudotlbsсt,lrasvrrrpatriсwith D . persimilis сlisplay grеatег rеluсtanсеto nlatе with hеtеrospесifiсmаlеs than do fеmalеs 1rorn aIlopatгiс populations(Noсlr 1995)' F1 hyЬrid malеs arе stегilе,Ьut hyЬrid fеmalеs arе fеrtilе,allowing fсlr gеnе ехсhangе and sеlесtionagainst hyЬrids. onе of thе Ьеst-doсumеntеdехirmplеsof rеinforсеmеntoссurs in thе Ьеnthiс and limnеtiс есOtYpеsfound in lakе populations of thе thгееspinеstiсklе_ b a с k . H o w а r d R u n d l е a n d D o l p h S с h l u t е r ( 1 9 9 8 ) d е m o n s t r а t е dЬ o t h i n laЬoratoryсrossеs аnd in F1 lrr.bridsdеtесtеd in wild populations that hyЬrids suffеr a foraging disadvаntagеrеlativе to thеir parеntal spесiеs in thе parеntalеnvirсlnmеnts.In thе laЬoratory F1 hybrids rеarеd in a сommon еnviгonmеntwith ar-rrplе aссеssto food showеd growth ratеs similar to thosе of paгеntalspесiеs.Howеvеr, in fiеld studiеs F1 h,vЬгidsrеarеd in еitlrегtypе of parеntalеnvirсlnmеnt,littoral :rnd limnеtiс zonеs of lakеs' had lowеr growth ratеsand wеrе smаller at maturity than еithеr purе parеntal spесies.HyЬrids Wеrеpoorеr at сatсhing Ьеnthiс invеrtеЬratеsand plankton in thе diffеrеnt fiеld еnvironmепtsЬесausеof intегmеdiatеgill-rakеr numЬеr and Ьody sizе. In аdditiсln, Ьеrrtlriсfеmаlеs from svmpatriс poptrlаtions wеrе rrruсh lеss likеly to mаtе rvith intеrmеdi:rtе-sizеd F1 hyЬrid mаlеs than rvеrе Ьеnthiс fеmalеs from allopatriс populatiсlns whеrе limnеtiсs did not oссur. Thеsе rеsultssupport a modеl of rеinforсеmеntof sizе-assortativеmating prеfеrеnсеs through natural sеlесtiсlnagainst intеrп-rеdiatе-sizеd hyЬrids that havе lower fitnеssin еithеr pаrеntаl environmеnt. How irrrpoгtanthas rеinf
196
The Pаttern аnd Prrlс.,еssсlf SDeсiаtiсlп
sЕxUAL sЕLEст|oN AND ЕсoLoG|сAL sPЕсlAт|oN Sеxual sеlесtion' a forсе that aсts on traits that inсrеasеmаting suссеss'сan Ье influеnсеd Ьy thе еnvironmеnt and' as suсh' miry сontriЬutе to есologiсal spесiation.Sеxuаl sеlесtionthat lеads to spесiаtionirs a rеsult of divеrgеntsеlесtion Ьеtwееn еnvironmеnts сiln rеsuit fronr spаtial vагiation in sесondaгy sеxual traits, suсh as сlinal variation in malе plumagе or сoloration in rеsponsе to a vaгying еnvironmеntal gradiеnt. For ехamplе, сlinal variation in thе availaЬility of foods high in сarotеnoids that lеаd to Ьright rеd and orangе сoloration in malе Ьirds has Ьееn suggеstеdas thе primary сausе for divеrgеnсе in plumagе among populаtions in malе lrousе finсhеs, Саrpodасus mехiсапus (Hill 1994). A rr-roс{еl that dеmonstratеsthе importanсе of pаrailеl сlinal variation in fеmаlе mаting prеfеrеnсеsas a геsult of еnvironmеntal variation in malе signаling traits was first proposеd Ьy Russеll Landе (1982), Ьut good ехamplеs of сlinal variation that lеads to spесiation via sеxual sеlесtion arе laсking. Natural sеlесtion through variation in fеaturеsof thе еnviгonmеnt whеrе mating signals arе propagаtеdсаn геsult in divеrgеntsеxual sеlесtionof malе mating signаls' suсh as сourtship displays or nuptial сoloration' lеading to prеmating isolation Ьеtwееn populations from divеrgеnt signaling еnvironmеnts (Ryan and Rand 199З; Boughman 2ОО2).Natural sеlесtion сan also aсt upon thе sеnsory systеm of fеrтalеsas wеll, lеаding to sеnsory Ьiasеsfor сеrtain propеrtiеsof mаlе signals (е.g',brightеr сoloration, largеr sizе, loudеr and longеr durаtion of voсаlizations). Partiсular fеaturеs of lосal еnvironmеntal сonditions сould altеr sensory Ьias or mаkе somе malе traits Ьеttеrat ехploiting biasеs in сеrtain еnvironmеnts than in othеrs. In addition, fеmalе mating prеfеrеnсеs for malе traits that arе indiсators of supеrior quality сan also Ье influеnсеd Ьy thе signaling еnvironmеnt' For еxamplе, if partiсular mаlе traits arе morе rеliаЬlе indiсatoгs of quality in somе еnvironmеntsthan in othеrs (Sсhlutеrand Priсе I99З), divеrgеnсеirr prеfеrеnсеsbеtwееn еnvironmеnts for thеsеmalе traits сould lеad to prеmating rеproduсtive isolation Ьеtwееn thеm. Thus diffеrеnt сoеvolutionary paths of signals аnd prеfеrеnсеs in diffеrеnt еnvironmеnts сould Е]еnеratеspесiatiorl. Thе Ьеst еxamplеs of an importirnt rolе for sехual sеlесtionin prolnoting spесiation as а rеsult of varying signaling еnvironпrеIrtsсomе from spесiеs that livе in environmеnts that vary in light irrtеnsiryor transmission propеrtiеs that influеnсеthе spесtral quality of signals (i.е.'whiсh сolors irrе Ьеst rеflесtеd Ьy partiсular еnvironmеnts).For еxamplе, allopatriс populations of Aпolis cristаtеllцs lizards oссur in two diffеrеnt еnvironmеnts (хеriс and mеsiс) that diffеr with rеspесt to light intеnsity and thе spесtral quality of сolors thаt аrе Ьеst геflесtеd.Маnuеl Lеаl and Lеo Flеishman (2004) havе shown thаt malе anolеs frorrr thе two еnvironпrеnts diffеr in thе сolor and pattеrn of thеir dеwlaps (folds of skin undеr thе throat that arе distеndеdin malе displays usеd aS tеfritorial аnd mating signals)in thе dirесtion that inсrеasеssignаl dеtесtaЬilityin еaсh haЬitat. Мalеs fгom thе xеriс еnvironmеnt havе darkеr and slightly rеddеr dеwlaps that mахiпrizе сontrаst whеrе thе
Ьaсkgrсlund radianсе i ovеrall Ьrightnеss of tJ m е n t h i r v ее v t l l v е dЬ r i аnd tгallsmissiun аt а| hаЬitats'whеrе thе Ьa i n d е w l . r ps i g n a l sw l l u wirlr tlrеWrongdеw|.r and hеrrсеlеss likеly tс
тHЕ RoLЕ oF s NoNЕсoLoG|с
М o d е l s t r f s е х u a Is е | с mating prеfеrеnсеsfor u [ а r i o n sс а n d i v е г g еl l and spесiation. Supеrf s p е с i e t i с l l l .е х с е p t t h i t m а l е n l а t i n g ,s i g n l r l sr h p r o p е r г i е st o t h е s i g n l I p r o m < l г е dг h r t ' u g hd i v t onе modеl of fеma runаWaу proсеss (or .. F i s h е r i а n p Г o с е s s е sa r с tlrе tttсlstеxгrеmе rtr.tl p а r а J i s еo r t h е Ь г i g h r tion of thеsе traits аris that еnсodе thе attraсt foг that tгeit. FisЬеr.s a n d t h с г еi s а Ь u n d a n tt promoting thе еvolr.rti 1994); howеvеr, studiе сult to pinpoint. Onе span length in stalk-е Gеrald Wilkinson and wild fliеs' a slrort-еyеo Г s е l е с г i o n .t h е y f o L r n a I l y s е I е с t е dm a | е t r e i t from thе linе sеlесtеdf with short еyе spans' . prеfеrrес1malеs with lс е r е n с е s i o r е у е - s p a nl t s t a l k - е y е df l i е s t h e t d i Г S е x u а l s е l е с r i о nm l g е п е s \ .U n d е г t h i s m o d fеmalе lvith informatiсl mаkе mating dесision
Thе Раttеrп апd Prrlссssrlf S1lесiаtiсltt 1 9 7 oG|сAL sPЕс|Aт|oN ts that inсrеasеmating suссеss'сan suсh, mаy сontribr.rtеto есologiсal pесiationas a rеsult of divеrgеnt sеfrom spatial variation in sесondary m a | еp l u m a g еo r с o I o г а t i o n i n r е )nt.For ехаtrrplе,сlinal vaгiаtion in lids that lеad to Ьright rеd and orggеstеdаs thе primary сausе for diin malе housе finсhеs, Саrpodасus ionstratеsthе importanсе of parallеl еnсеs as a rеsult of еnvironmеntal proposеdby Russеll Landе (|982)' at lеads to spесiation via sеxual sеfеaturеsof thе еnvironmеnt whеrе in divегgеntsехual sеlесtionof malе ys or nuptial сoiorаtion, lеading to s from divеrgеntsignаling еnvirono 2002\. Natural sеlесtion сan also s wеll, lеading to sеnsory Ьiasеs for ightеrсoloration,largеr sizе, loudеr 'artiсillaг fеаturеs of loсal еnvirons or mаkе somе malе traits Ьеttеr at i than in othеrs.In addition, fеmalе ге indiсatorsof supеrior quality сan :onmеnt.For ехamplе' if partiсular f quality irr somе еnvironmеnts than rgеnсеin prеfеrеnсеsЬеtwееn еnvito prеmating rеproduсtivе isolation lary pathsof signalsand prеferеnсеs spесiation. I е f o r s е х t r a sl е l е с t i o ni n p r o m o t i n g tg еnvironmеntsсomе from spесiеs h t i n r е n s i r yo r t r a n s t n i s s i o np г o p е r ;ignals(i.е.,whiсh сolors arе bеst fееxamplе,allopatriс populations of diffеrеnt еnvironmеnts (хеriс and ntеnsityand thе spесtral quality of еal and Lеo Flеishman (2004) havе nvironmеnts diffеr in thе сolor and rdеr thе throat that arе distеndеd in ing signаls)in thе dirесtion that int . М а l е sf r о m t h е x е r i с е n v i r o n m е t r t ; thаt maхimizе сontrast whеrе thе
baсkgroundradianсе is rеlаtivеlу high (i.е.,thеy will appе?1гdarkеr than thе ovеrаllЬrightnеssof thе Ьaсkgrоund), whilе rтalеs from thе mеsiс еnvtrtlnmеnthavе еvolvеd Ьright dеwlaps Ьесausеof thеir rеlativеly higЬ геflесtanсе and transmissionаt all wavеlеrrgths.Suсh mаlеs arе morе dеtесtaЬlеin mеsiс hаЬitats,whеrе thе bасkgrounсl haЬitat light lеvеls arе low. Tlris divеrgеnсе in dеwlap signalswould minimizе gеnе fltlw ЬеtwееnhaЬitats, Ьесausеmalеs with thе Wrong dеwlaр сolor pattеrn would Ье lеss dеtесtаЬlеЬ,vсonspесifiсs and hеnсеlеss likеlу t() sесurеa tеггitory or oЬtаin nlаtings. тHЕ RoLЕ oF sЕxUAL sЕLEст|oN IN NoNЕсoLoG|сAL sPЕс|Aт|oN Modеls of sехu;rl sеlесtion, partiсtrlarly mtldеls of thе еvollttioll сlf fеmаlе matingprеfеrеnсеsf
198
Тhе Pаttеrп апd Proсеss of Spесiаtioп supеrior quality to hеr offspring. Although this mесhanism may potеntially lеad to spесiation if thе indiсator traits diffеr Ьеtwееnpopulations, likе runaway sеlесtion,еmpiriсal еxamplеs arе rarе. Somе еvidеnсе indiсatеs that a good.gеnеs mесhanism may promotе diffеrеnсеs in mаlе gеnitalia that lеad to divеrgеnсе in somе insесt taхa, although this hypothеsis is still undеr dеЬаtе (Нoskеn and Stoсkleу 2004).It should Ье notеd that for Ьoth indiсatоr and Fishеrian traits' thе laсk of сonсlusivе еmpiriсal еvidеnсеdoеs not mеаn that divеrgеnсеis unlikеly to Ье a produсt of thеsе mесhanisms;rathеr, it is oftеn diffiсult to distinguish whiсh mесhanism may hаvе opеrаtеd in thе past. An additional rolе of sехual sеlесtionin spесiationсan Ье traсеd to undеrstanding thе mесhanisms assoсiatеd with sехual сonfliсt. Sехual сonfliсt arisеs whеn thе Ьеst stratеgy for сlnе sеx is diffеrеnt (or еvеn dеtrimеntal) сomparеd with thе Ьеst strаtеgy in thе othеr sех. This antagonism is prеdiсtеd to lеad to a сoеvolutionary arms raсе whеrе diffеring sеts of traits Ьеtwееn thе sехеs intеraсt to dеtеrminе thе naturе of malе-fеmalе intеraсtions (Arnqvist and Rowе 2005). An ехamplе of within-spесiеssехual сonfliсt is thе еffесts of sеminаl fluid in Drosopbilа melаnogаstеr. Sеminal fluid has Ьееn shown to Ье Ьеnеfiсial to malе fitnеss' rеduсing fеmalе rеmating and inсrеasing ovulation, Ьut it is toхiс to fеmalеs; thе morе sеminal fluid thеy rесеivе, thе fastеr thеy diе. Sехual сonfliсt appеarsto oссur aсross a widе rangе of taxa (Arnqvist and Rowе 2005), Ьut prеdiсtaЬly,somе of thе Ьеst еvidеnсе for a гo1еof sехual сonfliсt in spесiation сomеs from insесts (Arnqvist еt al. 2000). Bесausе sехual сonfliсt may lеad to rapid еvolutiоn in thе rеproduсtivе traсt, it follows that it may also inсrеasеthе paсе of rеproduсtivе isolation Ьеtwееnpopulations. sЕXUAL sЕLЕст|oN' lsoLAт|oN' AND RAтЕs oF sPЕсlAтloN Sехual sеlесtion,Ьесausеof its rolе Ьoth in promoting thе еvolution of prе. mating rеproduсtivе isolating Ьarriеrs and in сontinuеd divеrgеnсе Ьеtwееn spесiеs,may havе а сonsidеraЬ1еimpaсt on thе ratе of spесiation (rеviеwеd by Panhuis еt al. 2001). For еxamplе, taхa with a widе rangе of sеnsory pеrсеption сapaЬilitiеs may bе partiсularly pronе to spесiation through sеxual sеlесtion, sinсе thеy havе аn еlеvatеd aЬility to produсе or dеtесt a Ьroad rangе оf signals, Ье thеy visuаl' aсoustiс, or phеromonal (Andеrsson 1994). Spесiеs-riсh groups оf frogs' for instanсе, сan dеtесt a widеr rangе of advеrtisеmеnt-сall frеquеnсiеs than thosе in lеss spесiosе linеagеs, potеntially aссounting for why suсh linеagеs of frogs arе morе spесiosе сomparеd with thosе with narrowеr frеquеnсy pеrсеption rangеs (Ryan 1986). In addition, rеinforсеmеnt,as dеsсriЬеdеarliеr, сan сomplеtе thе spесiationproсеss upon sесondary сontaсt Ьy еnhanсing divеrgеnсе of fеmalе mating prеfеrеnсеs. Sеxual sеlесtionplays an important rolе in sympatriс spесiation as wеll. Assortativе matin8' thе propеnsity to matе with likе individuals, hаs Ьееn proposеd аs onе way to quiсkly еvolvе rеproduсtivе isolation (Ссlynе and orr 2004) and is a nесеssaryсomponеnt of thе sympatriс spесiation proсеss.
Sеxual sеlесtion has Ьt part Ьесausе of its dirес 2 0 0 1 ) . S p е с i е so f Ь i r d s r thought to еxpеriеnсе st monogamous linеagеs;tJ spесiosе (Mitra et a|. 199 r a t е si of high sPесiаtioI1
pаrisonsof diсhromаri with fеmalеs dull) сladеs usually Ьright) сladеs (l
amountS of fеаthеrornar havе Ьееn oЬsеrvеd in an and othеr invеrtеЬratеs е t a l . 2 0 0 1 ) . A r е с е n tе x rеsult оf sехual sеlесtio Lаupаlа. Tamrа Mеndеl spесiеs at molесular mar tivе agеs of thе diffеrеnt i n o n е с l а d е o f t h е s ес r i с spесiеs pеr million yеars сiation in this group app song trill ratе, whiсh fеп appеar to Ье any есolog сriсkеt spесiеs.Thеsе aг tion сan Ье an importаn Prеmating isolating baгr
тHЕ RoLЕ oF Ml
Mutаtional сhangеsass thought to Ье a primar rWhitе (7978, 336) сonсl thе primary rolе in thс widеsprеad rolе of kaгy сausе thе aссumulation t h t t u g h t t о h е l a r g , е l уi r problеm with thе viеw tion сеntеrs on thе diffiс lations rеасhing fiхatto аltеrnativе rеarrangеm Ьrids, thеrеЬy rеduсing mosomаl rеarrangеmе ехtrеmе сhromosomal r
in сhangеs in сlrromos сhromosсrmal rеarrang arе inеffесtivе Ьаrriеrs1
Tllе Раttеrn апd Process of Spесiаtioп gh this mесhanisnrmay potеntially .ffеrЬеtwееnpopulations, likе runrrе. Somе еvidеnсе indiсatеs that a fеrеnсеsin malе gеnitаlia that lеad gh this hypothеsisis still undеr dеrld Ье notеd that for Ьoth indiсator е еmpiriсalеvidеnсеdoеs not mеan ;t of thеsеmесhanisms:rathеr. it is nisrrrmay havе opеratеd in tlrе past. r spесiаtionсan Ье traсеd to undеrth sехr'rаlсonfliсt. Sехual сonfliсt к is diffеrеnt(or еvеn dеtrimеntLrl) o r h е r s е х . T h i s . r n t а g o n i s mi s p r е lсе wlrеrе diffеring sеts of traits Ье. n a t u r еo f m а l е - f е m а l еi n t е r a с t i o n s of within.spесiеssеxual сonfliсt is lа mеlапсlgаsler.Sеminal fluid has s, rеduсingfеmalе rеmating and inrlеs;thе morе sеminal fluid thеy rеp p е а r st o O с с u ra с r o s sa w i d е r a n g е 'еdiсtaЬly, somе of thе Ьеst еvidеnсе сoпrеsfrom insесts (Arnqvist еt al. to rapid еvolution in thе rеproduсеasеtI]еpaсе of rеpгoduсtivе isola-
Sехuаl sеlесtiorrhas Ьееn linkеd tсl rеlativеly higlr rаtеs of spесiation, in part Ьесausе of its dirесt еffесt on matе rесognition traits (Panlruis еt al. 200l). Spесiеs of Ьirds with highеr lеvеls of promisсuity, for ехamplе, arе thouglrt to ехpеriеnсе strongеr sехual sс.lесtionthan сlosеly rеlatеd, morе moпogamous linеagеs;thеsе promisсuolls linеagеs gеnеrally arе also morе spесiosе(Мitra et al'.1'996).othеr studiеs of Ьirds сoпform to thе prеdiсtion of high spесiation ratеs in taхa with strong sеxual sеlесtion,inсluding сomparisons of diсlrromatiс (sехеs of diffеrеnt сolors; nralеs gеnеrally Ьright, with fеmalеsdLrll)сladеs vеrsus monoсhromatiс (Ьotlr sехеs thе samе сolor' usually Ьright) сladеs (Bаrraсlough еt аl. 1995) and сladеs with vaгying amountsof fеаtЬеrornamеntation (Мollеr and Сuеrvo 1'998).Similar trеnds havе Ьееn oЬsеrr,еdin angiospеrnrs(аnd thеir assoсiatеdpollinatoгs),insесts аnd othеr invеrtеЬratеs,arrd fishеs (rеviеwеd in Andеrsson |9941 Pаnhuis е t a l . 2 0 0 1 ) . A r е с е n tе x a m p l е h i g h l i g h t i n gt h е r a p i d r a t е o f s p е с i a t i o na s а rеsrrltof sехual sеlесtion hаs bееn shown in Hawaiiаn сriсkеts in thе gеnus Lаupаlа. Tamra Jv{еndеlsonand Kеrry Shaw (200.5)usеd divеrgеnсеamong spесiеsat rnоlесularmarkеrs саliЬratеd with gеologiсаl еstimаtеsof thе rеlativе agеsof thе diffеrеnt Hawaiian islands to show thаt thе ratе of spесiation in onе сlаdе of thеsесriсkеts from а singlе islаnd was сalсulatеd at ovеr four spесiеspеr million yеars,thе highеst ratе еvеr сalсulаtеd for arthropods. Spесiatioп iп tlris group appеars t
{, тHE RoLЕ oF MUтAт|oN lN sPЕс|Aт|oN in promoting thе еvolution of prе_ rd in сontinuеd divеrgеnсе Ьеtwееn on thе ratе of spесiation (rеviеwed :a with a widе rangе of sеnsory Pеrpronе to spесiationthrough sехual lility to produсе or dеtесt a Ьгoad , or phеromonal (Andеrsson 1'994). nсе' сan dеtесt a widеr rаngе of in lеssspесiosеlinеagеs,potеntiаlly 's arе morе spесiosе сomparеd with ln rangеs(Ryan 1986). In addition, эmplеtеthе spесiationproсеss upon :nсе of fеmalе mating prеfеrеnсеs. in sympatriсspесiation as wеll. Aswith likе individuаls, has Ьееn pro:oduсtivеisolation (Сoynе and orr 1еsymPatгiсspесiation pfoсеss.
Мutаtional сlrerngеs assoсiatеdwith сhromosomal rеarrangеmеntswеrе onсе thought to Ье а primary nrесhanism of spесiation. For ехamplе, М. .}. D. whitе (1978, 336) сonсludеd that сhromсrsomalrеarrаngеmеntshаvе ..playеd thе pгimary rolе in thе majоritv of spесiatiсln еvеnts..'Мorе rесеntly thе ш,idеsprеad rolе of karyot,vpiссhangе in spесiatiorrlras Ьееn qtlеstionеd,Ье. саusеthе aссurnulation of сhromosomаl diffеrеnсеsЬеtwееn populations is thought to Ье largеly inсidеntal to spесiation (Sitеs and Мoritz 1987). The proЬlеm with tЬе viеw that сhromosomal rеarrangеmеntspromotе spесiatiсlnсеntеrson thе diffiсulty оf аltеrnzrtivеrеаrrangеmеntsin divеrging populаtionsrеaсhirrgfiхation. All modеls of сhromosomаl spесiation assumе that altеrnativеrеarrangеmеnts impair thе fеrtility or viaЬility of intеrspесifiс hyЬrids,thеrеЬуrеduсing gеnе flow and promoting fiхation of altеrnаtivесhro. mosomal rеаrrаngепlеrrts.Although tlris nrаy iikеh' Ье truе in ехапrples of ехtrеmесhroпrсlsomalrеаrratrgеmеnts(suсh as lтutational еvеnts that rеsult in сhangеsin сl.rromosomеnumЬеr)' а numbеr of studiеs havе shown that сhгomosomalrеarrangеmеntsOftеn hаvе littlе еffесt on fеrtility аnd hеnсе arе irrеffесtivеЬaггiеrstO gеl1еflow (Spiгito |998),
199
200 Tbe Pаttеrп апd Proсеss of Spесiаtioп Lorеn RiеsеЬеrg and сollеaguеs havе studiеd rесomЬinational spесiation in sunflowеrs (Heliапtbus spp.) and thе еffесts of сhromosomal rеarrangеmеnts in сontгiЬuting to thе spесiation proсеss.RесomЬinational spесiation oссurs whеn two diploid spесiеs intеrbrееd and givе risе to a nеw linеagе that is both fеrtilе and truе Ьrееding br.rt is rеproduсtivеly isolatеd from both parеntal spесiеs.RiеsеЬеrg (2001) arguеs that сhromosomal rеarrangеmеnts that arе hеtеrozygous in hyЬrids havе majоr еffесts on supprеssing rесomЬi. nation Ьеtwееn сhromosomеs that сaггy thе rеarrangеd sеgmеntsand gеnеs linkеd to thеsе sеgmеntson thе сhromosomеs. Gеnеs unlinkеd ro thе сhгomosomal rеarrangеmеnt sеgmеnts,еspесially those that arе nеutral' frееly introgrеss Ьеtwееn the hyЬridizing parеnt,al spесiеs. Rеarrangеmеnts that supprеss rесombination Ьut laсk a сausal еffесt on hyЬrid fitnеss сould aсt synеrgistiсally with linkеd isolation gеnеs to еxtеnd thеir еffесts ovеr a largеr gеnomiс rеgion. Thus сhromosomаl rеarrallgеmеntsproЬaЬly do play an im. portant rolе in rеduсing gеnе flow aсross spесiеs Ьаrriеrs, Ьut not Irесеssarily through thе mесhanisms of rеduсеd hybrid fitnеss traditionally еnvisionеd. Thе hyЬrid sunflower spесiеs H' апomаlus, whiсh rеsults from hyЬridization Ьеtwееn H. аппuцs and I.I' petiolаris, is thought to havе arisеn in suсh а mannеr. In аddition, H. апomаlus has highеr fitnеss in novеl еnvironmеnts whеrе Ьoth of its parеntal spесiеs pгogеnitors do poorly. Suсh аn adaptivе rolе for hyЬridization in fostеring spесiation has bееn suggеstеdfor a numЬеr of plant and somе animal spесiеs (Arnold 19971Dow|tng and Secot 1997). sPЕсlAтloN
вY PoLYPLolDY
Polyploidization oссurs through thе dupliсation of еntirе sеts of сhromosomеs and is onе of thе fеw mесhanismsthat сan produсе instantanеousspесiation (polyploid spесiеsarе rеproduсtivеly inсompatiЬlе with thеir diploid progеnitors). Polyploid spесiеs arе formеd еithеr tЬrough gеnomе dupliсation of a singlе diploid spесiеs(autopolyploidy)or through thе fusion of two or morе diploid gеnomеs as a rеsult of intеrspесifiс hyЬridization (allopolyploidy). Both mесhanisms of pоlyploidy arе сommon in fеrns' mossеs,algaе, and virtually all groups of vasсulaг plants, partiсularly angiospеrms (StеЬЬins 1950;Lеvin 2002). How polyploid spесiеsЬесonrееstаЬlishеdis not fully undеrstood.Sеvеral сonditions, partiсulaгly сommon in plants, might еnaЬlе a nеw polyploid to inсrеasе and form a viaЬlе population. Thеsе inсludе sеlf.fеrtilization' vеgе. tativе propagation' highеr fitnеss than thе diploid progеnitor spесiеs, or niсhе sеparation from thе diploid progеnitor spесiеs'Indееd,many polyploid taxа rеproduсе Ьy sеlfing or vеgеtultivеpropagation, аnd most diffеr from thеir diploid progеnitors in haЬitat and distriЬution. lnсrеasеsin ploidy altеr сell sizе, watеr сontеnt ratе' ratе of dеvеlopmеnt, and many othеr physiologiсal propеrtiеs' so many polyploids may havе sеlесtivеadvantagеSin nеw есologiсаl niсhеs imnrеdiatеlyupon thеir origin. An цnusual сasе of polyploid spесiation in animals oссurs in thе gгay rrее frog spесiеsсomplеx found throughout thе еastеrn Unitеd Statеs.Thе сomplеx
сontаirrs а diploid spе spесiеs Hуlа uersiсolor lopiltгy (H. сhrуsosсelis northегl.l lralf), Ьut thеy tlrеir rarrgеsovеrlap. Di1 produсtivеly isolаtеd frt nаl diffеrеnсеs) and pс intеrЬrееding. Мalеs pl ratеs, with thе diрlkt.Us mitoсhondrial gеnе rеgr this study showеd thirt а г r i Ь u г е dt o m t r l r i p l еo r i g , 8). Two of thе thrее dip suggеstеd Ьy thе oссurrе not in thе iiving diplс t е t r а р l l l i d sa r o \ е t h r ( ) u diffеrеnt diplсlid аnсеsto аrсlsе from diffеrеnt dip sympаtry. Bесаusеthе dl latеd from onе antlthеr,, u с r s iс tl l t , r . P о l у p l t ' i di z . r t sisсеntсharrgеin thе аdv сеll sizе, whiсh hаs Ьееn сially prodцсеd аutotrip сhаngеs in trill ratе аs a r til.ltlitу Ьеtwееn lirrеаgеs rеinftlrсеd tri Il-reltеdiffеl grаy trее frogs illustratе aгisе аnd furthег shows mеnt саlls, сan Ье сlirесt
тHЕ RoLЕ oF GЕ
Irr thеory, gеnеriс drift outward from thе еdgе whеn a small nulrlЬеr tl] а nеw popr-rizrtiсlr-r. Irrpr: foгmatiсrn сrf rrеw spесt
Thе Pаttеrп аnd Procеss of Spесiаtion rdiеdrесomЬinationalspесiation in ts of сhronrosomаl rеarrangеmеnts R е с o m Ь i n а t i o n аslp е с i a r i o no с с u r s givе risе to a nеW linеagе that is еproduсtivеly isolatеd frоm Ьoth that сhromosomal rеarrangеmеnts jor еffесtson supprеssing rесomЬithе rеarrarrgеdsеgmеnts аnd gеnеs omеs.Gеnеs unlinkеd to thе сhгorlly thosеthat arе nеutral, frееly in. Ltal spесiеs. Rеarrangеmеnts that l еffесt on hyЬrid fitnеss сould aсt to еxtеnd thеir еffесts ovеr а largеr angеmеntsproЬaЬly do play an imspесiеsЬarriеrs'Ьut not nесеssariIy rid fitnеsstraditionally еrrvisionеd. s, whiсh rеsultsfrom hyЬridization thought to havе arisеn in suсh a i g h е rf i t n е s si n n o v е l е n v i r o n m е n t s ritors do poorly. Sцсh an аdaptivе on has Ьееnsuggеstеdfor а numЬеr 1 9 9 7 ;D o w l i n g a n d S е с o r t 9 9 7 ) '
lliсation of еntirе sеts of сhromo. hat сan pгoduсеinstantanеousspееly inсonrpariЬlеwith thеir diploid эd еithег through gеnomе dupliсa,loidy)oг thrоugh thе fusion of two rtеrspесifiсhyЬridization (аllopolytrесommon in fеrns, mossеs, algaе, .ts,partiсularly angiоspеrms (Stеbhеd is not fully undеrstood. Sеvеral s, might еnаblе a nеw polyploid to h е s еi n с l u d еs е l f - f е r t i l i z a t i o nv,е g е . t h е d i p l o i d p r o g е n i t o r s p е с i е s ,o r toг spесiеs.Indееd,many polyploid propаgation' and most diffег from istribution'Inсrеasеsin ploidy altеr )pmеnt'and many othеr physiolog'havе sеlесtivеadvantаgеs in nеw origin. n in animals oссurs in thе gray trее ) еastеrnUnitеd Statеs.Thе сomplех
сontains a diplкliсl spесiеs, Hуlа сhrу51lsсеlis(2N=24) and a tеtraplоid spесiеsНуlа uеrsicolor (4N=48). Both spесiеs oссupy laгgе rеgions of al. l o p a t r y( I J . с h r l s o s с e l i s i n t h е s o u t h е r n h a l fo f t h е r a n g е ,H . u e r s i с o l o r i r r t h е northеrn half), Ьut thеy also ехist irr Sympatry in multiplе loсalitiеs whеrе thеir rаngеs ovеrlap. Diploids and tеtraploids rеproduсе sехually and arе rеproduсtivеlyisoIatеdfrom сlnе anothеr through Ьoth prеmating (mаting signal diffеrеnсеs)аnd postmating (tгiploid hyЬrids arе stеrilе) Ьarriеrs to intеrЬrееding.Malеs produсе advегtisеrтеntсalls thаt diffеr in thеir trill ratеs,rvith thе сliploid H. cЬr\,sсlsсеlЬаlrvays produсing сillls with fastеr trill ratеsthan tlrоsе of the tеtraploid H. uеrsiссllсlr(Gеrh:rrdt2005). Studiеs Ьy Сarl Gеrhardt аnd сollеaguеshavе shown that fеmalеs of Ьoth diploids and tеtraploids arе highly sеlесtivе (еsресially in sympatriс populations) whеn еvaluatingсall сharaсtеristiсsof malе advеrtisеmеntсalls, strongly disсriminatingagainst саlls with thе trill rate of thе ..wrong'' spесiеs. A rесеntstudy Ь,vAliсia Hollowаy аnd сollеаguеs(Hollowау еt al. 2006) has dеmonstratес] аn unusuаl pattеrn of p
201
202
t: tЕ
The Pаttеrп апd Process of Spесiаtion
Е Е
H, avivoсa
Еxtinоt |iyla sp.А (2N)NЕ
Figurе 8. A modеl of tеtraploidoriginsfrom diploid anсеstorsillustratеsmultiplе allopolyploid origins for thе gray trее frog Hуlа uersiсolor.Thе rеlationshipsof diploid gray trее frogs аnd a rеlаtеd spесiеs,H. аuiuoса,arе dеpiсtеdat thе Ьotto- of thе trее. Ехtinсt diploids (2N), l-/. sp. A and H. sp. B, wеrе infеrrеd from tеtraploid аllеlе linеagеs.Tеtraploid gray tгее frogs, H. uersiсolor (4N), wеrе formеd multiplеtimеs from еxtinсtdiploid anсеstors(AxB, AхС' and B x С). Tеtrаploid gray trее frogs from diffеrеntlinеagеs(е.g.,NЕ, NW) arе intеrfеrtilеand thus form a singlе Ьiologiсal spесiеsthаt sharеsa divеrsеgеnе pool of multiplеanсеstrаlprogеnitorspесiеs.(From Holloway еt аl. 2006.)
Ьy gеnеtiс drift. Thе idеa of fouпder-effeсt spесiаtioп (Figurе 4) was hrst proposеo o'y йnsт йЬyr 1i-У}.+i,Ьt6..;retrnеu'pz?rijъtri "if.tсittiлt1\.ltl "r';ъ. Ьasеd on his oЬsеrvation that in manу Ьirds and mammals, populations pеriphеral to thе distribution of a proЬablе..parеnt'' spесiеswеrе oftеn highly divеrgеnt,to thе point of Ьеing сlassifiеdas diffеrеnt spесiеs.Maуr proposеd that gеnеtiс сhangе would Ье vеry rapid in suсh loсalizеd founding populations
Ьесausе of random fiхat of anсеstral сoadaptеd 1 would lеad tо thе potеrsеts of gеnеs in thе nеr сould inсidеntally yiеld for rapid spесiation. Al p г o Ь а Ь | уd t l o с с u r i n f t t jor gеnе rеorganization son (1975) and Alan Tе onе potеntial еxamp drift, howеvеr, сomеs f: tion of shеlls) Ьеtwееn gеnus Еuhаdrа' TЬese :
Ь е t w е е nt h е m . С h i r а l i г with dехtral (right-han handеd) сoiling. Bесau (thеsе snails аrе hеrma f i х е d f o r o p p o s i r ес o i l i n lаtеd from onе anothеr positе сoiling typеs arе l gеnеtiс drift is likеly tс typеs аm()ng pllpulаtr drift is thе most plaus сhirаlity (vаn BatеrrЬu of at lеast four indеpеn through phylogеnеtiс (Uеshima and Asami 2
Consеquеnсеsof s
Thе Ьulk of this еssayh mесhanisms Ьy whiсh t sultеd in thе еnormous unсovеrеd in thе foss сhallеnging;hеnсеmot plеs. Although mrrсh d as illustratеd Ьy thе fс
onе spесiеs into anotht vеrsifiсation and spесt ologists gеnеrally agrе ditzеrgеnсеtоdav amo s p o n s i Ь l еf o г s p е с i e t i Thе tеmpo of spес groups' suсh as horsс for ovеr 1.50 million
.l'hе
Еxtinоt yla sp.A 2N)NЕ
diploidаnсеstorsillustratеsmLrltiplе |уlаuеrsiсolor.Thе rеlationshipsof H. аuiuoса,arе dеpiсtеdat thе ' sp.A and H. sp. B' wеrе infеrrеd ay trееfrсlgs,H. uersiсolor (4N), loid arrсеstors(A x B, A x С, arrd еntlinеаgеs(е.g.,NЕ, NW) arе spесiеsthat sharеsa divеrsеgеnе . (FromHollowаy еt al. 2006.)
' spеciаtion(Figurе4) was first рroed pеripаtriс spесiаtioп) and was rds and mаmmals, populations pе..parеnt'' spесiеs wеrе oftеn highly rs diffегеntspесiеs.N4ayr proposеd populations suсhloсаlizеdfoundir-rg
Pаttеrп апr] Prсlсеsso|.Spесiаtiсltt 20.з
bесausеof rarrс]omfixаtitrrr
Соnsеquеnсеsof Spесiation Thе Ьulk of this еssayhas foсr"rsеd on ехamplеsof living spесiеsand thе veгioLts mесlranismsЬy lvlriсh thеу arе thought tсl lravе spесiаtес.l. Yеt spесiatifspесiаtion аs illustratеd Ьy thе fossil rесord (phуlеriс gгаduirlisnl, tlrе slсlrv trаr-rsitiorr of onе spесiеsinto anothеr' vеrsuspunсtuatеdеqr'riliЬriurrr' rapid еvolutionarydivеrsifiсationand spесiationfollowеd Ьy long pеriods of stasis),еvolutionar,vЬiologistsgеnеrallvagrее that thе samе еvolr'rtionaryпlесhanismsthat proпrotе divеrgеr-rсe todа1,аnrong populаtitlnsof living spесiеs(nriсroеvt>lutiolr) аrе rе_ sponsiЬlеfсlr sресiationеvеnts(mасroеvtllution),Ьotlr сlngoingar-rdin thе past. Thе tеmpo of spесiation vaгiеs dramiltiсally among diffеrеnt taхa. Somе groups'suсh as hоrsеshoесraЬs (gеnus l-imulus), havе rеmаinеd unсhangсd for ovеr l 50 million vеars, w,hilе othеrs' sr'lсЬаs Hаr'r.аiianсriсkеts (gеnus
TЬe Pаttеrn апd Proсеss of Spесiаtioп Lаupаlа), havе spесiatеd rapidly, with up to 4.17 spесiеs pеr million yеars (Меndеlson and Shaw 2005). Thus spесiation сan oссur quiсkly or slowly, undеr а variеty of есologiсаl сonditions, and with or without thе еvolution of rеproсiuсtivе isolation. Unravеling thе mystеriеs of how nеw spесiеs arisе is onе of thе nrost еxсiting аrеas of еvolutionarу Ьiology' and although wе havе madе muсh progrеss in undеrstanding spесiation sinсе William Batеson's еarly сonсеrns, futurе studiеs promisе to yiеld еvеn morе nеw and fasсinating disсovеriеs. Thе hopе of thе futurе, in prеsеrving and protесting our plaпеt's Ьiodivеrsity, liеs in an r.rndеrstanding of thе proсеss of speсiation and а сommitmеnt
to saving thе produсts of this proсеss: thе spесiеs that ехist on еаrth today and thosе that hаvе yеt to еvoivе in thе ftrtr-rrе.
вlBL|oGRAPHY Andеrsson' IvI. 7994. Sехuаl Sеlесtioп. Prinсеton, NJ: Pгinсеton Univеrsity Рrеss. Arnold, М. L. 1997. Nаturаl Hуbridizаtiсlп апd Еuolиtiсlп. Nеw York: Oхford Univеrsity Prеss. Arnqvist, G., М. Еdvardssоn,LI. FriЬеrg, аnd T. Nilsson. 2000. Sеxual сonfliсt promotеs sресiation in insесts. Prосееdiпgs of thе NtttiсlttаlАcаdеmу сlf Sсiепсеs USА 97: 10460-10464. Arr-rqvist,G., and С. Rowе' 2005. SехнаI Сoпfliсt. Pгinсеtоn,NJ: Pril-rсеton Univеrsity Prеss. Bаrrасlough, Т. G.' P. H. Haгvеy, аnd S. Nее. 1995. Sехual sеlесtionand tахonotntс divеrsity in passеrinе Ьirds. Proсееdiпgs of thе Rol,аl Stlсiеtу of Loпdсlп, Sеriеs B 259: 211-215. Bаtеson,'w.1922. Еvolutionary faith and modеrn douЬts. Sсiепcе55: 5.5_61. Blair' W. F. 1955. Мating сall аnd stagе сlf spесiаtion in tllе Мiсrobуlа сlliuасеа_ М. саroliпепsls сomplех. Еuolиtkln 9: 469480. Boughman, J. .iи. 2002. How sеnsоry drivе сan promotе s1-lесiirtion. 7,rепdsiп Есоlogу апd Еuoluti
Г)iаz, A., and M. R. Масnаrr' p r е z r . g tilсt r е p r o d u с r i v еi p г . l g е r l i t o rМ . g u t t а t u s .i DoЬzhаnsk,v,T, 1937. Gепеt LIr-rivегsitуPrеss. l 946. (ioп.rplеtегt'pr spесiеs сlf Drostphilа. Е Dowlir'rg,Т. Е., апd С. l,. Sес in thе divеrsifiс:rtiol.ttlf : 28 59З_61'9. F е d е г , . | .L , | 9 9 8 . T h е a p p l el сOnvеntionalwisdom aЬ еds., Еlld/ess Fсlrnts:Sрс Urrivеrsit,vPrеss. Fishеr,R. A. l930. Thс С,еt Prеss' F u t r t v п t а ,D . J . , J . S . W а l s h T G с n е t i с v l r i l r t r с l litr l l t p l Ьееtlеs(Cоlеoptеrа:СJh F l ч ' l u Ii , l п а D , B i , ' l ' ' д 1 ' : Gеrhаrdt, Н. С. 2005. Aсlvе (H1'lа сhrуsсlsссlis tэ,ndL еvolution of сoпrmutrtс G г a n t , P . B . ' B . R . G r а n t , . | .J Darwin's finсhсs: p
Tlэе Pаttеrп апd Рroсеss of Spесiаtioп
p to 4.17 sPесiеspег million yеars latlon сan oссur quiсkly or slowly' 'nd with or Without thе еvolution of ) е с i е sa г i s еi s о n е o f t h е m o s t е х с i t lough wе havе madе muсh progrеss m Batеson'sеarly сonсеrns' futurе rd fasсinatingdisсovеriеs. Tlrе lropе ] our Planеt'sЬiodivеrsity,liеs in an )n аnd a сommitmеnt to saving thе ехist on еarth today and thosе that
гon, N-J:Prinсеtоtl Univеrsity Рrеss. пd Еuolutioп. Nеw Yоrk: Oхford r. Niissorr' 2000. Sехuаl сorrfliсt 4sof thе Nаtioпаl Асаdеmу of Sсieпсеs NJ: Prinсеton flсr. PrinсеtoI-r, 1995. Sехuаl sеlесtiorrand taxсlnomiс f the Rowl Soсietу rlf Lспсloп, Sеriеs dеrn doubts.Sсiеnсе.55:5.5_61. есiation in tЬе Мicroh1'lа oliuасеа9-.180. n promotе spесiаtion.Тrепds iп |tlvеpfеssurеs'vаriaЬility' irnd sехu:rl ;епsсhаfteп72: 204-2О6. пd Еuolutioп of thе Gепus Rhagolеtis Саmbridgе, lvIA: Mrrsеum оf and spесiationin trugivorousfliеs of e). Еuolutioп 2З: 2З7_251,. l at thе diploid Ieуе|,Аmеrrcап Sundеrland,МА: Sinаuеr Assoсiatеs. :ion analysis. Сurrепt Оrnithologу е еmpiriсаlсonsеquеnсеsof altеrnаtivе rs аnd proсеssеsot diffеrеrrtiation.In t аnd lts Сoпsеquепсes,28-59, lndоn: Jolrn lV{urrаy. zski.and R. Е. SilЬеrglied.1997. lxrеnding H:rldаnе's ru|e. I'rсlсееdiпgs 164:845-8-51.
Diаz, A., and N'I.R. Масruil:. 1999. Pollеn trrЬесoпrpеtitionаs a mесhanism of рrеZygotiс rеpгoduсtivе isolаtiоn Ьеtwееn Мilтшlus п[rsl|tusand its prеsumеd рrogеnitor М. gLtttаtus.Nсlu Phуtсllogist 144: 47 \478. Dobzhansk1.,T . 19з7 . G епеtiсsапd tbе Оrigiп of Spесlс's.Nеw York: СolumЬia Univеrsitr'l,rе's. 1946. Сoпlplеtе rерrodLrсtivеisolаtiorrЬеtwееntll,o rтorphologiсal11. similar spесiеsof Dкlsophilа. Есoklgу 27:2()5_211. Dowling, T. Е., and С. L. Sесor. 1997. Tb,erolс of hyЬridization and introgrеssion in thе divеrsifiсation()faniпlаls. Аппцаl Rсuieн' of ЕссlIogl'апd Sуstеmаtrcs 2 8 : 5 9 3 - 6 19 . Fеdеr,J. t-. 1998. Thе,rpplе lnаggot flу,Rhаgсllеtisponюпеlld fliеs in thе tЪсеof сonvеntiollаl .uvisdomаЬout spесiatiоп?In D. J. Howard and S. H. Bеrloсlrеr, еds., Еиdlсss l:orms: Spесiеs апd Spес:iаtitlп,1.3О_|44. Oхford: oxford Urrivеrsit1, Prеss. Fishеr,R. A. 1930. Тhc Gепetiсаl Тbеltу of Nаtиrаl Sеl,есtiс>п. oxford: Сlarеndon Рrеss. .Walsh.)г., F u t u } . l l l аD' . J . , J . S . T . M o r t r l n , D . . I . F . u n k ,a n d М . С ' K е е s е .1 9 9 4 . Gеrrеtiсvirriation in а рhуlogеnеtiссontсхt: Rеsponsеsof two spесializеdlеaf bееtlсs(Ссllесlptеrа: Сlrrysсlmеlidас)tgs.Pпlсaеdiltgs tlf thc Rol,аl SftЬe Мoпtаstrаесt аппulаris ссlпiplех.Маriпе Biollэgу |27: 705-7|1. Lаndе,R. 19ti2. Rаpid origin I Аltсllislizards. Amеriсап Nаtиrаlist 16З 26_З9. Lеl.in, D. A. 2002. Тhе Rolе of Сhrtlmtls
205
206
Тhе Pаttеrп аttd Proсеss сlf Spесiаtioп Мayr, Е. 1942. Sуstеmаtiсs апd the Оrigiтt of Spссiеs.Nеw York: СolurтЬra Univеrsity Prеss. 19.5.1. Сlrarrgеot gеnеtiс еnr,ironшеnгalld еvolution. IrrJ. Huхlеv, A. С. Hаrdy, аnd Е. B. Ftrrd, еds.' Еuсllutiсlпаs а Pкlсеss' 157-1B0. [-ondоn: G е o r g с A l | е l l. l l l d I j n w i n . 1'96З.Апilпаl S1lесiеs апd Еt'olutiсlп.СarnЬridgе,МA: Bеlknаp Pгеssof Нaгvаrd Unir,еrsiгуPrеss. МсКinnon' J. s.' s. Мсlri, B. K. Blасkn.ran,L. Dаvid, D. М. Кingslе1',L..|anriеs.ln, rolе in spесii]tion. J' С1rou,arrd D. Sсhlutсr' 2004' Еvidеnсе ftlг ессllt>gу's Nаtttrе 429 294_298. Меad, L. S., аnd S. J. Aгnold. 2t)04. Quаntitаti\,еgеnеtiсrтосlеls
Sitеs' J. W.' J.., and С. Nlоrl rеvisitеd. Sу stеmаtiс ZtSokal, R. R., and Т. J. Сrov, еvaluation. Alпеriсап Ь Sorепson, J' D., K. М. Sеfс, brood pа rаsitiс indigс'b S p i r i t t - lр. . 1 9 9 8 .T h е г t l l ео f D. J. Howard аnd S. H'
32o-3z9.Oxford:Oхf.
StеЬЬins, G. L. 195О. Уаriаt Ul-rivегsitуPrеss. Sturtеvant' A. H. 1920. Gеr HyЬrids wtth Drosophl Tеmplеton, A. R. 1980. Tht
94 1О|1-1038. l989. Тhе mеaning а n d J . A . Е n d l е r ,е d s . , М A : S i n а u е rA s s o с i а t е Тing, С.-T.' S. С. Tsaur, М. homеoЬox at thе sitе O U е s h i r n a ,R . . а n d Т . A ч a m i . Nаturе 425 679. van BatеnЬurg, F. H. D., аn сoiling: Сomputеr ехpt van valеn' L. 1976, Есologi Whitе, М.J.D' 1978'Мod'
Сompany. -l Wilеy, Е. o. 978. Thе еvo Zoologу 27:17-26. .Wilkirrson, G. S., аnd P. R. sеlесгion on irn ехадgе Roуаl Soсiеtу' of Loпdt
Тhе Раttепt апd Prс.>cеss с;f Spесiаtiotl f Spесiеs'Nеrv Yoгk: СolumЬiа t and еvolution.IrrJ. L{uхlеv, t|o|1|lsа Proсеss,1.57-180' I,otrdоn: Саmbridgе,МA: Bсlknаp Prеss of David, D. М. Kingsiе1',[,..|an-riс'son, -.Iсlгесоlttgr..' г.llс ilt sресiltitllt.
ltivе gеnеtiстllodеlsof sехuаl sе|есtion. 4-27 1. spесiatiorrin аn arthropod. Nаturе )6' SPесlеsriсhлеssсovагiеswitЬ l4--s.51. ion and fеаthеroгnаrmеntationin Ьirds. ttttrаIsеIесtionin Druьrphilа. Nаtиrе 3quеnсеsof sr,rnpаtry.Herеditу ;pесiation:Tlrе еvolutior.rof lryЬrid il3. gеnеtiсsоf sрlесiаtitln. Gепсtiсs 744: Trсsсnzа.200l. Sехual sеlесtiorrand tioп 16:364-з71. lсеptof spесiеs.In Е. S. VrЬa, еd., l Мusеurn Mсlnograph no. 4. Prеtoria, Itrllt,gyltntJrrtс1|sig11.11 5tгl'lсгI-lге in .|oсusаntagoтlistiс сoеvсllutiсll.t, аnd thе ' J. Ноwаrd .rndS. Н. BеrlосIrег,еds., 61-270. Nеr,vYсlrk: Oхford Univеrsity lсlrv ехpсrimеnts сln sр.lесi:lгiсln: WIr:rг 7:1637-1653. gеmеntsand spесiatioll.Тrепds iп rсеmеntof stiсklеЬaсkmatе Еtlrllutioп 52: 200_208. ipесiаrionГatеsаmon8 l1пurаns. S с i c п с е sU S А 8 З : \ з 7 9 _ | з 8 2 . сognitionаnсlsеxual sеlесtlоnаs a 'n.L.uolution17: 647-657. sресiationЬ1'natural sеlесtton. сеption'and рoрulаtiсlndivеrgеllсеin е Rоуаl Sllсit'tусlf I'сlttdоп, Sеriеs lJ |хo||orтIJ'. Nеrv York: СolLtmЬia
.!7., Sitеs'J. Jr., anс.lC. Мoritz. 1987. Сhromosomаl еvсllutiоnаnd spесiation rеvisitеd.SуsttlпtаticZoolсlgу 36: 1 53-|7 4. Sоkаl, R. R., and T. J. Сrоvеllo. |970. Тhе Biоlogiсal SpесiеsСonсеpt: A сritiсal еvaluаtion.Атпеriсаn N аturаlist,l04: |27 -7 5 З. Sоrеnsсln' J. D., K. lt{. Sеfс, аnd R. B. Paynе. 2003. Spесiation Ьy host switсh in Ьrood parasitiс indigobirds. Nаturе 424: 928_93|. Spirito,F. 1998. Thе rolе of сhrоmosomal rеarrangеmеntsin spесiation.In D. J. Howard аnd S. Н. Bеrloсhег, еds., Еlldless Forms: Spесiеs апd Spесiаtiсtп, 320_з29. Oхford: Oхford UrrivеrsityPrеss. Stеbbins,G. l,. 19.50. Vаriаtioп апd Еuolиtiott iп PIапts. Nеw York: СolumЬia Univеrsity Prеss. stuгtеvant'^. L1. 192О. Gеnеtiс strrdiеson Dпlsсlphilа sinlulаns.I. Introdrrсtion. HyЬrids with Drosophilа mеIапсlgаstеr, Gепеtiсs.5:488-500. Tеmplеton,A. R. 1980. Thе thеory оf spесiationvia thе fоundеr prinсiplе. Gепеtiсs 9 4 : 7 О 1l,l _ 1 0 3 8 ' 1989. Thе mеaningof spесiеsаnd spесiatiоn:A gеnеtiсprrsресtivе.In D. Ottе and.|. A. Еrrdlеr, еds.' Spссiаtit,папd lts Сoпsеquеnсеs,2_27. Sundеrland, MА: Sinauеr Assoсiatеs. -l998. Тing, С.-T., S. С. Tsaur, М.-L. Iй/u,аnd С.-I. Yu' A rapidly еvolvirrg homеoЬoх аt thе sitе of а hyЬrid stеrility genе.Sсiепсе282: 150i_1504. Uеshima,R.' and T. Asami. 2003. Singlе-gеnеspесiationЬy lеft-rightrеvеrsal. Nаtt'trе 425: 679. van Bаtеnburg'F. H. D.' and Е. GittсnЬеrgеr. 1996. Еase of fiхation of a сha ngе in сoiliпg: Сomputеr ехpегimеntsoп сhirality in snаils' Hеrеditу 76:278-286. vаn Vаlеn, L. 1976. Есoiogiсal spесiеs,multispесiеs,and оаks. Tахoп ) 5:2зз-2з9. .W. Whitе, М. .J.D. 1978. Мodcs of Spесiаtio|1.Sаn F-ranсisсo: H. Frееmаn and Сompany. !Иilеy,Е. o.1978. Тlrе еvоlutiсlnаrvspесiеsс()nсеptгесorrsidеrеd'Sуstеmаtiс Zoolсlgу 27: 17-26. \{/ilkinson'G. S., and P. R. Rеillo. 1994. Fеmalе сhoiсе rеsponsеto аItifiсial sеlесtion on an ехaggеrаrtеdmalе trait in а stalk-еуеd flу. Proсеediпgs of thе Rolа! 5u,i,'.r' of Loпdoп, Sеriеs B 255: l_6.
207
Еvolution and Dеvеlopmеnt GrеgorуA. Wrау
i I Y
/Ft genoryрe
Thе intеllесtual histсlriеs of dеvеlopпrеntaland еvolutiсlnaгy Ьiology havе frolrr thе ЬirtЬ of Ьiology as a distiIlсt sсiеntifiсdis. Ьееn intеrtlvinеd alr.l-rost с i p l i n е ( М a v r 1 9 8 2 ; R i с h a r d s 1 9 9 2 ) . . Г h е r е a s t l n sа r е n o t d i f f i с u ] tt t l 1 i n d . Both еv
Tеmporal Parallеls Rссapitulаtion has by ttlгl1sеrrlightеnеd,еntеrtailrеd,lrnd ехаspеratеdgеrrеr. а t i o n s с l f Ь i o l o g i s t s( d е B е е r 1 9 4 0 ; G < l u l d| 9 7 7 ; С Ь u r с h i l l 1 9 8 0 ) .T h е r е с o g . nition of parallеls Ьеtwееn еmЬrуologiсаl еvеt-ltsаlld rеlationships among spесiеs prсdatеd thе сonсеpt tlf lriologiсal еvtllutitln, at [еast in its modеrn sеtrsеof trаnsmtltation irеtwееnspесiеs.Indееd,thе rvords еuriutiсlп and dе. uеlopпtепtwеrе usсd intеrсhangеaЬlyto rеfеr tсl thе unfolding of Ьoth indi. arrd plrуlеtiссllangе until tЬе Lrеginningrlf thе tц.еntiеth vidual dеvеlopn-rеnt 208
bitэt
lntе
Figuге 1. Gеnotypе to p gеnеtiс information into Ьеhavior,and physiolog whеre thеy influеnсеsur' еvolutionarymесhanism suссеssivеgеnеration.A how proсеssesopегаtеа1 link in our knowlеdgе w
сеntury (Hall 1992; Ri proсеssеswеrе сonsidе Еarly desсriptions o{ сast in tеrms of thе sса emЬryos of morе сomp sеmЬlеd simplеr onеs tееnth-сеntury prеforп t h е s а m е p г o с е s s .D u r i tors notеd that сhiсkеn that сontain fеaturеs of for instanсе, thаt humа w i t h l i m Ь s а p p е a r i n gi
still. Karl Еrnst von Baеr' vations of divеrsе аnirг tion (Hall 1'992i RicЬal thе еmЬryos of vеrtеЬr rеpгеsеnt adults of oth lowеr spесiеs do not a sеnсе of fins in thе еmЬ Ьryos of distinсt group
Еuolutioп апd DeueloDmепt 209 ev0li"rtr0nary meсhаПisms
g
)еvеlopmеnt
t
i
genOtype ntal and еvoiutitlnary Ьiolсlgy havе lf Ьiology as a distinсt sсiеntifiс dishе rеasonsаrе not diffiсult to find. nporal proсеssеs,and еvеry individwithin, and rеflесts'a muсh dееpеr rllеl forms thе Ьasis for thе сonсеpt ,pmеntlitеrally rеplаys еvolutionary еst аnd most pеrsistеntlyсontrovеrrtal Ьiol
biосhemiсal interaсt|Ons
deve|орmеntal рrOсess8s
оrgantsmaI рnenolypё
Figurе 1. Gеnotypе to phеnotypе.Thе proсеssеsof dеvеlopmеnttransmutе genеtiсinformationinto organismalphеnotypе,whiсh inсludеsanatomy' Ьеhavior,and physiolоgy. Thеsе traits, in turn' intеraсt with thе еnvironment, whеrеthеy influеnсеsurvivоrship and rеproduсtion. Naturаl sеlесtionand othеr evolutionarymесhаnismsсhangе thе rеlativе frеquenсiеsof gеnotypеsin еaсh suссеssivеgеnеration.A сomplеtе undеrstandingof еvolution rеquirеs knowing how proсеssеsopеratеat еaсh сlf thеsеstеps.Until quitе rесеntly,thе wеakеst link in our knowlеdgе was dеvеlopmеnt.
20021. lg gеllotypе into phеnotypе providеs ing thе intеraсtionsЬеtwееn еvoluRatf and Kaufiтan 1983; Wilkins thе еvolutior-r of orgаnismal phеnot h е yw е r еs е P a r a t еГ r o с е s s е sа. r е i n ; s е so f d е v е l с l p m е n(tF i g u r е 1 ) . T h е to do with есoiogiсal сontехt and с r a t i n gа p а г t i с t r l l rp h е n с l t y p i сo u г of a group o{ rеlatеd spесiеsсan Ье Lraсtеristiсsas it is Ьy adult anatсlmy,
еntеrtainеd,аrrdеxaspеratеdgеrrеrJ 1 9 7 7 1 С h u r с h i l l1 9 8 0 ) .T h е r е с o g :al еvеnts аnd rеlаtionships among ;al еvolution,at lеast in its modеrn Indееd,thе words еuolutioп aлd dеl rеfеr to thе unfolding of Ьoth indiuntil thе Ьеglnningof thе twеntiеth
сеntury (|1a|| 1992 Riсhards 1992)..sИhat wе rесognizе today as distinсt proсеssеswеrе сonsidеrеd inехtriсaЬly intеrtwinеd. Еarly dеsсriptions of parallеls Ьеtwееn dеvеlopmеnt and еvolution wеrе сast in tеrms of the scаlа nаturа (сhain of Ьеing). Aristotlе rесognizеd that еmЬryosof morе сomplех сrеaturеspassеd through stagеsin whiсh thеy rеsеmЬlеd simplеr оnеs (Gould 1977|. For Сharlеs Bonnеt, an еarly-еightееnth-сеnturyprеformationist, еvolution and dеvеlopmеnt Wеrе litеrally thе samе proсеss. During thе latе 1700s and еarly 1800s sеvеral invеstigators notеd that сhiсkеn and human еmЬryos pass through a sеriеs of stagеs ..lowеr'' or ..infеrior'' animals. thаt сontain fеaturеs of Johann Mесkеl, notеd, for instanсе'that human еmЬryos сontain gill slits and a tail at еarly stagеs' with limЬs appеaring aftеrwards' and dеfinitivе mammalian fеаturеs latеr still. Karl Еrnst von Baеr' who madе ехtеnsivе and mеtiсulous firsthand oЬsеr. vations of divеrsе animal еmЬryos, ехpliсitly rеjесtеd thе idеa of rесapitulation (Hall 19921RiсЬards \992). Hе сitеd thе prеsеnсе of uniquе fеaturеs in thе еmЬryos of vеrtеЬratеs,suсh as thе yolk saс) as еvidеnсе that thеy did not rеprеsеntаdults of othеr spесiеs;сonvеrsеly,hе notеd that somе fеaturеs of lowеr spесiеsdo not appеar in thе еmЬryos of higher onеs, suсh as thе absеnсеof fins in thе еmЬryos of Ьirds (Baеr 1 82 8 ). Baеr also notеd that thе еmbryоsof distinсt groups of animals did not pass through stagеsrеprеsеnting
2 1 0 Еuоlutiсlп апd D еuelopm епt othеr Onеs:..TЬе еmЬryil tlf а vеrtеЬratеis at tЬе Ьеgirrrringalгеасlуa vеrtеЬratе'' (translationfrom Riсhards |992, 59). Dеspitе Baег's potеnt сritiсisnrs,support for thе nсrtiоn of rесapitulation pеrsistеd for anothеr сеntury. Rесapitr.rlationthеory rеасlrеd its zеnith in thе ..ontogеnyrесаrvгitingsof ЕгrrstHaесkеl (1866, l875), whosе sгatеmеntthat pitrrlatеsphylсlgеny'' (..diе ontogеniе wеitеr niсhts ist als еinе kurzе Rесapitufсlr rтany Ьiologists lation dеr Phylogеniе'';1866,2,7) еr,еntсldayеrrсapsulatеs thе rеlаtionships Ьеtwееn еvlrg supportеr of Darwin, viеwеd dеvеlopnrеnt as an ехhiЬit of phylоgеnеtiс history' with thе adults of anсеstorsdisplayеd in sеquеnсеduring thе dеvеlopmеntof an individual. His rvoоdсuts сlеpiсting thе progrеssivе divеrgеrrсесlf initially simil;rr vertеЬratе еmЬryos into distinсtivе fish, turtlе, Ьird, and humаn еnrЬryos havе Ьесomе iсons of latе-ninеtееnth-сеnturyеvolutionary dеvеlopmеntal Ьiol ogy (Figurе 2). Lеss widеly apprесiatеdis Haесkеl's viеw of rесapitulirtionas thе irсtual mесhilnism that prodtrсеs еv
ЕmЬryos as Еvidеnсе of Еvolution, Phylogеny' and Homology If еmЬryos do not infalliЬly rесapitrrlatееvolutionary history, thеy ntlnеthеlеss providе еvidеnсеof thе prосеssof еvolution.оf phylogеnеtiсrеlationships
Figurе 2. Rссapitulаtitln ; аnatomist Еrnst Hrrесkеl ' thе еvolutitlnarу history с dеvеlopl-nеnt (Haесkеl 1 8 onе of whiсh is shoц,n hе among sресiеs as dеvеlсlp thosе of а fish, аr-rrphiЬia аll thе сmЬryos havе gill s еmЬryo hаs а tаil (middlе wаs thе prеsеl1сеоf tlrеsе t h е i r а Ь s е n с с i n а с l u l t s ,t h
among taxa, and of thе appliсations wеrе all fir somеwhar diffеrеnt rеirs Not пrany rеadегsof l of еvolutiсln takеs plaсс marshalеd all thе еvidеn tation ап1ot1Е] spесiеswh Baеr, wlro rеjесtеd thе nl dеvеloprnеntaltraits' Dа pеlling еvidеnсе of сon strongеst singlе сlilss of tеr to Asа Gray (Sеptеm giz (Burklr:rrdtеt al. t99
Еuolиtioп аltd DеuеloDпlеnt
is at thе Ьеgirrningalrеaс1ya vеrtе-
se).
Эrt fоr thе nсltitln of rесapitulation tiorr thеory rеaсhеd its zеrrith in tlrе ,hosеstatеmеntthat ..ontogеnyrесatеr niсhts ist als еinе kurzе Rесаpitu'dayеrrсapsulatеs foг rтany Ьiologists Jеvсlopmеnt.Наесkеl, а strong suрs an ехhiЬit of phylogеnеtiсhistory, quеnсеduring tlrе dеvеlopnrеntof an ogrеssir.е dir,егgеrrсе of initiаlly simi_ lh, turtlе,Ьird. and humаn еmЬryos ury еvolutionarуdеvеlopmеntal Ьiol. ; H:rесkеl'sviе'uvof rесapitrtlation as ltionaryсhаrrgеrathеr thаn simply а rеd this mесharrismto сonsist of two Геsonto thе еnс1of dеvеlopnrеnt and .morе аЬЬrеviаtеdеarliеr stagеs. ехсеptions to striсt rесapitulation Ьy Baеr (1828). Hе сallеd thеm in muсh thе sаmе light tЬat most еs thаt havе сonvеrgеd in foгm ЬLtt аnr-roying oЬfr.rsсаtion of еvolutionnds of сеnogеnеtiс features.. hеtееlopr-nеntеvеnts' and hеtеrсltopу' or t struсturе.Both tеrms ilrе now usеd any сhangеin thе timing oг loсation Ly (Raff 1996; KlingеnЬеrg 199s). е сLlгrеnt'morе gеnеrаl us:rgеof thе rесаpitulаtоrу. tеmporal сhangеs, as гory onеs' aсk rесapitulation thеoryt nor Wаs , dеЬаtеsaЬor-rtгесapitulirtiorrlvеrе е modеrn synthеsiswas undеr way; l mr'ltualapathv that arosе Ьеtwееn aЬout this timе irnd lastеd trntil thе Although tlrе influеnсеof rесapitr.r. rЬrvologyсontinuеd to play an im-
ln, Phylogеny,
еvоlutionarylristory, thеy nonеthеllution,of phylоgеnеtiсгеlаtionships
Figurе2. Rесapitrrlаtitln as еnvisiоnеdЬ1.Haесkсl. Thе grеatсomparativе Еrnst Наесkсl was tlnе of tЬе strongеstProPonеntsof tЬе notion that anatсlt-t-tist thееvoIutionаr,v historyof 'r spесiеsis rеplavеddrrгingits еп-rЬryоlogiсal -l dеvеloрmеnt(Haесkеl tl66).His famoцs illustratiоnsof vеrtеЬratееmЬryсls, onеof whiсh is shown hеrе,сlеpiсtprоgгеssivеdivеrgеnсеin ovеralisimilaritiеs amоngspесiеsas сlеvеlopnlеlrtproсесds.Thе еmЬryos arе (from lеft tсl right) thosеоf a 6slr,arrrphiЬian. tr-rrtlе, Ьird, pig, сow, rzrЬllit,and huпrаt-t. Notе that all tlrе еmЬryos lrаvеgill slits аt an еаrlу Stagе(top rслu) and thаt thе Ьumаn е m Ь r v o h а s а t а i |( m i d d l е r o t u , r i g h tt)l - r a t i s l а t е r \ o s t ( b o t t o m r с l ш , r i g h t ) . I t Wasthе prеsеllсеtlf thеsеpЬуlt>gеnеtiсaIlv аnсiеntfеаturеsin еrrrlrryos, dеspitе Hаесkеl.(FrсlmНаесkеl 1866.) tlrеirаЬsеnсеirl аdults,thaг strопgl}.iп.rрrеssеd
amollg taха' al1d of thе lristory of spесifiс сharirсtеrs.Тhеsе thrее prасtiсal appliсationswеrе all first proposеd during thе ninеtееnth сеntury, Ьut for somеrvhatdiffеrеrrtrеasons thеy rеmairrimportant todаy. N()t mаnу rеadеrs of tlris Ьoсlk lvilI nееd to Ье pеrsuadеd that thе proсеss of еvolution takеs plaсе. Antiсipatirrg a rathеr diffеrеnt audiеnсе, Dаrwin mаrshalеdall thе еvidеnсе hе сould fiпd to support thе сonсеpt of trаnsmutationi]mong,spесiеswhеn lrе wrotе oll the Оrigiп of Spесiеs(1859). \Whеrе .,spесifiс'' Baеr,who rеjесtеdthе noti
211
rt 21 2
Еuolutiolt аnd DcuеlrlРmеttt
I
i
traits not manifеst in adult anatomy' suсh аs thе prеsеnсеof gill slits and a tail in hurrratlеmЬr1'giсal еvеnts has аlso Ьееn invokеd аs а Ьasis for polarizing сharaсtеr-statеtransftlrmаtion in fornral phylogеnеtiс analysеs (Nеlson \978). Тhis сlпtrlgе|tеtiL. сrit('ri(,tllis Ьzrsеdon ir litеrаl ге:rdingof Bаеr's laws: that еаrliеr еvеnts duгing dеvеloprrrеnti1rе morе gеnеral ;rnd thеrеforеarosе еarliеr during phylogеnеtiсhistory than latеr onеs. Thе utility o i t h i s с г i t е г i o n h а s Ь е е n q u е s t i o n е do n f i r s t p r i n с i p l е s( d е Q u е i r t l z 1 9 8 4 ) , а n d i t с l е a r l y f a i l s i n r n a n y r е a l - w o r l dс a s е s( M a Ь е е 1 9 8 9 ; R a f f l 9 9 6 ) . o u t group сomparistln is far morе widеly usеd today, аnd thе ontogеnеtiссritеriсln is intеrеstingpгinrarily as :rnехamplе of thе pегsistеnсеоf rесaglirr-rlationist thinking a сеnturY aftеr Hаесkеl. Thе third praсtiсal appliсation of сomparativе еmЬrytllogyis аs а сritеrion сlf homolсlgy aпlon€ ] spесifiссharасtеrs.of thе tlrrееаppliсаtions rrrеntionеd lrеrе,this rеmains Ьy thе far thе most impoгtant todау (Hаll 1994; Wilkins 2002). Riсhard owеn originally proposеd thе tеrms homologу and апаlogу in 184З with rеfегеnсеto his lloti()not thе arсl-rеtypе' а gеnеrаlizесlЬсldy organizatiсll-lsharеd among spесiеs rvithin a largе gгottp (Palrсhеn 1994). Owеn, who was ostеnsiЬly strongly opposеd to thе idеir of еvoltltion, introduсеd thе tеrms t() сontrаst Ьеtwссtl two kirrds tlf аrrаtomiсаl sinrilагitv among spесiеs:homology for сorrеsponсlingpаrts of atl arсhеtypеand аnlrlogy for nonhomologous traits with siпrilаrfunсtions (Owеn 1848). Btlth tеrms wеrе soon ехpropri:rtеdЬy еr,olutitlnarl'Ьiсllogists(PаnсhеrrI994) ltndarе still trsеdto distinguisЬЬеtwеепtwo funсlаrmеntallv diffеrеntlristoriсalhypothеsеs: сommon vеrsusindеpеndеntеvtllutionaryоrigins of a trait (Hall 1994). Distingшishing Ьеtwееn homсllogоr.rsand аrralogous struсturеs is
and sеnsе or$ans prеsr anсеstor or arosе indr similaг еmЬryologiсal sinсе сorrеspondеnсе 1994). ЕnrЬrуologiсal mologiеs' suсh as thе origin of vеrtеЬrаtеja' as еvinсеd Ьy thе rеr (Burkе and Fеduссia сan oссur (dе Bееr 1: пrains onе of thе nros, In rесеnt yеaгs thе to thе ехprеssion of Ьаsеd
FIеtегoсhrony
N{any еvеnts during partiсular paсе Ьесa еvеnts; еvеn dеvеlop in a сonsistеnt sеqu еvеn largеly indеpеn most ilny сhangе in о of othеr aspесts (Ra
сhangе in thе tinring lеd to thе viеw that а hеtеroсhroniс (Goulс
Еuolцtitlп шtd D еuelсlpmeпt 2 1 З l аs thе prеsеnсеof gill slits and а tсе tlf dеsсеntwith пrodifiсation. rIаtivееmЬryologyis in pЬylogеnеigiп tЬat..сommunity in еmЬryoniс 1859' 449). Systеmatistsl.ravеЬееп r sitrсе.Sеvеral signifiсant insights lut through usе of tl-risapproaсh, arthropods rathеr than mollusks сidiansаrе сlosеly rеlаtеd to vеrtе_ Lltsаrе highlу dеrivеd anatomiсally, s. Similaritiеsin еmЬryos oг lаrvaе с rеlаtionslripsаmong many othеr_ rеmainеdthе onlv dirесt еvidеnсе hе namеsof many сladеs arе Ьasеd ipiгaiia (for thе spirаl gе
and sеnsеorgans prеsеnt in diffеrеnt animal phyla arе dеrivеd 1rom а сommon anсеstoror arosе indеpеndеntly (Мсlorе and lr)Иilmеr1997; Niеlsеo2ОО2\. t similar еmЬryologiсal origin has long Ьееn сonsidеrеd а сritеrion of lromology' sinсе сorrеspondеnсеs in anаtomiсal оrganization arе oftеn сlеarеr (Нall 1994).ЕmЬryologiсal сompаrisons havе idеrrtifiеdsomе initially surprising homologiеs,suсh as thе oгigin of nrаmrrralianеar ossiсlеs from jawbonеs аnd thе origin of vеrtеЬratеjaws from gill arсhеs.This approaсh сontinuеs to Ье usеful' as еvinсеd by thе rесеnt dеЬatе aЬout digit homologiеs among arсhosaurs (Burkеand Fеduссiа 1997;Wagner arrd Gauthier 1999). Although еxсеptions сan oссur (dе Bееr 1971; Roth 1984), similarity of еmbгyologiсal origin rе. mains onе of thе rnost usеful сritеria of homology in anatomy' In rесеntyеars thе еmЬryologiсal сritегion of lroпrologyhas Ьееn ехtеndеd to thе ехprеssion of dеvеlopmеntаl rеgulatory gеnеs. This appliсaгion is basеdon thе oЬsеrvаtion that thе samе rеgulatory protеin is oftеn prеsеnt duringthе dеvеlopmеntof horrrologousstruсturеsеvеn whеn thеy give risе to highly divеrgеnt anatomiеs and еvеn in distаntly rеl:rtеdtaхa (Holland and Hollаnd \999). For instanсе, musсlе сеlls throughout thе animаl kingdom еxprеss rrot only thе struсtural protеins that еndow thеm with tlrеir spесifiс funсtion (myosin,асtin' аnd сr-асtinin)Ьut also rеgulаtory protеins that сontrol thе transсription of thеsе struсtural gеnеs (МyсlD and MЕF.2). Thе oЬsеrvation that dеvеlopmеntal rеgulat
Hеtеroсhrony Мany еvеnts during dеvеlсlpnrеnt happеn in а partiсular sеquеnсе and at a partiсular pасе Ьесausе thеу aге triggеrеd by, or dеpеndеnt upon, еarliеr еvеnts;еvеn dеvеlopmеntalеvеnts that arе not сausally rеlatеd oftеn unfold in a сonsistеnt sеquеnсе Ьесausе of gloЬal сoordination or simply Ьесausе еvеnlargеly indеpеrrdеntproсеssеs аrе еасh tighrly сorrtroliеd. As a rеsult, al_ most any сhangе in onе aspесtof dеvеlopmentwill altеr thе ratе or sеquеnсе of othеr aspесts (Raff 1996). Thе rеsult is a bеterсlсhroпу'an еvolutionaгy сhangеin tlrе tinring of dеvеlopmеntalproсеssеs.This simplе сonnесtion hаs lеd to thе viеw thаt all еvolutionary сhangе in dеvеlopmеntis fundamеntally hеtеroсhroniс(Gould 1977; МсKinnеy and МсNamara 1991|'
21 1
F'uсllutiсlп апd Dеuеlopmепt Mсldеrn idеas aЬout еvolutionary сhangеs in thе timing of dеvеlopmеnt grеW Out сlf rесapitr.rlationthеory. Thе aссumulating wеight of ехсеptions stеadily еrodеd thе gеnеrality of Нaесkеl's tеrminal addition and сondеnsation as еvolutionary mесhanisms.Howеvеr, thеrе wеrе two additional faсtors that brought aЬout thе dowrrfall of rесapitulationthеory: a сlеar undеrstanding of thе mесhanismsthat undеrliе hеrеdity and thе rесognition that natural sеlесtionсаn aсt tЬroughout thе lifе сyсlе (Goшld 1977;kaff 1996; \Wilkins 2002). By thе 19З0s it was widеly aссеptеdthat thе Ьiogеnеtiсlaw is nеithеr a mесhanism of еvolutionary сhangе nor an aссuratе dеsсription of it. Еvеn thе most voсifеrous сritiсs of rесapitulatitlnthеory rесognizеd,howеvеr,that par:.rllеlsfrеquеntly do ехist Ьеtwееn еvolutionаry history and еmЬryologiсal еvеnts. out of thеsе dеЬatеs сamе nеw and ultimatеly mсlrе rеwarding pеrs p е с tV l еs. Onе important insight Was that сhangеs in thе timing of dеvеlopmеntal .!7аlеvеnts сlftеn rеprеsеnt adaptati()nsrathеr than Ьy-prсlduсtsof сhangе. tеr Garstаng, a pugnaсious and witty сritiс of rесapitulation, assеrtеdthat ..ontogеny d
pеrspесtivе that was soli and N4сNamara 1991')' H е t е г o с h r o n yi n е а r l y fiсation of dеvеlopmеntа 1980s and 1990s. Dеvе Ьryos and in сomplеx l roсhrony in thе fossil rесr 1991)' Dеvеlopmеntal Ь to suсh pfoсеssеs as mor p а r i s o n s o f g е n ее x p r е s s p o r а l с h a n g е s .s o m е i n Diсkinson 1988; Сavеnе formations (е.g., Wray l сlеar that hеtеroсhrony сould arisе through a va A third important rns rathеr than proсеss (Raf timеs сonsidеrеd to Ье al сhangе (Gould 1'9773М original сonсеption. To t traits, howеvеr, hеtеroс сannot сausе сhangеs lп еnсompassеs a riсh arr: Еmbrуos апd Aпсеstors sifiсation of modеs of hе 1977; Ь|ЬerсЬet a|.197 thе variеty of tеmporal vidеd a prесisе voсaЬula Hеtеroсhrony has fad opmеntal еvolution, in р pervasivе that doсumеnt Iй/ilkins 2002). Thе еmp for еvolutionary сhangе сhangеs arisе, аnd how t of phеnotypе.
Dеvеlopmеntal Сor
A сеntral gоal of еvolutr rypе produсе сhаngеs in tеntion on сhаrасrеri idеntifying whiсh сompl еstaЬlishing thе numЬеr ifiсations in traits. Thеs еrеnсе to thе dеvеlopm
Еuolutioп апd DеuеloРmeпt 215 ngеSin thе timing of dеvеloprrrеnt rссumrrlаtingrvеight tlf ехсеptions 's tеrminal addition and сondеnsa'r, thеrеWеrеtwo additional faсtors trrlаtiсln thеory:a сlеirr undеrstandlty and thе rесognition that natural э (Gould1977;Raff 1996;Wilkins еd thаt thе Ьiogеnеtiсlaw is nеithеr an aссLlrаtеdеsсription of it. Еvеrr )n thеoryrесognizеd,hоwеvеr' that utionar1'history аnd еmЬryologiсal nd Llltinratеlymсrrеrеwardiтrgрlеr_ gеsirr thе timing of dеvеlopmеntal .Walr thаn Ьv-;lroduсtsof сhangе. i t i с o t r е с a p i t u l a t i o n a, s s е r t е dt h a t е n y , i t с r е a t е si t , ' ( G a r s t a n g 1 9 2 2 , еlian viеrv of ontogеny as a гесord l1аtnilturаl sеlесtioll aсts on dеvеlangеs irr anatom\.. Не intеrprеtеd r l y d е v е I o p m е nats a d a p r a г i < l n isn' 'val stagеs,сhangеs in mеthot]s of timing
pеrspесtivеthat was solidifiеd Ьy influеntial Ьooks (Gould 1977;МcKinneу аnd МсNamara 1991). Неtеroсhrony in еarly dеvеlopmеnt аttraсtеd rеnеwеd intегеst as thе rеunifiсation of dеvеlopmеntal and еvolutionary Ьiology gathеrеd paсе during thе 1980s and 1990s' Dеvеlopmеntal Ьiologists ехaminеd hеtеroсhrony in еmbryos and in сomplех lifе сyсlеs, whilе palеorrtologistsdoсumеntеd hеtеroсhrony in thе fossil rесord (Raff and Wray 1989; МсKinnеy and МсNamara 1991).Dеvеlopmеntal biologists Ьеgarrto apply thе сonсеpt of hеtеroсhrony to srrсhproсеssеsаs mсrrphogеnеsis,сеll linеagе,аrrd gеnе ехprеssion. Сomparisonsof gеnе ехprеssionamong сlosеly rеlated spесiеsrеvеalеdmany tеmporal сhangеs' somе in thе aЬsеnсе of oЬvious anatomiсаl сorrеlatеs (е.g., Diсkinson 1988; Сavеner 1992) and otlrеrsсorrеlatеdwith phеnotypiс transformаtions (е.g.,Wray and Bеly 19941 tverot and Patеl |997).It Ьесamе сiеar that hеtеroсhrony, likе othеr kinds of phеnotypiс transformations' сould aгisеthrough a variеty of еvolutionary mесhanisms. A third important insight was а shift to viеwing hеrеroсhrony аs pattеrn rathеr than proсеss (kaff 1996). Until quitе rесеntly hеtеroсhrony Was somеtimеsсonsidеrеdto Ье an еvolutionary mесhanism that produсеs phеnotypiс сhangе(Gould 1977; МсNamаra 19B8), a сurious pеrsistеnсеof НaесkеlЪ original сonсеption. To thе ехtеnt that dеvеlopmеntal proсеssеs arе hеritaЬlе traits, howеvеr, hеtеroсhrony is an aspесt of phеnotype likе any othеr and сannot сausе сhangеs in phеnotypе (Raff 1996). Hеtеroсhrony nonеthеlеss еnсompassеsa riсh arraу of phеnotypiс transformations. Gavin dе Bееr's Еmbrуos апd Аncestors (1940\ was thе first attеmpt at a ссlmprеhеnsivе сlassifiсаtionof modеs of hеtеroсhrony, arrd sеvеral othеrs havе followеd (Gould .Wray 7977;А|Ьеrch еt al. 79791Raff and 1,989I.Тhеsе analysеsеmphаsizеd thе variеty of tеmporal сhаngеs that arе possiЬlе in dеvеlopmеnt and providеda prесisеvoсabulary for dеsсriЬingthesесlrangеs. Hеtеroсhrony has fadеd somеwhаt as a сеntral thеmе in studiеs of dеvеl_ opmеntalеvolution, in part Ьесausеtеmporal сlrаngеsin dеvеlоpmеnt arе so pеrvasivеthat doсumеnting anothеr сasе is no longеr surprising (Raff 1996 Wilkins 2002i' Thе еmphasis has shiftеd to undеrstandingthе gеnеtiс Ьasis for еvolutionaryсhangеs in phеnotypе, thе есologiсal сontехt in wlriсh suсh сhangеsarisе,and how thе organization of dеvеlopmеntЬiasеsthе еvolution of phеnotypе.
DеvеlopmеntalСonstгaint and DissoсiaЬility A сеntralgoal of еvolutionary Ьiology is undеrstаndinghow сhangеs in gеnotypеproduсе сhangеs in phеnotypе. Еvolutionary gеnеtiсists havе foсusеd att е n t i o n o n с h a r а с t е r i z i n gg е n е t i с v a r i а t i o n w i t h а p Ь е n o t y p i с i m p a с t , idеntifyingwhiсh сomponеnts of this vaгiation sеlесtionopеratеs upon, and еstaЬlishingthе numЬеr and rеlativе impaсt of mutаtions that undеrliе modifiсationsin traits' Thеsе quеstions havе Ьееn addrеssеdlargеly without rеfеrеnсеto thе dеvеlopmеntal пrесhаnisпrsthat link gеnotypе to phеnotypе
216
Еuolutioп апd Dеuеlopmeпt sinсе thе sсhism Ьеtwееnеvolutionary and dеvеlopmеntalЬiology during thе 1930s and 1940s (Мayr |9821Wilkins 2002), Еvolutionary and population gеnеtiсistshavе gеnеrallytrеatеd dеvеlopnrеntas a Ьlaсk Ьox whosе сontents havе littlе to сontriЬutе toward undеrstаndingеvolutionary proсеssеs. Thе validity of this approaсlr has Ьееn сhallеngеd rеpеatеdly. Сharlеs .Whitman, an еarly еvolutionary 8еnеtiсist'wondеrеd whеthеr ..thе laws of dеvеlopmеnt ехсlrrdеsomе linеs of [phеnotypiс]variation аnd favor othеrs'' ( 1 9 | 9 , 1 1 ) . B y t h е 1 9 8 0 s s е v е r a lе v o l u t i o n a r yЬ i o l o g i s t sW е r еp r е p a r е dt o а n swеr in thе аffirmativе (Мayr 1982; Holdеr 1983; Мaynard Srтith еt al. 1985; Aгthur 1988; AlЬerсh 1989I. Thе notion that thе orgаnization of dеvеlopmеnt imposеs Ьiasеson thе prrrduсtionof phеnotypеs sееmsrеasonaЬlеto Ьеliеvе othеrwisе is to assumе that еvеry posslЬlе phеnotypiс outсomе is еqually likеly, whiсh is manifеstly not thе саsе (AlЬеrсh 1989; \Х/ilkins2002). Thе truе сhallеngеhas Ьееn idеntifying thе undеrlying sourсеsand lоng-tеrm сonsеquеnсеsof suсh dеvеlopmеntalсonstгaints. Еvidеnсе of dеvеlopmеntalсonstraint has сomе from two sourсеs.onе is forbiddeп morphologies, phеnotypеs that onе сan imaginе and thаt sееm funсtionally rеasonaЬlе Ьut arе nеvеr oЬsеrvеd.Thе sесond is thе rеstriсtеd rangе of phеnotypеsthat еmеrgеfollowing natural or ехpеrimеntalpеrturЬation of devеlopmеnt. In Ьoth сasеs somе of thе Ьеst ехamplеs сomе from t е t r a p o dd i g i t p a t t е r n s( F i g u r е3 ) ( H o l d е r 1 9 8 З ; A l Ь е r с h a n d G a l е 1 9 8 5 ) . Although thesе approaсhеs сonvinсingly dеmonstratеthat thе produсtion of phеnotypеsсan Ье Ьiasеd,thе сausеsof thеsеЬiasеshаvе rеmainеd еlusivе. A phеnotypе сould Ье ..missing'' bесausе it is diffiсult to produсе dеvеlopmеntally, or Ьесausеof a physiсal or gеomеtriс limitation, a laсk of gеnеtiс variation, or an unrесognizеdfitnеssсost. Distinguishing among thеsеpossiЬilitiеs has provеn quitе diffiсult. Еvеn whеn it is possiЬlе to infеr thе еxistеnсе of dеvеlopmеntal сonstrаints Ьy pгoсеss of еlimination' idеntifying what aspесts of dеvеlopmеnt Ьias phеnotypiс vагiаtion reisеs furthеr сhal' lеngеs,and fеw сlеar ехamplеs ехist. A rеlаtеd quеstion is why suсh Ьiasеsехist. onе ехplanation is that dеvеlopmеnt is aсtivеly ..Ьuffеrеd''to produсе сonsistеntphеnotypiс outсomеsin spitе of gеnеtiсor еnvironmеntaIpеrturЬations.This idеa was сarеfully artiсulatеd Ьy Сonrad \Х/addington(7957), who nаmеd it сапаlizаtitlи.Dеvеlopmеntal biologists havе long rесognizеd a similаr phеnomеnon thеy саll regulаtioп:thе aЬility of an еmЬry()to сonvеrgе on a normal phеnotypеfollowing ехpеrimеntal manipulation. \й7addingtonbеliеvеd саnаlizаtion to bе thе produсt of gеnеtiс assimilation' a proсеss whеrеЬy a phеnotypе that was initially invokеd Ьy thе еnvironmеnt is suЬsеquеntlygеnеtiсallyfiхеd through sеlесtiсlnto maintain that phеnotypе. Ivan Sсhmalhausеn (1949) proposеd that staЬilizing sеlесtion produсеd muсh thе samе rеsult. othеr possiЬlе sourсеs of dеvеlopmеntalсonstraint arе a progrеssivеloss of flехiЬility аs thе proсеssеsof dеvеlopmеnt Ьесomе Ьurdеnеd Ьy historiсal lеgaсiеs (.Wimsatt 1986) and thе likеlihood that modifiсаtions in еarly dеvеlopmеntwill hаvеa Ьroadеr phеnotypiс impaсt thаn latеr modifiсations (Arthur 1988; Gould 1989\.
А evolutionary redL
Frogs
Salamanders
B experimental redL
mitotiсinhib
developinglim
Figurе 3. Biаsеd produсtio may rеstгiсtthе rangе сlf pl froп-rехpеrimеntalpеrturЬ r a n g еo i p h е n o t y p е sr h а гi s i n d е p с n d с r lсt a s е st l f d i g i t r amphiЬiirns.AIthough four thеsегеsult from thе loss ol trеatingthе dеvеlopingliml A l Ь е г с ha n d G i r l е ( 1 9 8 . 5w ) frogs and salаmandеrs.ln е random Ьut instеirdсоnfor spесiеs.(Bаsеdon AlЬеrсh l
А evolutionaryreduсtionin digit number l dеvеlоpmеntalЬiologv dr-rringtlrе )02). Еvolutionary and populatitln nеntаs а Ьlaсk Ьoх whosе с()ntеnts ding еvolutionaryproсеssеS. еn сlrаllеngеdrеpеarеdly. Сharlеs ..thе laws of ;t' wondеrеdwhеthеr оtypiсl variirtionаnd favor oгhегs'' raryЬiologistsWеrе prеparеd to anlldеr 198З; Мaynard Srnith еt al. эtion tl"rаtthе organizlrtionof dеvеlLof phеnotypеssееmsгеasonaЬ1е. . r yp o ь s i h l еp h е r l o г у p i сo u г с o п r еi s с a s е( A l Ь е r с h1 9 8 9 ;! И i l k i n s 2 0 0 2 ) . Lеundеrlyingsourсеsаnd long-tеrm ;tгi]ints. has ссlmеfrom two sourсеs. onе is lt onе саn irlaginе аnd thаt sееп-r sеrvеd.Thе sесond is thе rеstriсtеd g natr-rral or ехpеrimеrrtalpеrturl"laе of thе Ьеst ехamplеs сomе from . 1 9 8 3 ;A l Ь е r с h a n d G а l е 1 9 8 . 5 ) . ;l1,dеmonstrаtеthat thе produсtion f thеsеЬiasеshavе rеmainеd еlusivе. 'е it is diffiсult to proсluсе dеvеlop)mеtriс limitation' a laсk of gеnеtiс :. Distinguishingamorrgthеsе possi. мhеn it is possiЬlеto infеr thе еxisproсеss of еlimir"rаtion,idеntifying otypiс variation raisеs furthеr сhalехist.onе ехplanatioll is tlrilt dеvеl. е сonsistеntphеnotypiс outсOmеs in ations.This idеa was саrеfully artiсylronamеd it сапаlizаtiс,,n. Dеvеlopl a similar phеnomеnon thеy сall а nornrаl рhеnotypе folonvеrgе
IV
Frogs
^fl/И
\l ill
Salamanders
,.''/lil' \l
B eхperimentalreductionin digit number mitotiсinhibitor
developing limb
Figurе.3.Biasеd produсtiсln o1 phеnotypеs. Tlrе orgzrnizаtiоn of dеvеlopmеnt m;ivrеstriсt tЬе rengе of phеnсltypеs it is сapaЬlе of ;lroduсing. Еvidеnсе сomеs from ехpеrimеntal pеrturЬation of dеvеloping аmplriЬiarl limЬs, whiсh show a rаngеof phеnotypеs thаt is siпrilar to that fсlund in rеlatеd spесiеs. (A) Sеvеral indеpсndеntсasеs of digit rеduсtion havе oссurrеd during thе еvolution of аmphiЬiаns.AlthoLrsh four-toеd spесiеs havе еvolvесl in frogs аnd salamandеrs, thеsеrеsult from thс ltlss of diffеrеnt digits (dеnotеd Ьy гoman numеrals). (B) By trеatingthе dеvсloping lirnЬs tlf amphiЬiаns with аn inhiЬitor of mitсlsis' Albеrсlrаnd Galе (198.5)wеrе aЬlе to еxреrimеntally rеduсе digit nr-rmbеrin frogsand sаlamandеrs. lrl еасh сasе thе rirngе of rеsillting phеntltypеs is not random Ьut instеad сonforms to thе rangе оf phеnсltypеs found among rеlatеd spесiеs.(Basесlon AlЬеrсh and Galе l 98.5')
218
Еuolutioп апd Dеuеlopmепt If dеvеlopmеnt somеtlmеs aсts as a сonstraint on еvolutionаry сhangе, how do modifiсations in dеvеlopmеntarisе?Josеph Nееdham (19З3) pointеd out that fundamеntal dеvеlopmental proсеssеs' suсh аs сеll division' morphogеnеsis' and diffеrеntiation, сan oftеn сontinuе indеpеndеntly aftеr ехpеrimеntal pеrturЬations. Hе сallеd this phеnomеnon dissoсiаbilitу and assеmЬlеda long list of ехamplеs.Thе undеrlying basis for dissoсiaЬilitymay diffеr in dеtail from саsе to сasе' Ьut a сommon gеnеral fеaturе is proЬaЬly modularity, thе pгopеrty of partial or сomplеtе funсtional indеpеndеnсеЬеtwееn dеvеlopmеntalpгoсеssеs(Gеrhart and Kirsсhner 19971Hansеn 2003). Thе еvolutionary signifiсanсе of dissoсiaЬility is that it allows modifiсations in partiсular aspесts of dеvеlopmеnt without fata||усompromising thе еntеrpгisе (Gеrhart аnd Kirsсhner 1997). In gеnеtiс tеrms dissoсiaЬility is roughly еquivalеnt to сirсumsсriЬеd plеiotropy (Wilkins 2002).In an influеntial Ьook Ronald Fishеr (1930) arguеd that mutations of small effeсt are far morе likеly tо form thе gеnеtiс Ьasis of phеnotypiс сhangе; his argumеnt turnеd on thе intuitivе assumption that Ьroadеr plеiotropy is' in gеnеral, morе likеly to rеsult in а nеt nеgativе fitnеssсonsеquеnсе.Fishеr's viеw has Ьееn rеfinеd (Оrr 2002) Ьut rеmains a Ьasiс еxpесtation for most еvolutionary gеnеtiсists. Dеvеlopmеntal pгoсеssеsаrе somеtimеs strongly dissoсiatеd from еvolutionary сhangеs in аdult anatomy. Striking instanсesof divеrgеnсеin dеvеlopmеntal mесhanisms with no oЬvious impaсt on adult morphology havе Ьееn doсumеntеd in sеvеral diffеrеnt сladеs, inсluding nеmatodеs (Goldstеin et a|. 1998; F6liх and Stеrnbеrg 1998I, arthropods (Patеl еt a|. 1994; GrЬtc et a|.1998), and sеa urсhins (Hеnry and Raff 1990; Wrаy and Raff 7990|. Somе of thеsе саsеs involvе сhangеs in lifе history' suggеsting that thе way dеvеlopmеnt proсееds, rathеr than its adult produсt, has Ьееn thе targеt of sеlесtion,as disсussеdlatеr in this еssay. If somе ways of organizing dеvеlopmеnt limit сhangе, othеr ways of organiztng it may faсilitatе сhangе. Thе propегtiеs of dissoсiaЬility and сanalrization may сontriЬutе to thе еasе with whiсh modifiсations arisе in dеvеlopmеnt (Gеrhart and Kirsсhner 1997; Stеrn 2000). Somе authors havе arguеd that сhangеs in thе organizatton of dеvеlopmеnt' or in its gеnеtiс Ьasis' сan Ье kеy еvolutionary innovations with far-rеасhing еffесts.Тhе Ьasiс idеa of a kеy еvolutionary innovation is that a novеl fеaturе еlеvatеsthе ratio of spесiation to еxtinсtion, pеrmits аn еxpansion of anatomiсal disparity, or Ьoth' ovеr maсroеvolutionary timеsсalеs (Lеvinton 2001). PossiЬlе dеvеlopmеntal ехamplеs inсludе thе ехpansion of Hoх gеnе numЬег еarly in vеrtеЬratееvolution (Holland 1'992)and thе appеaranсеof holomеtabolous dеvеlopmеntin insесts (Yang 2001). Thеsе hypothеsеsarе diffiсult to tеst' sinсе еaсh rеprеsеnts a uniquе historiсal еvеnt' Ьut thеy raisе thе possiЬility that thе organization of dеvеlopmеnt might havе а long-tеrm positivе impaсt on thе evolutionary fatе of а сladе. .s7е arгivе at a proЬlеm that has not Ьееn adеquatеly addrеssеd:is сanalizatjon an impеdimеnt to or a faсilitator of еvolutionary сhangе? on thе onе hand, сanаlization allows thе aссumulation сlf additivе gеnеtiс variation
within a population Ьy n givеn individual; thе inсr the mill of sеlесtion undt еnt gеnеtiс Ьaсkgrounds { nеtiс variants that migh thеrеЬy bесomе visiЬlе tо drift as nеutrаl аllеlеs.\X grее to whiсh sеlесtionеs tion and thе dеgrееtсl wl fatе of сlаdеs (.Wеst-ЕЬе
Еvolutiоnary vеfsus
Thе fiеld of еv
dominant rolе for maсrol that hе proposеd lеd to ,. implausiЬlе. It was not ut mutations gainеd intеllе (Wilkins 2002). Thе wаy ogists' who arguеd that г е s u l t < t fm t l г а t i o n si n g ( аnd Monod 1961;Brittе son 1975). Thе risе of dе highlightеd thе potеntia1 notypiс transformations ( Dеvеlopmеntal rеgulat Ьiologists for sеvеralrеas bitborах and Апteппа1le 1 9 7 8 ; S с о t t е t a l . 1 9 8 3 ) .l Batеson's (1'894) homеot into lеgs (Figurе 4). A rеr s с г i Ь е d p l е i r l t г t l р y t: h е i г1
Еuсiutiсlпапd Dеuеlo1lmепt 21L) nstraint on еvolutionaгy сhangе' ) J o s е p hN е е d h a m ( 1 9 3 3 )p o i n t е d е s s с s ,s u с h a s с е l l d i v i s i o n , m o r сontinuе indеpеndеntly aftеr ехphеnomеnon dissoсiаbilitу and эrlyingbasisfor dissoсiаЬility may :nmongеnеralfеаturе is proЬaЬly plеtеfunсtionalindеpеndеnсеЬеrd Kirsсhnеr 19971Hansen 2003). lity is that it allows modifiсations ut fаtirllyсompromising thе еntеr4hly еquivalеnt tо сiгсumsсriЬеd al Ьook Ronald Fishеr (1'930\ armorе likеly to form thе gеnеtiс Ьar г n е do n t h е i n t u i т i v еa s s u m p t i o n г е l i k е l y t o r е s u I ti n а n е t n е g a t i v е l r е t i n е d( o r г 2 0 0 2 ) Ь u t r е m a i r r sa :nеtiсists. s s г г o n g l yd i s s o с i a t е df r o m е v o l u g instanсеsof divеrgеnсе in dеvеlmpaсt on adult moгphology havе эs,irrсludingnеmatodеs(Goldstеin .thropods(Patеlеt аl. 1994; Grbiс .sИray and Raff 1990). Raff 1990; [е history, suggеstingthat thе way u l t p r o d u с t .h а s Ь е е n r h е t а r g е t o f 't limit сhangе,othеr ways of orgartiеs of dissoсiaЬilityand сanaliza. ' modifiсations arisе in dеvеlopmеnt )). Somе authors havе aгguеd that -tt,oг in its gеnеtiсЬasis,сan Ье kеy ng еffесts.Thе Ьasiс idеa of a kеy tturееlеvatеsthе ratio of spесiation 'nаtomiсaldisparity, or Ьoth, ovеr 2001). PossiЬlе dеvеlopmеntal ехе numЬеr еarly in vегtеЬratе еvoluof IrolomеtaЬolousdеvеlopmеnt in "е diffiсultto tеst' sinсе еaсh rеprе:aisеthе possiЬilitvthat thе organilong-tеrm positivе impaсt on thе ееn adеquatеlyaddrеssеd:is сanalof еvolutionаryсhangе? On thе onе r r i o n o f a d d i t i v е q , е n е t i сv a г i a t i o n
within a population Ьy minimizing its immеdiatе phеnoгypiс impaсt On аny givеnindividr-ra[; gгist for rlrе inсrеasеdgеnеtiс variatiotl rnight latеr Ьесot-t-tе irr thе mill of sеlесtiorrunder altеrеd еnvironmеntal сiгсumstanсеsor diffеrеntgеnеtiсЬaсkgrounds (GiЬson and Dworkin2004). On thе othеr hаnd, gеnеtiс variants that might othеrwisе produсе phеnotypiс сonsеquеnсеsand thеrеbybесonrеvisiЬlе to sеlесtionmight bе maskеd and thеrеforееffесtivеly drift аs nеutrаl аllеlеs.Wе still havе only ir limitеd undеrstanding of thе dеgrееto whiсh sеlесtionеstaЬlislrеdrnесhanismsrhat Ьuffеr phеnotvpiс veriation and thе dеgrеегo whiсh suсh mесhanisms limit сlr Ьias thе еvсrlutionaгy fatеof сladеs (\йiеst-ЕЬеrhard 2003).
ЕvolutionaryvеrsusDеvеlopmеntalGеnеtiсs Thе fiеld of еvoIutionarygеnеtiсs,as notеd еarliеr, largеly ignorеd thе quеstiоn of how gеnotypiс diffеrеnсеspгoduсе phеnotуpiс diffеrеnсеs.William BatеSOn'who сoinеd thе tеrm gепсtiсs,Was Onе of tЬе first Ьiologists t() сotl. sidеrthе bаsis fсlr plrеrrotypiсvаrilrtion and diffеrеrlсеsamOng spесiеs.His МаtеriоIsfor tЬе Studу of Vаriаt jrп Тrеаtеd шitЬ F|spесiаlRеgаrtl tо Disсoпtiпuitуitl thе Оrigiп of Spесiеs (l894) еmphasizесlthе rolе of сhаrrgеsthat arehomeotiс (anothеr tеrm hе сoinеd, to dеsсriЬе s;latial transpositiсlnsаnd d u p l i с a t i o n si n а n i l t o m y ) .B a t е s o n ( \ 9 0 2 ) l a t е r a r g u е d t h a t М е n d е l i a n g е nеtiсsprovidеs а stlffiсient ехplanatiсlr.r for thе hеrеditr.dеrrrandеdЬ1.Dar. win's hypothеsis of nаtural sеlесtiсln. Durilrg thе l930s arrсl l940s thе nrodеrnsynthеsisсoпrplеtеd this histсlriс intеllесttrаlmrrgеr' and thс еarly nеo-Darwinianspostulatеd a dominant rolе fсlr mutations of srrrallphеnсlt v p i се f f е с t( F i s h е r1 9 3 0 ) . Riсhard GoIdsсhmidt (1940) Ьuсkеd thе trеnd of tl.rеtimеs to аdvtlсatе a donrinаlrtrolе fсlr n1асr()l11Lltаtions. Еvеn аt thе timе, thе gеllеtiс mесЬlrrrisп-ts ..hopеful thathе proposес1lеd to rrronstеrs''(Goldsсhnlidt 1960, .3)6) sееlnеd implausiЬlе.It wirs not until thе 1980s that Goldsсhmidt's сonсеpt сlf mасromutationsgainеd intеllесtual traсtion, alЬеit in сonsidеraЬly altеrеd guisе (\filkins 2002). Tlrс way Was prеpi1lеdЬy sеvеral ir.rfluеntial r-nolесulаrЬiolоgists'who aгguеd tlrаt phеnotуpiс iliffеrеnсеsаmol1g spесiеs erе lагgсlv a (JaсoЬ rеsultсlf mutаtiorrs in gеnе геgr.rlzrtion rathеr than protеin flttrсtiсlt-t а n dМ o n o d 1 9 6 l ; B r i t t е nа n d D : r v i d s o n\ 9 6 9 1 K i r r g a n d \ й / i l s o nl 9 7 ' 5 ;W i l son 1975).Thе risе of dеvеlopmеrrtalgеnеtiсsduring thе sr-rЬsеquеnt dесadе highlightеdthе potеntial rсllе of rеgulatсlrygеrrеsin mеdiating dramlltiс phеnotуpiсtransformirtions(Raff and Klrr'rfmen1983)' Dеvеlоpmеnralгеgulаttlr1'gеnеs сaptuгеd thе imirgir-ration of еVoltlti()llаry for sеvеrаlгеasons.Tlrе most famous rеgulаtoгygеnеsЬеlong t
220
Еuolution апd Dеt,eloDmепt
Figurе 4. Hоmеotiс mutations. Thе fruit {|у DrosophiIа melапсlgаs,erhаs Ьееn an important rеsеarсlr suЬjесt for Ьoth еvolutionar,v and dеvеlopn-rеntаl Ьiologists. Hоmеotiс mutаtions in this spесiеs arе aпlong thе mсlst famоus and spесtaсular mutаtions thаt havе Ьееn rесovеrеd from any organism. (A) Hеad of a fly that is homozygous for wild-typе i-rllеlеsattЬe Апteпnаpеdiа loсus. Notе thе smаll, fеathегy аntеnnl]е (шhitе аrrrлt,). (B) Hеad oi a fly that is homozygous for Aпteппаpеdiа |oss-of-funсtion allеlеs. This mr.rtаtiontransforms thе antеnnaе in into еnormolls' nеarly pегfЪсtlеgs. A rеmarkaЬlе fеaturе of this and many othеr homеotiс mutations is thеiг highly loсalizеd phеnotypiс еffесts. (Photos Ьу Itudi Turnеr.)
homеotiсall,v transformеd organ. This еffесt is ir gеnеtiс manifеstation of Nееdhаnr's сonсеpt of dissoсiation and' wе now know' a rеsult of tlrе way gеnе ехprеssion is rеgr.rlatеd(Wray еt al.200З). Anothеr intеrеstingfеаttrrе of thе fly homеotiс loсi is thе rеsеmЬlanсе of mutant phеnotypеs to thе anatomiеs of distantly rеlatеd insесt spесiеs.For instanсе,somе mutations in (ibх produсе four-rvingеd fiiеs, rесiriliпg аrr апсеsсrаl anatoIl1усhас has bееn aЬsеnt in diptеrans for rnorе thаn 200 million yеzrrs(Lеwis I97s). Dеvеlopmеntal gеnеtiсists havе idеntifiеd hundrеds оf loсi whosе mutant phеnotypеs indiсаtе kеy rolеs in dеvеlopmеnt. During thе 1990s loсi wеrе disсovеrеd in plаnts that геsеmЬlеthе homеotiс gеnеs of aninrаls in sеvеrаl rеgards:thеy produсе dramatiс transformationsof floral оrgаn idеntity' tlrеir phеnotypiс impaсt is gеnеrally сirсumsсriЬеd' and somе mutаtions prсlduсе flowеrs that геsеmЬlеthе floral organizаtion of Ьаsal angiospегms(Jaсk еt al. 1992; Ror:nslеyеt al. 7995)' Not all dеvеlopmеntalrеgulаtory gеnеsproduсе homеotiс phеnotypеs whеn thеy аrе mutаtеd. Sеvеral loсi in thе nеmatodе Саenorbаbditis elеgапs produсе hеtеroсhгoniс phеnotypеs (AmЬros and Horvitz 1984). Мany mutations arе known that аffесt dеvеlopmеntal pro. сеssеs; thеy dеlеtе speсifiс organs сlr сеll typеs, аltеr Ьody propoгtions' сhangе thе timing of rеpгoduсtion сlr feсunditv, modify сoloг pattеrns or othеr intеgumеntary struсturеs' and сrеatе a host of othеr spесifiс phеnotypеs (Wilkins 199З; GilЬеrt 2006|' As soon rrsit Ьесаmе possiЬlе to сhaгaсtеrizеthеsе gеnеs at tlrе molесular lеvеl, it wаs сlеar thаt most еnсodе protеins rvitlr rеgulatory funсtions (Gеr-
hart аnd Kirsсhirеr 19j protеil-lsthat rеgulatе tl сommulliсаtiсln anlong trаnsduсеs а pеrсеivеds as mirosisand сеll dеatЬ rах and Апtеппа|lеdiа t found t.l соntlrin lr sеq prorеins' In а histoгiса h oпtеobrм, :rnd rnеmЬе pondегаnсе of loсi that fiеd in mlltant sсrееn prесi sеlr' rvhat dеvеIсl1.l opmеnt:сommuniсаtio i n t u r n a с t i v a t е sd i f f с gгOWr|lm ' t,гphogеIlеs Thе rvеаlth of informi m o s t o f i t d u r i r r gt h е p а pliсations. Fiгst, tl-rеprr not unusual for phеnot (\ struсturе or сеll t1.1..lе
еurrl,vеmbryos sоп1еtim tal еvеnts. This iпrpliеst dеlimitеd aspесtsof аn 2000). Sесtlnd, many nluсаti histсlry, or mating, systе and Kiгsсhnеr 1997).W Ьаsis for suсh diffегеnсе tаtions lvould tvpiс:rll1 d е n l < l l r s t r ntthеe rе v с nч i pесts of phеnotypе thа monstеrs sееm lеss faг thr>ught. Tlriгd, and pеrl.rаpsr opеn thе Ьlасk Ь
Еuolиtion апd,Dеuеlopnlепt 221
)rosophilа mеlаtкlgаsterhаs Ьееn tionaryand dеvеlopmеntal )sarе аmongthе most famоus and (A) Hеаd of iеd froпl ilnv orgi.tnism. , at thеАпtеппttpеdiаloсus. Notе B) Hеad оf a fly thаt is hоmоzygous rismutationtrаnsformsthе qs.A rеmarkaЬlеfеirturеof this and .lyloсalizеdphеIrоtypiсеffесts.
Гfесtis a gеnеtiс manifеstаtion of Wе now know, a геsult of thе way 2003). Anothеr intеrеstingfeaturе nсе of mutant phеnotypеs to thе еs.For instanсе,somе mutations in ln anсеstralanatomy tlrаt has bееn lion yеars (Lеwis 1978)' еd hundrеds of loсi whosе mutant mеnt. Dllring thе 1990s loсi wеrе |mеotiсgеnеsof animals irl sеvеral ations of floral organ idеntity, thеir iЬеd, and somе mrrtationsproduсе on сlf Ьаsalangiospеrrns(Jaсk еt al. gеnеs produсе opmеntalrеgul:1tory :atеd.Sеvеralloсi in thе nеmatodе сhroniс phеnotvpеs (AmЬгos and )wn that affесt dеvеlopmеntal proе l l r y p е s ,а l r е r Ь о d y p r o p o r t i o n s ' :сundity,modifу сolor pattегns or lге a host of othег spесifiс phеnoсtеrizеthеsеgеnеsat thе пrolесular lins witlr rеgulatоry funсtions (Gеr.
hart irrrd Kirsсlrrrеr 1997; Wilkins 2002). Somе arе trаnsсriptiсln tllсtors' protеinsthat rеgulatе thе ехprеssion of othеr gеnеs;othеrs аrе involvеd in сommuniсation alnong сеlls (signals' reсеptors, аnd thе пrасhinеry tЬat tгаnsduсеsa pеrсеivеdsignal);e.tпdsomе геgrrlatеkеy сеllular pгoсеssеs,suсЬ .Whеn as mitosisanсl сеll dеаth. thе holrrеotiсgеnеs of thе Drr;sr4lhilа bitho' rах ald Апtеппаpеdllzсomplеxеs Wеrе isolatеd, for instanсе, thеy wеrе all found to сtlntein il sеquеnсе motif сhагасtеristiс of сеrtain DNA-Ьinding protеins.In а lristoriсal nсlсl to Batеs
2000 ). Sесond,many mutiltions rnilrriсdiffеrеrrсеsam()llgspесiеsiп nnatomy' lifе historу,or matinЕ.systеms (Raff and Kaufmarr 1983; Fitсlr |997., Cеrhart and Kiгsсhnеr 1997|' Whеthеr or not thеsе mutations also rnimiс thе gеnеtiс Ьasisfoг suсh diffегеnсеs,anсl whеthеr ()r not individuals that Ьeаr thеsеrnutationswould п'piсally sLrгvivеirr thе ц'ild (poinrs disсussеd lаter), thеy do dеmonstratеthat еvеn simplе mutations саn prodLlсеprofound сhangеs in аspесts of phеnotypе that arе есologiсirlly rеlеvant; Goldsсhmidt's hopеful monstегssееm lеss farfеtсhеd, at lеast :]t a gеnеtiс lеvеl, tЬan Wе onсе thought. Third, and pегhaps пrost gеnеrally, dеvеlopmеntal gеnеtiсs has thrсlwn opеnthе Ьlaсk Ьrlх that еvolutiсlnaryЬiolсlgistslaгgеly ignorеd for half а сеnpopulation gеl1еtiсists't]tlal]titаtivеgеnеtiсists,and turу.Utltil quitе rесеrrtl1, еvеn't()somе ехtеnt' еvсllurionarygеrrеtiсiststrеiltсd gеnеs for tlrе most part as abstraсtеntitiеs;fеw thought dееply abсlut how diffеrеnt kinds of gеnеs and mrrtlrtiоnsmight сontriЬtltе to phеnotvpiс еvсllrrtion.Ссlr-rvеrsеly, dеvеlgеnеtiсiststhought a lot aЬсlLttthеsе issltеs,Ьut гzrrеlyin an еvсllu. oprrrеntal tionar1.сontехt. Thе intеrsесtion Ьеtrvееn thеsе pеrspесtivеs has lrаd a profourrdand pсlsitivеimpасt сln Ьoth dеvеiсrpmеntalаnd еvolutiorrаrуЬiologv' Trlday, thеrе is widеsprеad intеrеst irr undегstanding r,vЬаtkinds of (Niеlsеn еt al. 200.i; Haygood еt al. gеnеsаrе suЬjесt to positivс sеlесtior-r
2007\.
222
Еuolutiсlп,апd Dеuеlopmепt
Body Plans and thе Hoх Paradoх Тhе rеunifiсation сrfdеvеlopmеntirland еvolutionary Ьiology was wеll undеr way by thе еaгly |99Оs. A foгtuitous сomЬinаtiorrсif еvеnts-thе еarliег puЬliсation of insightftrlЬooks (Gould 1977; Rаff and Кaufп-rаn19sЗ)' tесhniсal advanсеs (most notably thе infusion сlf molесular tесhniquеs into virtually еvеry faсet of Ьiologv), improvеmеnts in аnаlytiсal tсlсlls(еspесiallyphylogеnеtiс mеthods), and a sеriеs of ехсiting disсovеriеs (nrorе on thеsе latеr)_ prоpеllеd thе mеrger forwаrd. Мuсh of thе initial ехсitепrеnt rеvсllvеd around thе еvolution of animal Ьt>dyplans. As thе first dеvеloprnеntalrеgulator,vgеnеswеrе сhаrraсtеrizесl at а rnolесular lеvеl, a majoг suгprisе еmеrgеd:homologous dеvеlopmеntalrеgulator.v gеnеs arе shаrеd among organisп-rswith vеry diffеrеnt Ьody plarrs.Thе first сlеar instanсе was thе геаlizаtion tЬat liп-12, Notсh, аnd ЕGЛl , impoгtаnt rеgulatory gеnеs indеpеndеntly idеntifiеd in nеmatodеs, arthropods, and с h o г d a t е s ,a r е h o r n o l o g o u s( G r е е n w а l d 1 9 8 5 ; Y o с h е m е t а l ' 1 9 8 8 ) .B u t t h i s finding was quiсkly ovеrshadowеd Ьy thе disсovеry thаt vеrtеЬrаtеsсontain Ёlox gеnеs homоlogous to thosе in l1iеs,and thаt thеy arе сlustеrеd in thе g е n o m еi n t h е s a m е r е l а t i v еo r d е r ( A k a r т 1 9 s 9 ) . I } yt h е m i d - 1 9 9 0 st h е l i s t o f rеgulatory gеnеs sharеd among thе mlljtlr modеl systсn1sof dеvеloprnеntal Ьiologv ran to sеvегaldozеn (Raff 1996; Gегhart аnd Kirsсlrnеr 1997). Sur. vеys of othеr phyla rеvеalеd a rеmarkirЬly Ьroad phylogеnеtiс distriЬution, irrсluding Ьasal nrеtаzс)аngroups (suсh as сnidаrians :rnd сtеnсlphсlrеs)arrd anatomiсally ехotiс onеs (suсh as есЬinodеrms ilnd rnollr:sks).It Ьесamе сommonplaсе to spеak of a shаrеd ,.toсllkit''of аrrimal dеvеlopmеnt (Сarroll еtal.2001). All of this was сomplеtеly unеxpесtеd.Animals in diffеrеnt phyla arе so anatomiсaily distinсt that idеntifying hопlologoLlssrruсtufеsand dеtеrmin. ing phylogеnеtiс rеlationshipsrеmain сontеntious (NiеIsеn 2oo2). This phеnotypiс distinсtnеss hаs foгmеd onе сlf thе сеrrtrаl tlrеmеs of сomp.rrativс аnatomy for as long аs thе fiеld hаs ехistеd (HalI l992: Raff 1996\, Thе notion оf a Ьody plan is that еaсh phylum of ar-rimalshas а uniquе ссlmЬination of аnаtomiсal trаits, most of whiсlr аrе аrсhitесгural(suсlr аs Ьoсiy s1,пrmе. try), еmЬryologiсаl (suсh as tlrе gеomеtry of сеll division), or Ьoth (suсh as thе nunrЬеr
bесomе an iсon of еvolu thе knоwn gеnе fаmiliеs systеms in аnimаls datе many to tlrе uniсеllulz Kirsсhnег 1 9 L)7; Сar r t>I tal rolеs of thеsе rеgular and Аr"lbidсlpszЗ zlrе сlеl zoans. Pеrhaps е\.еnп1orеrе tеins arе ехpгеssеd in ro fеrеnt phyla (Gеrhart аl gеnеs providеd thе firs othеr orthologous rеgt tantly rеlаtес]animal ph to ovеrlook thе faсt that s i m i l a r d o m а l i n so f е x p r that thеir dеvеlopr-r-rеn f i с a t i t l no f a n i m l l s 1 D a v sirrrilaritiеsirr gеrrеехprt tеЬratеs havе Ьееn usесr tor (DеRoЬеrtis and S l o n g - е х t i n с t а n с е s t o r ss с volvеs many аssumption of thе Ьiliаtеrian аnсеs Wilkins 20021.
Okl еln.|
"l
/
Ap
DП
Dlt hlt AР
Figurе 5. Тhе Hoх parad< fliеs аnd miсе dеspitеthс ; thеsе аnimаls. Тhе mosr fа еstaЬlish positiсln оf Ьodу hсlmtllog
Wrаy 2003.)
Еuоlцtiсlп аttd Dа,еl
Ьiology Was Wеll undеr llutior-rary inаtionof еvеnts-thе еаrliеr puЬ'aff aпd Kaufrrranl98З), tесhniсal olесulаr tесhniquеsinto virtually ralytiсаltools (еspесiаliyphylogеisсovеriеs(morе on thеsе latеr)i thе iпitial ехсitеmеt-ttrеvolvеd at a nlolесn., *.,. сharaсtеrizес] ologousdеvеlopmеrrtalrеgtrlatory еry diffеrеntЬody plans. Thе first I 2 ' | i , i с h . . r n d Е ( i / r 1 ,i m p o r r а n t l in nеmatodеs' arthropods, and ) 8 5 ;Y o с h е m е t a l . 1 9 8 8 ) . B u t t h i s d i s с o v е r уt h a t v с r t е l r г l t е sс о n t a i n and tЬirt thеy arе сlrrstеrеdin thе l 9 8 9 ) . B y t h е m i d - 1 9 9 0 st h е l i s t o f : modеl systеmsof dеvеloprnеntal ] е r h а r t a n d K i г s с l r n е r1 9 9 7 ) . S u r y Ьroаd phylсlgеnеtiсdistriЬution, ; с n i d а r i a n sа n d с t е n o p h o r е s )а n d :ldеrmsаnd пrollusks). It Ьесamе (Сarroll it'' of апimаl с1еvеlopnrеnt Anirтals in diffеrеnt phyla arе so nologous strLlсturеsаnd dеtеrmin. tеntiotls(Niеlsеn 2002)' This phе. 'lrе сеntгai thеnlеs of сompагаtivе .d (Hall 1992 kaff |996). Thе no. a n i m a l sh a s a t r n i q u ес o m Ь i n а t i o n rсhitесtural(suсh as Ьody symmе. ' of сеll divisitln)o , r Ьoth (suсh аs lody-pIanсol1сеptlras dееply inflr.ranimals up ttl thе prеsеnt (Gould 97). DеvеloprrrеntalЬiolоgists, foг rofouгrddiffегеnсеsin thе way in rrorphоgеnеsisсlссur ir-rеmЬryos of 7).No onе prеdiсtесlthat rnany of t to rеgulatесlеvеlopmеntthroughl dеvеlopmеntаlor еrкllutiсlnaryЬis h o w ' t h е r i r r l i I l rg е t l < l t n i(с) r g а n i and mousе: this imagе has osсl1lhilа
bесomеan iсon of еvoiutiсlnarydеvеlopmеntаlЬiоlogy (Figurе 5). Nеarly all thе knсlwn gеnе farniliеs that еnсodе transсription faсtors arrd сеll signаlirrg systеlnsin animals datе Ьirсk at lеast to thе anсеstоr o{ all Ьilatеrians, and manv to tlrе uniсеlIulаr аnсеstor of plarrts and :lnirnals (Gеrlrart and Kirsсhnеr1997.,Сarroll еt al.2001; wilkins20О2). Thе сurrеnt dеvеlopmеn. tаl rolеs of tlrеsеrеgulatory protеins in rlodеl organisшs suсh аs Drсlsopbilr,t and Аrаbidсlpsls arе сlеarly diffеrеnt from thеir original funсtions in protozoans. Реrhapsеvеn morе rеrnаrkaЬly, sonrе of thеsе сonsеrvеd rеgulаtory protеinsarе ехprеssеdin roughly sinrilar rеgions of еmЬrvos that Ьеlong to diff е r е r rpt h y l i l ( G е r h а r t a n с l K i r s с l r n e r 1 9 9 7 . ,С а r r o l l е t a l . 2 0 0 1 ) . Т h е H o x gеnеsprovidеd thе first irnd still thе most dramatiс ехamplе, Ьut many othег orthсllogor-rsrеgulаtory gеllеs shorv similar ехprеssion amсlng distantly rеlatеd animal phyla (Figurе 5). In all thе еxсitеmеnt it has Ьееn еasy to ovеrlook thе fасt thаt п.lсlstdеvеlopmеntal rеgulаtory gеnеs do zol hаvе similar dопrains сlf ехprеssion irr diffеrеnt phyla; this oЬsеrvation suggеsts thatthеir dеvеlоpmеntal гolеs havе еvolvеd сonsidеraЬly during thе divеrsi. fiсationof irnimals (Daviсison200 l; '0Иilkins2002). Thе sorrrеtimеs.striking similaritiеsin gеnе ехprеssion thаt arе sharеd Ьеtwееn arthropods and vеrtеЬrаtеshavе Ьееn usеd to rесonstruсt thе аnаtorny of thе Ьilаtеrian аnсеstor (DеRoЬеrtis and Sasai 1996; Сarroll еt al. 2001). Rесonstruсting long-ехtinсtl]nсеstorssolеly on tlrе Ьаsis of gепе-ехprеssionsimilaritiеs involvеsmany аssulnptions аnd muсh guеsswork, howеvеr, and thе anatoшy o f t h е Ь i l i а t е r i a na n с е s t o г r е m a i n s u n с е r t a i n ( Е r w i n a n d D a v i d s o n 2 О 0 2 з \)flilkins2002).
LHх2 Dlх Оtd е|nS
Hoх-t
BMP4 t:hoпlin
Ap DП
Dп hh Ap
Nkr2.2 Msх lG-Hз
Figurе5. ТЬе Hoх pаradoх. Homсllogous gеnеs pi]ttеrn tЬе еmЬrvos of fruit fliеsаnd miсе dеspitе thе plrylogеrrеtiсdistanсе аnd phеrrotypiс dispаrity сlf thesеanimаls. Thе mсlst fаmous of thеsе аrе gеnеs сlf thе Hoх ссlmplеx, whiсh еstaЬlishposition of l.odу rеgions а|ong thе аntегoPostеrior ахis. Mаnv othеr honr
224
Еuolutioп апd Dеuеlopmепt What is сlеar at this point is that thе samе Ьasiс сomplеmеnt of dеvеlopmеntal rеgulatory gеnеs' somе of whiсh arе ехprеssеd in roughly thе samе rеgions of thе еmЬryo' сan produсе a widе divеrsity of аnimal Ьody plans. Figuring out how this сlссurs is onе of thе grand сhallеngеs of еvolutionary dеvеlopmеntal Ьiology (Gегhart and Kirsсhner 1997; Сarroll еt al. 2001; Davidson 2001). A dеtailеd rеsolution of this Hoх paradoх liеs many yеars in thе futurе, Ьut сhangеs in thе organization of dеvеlopmеntаl gеnе nеtworks arе likеly to foгm an importаnt part of thе solution (Сarroll еt al. .Wrаy 2001; Wilkins 2002; еt аl. 200З). Two Ьasiс kinds of rеwiring within gеnе nеtworks havе Ьееn doсumentеd, roughly сorrеsponding to quantitativе and qualitativе сhangеs. Thе first, or quantitаtivе' сatеgory involvеs a сhangе in thе loсation or timing of ехprеssion of a rеgulatory gеnе. Suсh сhangеs сan arisе whеn a nеtwork is altеrеd upstrеam of thе gеnе of intегеst.Thе loсation or timing of thе dеvеlopmеntal proсеssеsthе gеnе сontrols will сhangе as a rеsult, potеntially altеring organismal phеnotypе. For еxamplе, thе spatial еxtеnt of Hoх gеnе еxprеssion diffеrs in ways that сorrеspond to sеgmеnt idеntity in сrustaсеans (Avеrof and Pate| 1997) and to vеrtеЬrаl anatomy in tеtrapods (Burkе еt al. 1995). Thе sесond, or qualitativе, kind of nеtwork rеwiring еntails a сhangе in whiсh dеvеlopmеntal proсеssеs arе rеgulatеd. Thеsе сhangеs сan oссur whеn a nеt. work is altеrеd dоwnstrеаm of thе gеnе of intеrеst.For instanсе,signalingvia thе rесеptor Notсh геgulаtеs spесifiсation of nеurоnal сеll fatе in insесts and spесifiсation of whitе Ьlood сеll fatе in vеrtеЬratеs (Hеitzlеr and Simpson 1991; Guidos 2002), involving two vеry diffеrеnt sеts of еffесtor gеnеs. Sim. ilarly, thе tгansсription faсtor Ьraсhyury rеgulatеsnotoсhord dеvеlopmеntin urсhordatеs and сhordatеs Ьut plays no suсh rolе in othеr phyla, whiсh laсk this struсturе; instеad, it rеgulatеs dеvеlopmеnt of thе gut and othеr struсturеs (Tесhnau and Sсholtz 2003). Dozеns of сasеs аrе now known whеrе an еvolutionary сhangе in thе еxprеssion prоfilе or downstrеаm targеts оf a rеgulatory protеin has altеrеd anatomy. Somе сasеs еnсompass сhangеs at thе sсalе of еntirе Ьody plans, suсh as thе transition from rаdial to Ьilatеral symmеtry during еarly mеtаzoan еvolution (Martindаlе еt al. 2002) and thе latеr transition Ьaсk to radial .Wray symmеtry in есhinodеrms (Lowе and 7997). Othеrs involvе modifiсations in organs' suсh as thе tгansition from fin to limЬ during thе origin of tеtrapods (ShuЬin et a|.7997), or еvolutiоnary innovations, suсh as arthro. pod wings (Avеrof and Сohеn 1997). Еvеn subtlе diffеrеnсеs in anatomy arе oftеn thе rеsult of modifiсations in gеnе nеtworks: ехamplеs inсludе diffеrеnсеs in Ьristlе pattеrns in fliеs (Stеrn 1998; Skaеr and Simpson 2000) and сolor pattеrns on Ьuttеrflywings (Brakеfiеldet a|. 1996i Brunеtti еt al. 2001; Gompеl еt al. 2005). How do сhangеs in dеvеlopmеntal gеnе nеtwoгks arisе? Thеrе arе many ways in whiсh this сan happеn-any spесifiс intеraсtion Ьetwееn maсromol. есulеs is a link in a gеnе nеtwork' and any diffеrеnсе in intеraсtions altеrs thе nеtwork. Thе two most сommon and important kinds of nеtwork сhangеs arе proЬaЬly intеraсtions Ьеtwееn protеins and intеraсtions Ьеtwееn protеins
and rеgulatoгy sеquеnсе a Ь o l i s h i n gs u с h i n t е r а с r of mutаtions, singlе Ьasе еt аl. 200J). Mаny protе nuсlеiс aсids, and small с . hаngi d r a m а t i се f f е с t sС tion or altеr affinity dr: сan сrеatе or modify a Ьi
rеgion. Сhangеs in dеvеlopmе paсt on thе history of lif and why gеnе nеtwсlrksа
Frоm ly{aсroеvoluti
Phеnotypiс сhangеs,inсlt variation within populati mеntal еvolution at thrs l aЬout thе gеnеtiс Ьasis ft wild populations (as opp thе laЬ) or aЬout what k tion in nеtwork funсtlon happеn ovеr lсlng timеsс This pauсity of inform D е v е | с l p m е n t aЬl i o l o g i s influеnсеs of gеnеtiс anс hаvе workеd largеly witl gеnt that сompаrisons 1 nisms. For thеir part' poГ a n d h а v е f t l с u s е dp r i m а r protеins, protеin struсtL rathеr than gеnе intеrасt Тhеrе arе, of сoursе' variation in thе сoding : u l a t o r y g е n е s ( е . g . ,A y a T h е s е р o p u l a t i o n - l е v е ll o f s е g r е g а t i n gv a r i а г i o n opmеntаl mесhanisrns а toriеs (е.g.' Wray and 1998), or among popu е t a l . 2 0 0 4 ) , с a n r е v е a ll сhangеs in sеlесtion. ( аЬout population gеnе opmеnt rеmlins a gleri vеlopmеntal Ьiology.
Еuolutiсlп dпd D eUе|opmепt amе bаsiс сomplеmеnt of dеvеlop'е ехprеssеdin roughly thе samе rеlе divегsit1,of аnimаl Ьody plans. е grand сhallеngеsof еvolutionary 'sсhnеr19971 Сarroll еt al. 2ОО73 this Hox pаradox liеs many yеars zation of dеvеlopmеntal gеnе nеtlart ot thе solution (Carroll еt al. e nеtworkshavе Ьееn doсumеntеd, d qualitativесhangеs.Thе first, or n thе loсation or timing of еxprеs:an arisе whеn a nеtwork is altеrеd tion or timing of thе dеvеlopmеntal a г е s u l tp ' o r е n t i e l l ya l t e r i n go r g a n еxtеnt of Hox gеnе еxprеssion difidеntityin сгLlstaсеans(Avегof and tеtrаpods(Burkе еt al. 1995). Thе wiring еntailsa сhangе in whiсh dе]sе сhangеsсan oссur whеn a nеt: intеrеst.For instanсе,signaling via Lof nеuronаlсеll fatе in insесts аnd vеrtеЬratеs(Hеitzlеr and Simpson jiffеrеnt sеts of еffесtor gеnеs. Sim:еgulatеsnоtoсhord dеvеlopmеnt in ,uсhгolе in othеr phyla, whiсh laсk )pmеnt of tlrе gut and othег struсз аn еvolutionаryсhangе in thе ехэf a геgulatoryprotеin has altеrеd s at thе sсаlе of еntirе body plans, ttеrаl symmеtry during еaгly mеtand thе latеr transition Ьaсk to radial aу 7997). othеrs ir.rvoivеmodifiсaom fin to limЬ during thе origin of ionarу innovations,suсh as аrthro:n suЬtlе diflЪrеnсеsin anatomy arе nеtworks: ехamplеs inсludе diffег)98; Skaеr and Simpson 2000) and еld еt al. 1'9961'Brunetti еt al. 2001; rе nеtwoгks arisе? Thеrе arе many :ifiс iпtеraсtionЬеtwееnmaсromoll diffеrеnсеin intеrirсtions altеrs thе :lportаntkinds of nеtwork сhangеs r s а n d i n t е r . t с r i o nbsе t w е е np г o t е i n s
and геgulilt()rysеqttеnсеsin DNA (Davidson 200 l). Crеating, rnodifvirrg'or aЬolishingsuсh intеraсtions сan