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Ardipithecus ramidus Contents Introduction and Author List
Research Articles
5 Light on the Origin of Man
29 Ardipithecus ramidus and the Paleobiology of Early Hominids Tim D. White et al.
Editorial 9 Understanding Human Origins Bruce Alberts
News Focus 10 A New Kind of Ancestor: Ardipithecus Unveiled 14 Habitat for Humanity 15 The View From Afar
Authors’ Summaries 18 Ardipithecus ramidus and the Paleobiology of Early Hominids Tim D. White et al. 19 The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday WoldeGabriel et al. 20 Taphonomic, Avian, and Small-Vertebrate Indicators of Ardipithecus ramidus Habitat Antoine Louchart et al. 21 Macrovertebrate Paleontology and the Pliocene Habitat of Ardipithecus ramidus Tim D. White et al. 22 The Ardipithecus ramidus Skull and Its Implications for Hominid Origins Gen Suwa et al. 23 Paleobiological Implications of the Ardipithecus ramidus Dentition Gen Suwa et al. 24 Careful Climbing in the Miocene: The Forelimbs of Ardipithecus ramidus and Humans Are Primitive C. Owen Lovejoy et al. 25 The Pelvis and Femur of Ardipithecus ramidus: The Emergence of Upright Walking C. Owen Lovejoy et al. 26 Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus C. Owen Lovejoy et al.
Credit: copyright T. White, 2008
27 The Great Divides: Ardipithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes C. Owen Lovejoy et al. 28 Reexamining Human Origins in Light of Ardipithecus ramidus C. Owen Lovejoy
41 The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday Wolde Gabriel et al. 46 Taphonomic, Avian, and Small-Vertebrate Indicators of Ardipithecus ramidus Habitat Antoine Louchart et al. 50 Macrovertebrate Paleontology and the Pliocene Habitat of Ardipithecus ramidus Tim D. White et al. 57 The Ardipithecus ramidus Skull and Its Implications for Hominid Origins Gen Suwa et al. 64 Paleobiological Implications of the Ardipithecus ramidus Dentition Gen Suwa et al. 70 Careful Climbing in the Miocene: The Forelimbs of Ardipithecus ramidus and Humans Are Primitive C. Owen Lovejoy et al. 78 The Pelvis and Femur of Ardipithecus ramidus: The Emergence of Upright Walking C. Owen Lovejoy et al. 84 Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus C. Owen Lovejoy et al. 92 The Great Divides: Ardipithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes C. Owen Lovejoy et al. 99 Reexamining Human Origins in Light of Ardipithecus ramidus C. Owen Lovejoy
See also related video, Science Podcast at www.sciencemag.org/ardipithecus/
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introduction
Light on the Origin of Man Charles Darwin’s seminal work On the Origin of Species, published 150 years ago next month, contains just one understated sentence on the implications of his theory for human evolution: “Light will be thrown on the origin of man and his history.” As Darwin implied in his introduction to The Descent of Man, he felt that those implications were obvious; he appreciated, as events quickly showed, that it would be only natural to look at evolution foremost from our human perspective and contemplate what makes us unique among other primates—our large brains and ability to communicate, to create, and to understand and investigate our history and nature; our culture, society, and religion; the ability to run fast on two legs and manipulate tools; and more innovations that separate us from our primate relatives. Tracing our evolution and how we came to acquire these skills and traits, however, has been difficult. Genetic data now confirm that our closest living primate relative is the chimpanzee. We shared and evolved from a common ancestor some 6 million or more years ago. But identifying our unique genes and other genetic differences between us and our primate cousins does not reveal the nature of that ancestor, nor what factors led to the genetic changes that underlie our divergent evolutionary paths. That requires a fossil record and enough parts of past species to assess key anatomical details. It also requires knowing the habitat of early humans well, to determine their diet and evaluate what factors may have influenced their evolution through time. Many early human fossils have been found, but with a few exceptions, these are all less than 4 million years old. The key first several million years of human evolution have been poorly sampled or revealed. This issue presents 11 papers authored by a diverse international team (see following pages) describing an early hominid species, Ardipithecus ramidus, and its environment. The hominid fossils are 4.4 million years old, within this critical early part of human evolution, and represent 36 or more individuals, including much of the skull, pelvis, lower arms, and feet from one female. The papers represent three broad themes. Five focus on different parts of the anatomy that are revealing for human evolution. These show that Ardipithecus was at home both moving along trees on its palms and walking upright on the ground. Three characterize Ardipithecus’s habitat in detail, through analysis of the hosting rocks and thousands of fossils of small and large animals and plants. These show that Ardipithecus lived and ate in woodlands, not grasslands. The first paper presents an overview, and it and the last two papers trace early human evolution and synthesize a new view of our last common ancestor with chimps. One conclusion is that chimps have specialized greatly since then and thus are poor models for that ancestor and for understanding human innovations such as our ability to walk.
These papers synthesize an enormous amount of data collected and analyzed over decades by the authors. Because of the scope of these papers and the special broad interest in the topic of human evolution, we have expanded our usual format for papers and coverage. The papers include larger figures, tables, and discussions, and the overview and two concluding papers provide extended introductions and analyses. In addition, to aid understanding and introduce the main results of each paper, the authors provide a one-page summary of each paper, with an explanatory figure aimed at the general reader. Our News Focus section, written by Ann Gibbons, provides further analysis and coverage, and it includes maps and a portrait of the meticulous and at times grueling field research behind the discoveries. Available online are a video interview and a podcast with further explanations. To accommodate this material and allow the full papers, this print issue presents an Editorial, News coverage, the authors’ summaries, and four papers in full: the overview paper and one key paper from each thematic group above. The other research papers, and of course all content, are fully available online. In addition, a special online page (www.sciencemag.org/Ardipithecus/) links to several print and download packages of this material for AAAS members, researchers, educators, and other readers. This collection, essentially an extra issue of Science in length, reflects efforts by many behind the scenes. Every expert reviewer evaluated, and improved, multiple papers, and several commented on all 11 of them. The authors provided the summaries on top of an already large writing and revision effort. Paula Kiberstis helped in their editing. The figures and art were drafted and improved by J. H. Matternes, Henry Gilbert, Kyle Brudvik, and Josh Carlson, as well as Holly Bishop, Nathalie Cary, and Yael Kats at Science. Numerous other Science copyediting, proofreading, and production staff processed this content on top of their regular loads. Finally, special thanks go to the people of Ethiopia for supporting and facilitating this and other research into human origins over many years, and for curating Ardipithecus ramidus for future research and for all of us to admire. Ardipithecus ramidus thus helps us bridge the better-known, more recent part of human evolution, which has a better fossil record, with the scarcer early human fossils and older ape fossils that precede our last common ancestor. Ardipithecus ramidus is a reminder of Darwin’s conclusion of The Origin: There is grandeur in this view of life, with its several powers, having been originally breathed into a few forms or into one; and that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved. – Brooks Hanson
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The Authors
Giday WoldeGabriel Earth Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USA. Antoine Louchart UMR 5125 PEPS CNRS, France, Université Lyon 1, 69622 Villeurbanne Cedex, France, and Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Lyon 1, CNRS, INRA, Ecole Normale Supérieure de Lyon, France. Gen Suwa The University Museum, the University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
C. Owen Lovejoy Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44240–0001, USA.
Stanley H. Ambrose Department of Anthropology, University of Illinois, Urbana, IL 61801, USA.
Berhane Asfaw Rift Valley Research Service, P.O. Box 5717, Addis Ababa, Ethiopia.
Doris Barboni CEREGE (UMR6635 CNRS/Université Aix-Marseille), BP80, F-13545 Aix-en-Provence Cedex 4, France. Raymond L. Bernor National Science Foundation, GEO:EAR:SEPS Sedimentary Geology and Paleobiology Program, Arlington, VA 22230, and College of Medicine, Department of Anatomy, Laboratory of Evolutionary Biology, Howard University, 520 W St., Washington, DC 20059, USA.
Michel Brunet Collège de France, Chaire de Paléontologie Humaine, 3 Rue d’Ulm, F-75231 Paris Cedex 05, France.
Brian Currie Department of Geology, Miami University, Oxford, OH 45056, USA.
Yonas Beyene Department of Anthropology and Archaeology, Authority for Research and Conservation of the Cultural Heritage, Ministry of Youth, Sports and Culture, P.O. Box 6686, Addis Ababa, Ethiopia. Michael T. Black Phoebe A. Hearst Museum of Anthropology, 103 Kroeber Hall, no. 3712, University of California Berkeley, Berkeley, CA 94720–3712, USA. Robert J. Blumenschine Center for Human Evolutionary Studies, Department of Anthropology, Rutgers University, 131 George St., New Brunswick, NJ 08901–1414, USA. Jean-Renaud Boisserie Paléobiodiversité et Paléoenvironnements, UMR CNRS 5143, USM 0203, Muséum National d’Histoire Naturelle, 8 Rue Buffon, CP 38, 75231 Paris Cedex 05, France, and Institut de Paléoprimatologie et Paléontologie Humaine, Évolution et Paléoenvironnements, UMR CNRS 6046, Université de Poitiers, 40 Avenue du Recteur-Pineau, 86022 Poitiers Cedex, France.
Mesfin Asnake Ministry of Mines and Energy, P.O. Box 486, Addis Ababa, Ethiopia.
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Laurent Bremond Center for Bio-Archaeology and Ecology (UMR5059 CNRS/Université Montpellier 2/EPHE), Institut de Botanique, F-34090 Montpellier, France.
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Raymonde Bonnefille CEREGE (UMR6635 CNRS/Université AixMarseille), BP80, F-13545 Aix-en-Provence Cedex 4, France.
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David DeGusta Department of Anthropology, Stanford University, Stanford, CA 94305–2034, USA.
Eric Delson Department of Anthropology, Lehman College/CUNY, Bronx, NY 10468; NYCEP; and Department of Vertebrate Paleontology, American Museum of Natural History; New York, NY 10024, USA. Stephen Frost Department of Anthropology, University of Oregon, Eugene, OR, 97403–1218, USA.
Nuria Garcia Dept. Paleontología, Universidad Complutense de Madrid & Centro de Evolución y Comportamiento Humanos, ISCIII, C/ Sinesio Delgado 4, Pabellón 14, 28029 Madrid, Spain. Ioannis X. Giaourtsakis Ludwig Maximilians University of Munich, Department of Geo- and Environmental Sciences, Section of Paleontology. Richard-Wagner-Strasse 10, D-80333 Munich, Germany.
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CREDITS: PHOTOS COURTESY OF THE AUTHORS
Tim D. White Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California at Berkeley, Berkeley, CA 94720, USA.
SPECIALSECTION Yohannes Haile-Selassie Department of Physical Anthropology, Cleveland Museum of Natural History, 1 Wade Oval Drive, Cleveland, OH 44106, USA.
Thomas Lehmann Senckenberg Forschungsinstitut, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany.
Gina Semprebon Science and Mathematics, Bay Path College, 588 Longmeadow St., Longmeadow, MA 01106, USA.
William K. Hart Department of Geology, Miami University, Oxford, OH 45056, USA.
Andossa Likius Département de Paléontologie, Université de N’Djamena, BP 1117, N’Djamena, Chad.
Scott W. Simpson Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106–4930, USA.
Jay H. Matternes 4328 Ashford Lane, Fairfax, VA 22032, USA.
Linda Spurlock Cleveland Museum of Natural History, Cleveland, OH 44106–4930, USA.
Alison M. Murray Department of Biological Sciences, University of Alberta, Edmonton AB T6G2E9, Canada.
Kathlyn M. Stewart Paleobiology, Canadian Museum of Nature, Ottawa, K1P 6P4, Canada.
Leslea J. Hlusko Human Evolution Research Center and Department of Integrative Biology, University of California at Berkeley, 3010 Valley Life Sciences Building, Berkeley, CA, 94720, USA. F. Clark Howell Human Evolution Research Center and Department of Anthropology, 3101 Valley Life Sciences Building, University of California at Berkeley, Berkeley, CA 94720, USA (deceased). M. C. Jolly-Saad Université Paris-Ouest La Défense, Centre Henri Elhaï, 200 Avenue de la République, 92001 Nanterre, France. Reiko T. Kono Department of Anthropology, National Museum of Nature and Science, Hyakunincho, Shinjuku-ku, Tokyo, 169-0073, Japan.
CREDITS: PHOTOS COURTESY OF THE AUTHORS
Daisuke Kubo Department of Biological Sciences, Graduate School of Science, the University of Tokyo, Tokyo, 113-0033, Japan.
Jackson K. Njau Human Evolution Research Center and Department of Integrative Biology, University of California at Berkeley, 3010 Valley Life Sciences Building, Berkeley, CA, 94720, USA. Cesur Pehlevan University of Yuzuncu Yil, Department of Anthropology, The Faculty of Science and Letters, Zeve Yerlesimi 65080 Van, Turkey.
Denise F. Su Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA.
Mark Teaford Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, 1830 E. Monument St., Room 303, Baltimore, MD 21205.
Paul R. Renne Berkeley Geochronology Center, 2455 Ridge Road, Berkeley, CA 94709, and Department of Earth and Planetary Science, University of California at Berkeley, Berkeley, CA 94720, USA.
Bruce Latimer Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106–4930, USA.
www.sciencemag.org
Haruo Saegusa Institute of Natural and Environmental Sciences, University of Hyogo, Yayoigaoka, Sanda 669-1546, Japan.
SCIENCE
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Elisabeth Vrba Department of Geology and Geophysics, Yale University, New Haven, CT 06520, USA.
Henry Wesselman P.O. Box 369, Captain Cook, Hawaii, 96704, USA.
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EDITORIAL
Understanding Human Origins RESPONDING TO A QUESTION ABOUT HIS SOON-TO-BE-PUBLISHED ON THE ORIGIN OF SPECIES,
CREDITS: (TOP) TOM KOCHEL; (RIGHT) ISTOCKPHOTO.COM
Bruce Alberts is Editorin-Chief of Science.
Charles Darwin wrote in 1857 to Alfred Russel Wallace, “You ask whether I shall discuss ‘man’; I think I shall avoid the whole subject, as so surrounded with prejudices, though I freely admit that it is the highest and most interesting problem for the naturalist.” Only some 14 years later, in The Descent of Man, did Darwin address this “highest problem” head-on: There, he presciently remarked in his introduction that “It has often and confidently been asserted, that man’s origin can never be known: but . . . it is those who know little, and not those who know much, who so positively assert that this or that problem will never be solved by science.” Darwin was certainly right. The intervening years provide conclusive evidence that it is very unwise to predict limits for what can be discovered through science. In fact, it now seems likely that, through synergistic advances in many disciplines, scientists will eventually decipher a substantial portion of the detailed evolutionary history of our own species at both the morphological and molecular levels. First, what can we expect from paleoanthropology? In this 200th anniversary year of Darwin’s birth, Science is pleased to publish the results of many years of scientific research that suggest an unexpected form for our last common ancestor with chimpanzees. This issue contains 11 Research Articles involving more than 40 authors, plus News articles that describe the life and times of Ardipithecus ramidus, a hominid species that lived 4.4 million years ago in the Afar Rift region of northeastern Ethiopia. This region exposes a total depth of 300 meters of sediments that were deposited in rivers, lakes, and floodplains between about 5.5 and 3.8 million years ago. Even considering only this one site (there are many others), it is staggering to reflect on the huge number of hominid remains that can in principle be discovered, given sufficient time and effort. Moreover, the history of science assures us that powerful new techniques will be developed in the coming years to accelerate such research, as they have been in the past. We can thus be certain that scientists will eventually obtain a rather detailed record showing how the anatomy of the human body evolved over many millions of years. What can we expect from a combination of genetics, genomics, biochemistry, and comparative organismal biology? We will want to interpret the history of the morphological transformations in the humanoid skeleton and musculature in terms of the molecular changes in the DNA that caused them. Genes and their regulatory regions control the morphology of animals through very complex biochemical processes that affect cell behavior during embryonic development. Nevertheless, experimental studies of model organisms such as fruit flies, worms, fish, and mice are advancing our understanding of the molecular mechanisms involved. New inexpensive methods for deciphering the complete genome sequence of any organism will soon accelerate this process, allowing scientists to analyze the recurring evolutionary morphological transformations that have been identified by organismal biologists,* so as to determine the specific DNA changes involved. And the DNA sequences that have changed most rapidly during recent human evolution are being cataloged, providing a new tool for finding important molecular differences that distinguish us from chimpanzees.† The majesty of the discoveries already made represents a major triumph of the human intellect. And, as emphasized here, there will be many more discoveries to come. Darwin’s summary of his own efforts to understand human evolution is thus still relevant today: “Man may be excused for feeling some pride at having risen, though not through his own exertions, to the very summit of the organic scale; and the fact of his having thus risen, instead of having been aboriginally placed there, may give him hope for a still higher destiny – Bruce Alberts in the distant future.” 10.1126/science.1182387
*R. L. Mueller et al., Proc. Natl. Acad. Sci. U.S.A. 101, 3820 (2004). †S. Prabhakar et al., Science 314, 786 (2006).
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NEWSFOCUS
A New Kind of Ancestor: Ardipithecus Unveiled The oldest known hominin skeleton reveals the body plan of our very early ancestors and the upright origins of humankind
From the inside out. Artist’s reconstructions show how Ardi’s skeleton, muscles, and body looked and how she would have moved on top of branches.
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CREDITS: ILLUSTRATIONS © 2009, J. H. MATTERNES
Every day, scientists add new pages to the story of human evolution by deciphering clues to our past in everything from the DNA in our genes to the bones and artifacts of thousands of our ancestors. But perhaps once each generation, a spectacular fossil reveals a whole chapter of our prehistory all at once. In 1974, it was the famous 3.2-million-year-old skeleton “Lucy,” who proved in one stroke that our ancestors walked upright before they evolved big brains. Ever since Lucy’s discovery, researchers have wondered what came before her. Did the earliest members of the human family walk upright like Lucy or on their knuckles like chimpanzees and gorillas? Did they swing through the trees or venture into open grasslands? Researchers have had only partial, fleeting glimpses of Lucy’s own ancestors—the earliest hominins, members of the group that includes humans and our ancestors (and are sometimes called hominids). Now, in a special section beginning on page 60 and online, a multidisciplinary international team presents the oldest known skeleton of a potential human ancestor, 4.4-million-year-old Ardipithecus ramidus from Aramis, Ethiopia. This remarkably rare skeleton is not the oldest putative hominin, but it is by far the most complete of the earliest specimens. It includes most of the skull and teeth, as well as the pelvis, hands, and feet—parts that the authors say reveal an “intermediate” form of upright walking, consid-
Ardipithecus Ardipithecus ramidus ramidusNEWSFOCUS NEWSFOCUS ered ered a hallmark a hallmark of hominins. of hominins. “We “We thought thought LucyLucy was the wasfind the find of the of the “The“The authors authors … are …framing are framing the debate the debate that will that will inevitably inevitably follow,” follow,” century century but, in but, retrospect, in retrospect, it isn’t,” it isn’t,” says says paleoanthropologist paleoanthropologist Andrew Andrew because because the description the description and interpretation and interpretation of theoffinds the finds are entwined, are entwined, Hill of Hill Yale of Yale University. University. “It’s “It’s worth worth the wait.” the wait.” says says Pilbeam. Pilbeam. “My“My first first reaction reaction is to is betoskeptical be skeptical aboutabout somesome of theof the To some To some researchers’ researchers’ surprise, surprise, the female the female skeleton skeleton doesn’t doesn’t looklook conclusions,” conclusions,” including including that human that human ancestors ancestors nevernever wentwent through through a a muchmuch like alike chimpanzee, a chimpanzee, gorilla, gorilla, or any or of anyour ofclosest our closest livingliving primate primate chimpanzee-like chimpanzee-like phase. phase. Other Other researchers researchers are focusing are focusing intently intently on on relatives. relatives. EvenEven though though this species this species probably probably livedlived soonsoon afterafter the dawn the dawn the lower the lower skeleton, skeleton, where where somesome of the ofanatomy the anatomy is soisprimitive so primitive that that of humankind, of humankind, it was it was not transitional not transitional between between African African apesapes and and they they are beginning are beginning to argue to argue over over just what just what it means it means to beto“bipedal.” be “bipedal.” humans. humans. “We “We havehave seen seen the ancestor, the ancestor, and itand is not it isanot chimpanzee,” a chimpanzee,” says says The The pelvis, pelvis, for example, for example, offers offers onlyonly “circumstantial” “circumstantial” evidence evidence for for paleoanthropologist paleoanthropologist Tim White Tim White of theofUniversity the University of California, of California, BerkeBerkeupright upright walking, walking, says says Walker. Walker. But however But however the debate the debate aboutabout Ardi’s Ardi’s ley, co-director ley, co-director of theofMiddle the Middle Awash Awash research research group, group, which which discovered discovered locomotion locomotion and identity and identity evolves, evolves, she provides she provides the first the first hardhard evidence evidence and analyzed and analyzed the fossils. the fossils. that that will will inform inform and constrain and constrain future future ideasideas Instead, Instead, the skeleton the skeleton and pieces and pieces of at of least at least 35 additional 35 additional individuals individuals aboutabout the ancient the ancient hominin hominin bauplan. bauplan. of Ar.oframidus Ar. ramidus reveal reveal a new a new type type of early of early hominin hominin that was that was neither neither Digging it it chimpanzee chimpanzee nor human. nor human. Although Although the team the team suspects suspects that Ar. thatramidus Ar. ramidussciencemag.org sciencemag.org Digging may may havehave givengiven rise to riseLucy’s to Lucy’s genus, genus, Australopithecus, Australopithecus, the fossils the fossils The first The first glimpse glimpse of this ofstrange this strange creature creature camecame Podcast Podcast interview interview “show “show for the forfirst the first time time that there that there is some is some new new evolutionary evolutionary gradegrade of of on 17onDecember 17 December 19921992 whenwhen a former a former graduate graduate with author with author hominid hominid that isthat notisAustralopithecus, not Australopithecus, that isthat notisHomo,” not Homo,” says says paleontolpaleontol-Ann Gibbons student student of White’s, of White’s, Gen Gen Suwa, Suwa, saw saw a glint a glint Ann Gibbons on on Ardipithecus Ardipithecus and and ogistogist Michel Michel Brunet Brunet of theofCollege the College de France de France in Paris. in Paris. among among the pebbles the pebbles of the of desert the desert pavement pavement fieldwork in theinAfar. the Afar. near near In 11Inpapers 11 papers published published in this in issue this issue and online, and online, the team the team of 47of 47fieldwork the village the village of Aramis. of Aramis. It was It the waspolished the polished researchers researchers describes describes how how Ar. ramidus Ar. ramidus looked looked and moved. and moved. The skeleThe skelesurface surface of a of tooth a tooth root,root, and he andimmediately he immediately ton, ton, nicknamed nicknamed “Ardi,” “Ardi,” is from is from a female a female who who livedlived in a in woodland a woodland knewknew it wasit awas hominin a hominin molar. molar. OverOver the next the next few days, few days, the team the team scoured scoured (see (see sidebar, sidebar, p. 40), p. 40), stoodstood aboutabout 120 centimeters 120 centimeters tall, tall, and weighed and weighed the area the area on hands on hands and knees, and knees, as they as they do whenever do whenever an important an important piecepiece aboutabout 50 kilograms. 50 kilograms. She was She thus was thus as big asas biga chimpanzee as a chimpanzee and had and ahad of a hominin of hominin is found is found (see story, (see story, p. 41), p. and 41), collected and collected the lower the lower jaw of jaw a of a brainbrain size size to match. to match. But she But did shenot didknuckle-walk not knuckle-walk or swing or swing through through childchild with with the milk the milk molarmolar still attached. still attached. The molar The molar was so was primitive so primitive that that the trees the trees like living like living apes.apes. Instead, Instead, she walked she walked upright, upright, planting planting her her the team the team knewknew they they had found had found a hominin a hominin both both olderolder and more and more primitive primitive feet flat feeton flatthe onground, the ground, perhaps perhaps eating eating nuts,nuts, insects, insects, and small and small mammamthan than Lucy.Lucy. Yet the Yetjaw thealso jaw had alsoderived had derived traits—novel traits—novel evolutionary evolutionary char-charmalsmals in theinwoods. the woods. acters—shared acters—shared withwith Lucy’s Lucy’s species, species, Au. afarensis, Au. afarensis, suchsuch as anasupper an upper She was She awas “facultative” a “facultative” biped, biped, say the sayauthors, the authors, still living still living in both in both canine canine shaped shaped like alike diamond a diamond in side in view. side view. worlds—upright worlds—upright on the onground the ground but also but also able able to move to move on allonfours all fours on on The The teamteam reported reported 15 years 15 years ago in agoNature in Nature that that the fragmentary the fragmentary top of top branches of branches in theintrees, the trees, with with an opposable an opposable big toe bigtotoe grasp to grasp limbs. limbs. fossils fossils belonged belonged to the to“long-sought the “long-sought potential potential root root species species for the for the “These “These things things werewere veryvery odd odd creatures,” creatures,” says says paleoanthropologist paleoanthropologist Hominidae.” Hominidae.” (They (They first first called called it Au.it ramidus, Au. ramidus, then,then, afterafter finding finding AlanAlan Walker Walker of Pennsylvania of Pennsylvania StateState University, University, University University Park.Park. “You“You partsparts of the ofskeleton, the skeleton, changed changed it to it Ar.toramidus—for Ar. ramidus—for the Afar the Afar words words knowknow whatwhat Tim Tim [White] [White] onceonce said:said: If you If wanted you wanted to find to find something something for “root” for “root” and “ground.”) and “ground.”) In response In response to comments to comments that he thatneeded he needed leg leg that moved that moved like these like these things, things, you’dyou’d havehave to gototogo thetobar theinbar Star in Wars.” Star Wars.” bones bones to prove to prove Ar. ramidus Ar. ramidus was an wasupright an upright hominin, hominin, White White jokedjoked that that MostMost researchers, researchers, who who havehave waited waited 15 years 15 years for the forpublication the publication of of he would he would be delighted be delighted withwith moremore parts,parts, specifically specifically a thigh a thigh and an and an this find, this find, agreeagree that Ardi that Ardi is indeed is indeed an early an early hominin. hominin. TheyThey praise praise the the intactintact skull,skull, as though as though placing placing an order. an order. detailed detailed reconstructions reconstructions needed needed to piece to piece together together the crushed the crushed bones. bones. Within Within 2 months, 2 months, the team the team delivered. delivered. In November In November 1994,1994, as theasfosthe fos“This“This is anisextraordinarily an extraordinarily impressive impressive workwork of reconstruction of reconstruction and and sil hunters sil hunters crawled crawled up anupembankment, an embankment, Berkeley Berkeley graduate graduate student student description, description, well well worth worth waiting waiting for,” for,” says says paleoanthropologist paleoanthropologist David David Yohannes Yohannes Haile-Selassie Haile-Selassie of Ethiopia, of Ethiopia, now now a paleoanthropologist a paleoanthropologist at theat the Pilbeam Pilbeam of Harvard of Harvard University. University. “They “They did this did job thisvery, job very, veryvery well,” well,” Cleveland Cleveland Museum Museum of Natural of Natural History History in Ohio, in Ohio, spotted spotted two pieces two pieces of a of a agrees agrees neurobiologist neurobiologist Christoph Christoph Zollikofer Zollikofer of the of University the University of of bonebone fromfrom the palm the palm of a hand. of a hand. ThatThat was soon was soon followed followed by pieces by pieces of a of a Zurich Zurich in Switzerland. in Switzerland. pelvis; pelvis; leg, ankle, leg, ankle, and foot and foot bones; bones; manymany of theofbones the bones of theofhand the hand and and But not Buteveryone not everyone agrees agrees withwith the team’s the team’s interpretations interpretations aboutabout how how arm;arm; a lower a lower jaw with jaw with teeth—and teeth—and a cranium. a cranium. By January By January 1995,1995, it wasit was Ar. ramidus Ar. ramidus walked walked upright upright and what and what it reveals it reveals aboutabout our ancestors. our ancestors. apparent apparent that they that they had made had made the rarest the rarest of rare of finds, rare finds, a partial a partial skeleton. skeleton. CREDITS: (LEFT) C. O. LOVEJOY ET AL., SCIENCE; (TOP) G. SUWA ET AL., SCIENCE; (BOTTOM) C. O. LOVEJOY ET AL., SCIENCE; (RIGHT) C. O. LOVEJOY ET AL., SCIENCE
CREDITS: (LEFT) C. O. LOVEJOY ET AL., SCIENCE; (TOP) G. SUWA ET AL., SCIENCE; (BOTTOM) C. O. LOVEJOY ET AL., SCIENCE; (RIGHT) C. O. LOVEJOY ET AL., SCIENCE
Online Online
Unexpected Unexpected anatomy. anatomy. Ardi has Ardianhas opposable an opposable toe (left) toe (left) and flexible and flexible hand hand (right); (right); her canines her canines (top center) (top center) are sized are sized between between thosethose of a human of a human (top left) (topand left)chimp and chimp (top right); (top right); and the andblades the blades of herofpelvis her pelvis (lower(lower left) are left)broad are broad like Lucy’s like Lucy’s (yellow). (yellow).
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NEWSFOCUS NEWSFOCUS Ardipithecus Ardipithecusramidus ramidus FOSSILS FOSSILSOFOFTHE THEHUMAN HUMANFAMILY FAMILY
H. H. floresiensis floresiensis
HOMO HOMO
Indonesia Indonesia
H. H. heidelbergensis heidelbergensis Europe Europe
Kenyanthropus Kenyanthropus platyops? platyops? Kenya Kenya
H. H. habilis habilis H. H. erectus erectus
Sub-Saharan Sub-Saharan Africa Africa andand AsiaAsia Africa Africa
SAHELANTHROPUS SAHELANTHROPUS AUSTRALOPITHECUS AUSTRALOPITHECUS Ar.Ar. ramidus ramidus
Ethiopia Ethiopia
Ardi Ardi Ethiopia, Ethiopia, Kenya Kenya
Ethiopia Ethiopia
Kenya, Kenya, Ethiopia Ethiopia
Au.Au. africanus africanus Au.Au. robustus robustus Taung Taung Child Child South South Africa Africa
South South Africa Africa
Au.Au. bahrelghazali bahrelghazali ? ?
O. O. tugenensis tugenensis
Au.Au. boisei boisei Eastern Eastern Africa Africa 2 2
4 4
5 5
3 3
Abel Abel Chad Chad Au.Au. aethiopicus aethiopicus Eastern Eastern Africa Africa
Millennium Millennium Man Man Kenya Kenya 6 6
Worldwide Worldwide
Eastern Eastern Africa Africa
Au.Au. afarensis afarensis Lucy Lucy Ethiopia, Ethiopia, Tanzania Tanzania
ORRORIN ORRORIN
Pliocene Pliocene Epoch Epoch
H. H. sapiens sapiens
? ? Au.Au. rudolfensis rudolfensis
Pleistocene Pleistocene Epoch Epoch
Today Today
Ar.Ar. kadabba kadabba
Toumaï Toumaï Chad Chad
7 Million Years Ago 7 Million Years Ago
S. tchadensis S. tchadensis
Miocene Miocene Epoch Epoch
Au.Au. garhi garhi
Au.Au. anamensis anamensis
Europe Europe andand AsiaAsia
1 Million Years Ago 1 Million Years Ago
ARDIPITHECUS ARDIPITHECUS
H. H. neanderthalensis neanderthalensis
Holocene Holocene Epoch Epoch
CREDITS: (TIMELINE LEFT TO RIGHT) L. PÉRON/WIKIPEDIA, B. G. RICHMOND ET AL., SCIENCE 319, 1662 (2008); © T. WHITE 2008; WIKIPEDIA; TIM WHITE; TIM WHITE; (PHOTO) D. BRILL
It It is is one one ofof only only a half-dozen a half-dozen such such skeletons skeletons known known from from more more than than onon thethe task. task. “You “You gogo piece piece byby piece.” piece.” 1 million 1 million years years ago, ago, and and thethe only only published published one one older older than than Lucy. Lucy. Once Once hehe had had reassembled reassembled thethe pieces pieces in in a digital a digital reconstruction, reconstruction, hehe It was It was thethe find find ofof a lifetime. a lifetime. But But thethe team’s team’s excitement excitement was was tempered tempered and and paleoanthropologist paleoanthropologist Berhane Berhane Asfaw Asfaw ofof thethe Rift Rift Valley Valley Research Research byby thethe skeleton’s skeleton’s terrible terrible condition. condition. The The bones bones literally literally crumbled crumbled when when Service Service in in Addis Addis Ababa Ababa compared compared thethe skull skull with with those those ofof ancient ancient and and touched. touched. White White called called it road it road kill. kill. And And parts parts ofof thethe skeleton skeleton had had been been living living primates primates in in museums museums worldwide. worldwide. ByBy March March ofof this this year, year, Suwa Suwa trampled trampled and and scattered scattered into into more more than than 100 100 fragments; fragments; thethe skull skull was was was was satisfied satisfied with with hishis 10th 10th reconstruction. reconstruction. Meanwhile Meanwhile in in Ohio, Ohio, crushed crushed to to 4 centimeters 4 centimeters in in height. height. The The researchers researchers decided decided to to remove remove Lovejoy Lovejoy made made physical physical models models ofof thethe pelvic pelvic pieces pieces based based onon thethe origorigentire entire blocks blocks ofof sediment, sediment, covering covering thethe blocks blocks in in plaster plaster and and moving moving inal inal fossil fossil and and thethe CTCT scans, scans, working working closely closely with with Suwa. Suwa. HeHe is also is also satsatthem them to to thethe National National Museum Museum ofof isfied isfied that that thethe 14th 14th version version ofof thethe Ethiopia Ethiopia in in Addis Addis Ababa Ababa to to finish finish pelvis pelvis is is accurate. accurate. “There “There was was anan excavating excavating thethe fossils. fossils. Ardipithecus Ardipithecus that that looked looked just just like like It It took took three three field field seasons seasons to to that,” that,” hehe says, says, holding holding upup thethe final final uncover uncover and and extract extract thethe skeleton, skeleton, model model in in hishis lab. lab. repeatedly repeatedly crawling crawling thethe site site toto Putting Putting their their heads heads together together gather gather 100% 100% ofof thethe fossils fossils prespresent. ent. AtAt last last count, count, thethe team team had had AsAs they they examined examined Ardi’s Ardi’s skull, skull, cataloged cataloged more more than than 110 110 specispeciSuwa Suwa and and Asfaw Asfaw noted noted a number a number mens mens ofof Ar.Ar. ramidus, ramidus, notnot to to menmenofof characteristics. characteristics. Her Her lower lower face face tion tion 150,000 150,000 specimens specimens ofof fossil fossil had had a muzzle a muzzle that that juts juts outout less less than than plants plants and and animals. animals. “This “This team team a chimpanzee’s. a chimpanzee’s. The The cranial cranial base base is is seems seems to to suck suck fossils fossils outout ofof thethe short short from from front front to to back, back, indicatindicatearth,” earth,” says says anatomist anatomist C.C. Owen Owen inging that that herher head head balanced balanced atop atop thethe Lovejoy Lovejoy ofof Kent Kent State State University University spine spine asas in in later later upright upright walkers, walkers, in in Ohio, Ohio, who who analyzed analyzed thethe postpost- Fossil rather than than to to thethe front front ofof thethe spine, spine, Fossil finders. finders. TimTim White White and and local local Afar Afar fossil fossil hunters hunters pool pool their their finds finds after after rather scouring thethe hillside hillside at Aramis. at Aramis. cranial cranial bones bones butbut didn’t didn’t work work in in scouring asas in in quadrupedal quadrupedal apes. apes. Her Her face face is is thethe f ield. f ield. InIn thethe lab, lab, hehe gently gently in in a more a more vertical vertical position position than than in in unveils unveils a cast a cast ofof a tiny, a tiny, pea-sized pea-sized sesamoid sesamoid bone bone forfor effect. effect. “Their “Their chimpanzees. chimpanzees. And And herher teeth, teeth, like like those those ofof allall later later hominins, hominins, lack lack thethe obsessiveness obsessiveness gives gives you—this!” you—this!” daggerlike daggerlike sharpened sharpened upper upper canines canines seen seen in in chimpanzees. chimpanzees. The The team team White White himself himself spent spent years years removing removing thethe silty silty clay clay from from thethe fragile fragile realized realized that that this this combination combination ofof traits traits matches matches those those ofof anan even even older older fossils fossils at at thethe National National Museum Museum in in Addis Addis Ababa, Ababa, using using brushes, brushes, skull, skull, 6-million 6-million to to 7-million-year-old 7-million-year-old Sahelanthropus Sahelanthropus tchadensis, tchadensis, syringes, syringes, and and dental dental tools, tools, usually usually under under a microscope. a microscope. Museum Museum techtech- found found byby Brunet’s Brunet’s team team in in Chad. Chad. They They conclude conclude that that both both represent represent anan nician nician Alemu Alemu Ademassu Ademassu made made a precise a precise cast cast ofof each each piece, piece, and and thethe early early stage stage ofof human human evolution, evolution, distinct distinct from from both both Australopithecus Australopithecus and and team team assembled assembled them them into into a skeleton. a skeleton. chimpanzees. chimpanzees. “Similarities “Similarities with with Sahelanthropus Sahelanthropus areare striking, striking, in in that that it it Meanwhile Meanwhile in in Tokyo Tokyo and and Ohio, Ohio, Suwa Suwa and and Lovejoy Lovejoy made made virtual virtual also also represents represents a first-grade a first-grade hominid,” hominid,” agrees agrees Zollikofer, Zollikofer, who who diddid aa reconstructions reconstructions ofof thethe crushed crushed skull skull and and pelvis. pelvis. Certain Certain fossils fossils were were three-dimensional three-dimensional reconstruction reconstruction ofof that that skull. skull. taken taken briefly briefly to to Tokyo Tokyo and and scanned scanned with with a custom a custom micro–computed micro–computed Another, Another, earlier earlier species species ofof Ardipithecus—Ar. Ardipithecus—Ar. kadabba, kadabba, dated dated tomography tomography (CT) (CT) scanner scanner that that could could reveal reveal what what was was hidden hidden inside inside thethe from from 5.55.5 million million to to 5.85.8 million million years years ago ago butbut known known only only from from teeth teeth bones bones and and teeth. teeth. Suwa Suwa spent spent 9 years 9 years mastering mastering thethe technology technology to to and and bits bits and and pieces pieces ofof skeletal skeletal bones—is bones—is part part ofof that that grade, grade, too. too. And And reassemble reassemble thethe fragments fragments ofof thethe cranium cranium into into a virtual a virtual skull. skull. “I “I used used 6565 Ar.Ar. kadabba’s kadabba’s canines canines and and other other teeth teeth seem seem to to match match those those ofof a third a third pieces pieces ofof thethe cranium,” cranium,” says says Suwa, Suwa, who who estimates estimates hehe spent spent 1000 1000 hours hours very very ancient ancient specimen, specimen, 6-million-year-old 6-million-year-old Orrorin Orrorin tugenensis tugenensis from from
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Filling Filling a gap. a gap. Ardipithecus Ardipithecus provides provides a link a link between between earlier earlier andand later later hominins, hominins, as as seen seen in in thisthis timeline timeline showing showing important important hominin hominin fossils fossils andand taxa. taxa.
Ardipithecus Ardipithecusramidus ramidus NEWSFOCUS NEWSFOCUS Kenya, ered awhich hallmark alsoofhas hominins. a “We thought Lucy was the find of the “The authors … are framing the debate that will inevitably follow,” thighbone century but, thatinappears retrospect, it isn’t,” says paleoanthropologist Andrew because the description and interpretation of the finds are entwined, to Hill have of been Yale University. used for “It’s worth the wait.” says Pilbeam. “My first reaction is to be skeptical about some of the upright Towalking some researchers’ (Science, surprise, the female skeleton doesn’t look conclusions,” including that human ancestors never went through a 21 much Marchlike 2008, a chimpanzee, p. 1599). gorilla, or any of our closest living primate chimpanzee-like phase. Other researchers are focusing intently on So,relatives. “this raises Even though the in-this species probably lived soon after the dawn the lower skeleton, where some of the anatomy is so primitive that triguing of humankind, possibility it was that not transitional between African apes and they are beginning to argue over just what it means to be “bipedal.” we’re humans. looking “We at have the same seen the ancestor, and it is not a chimpanzee,” says The pelvis, for example, offers only “circumstantial” evidence for genus” paleoanthropologist for specimens Tim White of the University of California, Berke- upright walking, says Walker. But however the debate about Ardi’s now ley,put co-director in three of genera, the Middle Awash research group, which discovered locomotion and identity evolves, she provides the first hard evidence says andPilbeam. analyzed the But fossils. the that will inform and constrain future ideas discoverers Instead, of theO. skeleton tuge- and pieces of at least 35 additional individuals about the ancient hominin bauplan. nensis of Ar. aren’t ramidus so sure. reveal “Asafor new Ardi type andofOrrorin early hominin being thethat same was genus, neither Digging it no,chimpanzee I don’t thinknor this human. is possible, Although unless theone team really suspects wantsthat to accept Ar. ramidus an sciencemag.org unusual may have amount given of variability” rise to Lucy’s within genus, a taxon, Australopithecus, says geologistthe Martin fossils The first glimpse of this strange creature came Podcast interview Pickford “show of forthe theCollege first time dethat France, therewho is some found new Orrorin evolutionary with Brigitte grade of on 17 December 1992 when a former graduate with author Senut hominid of thethat National is not Australopithecus, Museum of Natural thatHistory is not Homo,” in Paris.says paleontolstudent of White’s, Gen Suwa, saw a glint Ann Gibbons on Ardipithecus and ogist Whatever Michel theBrunet taxonomy of theofCollege Ardipithecus de France and in theParis. other very ancient among the pebbles of the desert pavement fieldwork in the Afar. hominins, In 11they papers represent published “an enormous in this issue jumpand to Australopithecus,” online, the team the of 47 near the village of Aramis. It was the polished next researchers hominin indescribes line (see timeline, how Ar. ramidus p. 38), says looked australopithecine and moved. The expert skelesurface of a tooth root, and he immediately William ton, nicknamed Kimbel of“Ardi,” ArizonaisState fromUniversity, a female who Tempe. livedFor in example, a woodland knew it was a hominin molar. Over the next few days, the team scoured although (see sidebar, Lucy’s p. brain 40),isstood only aabout little 120 larger centimeters than that oftall, Ardipithecus, and weighed the area on hands and knees, as they do whenever an important piece Lucy’s aboutspecies, 50 kilograms. Au. afarensis, She was was thus an as adept big as biped. a chimpanzee It walked upright and had a of hominin is found (see story, p. 41), and collected the lower jaw of a like brain humans, size toventuring match. Butincreasingly she did not knuckle-walk into more diverse or swing habitats, through child with the milk molar still attached. The molar was so primitive that including the treesgrassy like living savannas. apes.And Instead, it hadshe lost walked its opposable upright,big planting toe, asher the team knew they had found a hominin both older and more primitive seen feet in flat 3.7-million-year-old on the ground, perhaps footprints eating at Laetoli, nuts, insects, Tanzania, and reflecting small mam- than Lucy. Yet the jaw also had derived traits—novel evolutionary charan mals irreversible in the woods. commitment to life on the ground. acters—shared with Lucy’s species, Au. afarensis, such as an upper Lucy’s She was direct a “facultative” ancestor is widely biped,considered say the authors, to be Au. still anamensis, living in both canine shaped like a diamond in side view. a hominin worlds—upright whose skeleton on the ground is poorly but known, also ablealthough to move its on shinbone all fours on The team reported 15 years ago in Nature that the fragmentary suggests top of branches it walkedinupright the trees, 3.9with million an opposable to 4.2 million big toeyears to grasp agolimbs. in Dream fossils belonged thein“long-sought root species team. Gen Suwato (left) Tokyo focused onpotential the skull; C. Owen Lovejoyfor (topthe in Kent, Ohio,(They studiedfirst postcranial Yohannesthen, Haile-Selassie and Kenya “These andthings Ethiopia. wereArdipithecus very odd creatures,” is the current says leading paleoanthropologist candidate right) Hominidae.” calledbones; it Au.and ramidus, after finding and analyzed key itfossils in ramidus—for Ethiopia. forAlan Au. anamensis’s Walker of Pennsylvania ancestor, ifState onlyUniversity, because it’sUniversity the only putative Park. “You Berhane partsAsfaw of thefound skeleton, changed to Ar. the Afar words hominin know what in evidence Tim [White] between once 5.8said: million If you andwanted 4.4 million to find years something ago. for “root” and “ground.”) In response to comments that he needed leg Indeed, that moved Au. anamensis like these things, fossils you’d appear have in the to goMiddle to the bar Awash in Star region Wars.” climber probably moved on flatanhands andhominin, feet on top of branches bonesthat to prove Ar. ramidus was upright White joked that just 200,000 Most researchers, years after who Ardi.have waited 15 years for the publication of in he thewould midcanopy, a type of locomotion known as palmigrady. For an be delighted with more parts, specifically a thigh and this find, agree that Ardi is indeed an early hominin. They praise the example, four bones in theplacing wrist ofanAr. ramidus gave it a more flexible intact skull, as though order. Making strides detailed reconstructions needed to piece together the crushed bones. hand that could be bent the backward at the wrist. This is in contrast thefosWithin 2 months, team delivered. In November 1994, astothe But“This the team not connectingimpressive the dots between Au.reconstruction anamensis andand hands is anisextraordinarily work of of knuckle-walking chimpanzees and Berkeley gorillas, which havestudent stiff sil hunters crawled up an embankment, graduate Ar.description, ramidus justwell yet, worth awaiting morefor,” fossils. now they are focusing waiting saysFor paleoanthropologist David wrists that absorb forces on of their knuckles. Yohannes Haile-Selassie Ethiopia, now a paleoanthropologist at the on Pilbeam the anatomy of ArdiUniversity. and how she moved world. of Harvard “They didthrough this jobthe very, veryHer well,” Cleveland However, Museum several researchers soin sure about thesetwo inferences. of Naturalaren’t History Ohio, spotted pieces of a foot agrees is primitive, neurobiologist with an opposable Christophbig Zollikofer toe like that of the used University by living of Some skeptical that of thea crushed pelvis the by anatomical bonearefrom the palm hand. That wasreally soonshows followed pieces of a apes to grasp branches. But the bases of the four other toe bones details Zurich in Switzerland. needed to demonstrate bipedality. Theofpelvis is “suggestive” pelvis; leg, ankle, and foot bones; many the bones of the handofand were oriented so that they reinforced forefoot into a more rigid But not everyone agrees with the the team’s interpretations about how bipedality but notjaw conclusive, says paleoanthropologist Carol Ward of itthewas arm; a lower with teeth—and a cranium. By January 1995, lever she pushed off.upright In contrast, the toes of a chimpanzee curve University Ar. as ramidus walked and what it reveals about our ancestors. Missouri, Columbia. “does not appear to apparentofthat they had made theAlso, rarestAr.oframidus rare finds, a partial skeleton. as flexibly as those in their hands, say Lovejoy and co-author have had its knee placed over the ankle, which means that when walkBruce Latimer of Case Western Reserve University in Cleveland. ing bipedally, it would have had to shift its weight to the side,” she says. Ar. ramidus “developed a pretty good bipedal foot while at the same Paleoanthropologist William Jungers of Stony Brook University in time keeping an opposable first toe,” says Lovejoy. New York state is also not sure that the skeleton was bipedal. “Believe The upper blades of Ardi’s pelvis are shorter and broader than in me, it’s a unique form of bipedalism,” he says. “The postcranium alone apes. They would have lowered the trunk’s center of mass, so she could would not unequivocally signal hominin status, in my opinion.” Paleobalance on one leg at a time while walking, says Lovejoy. He also anthropologist Bernard Wood of George Washington University in infers from the pelvis that her spine was long and curved like a Washington, D.C., agrees. Looking at the skeleton as a whole, he says, human’s rather than short and stiff like a chimpanzee’s. These “I think the head is consistent with it being a hominin, … but the rest of changes suggest to him that Ar. ramidus “has been bipedal for a very the body is much more questionable.” long time.” All this underscores how difficult it may be to recognize and Yet the lower pelvis is still quite large and primitive, similar to define bipedality in the earliest hominins as they began to shift from African apes rather than hominins. Taken with the opposable big toe, trees to ground. One thing does seem clear, though: The absence of and primitive traits in the hand and foot, this indicates that Ar. ramidus many specialized traits found in African apes suggests that our didn’t walk like Lucy and was still spending a lot of time inArdi thehas trees. ancestors never knuckle-walked. Unexpected anatomy. an opposable toe (left) and flexible hand (right); But it wasn’t suspending its body beneath branches African apes That ofthrows a monkey wrench her canines (toplike center) are sized between those a human (top left) and chimpinto a hypothesis about the last or climbing vertically, says Lovejoy. (top Instead, wasthea blades slow, of careful of living apes and humans. Ever since Darwin right);itand her pelvis common (lower left) ancestor are broad like Lucy’s (yellow). CREDITS: (LEFT) C. O. LOVEJOY ET AL., SCIENCE; (TOP) G. SUWA ET AL., SCIENCE; (BOTTOM) C. O. LOVEJOY ET AL., SCIENCE; (RIGHT) C. O. LOVEJOY ET AL., SCIENCE
CREDITS (TOP TO BOTTOM): TIM WHITE; BOB CHRISTY/NEWS AND INFORMATION, KENT STATE UNIVERSITY; TIM WHITE
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Habitat for Humanity ARAMIS, ETHIOPIA—A long cairn of black stones marks the spot where a skeleton of Ardipithecus ramidus was found, its bones broken and scattered on a barren hillside. Erected as a monument to an ancient ancestor in the style of an Afar tribesman’s grave, the cairn is a solitary marker in an almost sterile zone, devoid of life except for a few spindly acacia trees and piles of sifted sediment. That’s because the Middle Awash research team sucked up everything in sight at this spot, hunting for every bit of fossil bone as well as clues to the landscape 4.4 million years ago, when Ardipithecus died here. “Literally, we crawled every square inch of this locality,” recalls team co-leader Tim White of the University of California, Berkeley. “You crawl on your hands and knees, collecting every piece of bone, every piece of wood, every seed, every snail, every scrap. It was 100% collection.” The heaps of sediment are all that’s left behind from that fossil-mining operation, which yielded one of the most important fossils in human evolution (see main text, p. 36), as well as thousands of clues to its ecology and environment. The team collected more than 150,000 specimens of fossilized plants and animals from nearby localities of the same age, from elephants to songbirds to millipedes, including fossilized wood, pollen, snails, and larvae. “We have crates of bone splinters,” says White. A team of interdisciplinary researchers then used these fossils and thousands of geological and isotopic samples to reconstruct Ar. ramidus’s Pliocene world, as described in companion papers in this issue (see p. 66 and 87). From these specimens, they conclude that Ardi lived in a woodland, climbing among hackberry, fig, and palm trees and coexisting with monkeys, kudu antelopes, and peafowl. Doves and parrots flew overhead. All these creatures prefer woodlands, not the open, grassy terrain often conjured for our ancestors. The team suggests that Ar. ramidus was “more omnivorous” than chimpanzees, based on the size, shape, and enamel distribution of its teeth. It probably supplemented woodland plants such as fruits, nuts, and tubers with the occasional insects, small mammals, or bird eggs. Carbon-isotope studies of teeth from five individuals show that Ar. ramidus ate mostly woodland, rather than grassland, plants. Although Ar. ramidus probably ate
suggested in 1871 that our ancestors arose in Africa, researchers have debated whether our forebears passed through a great-ape stage in which they looked like proto-chimpanzees (Science, 21 November 1969, p. 953). This “troglodytian” model for early human behavior (named for the common chimpanzee, Pan troglodytes) suggests that the last common ancestor of the African apes and humans once had short backs, arms adapted for swinging, and a pelvis and limbs adapted for knuckle walking. Then our ancestors lost these traits, while chimpanzees and gorillas kept them. But this view has been uninformed by fossil evidence because there are almost no fossils of early chimpanzees and gorillas. Some researchers have thought that the ancient African ape bauplan was more primitive, lately citing clues from fragmentary fossils of apes that lived from 8 million to 18 million years ago. “There’s been growing evidence from the Miocene apes that the common ancestor may have been more primitive,” says Ward. Now Ar. ramidus strongly supports that notion. The authors repeatedly
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Past and present. Ardipithecus’s woodland was more like Kenya’s Kibwezi Forest (left) than Aramis today.
figs and other fruit when ripe, it didn’t consume as much fruit as chimpanzees do today. This new evidence overwhelmingly refutes the once-favored but now moribund hypothesis that upright-walking hominins arose in open grasslands. “There’s so much good data here that people aren’t going to be able to question whether early hominins were living in woodlands,” says paleoanthropologist Andrew Hill of Yale University. “Savannas had nothing to do with upright walking.” Geological studies indicate that most of the fossils were buried within a relatively short window of time, a few thousand to, at most, 100,000 years ago, says geologist and team co-leader Giday WoldeGabriel of the Los Alamos National Laboratory in New Mexico. During that sliver of time, Aramis was not a dense tropical rainforest with a thick canopy but a humid, cooler woodland. The best modern analog is the Kibwezi Forest in Kenya, kept wet by groundwater, according to isotope expert Stanley Ambrose of the University of Illinois, Urbana-Champaign. These woods have open stands of trees, some 20 meters high, that let the sun reach shrubs and grasses on the ground. Judging from the remains of at least 36 Ardipithecus individuals found so far at Aramis, this was prime feeding ground for a generalized early biped. “It was the habitat they preferred,” says White. –A.G.
note the many ways that Ar. ramidus differs from chimpanzees and gorillas, bolstering the argument that it was those apes that changed the most from the primitive form. But the problem with a more “generalized model” of an arboreal ape is that “it is easier to say what it wasn’t than what it was,” says Ward. And if the last common ancestor, which according to genetic studies lived 5 million to 7 million years ago, didn’t look like a chimp, then chimpanzees and gorillas evolved their numerous similarities independently, after gorillas diverged from the chimp/human line. “I find [that] hard to believe,” says Pilbeam. As debate over the implications of Ar. ramidus begins, the one thing that all can agree on is that the new papers provide a wealth of data to frame the issues for years. “No matter what side of the arguments you come down on, it’s going to be food for thought for generations of graduate students,” says Jungers. Or, as Walker says: “It would have been very boring if it had looked half-chimp.” –ANN GIBBONS SCIENCE
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CREDITS (LEFT TO RIGHT): TIM WHITE; ANN GIBBONS
NEWSFOCUS
The crawl. Researchers hunt down every fossil at Aramis.
PALEOANTHROPOLOGY
The View From Afar
CREDITS (TOP TO BOTTOM): HENRY GILBERT; SOURCE: TIM WHITE
How do you find priceless hominin fossils in a hostile desert? Build a strong team and obsess over the details
MIDDLE AWASH VALLEY, THE AFAR DEPRESSION, ETHIOPIA—It’s of how upright walking evolved and how our earliest ancestors difabout 10 a.m. on a hot morning in December, and Tim White is fered from chimpanzees (see overview, p. 60, and main Focus text, watching a 30-year-old farmer inch his way up a slippery hill on his p. 36). But Aramis is just one of 300 localities in the Middle Awash, knees, picking through mouse-colored rubble for a bit of gray bone. which is the only place in the world to yield fossils that span the entire The sun is already bleaching the scrubby badlands, making it diffi- saga of hominid evolution. At last count, this team had gathered cult to distinguish a fragment of bone in the washed-out beige and 19,000 vertebrate fossils over the past 19 years. These include about gray terrain. The only shade in this parched gully is from a small, 300 specimens from seven species of hominins, from some of the thorny acacia tree, so the fossil hunters have draped their heads with first members of the human family, such as 5.8-million-year-old kerchiefs that hang out from under their “Cal” and “Obama for Pres- Ar. ramidus kadabba, to the earliest members of our own species, ident” baseball caps, making them look like a strange tribe of Berke- Homo sapiens, which lived here about 160,000 years ago. ley Bedouins. If there are fossils here, As they work in different places in the White is conf ident that the slender WESTERN AFAR RIFT, ETHIOPIA valley, the team members travel back and farmer, Kampiro Kayrento, will f ind forth in time. Today, this core group is HADAR GONA them. “Kampiro is the best person in the working in the western foothills near the world for f inding little pieces of fosBurka catchment, where an ancient river silized human bone,” says White, 59, a laid down sediments 3 million to 2 milpaleoanthropologist at the University of lion years ago and where the team has California, Berkeley, who has collected found specimens of Australopithecus Awash fossils in this region since 1981. garhi, a species they suspect may have River Watching Kayrento is a sort of spectagiven rise to the f irst members of our Afar tor sport, because he scores so often. Just genus, Homo. Rift Aramis minutes earlier, he had walked over the This season, after a rough start, the 25 crest of a small hill, singing softly to himscientists, students, cooks, and Ethiopian Addis Ababa self, and had spotted the fossilized core of and Afar officials and guards in camp are ETHIOPIA a horn from an ancient bovid, or antelope. working well together. Their tented camp is Bouri Peninsula hours from any town, graded road, or fresh Then he picked up a flat piece of gray bone Middle Awash Yardi Lake Hominid Localities nearby and showed the fossil to Ethiopian water. (They dug their own well to get Burka Ardipithecus paleoanthropologist Berhane Asfaw, askwater.) “The 1st week, it’s like an engine Australopithecus Homo ing, “Bovid?” Asfaw, 55, who hired that’s running but not running smoothly,” Kayrento when he was a boy hanging out says White, who, with Asfaw, runs a wellat fossil sites in southern Ethiopia, looked Ancestral territory. The area where Ardi was found is rich in organized camp where every tool, map, and over the slightly curved piece of bone the hominin fossil sites, including these worked by the Middle shower bag has its proper place. “By the size of a silver dollar and suggested, “Mon- Awash research team. 3rd week, people know their jobs.” key?” as he handed it to White. White The 1st week, White and a paleontoloturned it over gently in his hands, then said: “Check that, Berhane. We gist were sick, and White is still fighting a harsh cough that keeps just found a hominid cranium. Niiiice.” him awake at night. The 2nd week, some aggressive Alisera tribesAs word spreads that Kayrento found a hominin, or a member of men who live near the Ar. ramidus site threatened to kill White and the taxon that includes humans and our ancestors, the other fossil Asfaw, making it difficult to return there. (That’s one reason the hunters tease him: “Homo bovid! Homo bovid! Niiiice.” team travels with six Afar policemen armed with AK-47s and The Middle Awash project, which includes 70 scientists from 18 Obama caps, dubbed “The Obama Police.”) The day before, a stunations, is best known for its discovery of the 4.4-million-year-old dent had awakened with a high fever and abdominal pain and had to partial skeleton of Ardipithecus ramidus at Aramis, about 34 kilo- be driven 4 hours to the nearest clinic, where he was diagnosed with meters north of here. That skeleton is now dramatically revising ideas a urinary tract infection, probably from drinking too little water in www.sciencemag.org
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the 35˚C heat. “The best laid plans change every day,” says White, who has dealt with poisonous snakes, scorpions, malarial mosquitoes, lions, hyenas, flash floods, dust tornadoes, warring tribesmen, and contaminated food and water over the years. “Nothing in the field comes easy.” Calling the “A” team Nothing in the Afar, for that matter, comes easy. We are reminded of that as we drive across the dusty Saragata plain to the target fossil site at 8 a.m., making giant circles in the dust with the Toyota Land Cruiser so we can find our tracks home at the end of the day. Men clad in plaid wraps, with AK-47s slung over their shoulders, flag us down seeking help. They bring over a woman who looks to be in her 70s but is probably much younger. Her finger is bleeding, and the men tell White and Asfaw, in Afar, that a puff adder bit her the night before while she was gathering wood. A quick-thinking boy had sliced her finger with a knife, releasing the venom and probably saving her life. White gets out a first-aid kit, removes a crude poultice, and cleans and bandages the wound, putting on an antibiotic cream. “It’s good she survived the night,” he says as we drive off. “The danger now is infection.” After inching down the sandy bank of a dry river, we reach the socalled Chairman’s site. This is one of dozens of fossil localities discovered in the Burka area since 2005: exposed hillsides that were spotted in satellite and aerial photos, then laboriously explored on foot. The plan was to search for animal fossils to help date a hominid jawbone discovered last year. But in the 1st hour, with Kayrento’s discovery, they’re already on the trail of another individual instead. As soon as White identifies the bit of skull bone, he swings into action. With his wiry frame and deep voice, he is a commanding presence, and it soon becomes clear how he earned his nickname, “The General.” In his field uniform—a suede Australian army hat with a rattlesnake band, blue jeans, and driving gloves without fingers—he uses a fossil pick to delineate the zones in the sandstone
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Division of labor. Kampiro Kayrento (top left) homes in on fossils; he and others sweep the surface, and Giday WoldeGabriel dates sediments.
where he wants the crew deployed. “Get everybody out of the area,” he calls to the 15 people already fanned out over the gully, scanning for fossils. “I want the ‘A’ team.” He singles out Kayrento and three others and hands them yellow pin-flags, saying, “Go back to the bottom.” As he watches them move up the slope, he warns: “Go slowly. You’re moving too fast. … Don’t squash the slope. Move like a cat, not a cow.” By looking at the relatively fresh fractured edge of the bone fragment, White knows that it comes from a larger piece of skull that broke after it was exposed, not while it was buried. As Kayrento and the others find other bits of bone, they place yellow pin-flags at those spots. “This process establishes the distributional cone,” White explains. The top flag marks the highest point on the surface where the skull came out of the ground; the bottom boundary marks the farthest point where a fragment might finally have come to rest, following the fall line down the slope. This discovery also illustrates one reason why the team comes to the field right after the rainy season. If they’re lucky, rain and floods will cut into the ancient sediments, exposing fossils. But they have to get there before the fossils disintegrate as they are exposed to the elements or are trampled by the Afar’s goats, sheep, and cattle. Timing is everything, and this season they’re a bit late. “The ideal situation is to find a fossil just as it is eroding out of the bank,” says White. As they crawl the entire length of the gully, they turn over every rock, mud clod, and piece of carbonate rubble to make sure it doesn’t contain a fossil fragment. “Not good,” says Kayrento. “This is yucky,” agrees Asfaw, co-director of the team and the first Ethiopian scientist to join it, in 1979 when he was invited to earn his Ph.D. at Berkeley (Science, 29 August 2003, p. 1178). After 2 hours, the team has collected a few more pieces of skull around the temple, forehead, and ear. “It’s getting bigger by the minute,” White says. “If we’re lucky, we’ll find it buried right in here.” The team has to wait until the next day to find out just how lucky. At 9:45 a.m. Thursday, they return with reinforcements: Asfaw has hired two Afar men to help with the heavy lifting of buckets of dirt. With a button-down Oxford cloth shirt and a pistol stuck in the waistband of his khakis, Asfaw commands respect, and he is the best at negotiating with the Afar. In this case, he settles an argument by letting clan leaders select which men, among a large group, will get jobs. At the site, White sets up a perimeter of blue pin-flags that look like a mini slalom course, outlining the gully that he calls the “Hot Zone” where fossil pieces are most likely to be buried. The plan is to excavate all the rock and dirt around those flags, down to the original layers of sediment. White explains that the ancient landscape would have been flatter and more verdant before tectonic movements of Earth’s crust cracked and tilted the sediment layers. But the original soil is still there, a red-brown layer of clay beneath a gray veneer of sandstone. “Throw every piece of stone out of the channel,” he orders. “If you see a hominid, I need to know right away!” White and Kayrento literally sweep off the gray lag with a push broom and then scrape back the layers of time with a trowel to the ancient surface underneath. “Once we brush out the slopes, we’ll be
Ardipithecus ramidus
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sure no fossil is left in place,” says White. In case they miss a fragment, the loose sediment is carried to giant sieves where the crew sifts it for bits of bone or teeth. The sifted rubble is taken to a circle of workers who then empty it into small aluminum pans, in which they examine every single, tiny piece—a job that gives new meaning to the word tedium. “Sieving 101,” observes Asfaw, who supervises sieving and picking today. By 11:10 a.m., the pace of discovery has slowed. When the A team tells White it’s “not good,” he tries to infuse them with some of his energy, reminding everyone to stay focused, to keep going, to not step on fossils. But by midday, White is grumbling, too, because they’ve scoured the Hot Zone and it’s clear the skull is not there. “We’ve eliminated every hope of finding it in situ.”
NEWSFOCUS
Intensive care. Tim White uses dental tools and a gluelike adhesive to extract fragile fossils from matrix.
Time travel It’s a good time to take a walk with the four geologists, who are combing the terrain, hoping to find sediments with volcanic minerals to Luckily, the fossil hunters help them date the locality and its fossils precisely. While fossil have found a pig known to hunters move slowly, stooped at the waist and focused on the ground, have lived about 2.6 million the geologists move fast, heads up, scanning the next horizon for a to 2.7 million years ago, rock face with a layer cake of sediments, like those exposed in road which suggests that the sedicuts. The 6-million-year record of Middle Awash sediments is not ments and the new discovery are also that old. stacked neatly in one place, with oldest rocks on the bottom and At 9 a.m. Friday, 12 December, we’re back at the Chairman’s site youngest on top. (If it were, the stack would be 1 kilometer thick.) for a 3rd day, this time with a film crew from Sweden. After White Instead, the rocks are faulted and tilted into different ridges. By trac- and Kayrento jokingly reenact the discovery of the skull bone for the ing a once-horizontal layer from ridge to ridge, sometimes for kilo- film crew, they resume sweeping and sifting, exactly where they left meters, the geologists can link the layers and place different snap- off. At first, there’s little return. Berkeley postdoc Cesur Pehlevan shots of time into a sequence. from Ankara hands White a piece of bone: “Nope, tough luck. Right Today, Ethiopian geologist Giday WoldeGabriel of the Los color, right thickness. Nope, sorry.” Alamos National Laboratory in New Mexico, also a co-leader of the Finally, someone hands White something special. “Oh nice, frontal team (he joined in 1992), is searching for a familiar-looking motif— bone with frontal sinus. This is getting better. That’s what we’re after,” a distinct layer of volcanic tuff called the SHT (Sidiha Koma Tuff), says White. “If we can get that brow ridge, we can match it with the previously dated to 3.4 million years ago by radiometric methods. known species.” He turns over the new piece of frontal bone in his So far, the team has found just one species of hominin— hand, examining it like a diamond dealer assessing a gemstone. Au. garhi—that lived at this time in the Middle Awash (Science, By the end of 3 days, the team of 20 will have collected a dozen 23 April 1999, p. 629), although a more robust pieces of one skull, an average yield for this region. species, Au. aethiopicus, appears 2.6 million years “Nothing in the field Taken together, says White, those pieces show that ago in southern Ethiopia and Kenya. That’s also when “It’s an Australopithecus because it has a small braincomes easy.” the earliest stone tools appear in Gona, Ethiopia, case, small chewing apparatus.” There’s still not –TIM WHITE, UNIVERSITY enough to identify the species, though White thinks it 100 kilometers north of here. The earliest fossils of our genus Homo come a bit later—at 2.3 million years ago OF CALIFORNIA, BERKELEY is Au. garhi. He notes that “it’s a big boy, big for an at Hadar, near Gona, also with stone tools. That’s why australopithecine.” If it is Au. garhi, that would be it is important to date Au. garhi precisely: Was it the maker of the one more bit of evidence to suggest that Au. afarensis gave rise to stone tools left in the Afar? The team thinks Au. garhi is the direct Au. garhi; males are bigger than females in Au. afarensis—and so descendant of the more primitive Au. afarensis, best known as the perhaps in Au. garhi, too. species that includes the famous 3.2-million-year-old skeleton of For now, White and Asfaw are pleased with the new snapshot Lucy, also from Hadar. But did Au. garhi then evolve into early they’re getting of Au. garhi. On our way back to camp, White stops Homo? They need better dates—and more fossils—to find out. so we can take a photo of the moon rising over Yardi Lake in front “Now that we have the SHT as a reference point here, we have of us, the sun setting behind us. The landscape has changed since to try to trace it to where the new fossils are,” says WoldeGabriel. the australopithecines were here. But one thing’s been constant in The only problem is that the SHT is several ridges and basins over the Middle Awash, he notes: “Hominids have been right here lookfrom the excavation; linking the two will be difficult if not impos- ing at the moon rising over water for millions of years.” –ANN GIBBONS sible. The team will also use other methods to date the new fossils. www.sciencemag.org
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AUTHORS’SUMMARIES Ardipithecus ramidus and the Paleobiology of Early Hominids Tim D. White, Berhane Asfaw, Yonas Beyene, Yohannes Haile-Selassie, C. Owen Lovejoy, Gen Suwa, Giday WoldeGabriel
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CREDIT: ILLUSTRATION OF AR. RAMIDUS: COPYRIGHT J. H. MATTERNES
C
harles Darwin and Thomas Huxley were forced to ponder human origins and evolution without a relevant fossil record. With only a few Pan Pan Neanderthal fossils available to troglo paniscus Gorilla dytes g o r i l a l supplement their limited knowlCLCA edge of living apes, they specu• Partially arboreal • Striding terrestrial biped • Palmigrade lated about how quintessentially • Enlarged brain • Facultative biped • Postcanine megadontia GLCA arborealist human features such as upright • Dentognathic reduction • Feminized canine • Pan-African • Dimorphic canines • Technology-reliant • Woodland omnivore • Wide niche walking, small canines, dexterous • Forest A us • Old World range A hands, and our special intelligence r tralo dipi frugivore/ Ho pithe thecu mo ( s (~ 6 to 4 Ma) cus ( omnivore had evolved through natural selec< ~ 4 to 1 Ma) ~ 2.5 Ma ) tion to provide us with our complex way of life. Today we know of early Homo from >2.0 million Evolution of hominids and African apes since the gorilla/chimp+human (GLCA) and chimp/human (CLCA) last common ancestors. Pedestals on the left show separate lineages leading to the extant apes (gorilla, and chimp and years ago (Ma) and have a record bonobo); text indicates key differences among adaptive plateaus occupied by the three hominid genera. of stone tools and animal butchery that reaches back to 2.6 Ma. These demonstrate just how deeply tech- probably was more omnivorous than chimpanzees (ripe fruit specialnology is embedded in our natural history. ists) and likely fed both in trees and on the ground. It apparently conAustralopithecus, a predecessor of Homo that lived about 1 to 4 Ma sumed only small amounts of open-environment resources, arguing (see figure), was discovered in South Africa in 1924. Although slow to against the idea that an inhabitation of grasslands was the driving force gain acceptance as a human ancestor, it is now recognized to represent in the origin of upright walking. an ancestral group from which Homo evolved. Even after the discovAr. ramidus, first described in 1994 from teeth and jaw fragments, eries of the partial skeleton (“Lucy”) and fossilized footprints is now represented by 110 specimens, including a partial female (Laetoli) of Au. afarensis, and other fossils that extended the antiquity skeleton rescued from erosional degradation. This individual weighed of Australopithecus to ~3.7 Ma, the hominid fossil record before about 50 kg and stood about 120 cm tall. In the context of the many Australopithecus was blank. What connected the small-brained, small- other recovered individuals of this species, this suggests little body canined, upright-walking Australopithecus to the last common ances- size difference between males and females. Brain size was as small as tor that we shared with chimpanzees some time earlier than 6 Ma? in living chimpanzees. The numerous recovered teeth and a largely The 11 papers in this issue, representing the work of a large inter- complete skull show that Ar. ramidus had a small face and a reduced national team with diverse areas of expertise, describe Ardipithecus canine/premolar complex, indicative of minimal social aggression. ramidus, a hominid species dated to 4.4 Ma, and the habitat in which Its hands, arms, feet, pelvis, and legs collectively reveal that it moved it lived in the Afar Rift region of northeastern Ethiopia. This species, capably in the trees, supported on its feet and palms (palmigrade substantially more primitive than Australopithecus, resolves many clambering), but lacked any characteristics typical of the suspenuncertainties about early human evolution, including the nature of the sion, vertical climbing, or knuckle-walking of modern gorillas and last common ancestor that we shared with the line leading to living chimps. Terrestrially, it engaged in a form of bipedality more primchimpanzees and bonobos. The Ardipithecus remains were recovered itive than that of Australopithecus, and it lacked adaptation to from a sedimentary horizon representing a short span of time (within “heavy” chewing related to open environments (seen in later 100 to 10,000 years). This has enabled us to assess available and pre- Australopithecus). Ar. ramidus thus indicates that the last common ferred habitats for the early hominids by systematic and repeated ancestors of humans and African apes were not chimpanzee-like and sampling of the hominid-bearing strata. that both hominids and extant African apes are each highly specialBy collecting and classifying thousands of vertebrate, invertebrate, ized, but through very different evolutionary pathways. and plant fossils, and characterizing the isotopic composition of soil samples and teeth, we have learned that Ar. ramidus was a denizen of See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. woodland with small patches of forest. We have also learned that it When citing, please refer to the full paper, available at DOI 10.1126/science.1175802.
AUTHORS’SUMMARIES Authors’Summaries
The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday WoldeGabriel, Stanley H. Ambrose, Doris Barboni, Raymonde Bonnefille, Laurent Bremond, Brian Currie, David DeGusta, William K. Hart, Alison M. Murray, Paul R. Renne, M. C. Jolly-Saad, Kathlyn M. Stewart, Tim D. White
A
rdipithecus ramidus was found in exposed sediments flanking the Awash River, Ethiopia. The local geology and associated fossils provide critical information about its age and habitat. Most of Africa’s surface is nondepositional and/or covered by forests. This explains why so many discoveries related to early hominid evolution have been made within eastern Africa’s relatively dry, narrow, active rift system. Here the Arabian and African tectonic plates have been pulling apart for millions of years, and lakes and rivers have accumulated variably fossil-rich sediments in the Afar Triangle, which lies at the intersection of the Red Sea, Gulf of Aden, and Main Ethiopian Rifts (see map). Some of these deposits were subsequently uplifted by the rift tectonics and are now eroding. In addition, volcanoes associated with Map showing the Middle Awash area (star) and rift locations (red lines). Photo shows the this rifting have left many widespread deposits that we 4.4 Ma volcanic marker horizon (yellow bed) atop the locality where the skeleton and holocan use to determine the age of these fossils using type teeth of Ar. ramidus were discovered. Also shown are some of the fossil seeds. modern radioisotopic methods. Several of the most important hominid fossils have been found near between two key volcanic markers, each dated to 4.4 Ma. Their simithe Afar’s western margin, north and west of the Awash River (star on lar ages and sedimentology imply that the fossils themselves date to map), including Hadar (the “Lucy” site), Gona [known for the world’s 4.4 Ma and were all deposited within a relatively narrow time interval oldest stone tools at 2.6 million years ago (Ma)], and the Middle Awash lasting anywhere from 100 to 10,000 years. Today the unit is exposed (including Aramis). Cumulatively, these and nearby study areas in across a 9-km arc that represents a fortuitous transect through the Ethiopia have provided an unparalleled record of hominid evolution. ancient landscape. The western exposure, in particular, preserves a Fossil-bearing rocks in the Middle Awash are intermittently rich assemblage of plant and animal fossils and ancient soils. exposed and measure more than 1 km in thickness. Volcanic rocks Fossilized wood, seeds, and phytoliths (hard silica parts from near the base of this regional succession are dated to more than 6 Ma. plants) confirm the presence of hackberry, fig, and palm trees. There Its uppermost sediments document the appearance of anatomically is no evidence of a humid closed-canopy tropical rainforest, nor of near-modern humans 155,000 years ago. As is the case for many river the subdesertic vegetation that characterizes the area today. and lake deposits, fossil accumulation rates here have been highly Invertebrate fossils are abundant and include insect larvae, broodvariable, and the distribution and preservation of the fossils are balls and nests of dung beetles, diverse gastropods, and millipedes. uneven. Alterations of the fossils caused by erosion and other factors The terrestrial gastropods best match those seen in modern groundfurther complicate interpretation of past environments. To meet this water forests such as the Kibwezi in Kenya. Aquatic lower vertechallenge, beginning in 1981, our research team of more than 70 sci- brates are relatively rare and probably arrived episodically during entists has collected 2000 geological samples, thousands of lithic flooding of a river distal to the Aramis area. The most abundant fish artifacts (e.g., stone tools), and tens of thousands of plant and animal is catfish, probably introduced during overbank flooding and/or by fossils. The emergent picture developed from the many Middle predatory birds roosting in local trees. Awash rock units and their contents represents a series of snapshots Our combined evidence indicates that Ar. ramidus did not live in taken through time, rather than a continuous record of deposition. the open savanna that was once envisioned to be the predominant Ar. ramidus was recovered from one such geological unit, 3 to 6 m habitat of the earliest hominids, but rather in an environment that thick, centered within the study area. Here, the Aramis and adjacent was humid and cooler than it is today, containing habitats ranging drainage basins expose a total thickness of 300 m of sediments largely from woodland to forest patches. deposited in rivers and lakes, and on floodplains, between ~5.5 and 3.8 Ma. Within this succession, the Ar. ramidus–bearing rock unit See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. comprises silt and clay beds deposited on a floodplain. It is bracketed When citing, please refer to the full paper, available at DOI 10.1126/science.1175817.
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Authors’Summaries AUTHORS’SUMMARIES
Taphonomic, Avian, and Small-Vertebrate Indicators of Ardipithecus ramidus Habitat Antoine Louchart, Henry Wesselman, Robert J. Blumenschine, Leslea J. Hlusko, Jackson K. Njau, Michael T. Black, Mesfin Asnake, Tim D. White
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Coliidae <1% (2) Bucorvus <1% (2) he stratigraphic unit conOtididae 2% (3) Apodidae <1% (2) taining Ardipithecus rami6 other taxa (1 each) Coturnix <1% (2) dus was probably deposited Anatidae 3% (8) rapidly, thus providing a transect Numididae through a 4.4-million-year-old 5% (7) landscape. To help reconstruct Falconiformes and understand its biological 6% (7) setting as thoroughly as possible, Columbidae Psittacidae we recovered an assemblage of 6% (13) 36% (22) >150,000 plant and animal fossils. More than 6000 vertebrate speciPasseriformes Pavo 6% (4) mens were identified at the family 15% (16) Tyto 8% (7) level or below. These specimens Abundance of birds (left) associated with Ar. ramidus. represent animals ranging in size Francolinus These distributions are consistent with a mostly wood8% (10) from shrews to elephants and land habitat. (Above) An example of the many small mammal and bird bones. include abundant birds and small mammals that are usually rare in hominid-bearing assemblages. Many of these birds and small mam- damage patterns of the fossils representing small mammals and birds mals are highly sensitive to environmental conditions and thus are par- suggest that they are derived from undigested material regurgitated ticularly helpful in reconstructing the environment. by owls (owl pellets). Because of their fragility and size, bird bones Accurate interpretation of fossil assemblages can be challenging. have been rare or absent at most other eastern African fossil assemEven fossils from one layer can represent artificial amalgamations blages that included early hominids. However, we cataloged 370 that might have originated thousands of years apart. Moreover, the avian fossils; these represent 29 species, several new to science. Most remains of animals living in different habitats can be artificially of the birds are terrestrial rather than aquatic, and small species such mixed by flowing water or by shifting lake and river margins. as doves, lovebirds, mousebirds, passerines, and swifts are abundant. Ecological fidelity can be further biased by unsystematic recovery if, Open-country species are rare. Eagles and hawks/kites are present, for example, only the more complete, identifiable, or rare specimens but the assemblage is dominated by parrots and the peafowl Pavo, an are collected. Thus, interpreting the Ardipithecus-bearing sediments ecological indicator of wooded conditions. requires that we deduce the physical and biological conditions under The small-mammal assemblage includes up to 20 new species, which the fossils accumulated and the degree to which these biases including shrews, bats, rodents, hares, and carnivores. Extant counoperated at the time of deposition—a practice called “taphonomy.” terparts live in a variety of habitats, but their relative abundance in Both the large- and small-mammal assemblages at Aramis lack the fossil assemblage indicates that Ardipithecus lived in a wooded the damage that would result from transport and sorting by water, a area. Avian predators most probably procured the much rarer squirfinding consistent with the fine-grained sediments in which the rels and gerbils from drier scrub or arid settings at a distance. Most bones were originally embedded. Many of the limb bone fragments of the bat, shrew, porcupine, and other rodent specimens are compatof large mammals show traces of rodent gnawing and carnivore ible with a relatively moist environmental setting, as are the abunchewing at a time when the bones were still fresh. These bones were dant fossils of monkeys and spiral-horned antelopes. most probably damaged by hyenas, which in modern times are known The combination of geological and taphonomic evidence, the to destroy most of the limb bones and consume their marrow. The assemblage of small-mammal and avian fossils, and the taxonomic actions of hyenas and other carnivores that actively competed for and isotopic compositions of remains from larger mammals indicate these remains largely explain why the fossil assemblage at Aramis that Aramis was predominantly a woodland habitat during Ar. contains an overrepresentation of teeth, jaws, and limb bone shaft ramidus times. The anatomical and isotopic evidence of Ar. ramidus splinters (versus skulls or limb bone ends). itself also suggests that the species was adapted to such a habitat. As a result of this bone destruction, whole skeletons are extremely rare at Aramis, with one fortunate exception: the partial skeleton of See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. Ar. ramidus excavated at ARA-VP-6/500. The relative abundance and When citing, please refer to the full paper, available at DOI 10.1126/science.1175823.
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Macrovertebrate Paleontology and the Pliocene Habitat of Ardipithecus ramidus Tim D. White, Stanley H. Ambrose, Gen Suwa, Denise F. Su, David DeGusta, Raymond L. Bernor, Jean-Renaud Boisserie, Michel Brunet, Eric Delson, Stephen Frost, Nuria Garcia, Ioannis X. Giaourtsakis, Yohannes Haile-Selassie, F. Clark Howell, Thomas Lehmann, Andossa Likius, Cesur Pehlevan, Haruo Saegusa, Gina Semprebon, Mark Teaford, Elisabeth Vrba
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ver since Darwin, scholars have (red crosses in figure) account for speculated about the role that nearly a third of the entire large mamenvironment may have played in mal collection. Leaf-eating colobines human origins, evolution, and adaptatoday exhibit strong preferences for tion. Given that all living great apes live arboreal habitats, and the carbon isoand feed in trees, it has been assumed tope compositions of the fossil teeth are that the last common ancestor we consistent with dense to open forest shared with these forms was also a forarboreal feeding (see figure). est dweller. In 1925, Raymond Dart The other dominant large mammal described the first Australopithecus, a associated with Ar. ramidus is the child’s skull, at Taung, South Africa. spiral-horned antelope, Tragelaphus Its occurrence among other fossils (the kudu, green circle). Today, these indicative of a grassland environment antelopes are browsers (eating mostly prompted speculation that the open leaves), and they prefer bushy to grasslands of Africa were exploited by wooded habitats. The dental morpholearly hominids and were therefore ogy, wear, and enamel isotopic comsomehow integrally involved with the position of the Aramis kudu species origins of upright walking. are all consistent with such placeThe Ardipithecus-bearing sediments ment. In contrast, grazing antelopes at Aramis now provide fresh evidence (which eat mostly grass) are rare in that Ar. ramidus lived in a predomithe Aramis assemblage. nantly woodland setting. This and corThe large-mammal assemblage roborative evidence from fossil assemshows a preponderance of browsers blages of avian and small mammals and fruit eaters. This evidence is conimply that a grassland environment was sistent with indications from birds, not a major force driving evolution of small mammals, soil isotopes, plants, the earliest hominids. A diverse assemand invertebrate remains. The emerblage of large mammals (>5 kg body gent picture of the Aramis landscape weight) collected alongside Ardipithe- Carbon and oxygen isotope analyses of teeth from the Ar. ramidus during Ar. ramidus times is one of a cus provides further support for this localities. Species are listed in order of abundance, and isotopic woodland setting with small forest conclusion. Carbon isotopes from data separate species by what they ate and their environment. patches. This woodland graded into tooth enamel yield dietary information nearby habitats that were more open because different isotope signatures reflect different photosynthetic and are devoid of fossils of Ardipithecus and other forest-to-woodland– pathways of plants consumed during enamel development. Therefore, community mammals. Finally, the carbon isotopic composition of animals that feed on tropical open-environment grasses (or on grass-eat- Ar. ramidus teeth is similar to that of the predominantly arboreal, small, ing animals) have different isotopic compositions from those feeding on baboon-like Pliopapio and the woodland browser Tragelaphus, indibrowse, seeds, or fruit from shrubs or trees. Moreover, oxygen isotopes cating little dietary intake of grass or grass-eating animals. It is therehelp deduce relative humidity and evaporation in the environment. fore unlikely that Ar. ramidus was feeding much in open grasslands. The larger-mammal assemblage associated with Ardipithecus was These data suggest that the anatomy and behavior of early systematically collected across a ~9 km transect of eroding sediments hominids did not evolve in response to open savanna or mosaic setsandwiched between two volcanic horizons each dated to 4.4 million tings. Rather, hominids appear to have originated and persisted years ago. It consists of ~4000 cataloged specimens assigned to within more closed, wooded habitats until the emergence of more ~40 species in 34 genera of 16 families. ecologically aggressive Australopithecus. There are only three primates in this assemblage, and the rarest is Ardipithecus, represented by 110 specimens (a minimum of 36 individ- See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. uals). Conversely, colobine monkeys and a small baboon-like monkey When citing, please refer to the full paper, available at DOI 10.1126/science.1175822.
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The Ardipithecus ramidus Skull and Its Implications for Hominid Origins Gen Suwa, Berhane Asfaw, Reiko T. Kono, Daisuke Kubo, C. Owen Lovejoy, Tim D. White
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he key feature that distintus and are known as “robust” Australopithecus afarensis guishes Homo sapiens from Australopithecus. Pan troglodytes other primates is our unusuAr. ramidus had a small brain Ardipithecus ramidus ally large brain, which allows us (300 to 350 cm3), similar to that of 200cc 300 400 500 600 bonobos and female chimpanzees to communicate, make tools, plan, and smaller than that of Australoand modify our environment. Unpithecus. The Ar. ramidus face is derstanding how and when our 14mm16 18 20 22 24 also small and lacks the large cognitive ability evolved has been cheeks of “heavy chewing” Ausa special focus in anthropology tralopithecus. It has a projecting and, more recently, genetics. Fossil 44mm 48 52 56 60 muzzle as in Sahelanthropus, hominid skulls provide direct eviwhich gives it a decidedly ape-like dence of skull evolution and inforgestalt. Yet the Ar. ramidus skull is mation about diet, appearance, and not particularly chimpanzee-like. behavior. Skulls feature promi12mm 16 20 24 For example, the ridge above the nently in the characterization of species, in taxonomy, and in phy- (Right) Oblique and side views of a female chimpanzee (right) and the Ar. eye socket is unlike that of a chimlogenetic analyses of both extinct ramidus female reconstruction (left; the oblique view includes a separate panzee, and its lower face does mandible). (Left) Comparison of brain and tooth sizes (arrows) of chimps (Pan; and living primates. blue), Ar. ramidus (red), and Australopithecus (green). Means are plotted not project forward as much as a Unfortunately, hominid skulls except for individual Ar. ramidus and Au. afarensis cranial capacities. Canine chimpanzee’s face. Chimps priare relatively rare in the fossil unworn heights (bottom) are based on small samples, Ar. ramidus (females, n marily eat ripe fruits and have record. A number of partial skulls = 1; males, n = 3), Au. afarensis (n = 2), Pan (females, n = 19; males, n = 11). large incisors set in a projecting lower face. Ar. ramidus instead and crania (skulls without a lower jaw) of early Homo and its predecessor, Australopithecus (which lived was probably more omnivorous and fed both in trees and on the ground. ~1 to 4 million years ago), have been recovered, but relatively few are Additionally, in chimpanzees, forward placement of the entire lower complete enough for extensive comparisons. One surprisingly com- face is exaggerated, perhaps linked with their large tusklike canines plete but distorted cranium from 6 to 7 million years ago was discov- (especially in males) and elevated levels of aggression. This is not seen ered in central Africa (Chad). This fossil, Sahelanthropus tchadensis in Ar. ramidus, implying that it was less socially aggressive. Like Ar. ramidus, S. tchadensis had a brain that was less than (a.k.a. “Toumaï ”), is thought by many to represent the earliest known 400 cm3 in size. It also resembled Ar. ramidus in having small nonhominid, although some have argued that it is a female ape. The Ardipithecus ramidus skull is of particular interest because it sharpened canines. Details of the bottom of the skull show that both predates known Australopithecus and thereby illuminates the early Ar. ramidus and Sahelanthropus had a short cranial base, a feature evolution of the hominid skull, brain, and face. The Ar. ramidus skull also shared with Australopithecus. Furthermore, we infer that the rear was badly crushed, and many of its bones were scattered over a wide of the Ar. ramidus skull was downturned like that suggested for area. Because the bones were so fragile and damaged, we imaged Sahelanthropus. These similarities confirm that Sahelanthropus was them with micro–computed tomography, making more than 5000 indeed a hominid, not an extinct ape. These and an additional feature of the skull hint that, despite its slices. We assembled the fragments into more than 60 key virtual pieces of the braincase, face, and teeth, enough to allow us to digitally small size, the brain of Ar. ramidus may have already begun to develop some aspects of later hominid-like form and function. The steep orienreconstruct a largely complete cranium. The fossil skulls of Australopithecus indicate that its brain was tation of the bone on which the brain stem rests suggests that the base ~400 to 550 cm3 in size, slightly larger than the brains of modern apes of the Ar. ramidus brain might have been more flexed than in apes. In of similar body size and about a third of those of typical Homo sapi- Australopithecus, a flexed cranial base occurs together with expansion ens. Its specialized craniofacial architecture facilitated the production of the posterior parietal cortex, a part of the modern human brain of strong chewing forces along the entire row of teeth located behind involved in aspects of visual and spatial perception. its canines. These postcanine teeth were enlarged and had thick enamel, consistent with a hard/tough and abrasive diet. Some species See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. exhibited extreme manifestations of this specialized chewing appara- When citing, please refer to the full paper, available at DOI 10.1126/science.1175825.
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Paleobiological Implications of the Ardipithecus ramidus Dentition Gen Suwa, Reiko T. Kono, Scott W. Simpson, Berhane Asfaw, C. Owen Lovejoy, Tim D. White
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eeth are highly resilient to degradation and therefore are the most abundant specimens in the primate fossil record. The size, shape, enamel thickness, and isotopic composition of teeth provide a wealth of information about phylogeny, diet, and social behavior. Ardipithecus ramidus was originally defined in 1994 primarily on the basis of recovered teeth, but the sample size was small, limiting comparison to other primate fossils. We now have over 145 teeth, including canines from up to 21 individuals. The expanded sample now provides new information regarding Ar. ramidus and, using comparisons with teeth of other hominids, extant apes, and monkeys, new perspectives on early hominid evolution as well. In apes and monkeys, the male’s upper canine tooth usually bears a projecting, daggerlike crown that is continuously sharpened (honed) by wear against a Dentitions from human (left), Ar. ramidus (middle), and chimpanzee (right), all males. specialized lower premolar tooth (together these form Below are corresponding samples of the maxillary first molar in each. Red, thicker enamel the C/P3 complex). The canine tooth is used as a slic- (~2 mm); blue, thinner enamel (~0.5 mm). Contour lines map the topography of the crown ing weapon in intra- and intergroup social conflicts. and chewing surfaces. Modern humans have small, stublike canines which function more like incisors. In modern monkeys and apes, the upper canine is important in All known modern and fossil apes have (or had) a honing C/P3 com- male agonistic behavior, so its subdued shape in early hominids and plex. In most species, this is more developed in males than females (in Ar. ramidus suggests that sexual selection played a primary role in a few species, females have male-like large canines, either for territo- canine reduction. Thus, fundamental reproductive and social behavrial defense or for specialized feeding). The relatively large number of ioral changes probably occurred in hominids long before they had Ar. ramidus teeth, in combination with Ethiopian Ar. kadabba, Kenyan enlarged brains and began to use stone tools. Orrorin, and Chadian Sahelanthropus [currently the earliest known Thick enamel suggests that an animal’s food intake was abrasive; hominids at about 6 million years ago (Ma)], provide insight into the for example, from terrestrial feeding. Thin enamel is consistent with ancestral ape C/P3 complex and its evolution in early hominids. a diet of softer and less abrasive foods, such as arboreal ripe fruits. We In basal dimensions, the canines of Ar. ramidus are roughly as measured the enamel properties of more than 30 Ar. ramidus teeth. large as those of female chimpanzees and male bonobos, but their Its molar enamel is intermediate in thickness between that of chimcrown heights are shorter (see figure). The Ar. ramidus sample is now panzees and Australopithecus or Homo. Chimpanzees have thin large enough to assure us that males are represented. This means that enamel at the chewing surface of their molars, whereas a broad conmale and female canines were not only similar in size, but that the cave basin flanked by spiky cusps facilitates crushing fruits and male canine had been dramatically “feminized” in shape. The crown shredding leaves. Ar. ramidus does not share this pattern, implying a of the upper canine in Ar. ramidus was altered from the pointed shape diet different from that of chimpanzees. Lack of thick enamel indiseen in apes to a less-threatening diamond shape in both males and cates that Ar. ramidus was not as adapted to heavy chewing and/or females. There is no evidence of honing. The lower canines of Ar. eating abrasive foods as were later Australopithecus or even Homo. ramidus are less modified from the inferred female ape condition The combined evidence from the isotopic content of the enamel, denthan the uppers. The hominid canines from about 6 Ma are similar in tal wear, and molar structure indicates that the earliest hominid diet size to those of Ar. ramidus, but (especially) the older upper canines was one of generalized omnivory and frugivory and therefore difappear slightly more primitive. This suggests that male canine size fered from that of Australopithecus and living African apes. and prominence were dramatically reduced by ~6 to 4.4 Ma from an ancestral ape with a honing C/P3 complex and a moderate degree of See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. When citing, please refer to the full paper, available at DOI 10.1126/science.1175824. male and female canine size difference.
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Careful Climbing in the Miocene: The Forelimbs of Ardipithecus ramidus and Humans Are Primitive C. Owen Lovejoy, Scott W. Simpson, Tim D. White, Berhane Asfaw, Gen Suwa
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grasping hand and highly skeleton yet found, had only two mobile forelimb are defining hand bones—far short of the number characteristics of primates. needed to interpret the structure and The special ability to pick things up evolution of the hand. The Ardipithand manipulate them has probably ecus skeleton reported here changes been a central selective force in makthat. Not only is it more than 1 milG ing primates so unusually intelligent. lion years older than Lucy (4.4 milIt’s something that porpoises can’t do lion versus 3.2 million years old), its B E at all and crows can’t do very well. It hands are virtually complete and F may also be one reason why humans intact. They show that Ardipithecus A alone eventually evolved cognition. did not knuckle-walk like African D The hands of African apes are apes and that it lacked virtually all of specialized in a number of ways that the specializations that protect great C make them dramatically different ape hands from injury while they H from our own. Apes must support climb and feed in trees. their large body mass during climbArdipithecus hands were very ing to feed and nest, especially in the Two views of the left hand of Ar. ramidus showing primitive features different from those of African apes. middle and higher parts of the tree absent in specialized apes. (A) Short metacarpals; (B) lack of knuckle- Its wrist joints were not as stiff as canopy. Their hands must therefore walking grooves; (C) extended joint surface on fifth digit; (D) thumb those of apes, and the joints between withstand very high forces, and this more robust than in apes; (E) insertion gable for long flexor tendon their palms and fingers were much is facilitated by their elongated palms (sometimes absent in apes); (F) hamate allows palm to flex; (G) sim- more flexible. Moreover, a large and fingers. Our palms are much ple wrist joints; (H) capitate head promotes strong palm flexion. Inset: joint in the middle of the wrist (the shorter and our wrists more mobile. lateral view of capitates of Pan, Ar. ramidus, and human (left to right). midcarpal joint) was especially Dashed lines reflect a more palmar capitate head location for Ar. This allows us to grasp objects and ramidus and humans, which allows a more flexible wrist in hominids. flexible, being even more mobile compress them with great dexterity than our own. This would have and force—something often called a “power grip.” The differences allowed Ardipithecus to support nearly all of its body weight on its between ape and human forelimbs become less pronounced going palms when moving along tree branches, so that it could move from the hand to the shoulder. Ape and human elbow joints, for exam- well forward of a supporting forelimb without first releasing its ple, diverge only moderately in their manner of load transmission. grip on a branch. The high loads that apes bear during locomotion have required This discovery ends years of speculation about the course of them to greatly stiffen the joints between their fingers and palms. human evolution. Our ancestors’ hands differed profoundly from Because their thumb has not been elongated in the same way as their those of living great apes, and therefore the two must have substanpalms and fingers have, thumb-to-palm and thumb-to-finger opposi- tially differed in the ways they climbed, fed, and nested. It is African tions are more awkward for them. We are therefore much more adept apes who have evolved so extensively since we shared our last comat making and using tools. All of these forelimb characteristics in apes mon ancestor, not humans or our immediate hominid ancestors. have led them to adopt an unusual form of terrestrial quadrupedality, Hands of the earliest hominids were less ape-like than ours and quite in which they support themselves on their knuckles rather than on different from those of any living form. their palms. Only African apes exhibit this “knuckle-walking.” Other Ardipithecus also shows that our ability to use and make tools did primates, such as monkeys, still support themselves on their palms. not require us to greatly modify our hands. Rather, human grasp and It has long been assumed that our hands must have evolved from dexterity were long ago inherited almost directly from our last comhands like those of African apes. When they are knuckle-walking, mon ancestor with chimpanzees. We now know that our earliest their long forelimbs angle their trunks upward. This posture has ancestors only had to slightly enlarge their thumbs and shorten their therefore long been viewed by some as “preadapting” our ancestors fingers to greatly improve their dexterity for tool-using. to holding their trunks upright. Until now, this argument was unsettled, because we lacked an ade- See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. quate fossil record. Even Lucy, the most complete Australopithecus When citing, please refer to the full paper, available at DOI 10.1126/science.1175827.
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The Pelvis and Femur of Ardipithecus ramidus: The Emergence of Upright Walking C. Owen Lovejoy, Gen Suwa, Linda Spurlock, Berhane Asfaw, Tim D. White
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irtually no other primate has a human-like pelvic girdle—not even our closest living relatives, the chimpanzee and bonobo. Such uniqueness evolved via substantial modifications of a pelvis more originally suited for life in trees. This arboreal primate heritage has left us rather ungainly. Our legs are massive because they continue to house almost all of the muscles originally required for climbing. Our hamstrings, the large muscles in our posterior thighs, must decelerate the swinging limb with each step, and when we run, the limb’s inertia is sometimes too great and these muscles fail (not something one would want to happen on a savanna). Furthermore, when each limb leaves the ground to Homo sapiens Ar. ramidus Au. afarensis P. troglodytes be swung forward, it and the pelvis are unsupported and would slump toward the ground were it not for The Ar. ramidus pelvis has a mosaic of characters for both bipedality and climbing. Left to right: muscles acting on the opposite side of the body (the Human, Au. afarensis (“Lucy”), Ar. ramidus, Pan (chimpanzee). The ischial surface is angled anterior gluteals). One early anthropologist described near its midpoint to face upward in Lucy and the human (blue double arrows), showing that human locomotion as a process by which we alter- their hamstrings have undergone transformation for advanced bipedality, whereas they are nately almost fall on our faces. Chimpanzees and primitive in the chimpanzee and Ar. ramidus (blue arrows). All three hominid ilia are vertically other primates cannot prevent such slumping when short and horizontally broad, forming a greater sciatic notch (white arrows) that is absent in Pan. A novel growth site [the anterior inferior iliac spine (yellow arrows)] is also lacking in Pan. walking upright because they cannot reposition these muscles effectively. Their spine is too inflexible and their ilia—the large pelvic bones to which the gluteals attach—are almost entirely ape-like, presumably because it still had massive positioned and shaped differently than ours. Modifying a typical hindlimb muscles for active climbing. chimp or gorilla pelvis to facilitate upright walking would require Changes made in the upper pelvis rendered Ar. ramidus an effecextensive structural changes. tive upright walker. It could also run, but probably with less speed and Until now, the fossil record has told us little about when and how efficiency than humans. Running would also have exposed it to the early hominid pelvis evolved. Even 3 to 4 million years ago (when injury because it lacked advanced mechanisms such as those that our brains were still only slightly larger than those of chimpanzees), it would allow it to decelerate its limbs or modulate collision forces at had already undergone radical transformation. One of the oldest its heel. Australopithecus, which had given up its grasping foot and hominid pelves, that of Australopithecus afarensis (A.L. 288-1; abandoned active climbing, had evolved a lower pelvis that allowed it “Lucy”), shows that her species had already evolved virtually all of the to run and walk for considerable distances. fundamental adaptations to bipedality. Even the kinetics of her hip Ar. ramidus thus illuminates two critical adaptive transitions in joint were similar to ours. Although the human pelvis was later further human evolution. In the first, from the human-chimp last common reshaped, this was largely the result of our much enlarged birth canal. ancestor to Ardipithecus, modifications produced a mosaic pelvis Ardipithecus ramidus now unveils how our skeleton became pro- that was useful for both climbing and upright walking. In the second, gressively modified for bipedality. Although the foot anatomy of Ar. from Ardipithecus to Australopithecus, modifications produced a ramidus shows that it was still climbing trees, on the ground it walked pelvis and lower limb that facilitated more effective upright walking upright. Its pelvis is a mosaic that, although far from being chim- and running but that were no longer useful for climbing. Because panzee-like, is still much more primitive than that of Australopithecus. climbing to feed, nest, and escape predators is vital to all nonhuman The gluteal muscles had been repositioned so that Ar. ramidus primates, both of these transitions would likely have been a response could walk without shifting its center of mass from side to side. This to intense natural selection. is made clear not only by the shape of its ilium, but by the appearance of a special growth site unique to hominids among all primates (the See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. anterior inferior iliac spine). However, its lower pelvis was still When citing, please refer to the full paper, available at DOI 10.1126/science.1175831.
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Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus C. Owen Lovejoy, Bruce Latimer, Gen Suwa, Berhane Asfaw, Tim D. White
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CREDIT: RECONSTRUCTION, COPYRIGHT J. H. MATTERNES; CHIMPANZEE CLIMBING, J. DESILVA; BONOBO AND HUMAN FEET, S. INGHAM CREDITS (TOP TO BOTTOM):
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Pan Homo he special foot adaptations that the great toe closed during grasping, enable humans to walk upright has been relocated more toward the and run are central to underfront of the foot. This makes the tenstanding our evolution. Until the disdon run more parallel to other joints covery of Ardipithecus ramidus, it was that cross the midfoot, and allows generally thought that our foot evolved apes to grasp with great power withfrom one similar to that of modern out stiffening these other, flexible African apes. Apes have feet that are joints. Apes can thus both powerfully modified to support their large bodies grasp and mold their feet around and to facilitate vertical climbing, thus objects at the same time. However, allowing them to feed, nest, and seek their feet have become less effective safety in trees. Our foot differs from as levers, making them far less useful theirs in myriad ways, and its evoluin terrestrial propulsion. Ardipithecus ramidus tion from theirs would consequently The foot of Ar. ramidus shows that have required an extensive series of none of these ape-like changes were structural changes. Some mid–20thpresent in the last common ancestor century comparative anatomists were of African apes and humans. That so impressed with the profound differancestor, which until now has been ences between human and extant ape thought to be chimpanzee-like, must feet that they postulated a deep, prehave had a more monkey-like foot. ape origin for hominids. Not only did it still have an os perAr. ramidus brings a new perspeconeum, it must also have had all of the tive to this old controversy. Its foot other characteristics associated with turns out to be unlike those of the Foot skeleton of Ar. ramidus (bottom; reconstruction based on it (subsequently abandoned in chimAfrican apes in many ways. The par- computed tomography rendering shown) lacked many features panzees and gorillas). We infer this tial skeleton of Ar. ramidus preserves that have evolved for advanced vertical climbing and suspension because humans still have these charmost of the foot and includes a special in extant chimpanzees (Pan, top left). Chimpanzees have a highly acteristics, so we must have retained bone called the os peroneum that is flexible midfoot and other adaptations that improve their ability them from our last common ancestor. critical for understanding foot evolu- to grasp substrates. These are absent in Ar. ramidus. The mid–20th-century anatomists tion. This bone, which is embedded were correct to worry about the human within a tendon, facilitates the mechanical action of the fibularis foot as they did: Ours turns out to have evolved in one direction, longus, the primary muscle that draws in the big toe when the foot is while those of African apes were evolving in quite another. grasping. Until now, we knew little about this bone’s natural history, One of the great advantages of our more rigid foot is that it works except that it is present in Old World monkeys and gibbons but gen- much better as a lever during upright walking and running (as it also erally not in our more recent ape relatives. Monkeys are very accom- does in monkeys). However, Ar. ramidus still had an opposable big plished at leaping between trees. They must keep their feet fairly rigid toe, unlike any later hominid. Its ability to walk upright was thereduring takeoff when they hurl themselves across gaps in the tree fore comparatively primitive. Because it had substantially modified canopy; otherwise, much of the torque from their foot muscles would the other four toes for upright walking, even while retaining its be dissipated within the foot rather than being transferred to the tree. grasping big toe, the Ardipithecus foot was an odd mosaic that The African apes are too large to do much leaping. They have worked for both upright walking and climbing in trees. If our last therefore given up the features that maintain a rigid foot and have common ancestor with the chimpanzee had not retained such an instead modified theirs for more effective grasping—almost to the unspecialized foot, perhaps upright walking might never have point of making it difficult to distinguish their feet from their hands. evolved in the first place. Indeed, very early anatomists argued that the “quadrumanus” apes were not related to humans because of their hand-like feet. Extant See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. apes lack the os peroneum, and their fibularis tendon, which draws When citing, please refer to the full paper, available at DOI 10.1126/science.1175832.
AUTHORS’SUMMARIES Authors’Summaries
The Great Divides: Ardipithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes C. Owen Lovejoy, Gen Suwa, Scott W. Simpson, Jay H. Matternes, Tim D. White
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volutionary biologists have long recognized Pan that the living primates most similar to humans are the great apes, and comparative genomic Ardipithecus sequence analyses confirm that we are most closely related to chimpanzees and bonobos (genus Pan). Because of our great genomic similarity (sometimes even cited as ~99%), the presumption that we evolved from a chimpanzee-like ancestor has become increas ingly common wisdom. The widely held view that the genomic and phyletic split between Pan and humans was as recent as 5 to 6 million years ago also fuels the often uncritical acceptance of a Pan-like last common ancestor. Ardipithecus ramidus at 4.4 million years ago provides the first substantial body of fossil evi dence that temporally and anatomically extends our knowledge of what the last common ancestor we shared with chimpanzees was like, and therefore allows a test of such presumptions. Until now, Australopithecus afarensis, which lived 3 to 4 million years ago, represented the most primi- Cladogram adding Ar. ramidus to images of gorilla, chimpanzee, and human, taken from the tive well-known stage of human evolution. It had a frontispiece of Evidence as to Man’s Place in Nature, by Thomas H. Huxley (London, 1863) brain only slightly larger than that of chimpanzees, (with the positions of Gorilla and Pan reversed to reflect current genetic data). Numerous and a snout that projected more than in later details of the Ar. ramidus skeleton confirm that extant African apes do not much resemble our hominids. Assuming some variant of a chimpanzee- last common ancestor(s) with them. like ape ancestry, the bipedality of Au. afarensis has been widely interpreted as being so primitive that it probably apes such as Proconsul (which lived more than 15 million years could not have extended either its hip or knee joints and was a ago). Its lower back was mobile and probably had six lumbar verteclumsy upright walker. Some researchers have even postulated that brae rather than the three to four seen in the stiff backs of African Au. afarensis could walk but not run, or vice versa. Still others have apes. Its hand was unpredictably unique: Not only was its thumb suggested that Au. afarensis had a grasping ape-like foot. Similarly, musculature robust, unlike that of an ape, but its midcarpal joint (in it has been suggested that Au. afarensis had forelimbs that were ape- the wrist) allowed the wrist to bend backward to a great degree, like, including long, curved fingers used to forage daily in the arboreal enhancing its ability to move along tree branches on its palms. None canopy, and that its immediate ancestors must have knuckle- of the changes that apes have evolved to stiffen their hands for suswalked. Australopithecus males were noticeably larger than females, pension and vertical climbing were present, so its locomotion did and this has often been interpreted as signifying a single-male, not resemble that of any living ape. polygynous, Gorilla-like mating system. Unlike gorillas, it has The hominid descendant of the last common ancestor we shared diminutive canines, but these were argued to be a consequence of its with chimpanzees (the CLCA), Ardipithecus, became a biped by huge postcanine teeth. Early hominids have even been posited to modifying its upper pelvis without abandoning its grasping big toe. have possibly interbred with chimpanzees until just before the It was therefore an unpredicted and odd mosaic. It appears, unlike appearance of Australopithecus in the fossil record. Au. afarensis, to have occupied the basal adaptive plateau of The Ar. ramidus fossils and information on its habitat now reveal hominid natural history. It is so rife with anatomical surprises that no that many of these earlier hypotheses about our last common ances- one could have imagined it without direct fossil evidence. tor with chimpanzees are incorrect. The picture emerging from Ar. ramidus is that this last common ancestor had limb proportions more like those of monkeys than apes. Its feet functioned only partly like See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliations. those of apes and much more like those of living monkeys and early When citing, please refer to the full paper, available at DOI 10.1126/science.1175833.
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Authors’Summaries AUTHORS’SUMMARIES
Reexamining Human Origins in Light of Ardipithecus ramidus C. Owen Lovejoy
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himpanzees, bonobos, and presume a chimpanzee- or gorilla-like BIPEDALITY gorillas are our closest living ancestor to explain habitual upright relatives. The most popular walking. Ar. ramidus was fully capable reconstructions of human evolution of bipedality and had evolved a subPan during the past century rested on the stantially modified pelvis and foot with 1 cm presumption that the behaviors of the which to walk upright. At the same VESTED earliest hominids were related to (or time, it preserved the ability to maneuPROVISIONING even natural amplifications of) behavver in trees, because it maintained a iors observed in these living great apes. grasping big toe and a powerful hip and One effect of chimpanzee-centric thigh musculature. Because upright models of human evolution has been a Ardipithecus walking provided no energy advantage Reduced Intra-sexual tendency to view Australopithecus as for Ar. ramidus (it lacked many of the OVULATORY LOSS OF Agonism and Increased CRYPSIS HONING CANINE transitional between an ape-like ancesadaptations evolved in later hominids Social Adhesion tor and early Homo. such as Australopithecus), reproducArdipithecus ramidus nullifies these Breakthrough adaptations can transform life-history by deviating tive success must have been central to presumptions, as it shows that the from typical reproductive strategy. Early hominids show feminized its evolution in early hominids. anatomy of living African apes is not male canines [left] and primitive bipedality [right]. These suggest Loss of the projecting canine raises that females preferred nonaggressive males who gained reproprimitive but instead has evolved ductive success by obtaining copulation in exchange for valuable other vexing questions because this specifically within extant ape lineages. foods (vested provisioning). Success would depend on copulatory tooth is so fundamental to reproducThe anatomy and behavior of early frequency with mates whose fertility remained cryptic (e.g., tive success in higher primates. What hominids are therefore unlikely to rep- absence of cycling in mammary size). The result would be reduced could cause males to forfeit their abilresent simple amplifications of those agonism in unrelated females, and cooperative expansion of day ity to aggressively compete with other shared with modern apes. Instead, Ar. ranges among equally cooperative males, eventually leading to males? What changes paved the way ramidus preserves some of the ances- exploitation of new habitats. for the later emergence of the energytral characteristics of the last common thirsty brain of Homo? Such questions ancestor with much greater fidelity than do living African apes. Two can no longer be addressed by simply comparing humans to extant obvious exceptions are its ability to walk upright and the absence of apes, because no ape exhibits an even remotely similar evolutionary the large projecting canine tooth in males, derived features that trajectory to that revealed by Ardipithecus. Ardipithecus shares with all later hominids. When the likely adaptations of early hominids are viewed generally Ar. ramidus illuminates our own origins because it clarifies our rela- rather than with specific reference to living chimpanzees, answers to tionship to Australopithecus. For example, the enlarged rear teeth of such questions arise naturally. Many odd hominid characteristics Australopithecus have long been viewed as adaptations to a rough, become transformed from peculiar to commonplace. Combining our abrasive diet. This has led to speculation that canine teeth might have knowledge of mammalian reproductive physiology and the hominid become smaller simply to accommodate the emergence of these other fossil record suggests that a major shift in life-history strategy transenlarged teeth, or that the importance of canine teeth in displays of formed the social structure of early hominids. That shift probably male-to-male aggression waned with the development of weapons. reduced male-to-male conflict and combined three previously unseen Ar. ramidus negates such hypotheses because it demonstrates that small behaviors associated with their ability to exploit both trees and the land canines occurred in hominids long before any of the dental modifica- surface: (i) regular food-carrying, (ii) pair-bonding, and (iii) reproductions of Australopithecus or the use of stone tools. The loss of large tive crypsis (in which females did not advertise ovulation, unlike the canine teeth in males must have occurred within the context of a gener- case in chimpanzees). Together, these behaviors would have substanalized, nonspecialized diet. Comparisons of the Ar. ramidus dentition tially intensified male parental investment—a breakthrough adaptation with those of all other higher primates indicate that the species retained with anatomical, behavioral, and physiological consequences for early virtually no anatomical correlates of male-to-male conflict. Consistent hominids and for all of their descendants, including ourselves. with a diminished role of such agonism, the body size of Ar. ramidus males was only slightly larger than that of females. See pages 62–63 6–7 forfor authors’ affiliations. authors’ affiliation. The discovery of Ar. ramidus also requires rejection of theories that When citing, please refer to the full paper, available at DOI 10.1126/science.1175834.
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RESEARCH ARTICLES Ardipithecus ramidus and the Paleobiology of Early Hominids Tim D. White,1* Berhane Asfaw,2 Yonas Beyene,3 Yohannes Haile-Selassie,4 C. Owen Lovejoy,5 Gen Suwa,6 Giday WoldeGabriel7 Hominid fossils predating the emergence of Australopithecus have been sparse and fragmentary. The evolution of our lineage after the last common ancestor we shared with chimpanzees has therefore remained unclear. Ardipithecus ramidus, recovered in ecologically and temporally resolved contexts in Ethiopia’s Afar Rift, now illuminates earlier hominid paleobiology and aspects of extant African ape evolution. More than 110 specimens recovered from 4.4-million-year-old sediments include a partial skeleton with much of the skull, hands, feet, limbs, and pelvis. This hominid combined arboreal palmigrade clambering and careful climbing with a form of terrestrial bipedality more primitive than that of Australopithecus. Ar. ramidus had a reduced canine/ premolar complex and a little-derived cranial morphology and consumed a predominantly C3 plant–based diet (plants using the C3 photosynthetic pathway). Its ecological habitat appears to have been largely woodland-focused. Ar. ramidus lacks any characters typical of suspension, vertical climbing, or knuckle-walking. Ar. ramidus indicates that despite the genetic similarities of living humans and chimpanzees, the ancestor we last shared probably differed substantially from any extant African ape. Hominids and extant African apes have each become highly specialized through very different evolutionary pathways. This evidence also illuminates the origins of orthogrady, bipedality, ecology, diet, and social behavior in earliest Hominidae and helps to define the basal hominid adaptation, thereby accentuating the derived nature of Australopithecus.
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n 1871, Charles Darwin concluded that Africa was humanity’s most probable birth continent [(1), chapter 7]. Anticipating a skeptical reception of his placement of Homo sapiens as a terminal twig on the organic tree, Darwin lamented the mostly missing fossil record of early hominids (2). Following T. H. Huxley, who had hoped that “the fossilized bones of an Ape more anthropoid, or a Man more pithecoid” might be found by “some unborn paleontologist” [(3), p. 50], Darwin observed, “Nor should it be forgotten that those regions which are the most likely to afford remains connecting man with some extinct ape-like creature, have not as yet been searched by geologists.” He warned that without fossil evidence, it was “useless to speculate on this subject” [(1), p. 199)]. Darwin and his contemporaries nonetheless sketched a scenario of how an apelike 1
Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA. 2Rift Valley Research Service, Post Office Box 5717, Addis Ababa, Ethiopia. 3Department of Anthropology and Archaeology, Authority for Research and Conservation of the Cultural Heritage, Ministry of Youth, Sports and Culture, Post Office Box 6686, Addis Ababa, Ethiopia. 4Department of Physical Anthropology, Cleveland Museum of Natural History, 1 Wade Oval Drive, Cleveland, OH 44106, USA. 5Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44240–0001, USA. 6The University Museum, the University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. 7Earth Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USA. *To whom correspondence should be addressed. E-mail:
[email protected]
ancestor might have evolved into humans. That scenario easily accommodated fossil evidence then restricted to European Neandertals and Dryopithecus (a Miocene fossil ape). Javanese Homo erectus was found in the 1890s, followed by African Australopithecus in the 1920s. By the 1960s, successive grades of human evolution were widely recognized. Australopithecus comprised several Plio-Pleistocene small-brained species with advanced bipedality. This grade (adaptive plateau) is now widely recognized as foundational to more derived Homo. Molecular studies subsequently and independently confirmed Huxley’s anatomically based phylogeny linking African apes and living humans (4). They also challenged age estimates of a human/chimpanzee divergence, once commonly viewed as exceeding 14 million years ago (Ma). The latter estimates were mostly based on erroneous interpretations of dentognathic remains of the Miocene fossil ape Ramapithecus, combined with the presumption that extant chimpanzees are adequate proxies for the last common ancestor we shared with them (the CLCA). The phylogenetic separation of the lineages leading to chimpanzees and humans is now widely thought to have been far more recent. During the 1970s, discovery and definition of Australopithecus afarensis at Laetoli and Hadar extended knowledge of hominid biology deep into the Pliocene [to 3.7 Ma (5, 6)]. The slightly earlier (3.9 to 4.2 Ma) chronospecies Au. anamensis was subsequently recognized as another small-brained biped with notably large postcanine teeth and postcranial derivations shared with its apparent
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daughter species (7, 8). Late Miocene hominid fossils have been recently recovered from Ethiopia, Kenya, and Chad. These have been placed in three genera [Ardipithecus (9–12), Orrorin (13), and Sahelanthropus (14)]. They may represent only one genus (12, 15), and they challenge both savanna- and chimpanzee-based models (16) of hominid origins. Continuing to build on fossil-free expectations traceable to Darwinian roots, some hold that our last common ancestors with African apes were anatomically and behaviorally chimpanzeelike (17), that extant chimpanzees can be used as “time machines” (18), and/or that unique features of Gorilla are merely allometric modifications to accommodate its great body mass. Thus, early Australopithecus has routinely been interpreted as “transitional” and/or a “locomotor missing link” (19, 20) between extant humans and chimpanzees. Bipedality is widely suggested to have arisen as an opportunistic, or even necessary, response to a drier climate and the expansion of savannas. These views have been challenged on paleontological and theoretical grounds (9, 21). However, without additional fossil evidence, the evolutionary paths of the various great apes and humans have remained shrouded. In related papers in this issue (22–27), we describe in detail newly discovered and/or analyzed specimens of Ar. ramidus, including two individuals with numerous postcranial elements. All are dated to 4.4 Ma and come from the Middle Awash area of the Ethiopian Afar rift. Local geology and many associated fossils are also described (28–30). These new data jointly establish Ardipithecus as a basal hominid adaptive plateau preceding the emergence of Australopithecus and its successor, Homo. Inferences based on Ar. ramidus also facilitate understanding its precursors (22, 23, 27, 31). Here, we provide an integrated view of these studies and summarize their implications. The Middle Awash. The Middle Awash study area contains a combined thickness of >1 km of Neogene strata. To date, these deposits have yielded eight fossil hominid taxa spanning the Late Miocene to Pleistocene (>6.0 to <0.08 Ma) (32, 33). Hominids make up only 284 of the 18,327 total cataloged vertebrate specimens. Spatially and chronologically centered in this succession, the Central Awash Complex (CAC) (28, 34) rises above the Afar floor as a domelike structure comprising >300 m of radioisotopically and paleomagnetically calibrated, sporadically fossiliferous strata dating between 5.55 and 3.85 Ma. Centered in its stratigraphic column are two prominent and widespread volcanic marker horizons that encapsulate the Lower Aramis Member of the Sagantole Formation (Fig. 1). These, the Gàala (“camel” in Afar language) Vitric Tuff Complex (GATC) and the superimposed Daam Aatu (“baboon” in Afar language) Basaltic Tuff (DABT), have indistinguishable laser fusion 39 Ar/40Ar dates of 4.4 Ma. Sandwiched between
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Ardipithecusramidus ramidus Ardipithecus the two tuffs are fossiliferous sediments averaging ~3 m in thickness and cropping out discontinuously over an arc-shaped, natural erosional transect of >9 km (28). The rich fossil and geologic data from these units provide a detailed characterization of the Pliocene African landscape inhabited by Ardipithecus. We first surveyed the CAC during 1981 in attempts to understand the distribution of fossils within the region. We launched a systematic program of geological, geochronological, and paleontological investigation in 1992. Initial visits to the CAC’s northeastern flank documented abundant fossilized wood and seeds in the interval between the two tuffs. We collected and identified a highly fragmented sample of vertebrates, including abundant cercopithecid monkeys and tragelaphine bovids. The first hominid fossils were found at Aramis vertebrate paleontology locality 1 (ARA-VP-1) on 17 December 1992. Two initial seasons of stratigraphic and geochronological studies yielded 649 cataloged vertebrates, including a minimum number of 17 hominid individuals represented mostly by teeth (10). Because of its content, the Lower Aramis Member became the focus of our paleontological
efforts. Fourteen sublocalities within the original ARA-VP-1 locality were circumscribed and subjected to repeated collecting of all biological remains, based on multiple team crawls (35) across the eroding outcrops between 1995 and 2005. Analogous collections were made at adjacent localities (ARA-VP-6, -7, and -17), as well as at the eastern and western exposures of the Ardipithecus-bearing sedimentary units (KUSVP-2 and SAG-VP-7) (KUS, Kuseralee Dora; SAG, Sagantole). The Lower Aramis Member vertebrate assemblage (table S1) now totals >6000 cataloged specimens, including 109 hominid specimens that represent a minimum of 36 individuals. An additional estimated 135,000 recovered fragments of bone and teeth from this stratigraphic interval are cataloged by locality and taxon as pooled “bulk” assemblages. Analogous samples were collected from the Lower Aramis Member on the eastern transect pole (SAG-VP-1, -3, and -6). Fossils from localities higher and lower in the local Middle Awash succession (7, 12, 32) and at nearby Gona (36) are reported elsewhere. The ARA-VP-6/500 partial hominid skeleton. Bones of medium and large mammals were usually ravaged by large carnivores, then embedded
in alluvial silty clay of the Lower Aramis Member. Once exposed by erosion, postdepositional destruction of the fossils by decalcification and fracture is typical. As a result, the larger vertebrate assemblage lacks the more complete cranial and postcranial elements typically recovered from other African hominid localities. The identification of larger mammals below the family level is therefore most often accomplished via teeth. The hominid subassemblage does not depart from this general preservational pattern (29). There was consequently little initial hope that the stratigraphic interval between the two tuffs would yield crucially needed postcranial elements of Ardipithecus. The only relevant postcrania (arm elements) had come from slightly higher in the section in 1993 (10). However, on 5 November 1994, Y.H.S. collected two hominid metacarpal fragments (ARA-VP-6/500-001a and b) from the surface of an exposed silty clay ~3 m below the upper tuff (DABT), 54 m to the north of the point that had 10 months earlier yielded the Ardipithecus holotype dentition. Sieving produced additional hominid phalanges. The outcrop scrape exposed a hominid phalanx in situ, followed by a femur shaft and nearly complete tibia. Subsequent excavation during 1994
Fig. 1. Geography and stratigraphy of the Aramis region. Two dated volcanic horizons constrain the main Ardipithecusbearing stratigraphic interval in the Aramis region. The top frame shows these tephra in situ near the eastern end of the 9-km outcrop. The dark stripe in the background is the riverine forest of the modern Awash River running from right to left, south to north, through the Middle Awash study area of the Afar Rift. The lower frames are contemporaneous helicopter viewsoverARA-VP-1(Yonas Molar Site) to show the geographic position of the top photo and to depict the extensive outcrop of the upper tuff horizon (dotted lines show the DABT) across the local landscape. Vehicles are in the same position to provide orientation. Sediments outcropping immediately below this 4.4-million-year-old horizon yielded the floral, faunal, and isotopic contexts for Ar. ramidus. The frame to the left shows the slight eastward dip of the Sagantole Formation toward the modern Awash River. The contiguous frame to the right is a view up the modern upper Aramis catchment. The ARA-VP-6 locality where the partial Ardipithecus skeleton was excavated is near its top right corner (Fig. 2).
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Research Articles RESEARCH ARTICLES and the next field season (at a rate of ~20 vertical mm/day across ~3 m2) revealed >100 additional in situ hominid fragments, including sesamoids (Fig. 2 and table S2). Carnivore damage was absent. The bony remains of this individual (ARAVP-6/500) (Fig. 3) (37) are off-white in color and very poorly fossilized. Smaller elements (hand and foot bones and teeth) are mostly undistorted, but all larger limb bones are variably crushed. In the field, the fossils were so soft that
they would crumble when touched. They were rescued as follows: Exposure by dental pick, bamboo, and porcupine quill probe was followed by in situ consolidation. We dampened the encasing sediment to prevent desiccation and further disintegration of the fossils during excavation. Each of the subspecimens required multiple coats of consolidant, followed by extraction in plaster and aluminum foil jackets, then additional consolidant before transport to Addis Ababa.
Fig. 2. The ARA-VP-6/500 skeletal excavation. Successive zooms on the ARA-VP-6/500 partial skeleton discovery are shown. Insets show the application of consolidant to the tibia shaft and removal of the os coxae in a plaster jacket in 1994–1995. No skeletal parts were found articulated (the mandible excavation succession shows the close proximity of a proximal hand phalanx and trapezium). Only in situ specimens are shown on the plan and profile views. Note the tight vertical and wider horizontal distributions of the remains. Local strata dip ~5° to the east. The lower inside corner of each yellow pin flag marks the center point for each in situ specimen from the 1994–1995 excavation. The 1995–1996 excavation recovered additional, primarily craniodental remains between these flags and the vehicle. The boulder pile emplaced at the end of the 1996–1997 excavation marks the discovery site today. www.sciencemag.org
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Pieces were assigned number suffixes based on recovery order. Back-dirt was weathered in place and resieved. The 1995 field season yielded facial fragments and a few other elements in northern and eastern extensions of the initial excavation. Further excavation in 1996 exposed no additional remains. Each fragment’s position, axial orientation, and dip were logged relative to a datum (strata here dip east at ~4° to 5°). A polygon representing the outer perimeter and vertical extent of the hominid fragment constellation (based on each bone’s center point) was demarcated by a carapace of limestone blocks cemented with concrete after excavation, then further protected by a superimposed pile of boulders, per local Afar custom.
Fig. 3. The ARA-VP-6/500 skeleton. This is a composite photograph to show the approximate placement of elements recovered. Some pieces found separately in the excavation are rejoined here. Intermediate and terminal phalanges are only provisionally allocated to position and side.
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Ardipithecusramidus ramidus Ardipithecus The skeleton was scattered in typical Lower Aramis Member sediment (Fig. 2): fine-grained, massive, unslickensided, reddish-brown alluvial silty clay containing abundant decalcified root casts, fossil wood, and seeds. A 5- to 15-cm lens of poorly sorted sand and gravel lies immediately below the silty clay, and the spread of cranial parts to the north suggests that the bones of the carcass came to rest in a shallow swale on the floodplain. There is no evidence of weathering or mammalian chewing on ARA-VP-6/500. Bony elements were completely disarticulated and lacked anatomical association. Many larger elements showed prefossilization fragmentation, orientation, and scatter suggestive of trampling. The skull was particularly affected, and the facial elements and teeth were widely scattered across the excavated area. Bioturbation tilted some phalanges and metacarpals at high dip angles (Fig. 2). A few postcrania of a large Aquila (eagle) and other birds were recovered during excavation, as were a few micromammals. No largemammal remains (except isolated cercopithecid teeth and shaft splinters from a medium-to-large mammal limb bone) were associated. The cause of death is indeterminate. The specimen is judged to be female. The only pathology is a partially healed osteolytic lesion suggestive of local infection of the left proximal ray 5 pedal phalanx (ARA-VP-6/500-044). Laboratory exposure and consolidation of the soft, crushed fossils were accomplished under binocular microscope. Acetone was applied with brushes and hypodermic needles to resoften and remove small patches of consolidant-hardened encasing matrix. Microsurgery at the interface between softened matrix and bone proceeded millimeter by submillimeter, rehardening each cleaned surface with consolidant after exposure. This process took several years. The freed specimens remain fragile and soft, but radiographic accessibility is excellent. Most restoration and correction for distortion were accomplished with plaster replicas or micro–computed tomography digital data to preserve the original fossils in their discovery state. Environmental context. The Lower Aramis Member lacks any evidence of the hydraulic mixing that afflicts many other hominid-bearing assemblages. The unwarranted inference that early hominids occupied “mosaic habitats” (38) is often based on such mixed assemblages, so the resolution and fidelity of the Aramis environmental data sets are valuable. We estimate that the interval of time represented by the strata between the two tuffs at Aramis is <105 years, and perhaps just a few hundred or thousand years (28, 39). The lithology, thickness, taphonomic evidence, and similar age of the constraining marker horizons imply that geologically, the evidence can be viewed as “habitat timeaveraged” (40). Indeed, we do not see notably different environmental indicators in the fossils or geologic or chemical data sampled vertically
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throughout the interval. The wealth of data allows a high-fidelity representation [sensu (41)] of the ecological community and environment inhabited by Ar. ramidus 4.4 Ma. A variety of data indicate that the wooded biotope varied laterally across the Pliocene landscape (28–30). The hominid-bearing localities (centered on the ARA-VP-1 sublocalities) are rich in fossilized wood fragments, seeds, and animal fossils. Here, isotopic paleosol compositions indicate mostly wooded conditions (28). There was obviously more water at Aramis then (4.4 Ma)—supporting a much richer flora and fauna—than there is today. The higher water budget is possibly due to higher elevation during deposition (42) or to paleoclimatic factors such as a more continuous Pliocene El Niño effect (43). An abrupt transition occurs southeast of the SAG-VP-7 locality, where sedimentary, faunal, taphonomic, and isotopic data imply a more open rift-axial setting depauperate in faunal remains and lacking in primates, micromammals, and macrobotanical remains (29, 30). Along the northern slope of the CAC, all localities of the Lower Aramis Member yielded tragelaphine bovids, monkeys, and other data indicative of more wooded conditions. Carbon isotopes from the teeth of five Ardipithecus individuals found here imply that they fed largely on C3 plants in woodlands and/or among the small patches of forests in the vicinity. We interpret the combined contextual data to indicate that Ar. ramidus preferred a woodland-to-forest habitat (29, 30) rather than open grasslands. This finding is inconsistent with hypotheses positing hominid origins via climate-driven savanna expansion. Variation and classification. Initial (1994) description of the limited hominid sample from Aramis placed these remains in a newly discovered Australopithecus species interpreted as the most primitive then known (10). Subsequent recovery of the ARA-VP-6/500 skeleton showed that, relative to body size, its dentition was small, unlike Australopithecus. Strict cladistic practice required a new genus name for this sister taxon of Australopithecus, so the material was renamed as the new genus Ardipithecus in 1995, with the lack of megadonty added to the species diagnosis even as the partial skeleton’s excavation was still under way (44). Subsequent discovery of the earlier probable chronospecies Ar. kadabba in 1997 (11, 12) was followed by recovery of Orrorin in 2000 (13) and Sahelanthropus in 2001 (14). These Late Miocene fossils provide additional outgroup material useful in assessing the phylogenetic position of Ar. ramidus. Only two adjacent Ethiopian study areas (the Middle Awash and Gona) have yielded confirmed remains of Ar. ramidus to date (7, 36). Neither has produced any evidence to reject a single species lineage as the source of the combined hominid sample from these Pliocene sites. We thus interpret the Lower Aramis Member hominid assemblage as a single taxon (22). Pene-
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contemporary (~4.3 to 4.7 Ma) hominid remains from elsewhere are sparse (45, 46), and these are broadly compatible with the now expanded range of variation in Ar. ramidus (22, 23). Thus, although continental sampling is still obviously inadequate, describing hominid species diversity in this time frame (47) as “very bushy” seems unwarranted (48). The amount of variation within the known Afar Ar. ramidus sample appears to be lower than typical for species of Australopithecus. This is probably due to a lesser degree of sexual dimorphism in Ardipithecus, combined with the narrow time window represented by the interval between the two Aramis tuffs. Skeletal dimorphism is notably difficult to assess, except in rare instances of geologically isochronous samples of a species lineage (e.g., A.L. 333 “first family”) (49). For Ar. ramidus, the ARA-VP-6/500 skeleton (Figs. 3 and 4) provides a rare opportunity for guiding a probabilistic approach to sex attribution of conspecific fossils, relying on canines (22) and postcranially based estimates of body size (27). The implication is that there was broad overlap in body size between males and females of Ar. ramidus. Cranial and dental anatomy. The Ar. ramidus skull (23) is very similar to the larger, more robust Sahelanthropus cranium (TM 266-0160-1) from Chad, also interpreted as an early hominid (14, 50). Some of the differences are probably partly sex-related. Ar. ramidus shares with Sahelanthropus a small cranial capacity (300 to 350 cc) and considerable midfacial projection but a maxillo-premaxillary complex that is less prognathic than that of modern African apes [not necessarily a derived trait shared with Homo, in contrast with (51)]. The Ardipithecus and Sahelanthropus crania each lack a distinct post-toral sulcus, and both exhibit an anteriorly positioned posterior cranial base. Most aspects of the craniofacial structure of Sahelanthropus/Ardipithecus are probably close to the African ape and hominid ancestral state. Gorilla and chimpanzee cranial morphologies, as well as their specialized dentitions, are clearly divergently derived (22). In Gorilla, enhanced facial size and prognathism occur in relation to larger general size and an increasing adaptation to herbivory and folivory. In Pan (also with enhanced prognathism), derived cranial form (including anterior basicranial lengthening) probably occurred as a part of enhanced terrestriality accompanied by elevated agonistic behavior and its anatomical correlates, such as tusklike canines (22, 23). The bonobo cranial base and Ardipithecus craniofacial structure may be less derived, but even the bonobo seems to be derived in its relatively small face and global dental reduction (22). This was probably at least in part due to decreased intraspecific aggression in the bonobo lineage after separation from the common chimpanzee lineage. The superoinferiorly short but intermediately prognathic Ar. ramidus face lacks the
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Research Articles RESEARCH ARTICLES broadening and anterior migration of the zygomaxillary area seen to varying degrees in species of Australopithecus. The primitive craniofacial pattern shared between Sahelanthropus and Ardipithecus suggests that the genus Australopithecus would later evolve a craniofacial struc-
ture capable of increased postcanine mastication consequent to an ecological breakout from wooded habitats, expanding its foraging into more open environments (7, 10). The Ardipithecus dentition suggests omnivory (22). It exhibits none of the specializations
Fig. 4. Comparisons of Ardipithecus (left) and early Australopithecus (right). (A) Ulnar, radial, first rib, and talar comparisons of the Ar. ramidus ARA-VP-6/500 and Au. afarensis A.L. 288-1 (“Lucy”) skeletal individuals illustrate larger postcranial dimensions for the Ardipithecus individual relative to dental size. Comparison of the postcanine dentitions reveals the megadontia of the Australopithecus individual. (B) Occlusal and lateral views of three time-successive mandibles dated to 4.4, 4.12, and 3.4 Ma, respectively, from left to right: ARA-VP-1/401 Ar. ramidus; KNM-KP 29281 Au. anamensis holotype (mirrored); MAK-VP- 1/12 Au. afarensis (mirrored). www.sciencemag.org
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seen among modern apes; neither the large incisors of Pongo or Pan nor the specialized molar morphology of Pongo, Pan, or Gorilla. Postcanine size relative to body size was slightly larger than in Pan but smaller than in Gorilla, Pongo, or (especially) Au. afarensis. Ar. ramidus molars overlap considerably with Pan in some measures of enamel thickness but differ in overall thickness and structure. Chimpanzee molars have a broad occlusal basin with locally thin enamel not seen in Ardipithecus. Pan molar morphology is probably an adaptation to crushing relatively soft and nonabrasive food items such as ripe fruits, while retaining some shearing capacities. The Ardipithecus dentition shows no strong signals of ripe-fruit frugivory, folivory-herbivory, or feeding on hard objects. Its macroscopic and microscopic wear patterns, as well as the low bunodont cusps with intermediate enamel thickness (22), suggest that its diet was not particularly abrasive but may have included some hard foods. It is consistent with a partially terrestrial, partially arboreal pattern of feeding in a predominantly wooded habitat. Carbon isotopic evidence from the teeth of five Ar. ramidus individuals suggests that Ardipithecus and Australopithecus were distinct in dietary intake (30). “Robust” and “nonrobust” Australopithecus have enamel isotope values indicating a diet of more than 30% C4 plants, with variation ranging up to ~80% C4. In contrast, the known Ar. ramidus individuals vary only between ~10 and 25% C4, and thus also differ from Pan troglodytes, which prefers ripe fruit and is considered closer to a pure C3 feeder (30). Thus, Ardipithecus appears to have exploited a wider range of woodland resources than do chimpanzees, but without relying on the open biotope foods consumed by later Australopithecus. Evolution of the canine/lower third premolar complex (C/P3) potentially illuminates social and reproductive behavior. The Ar. ramidus canine sample totals 21 Aramis individuals. Some are small fragments, but all show informative morphology and/or wear. All specimens are either morphologically similar to those from female apes or are further derived toward the later hominid condition (22). Morphological and metric variation in the sample is small. Functionally important sex-related size dimorphism is not apparent. There is no evidence of functional honing (planar facets on the mesiobuccal P3 or sharpened edges on the distolabial upper canine margin). The largest, presumably male, specimens are as morphologically derived as the smallest, showing that dimorphic canine morphology was virtually absent in these hominids by 4.4 Ma. Furthermore, a juvenile probable male lacks the delayed canine eruption seen in chimpanzees, approximating the Au. anamensis and Au. afarensis conditions and indicating that the canine was not an important component of adult sociobehavioral relationships. The differential status of upper versus lower canine morphology is informative. In Ar. ramidus,
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Ardipithecusramidus ramidus Ardipithecus the lower canines retain modally more apelike morphology than do the uppers, and, in contradistinction to other anthropoids, the height of the maxillary canine crown is lower than that of the mandibular (22). This relationship is opposite that seen in great apes and cercopithecids, whose upper canine dominance is exaggerated, particularly in males of dimorphic species. In these primates, upper canine projection and prominence function in both weaponry and display. The Ar. ramidus canines are metrically and morphologically derived in the direction of later hominids, and we hypothesize that reduction and alteration of upper canine size and shape in this and earlier hominid species are related to changes in social behaviors (22, 31). The canines of Sahelanthropus, Orrorin, and Ar. kadabba are broadly equivalent to those of Ar. ramidus in size and function. However, the upper canines of Late Miocene hominids exhibit a subtle but distinctly more primitive morphology than their Ar. ramidus homologs, potentially including occasional residual (female ape–like) honing as part of their variation (12, 15). This suggests that upper canine prominence was reduced through the Late Miocene and Early Pliocene. In contrast, the C/P3 complex of the last common ancestor of hominids and chimpanzees probably had a moderate level of canine dimorphism combined with functional honing. This was subsequently generally retained in P. paniscus and enhanced in P. troglodytes. Body size and dimorphism. The partial skeleton ARA-VP-6/500 is identified as female based on probability assessments of canine size (its canines are among the smallest of those of 21 available individuals) (22). This interpretation is corroborated by its small endo- and exocranial size, as well as its superoinferiorly thin supraorbital torus (23). Bipedal standing body height for the ARA-VP-6/500 individual is estimated at approximately 120 cm, and body mass at ~50 kg (27). Although actual body mass may vary considerably in relation to skeletal size, this is a large female body mass. Of the Ar. ramidus postcranial elements, the humerus represents the largest minimum number of individuals (seven). ARA-VP-6/500 does not preserve a humerus, but detailed comparisons suggest that its forelimb was ~2 to 8% larger in linear dimensions than the partial forelimb skeleton ARA-VP-7/2 (24, 27), which does include a humerus. This would make ARA-VP-6/500 either the second- or third-largest of eight individuals within the Aramis humeral sample. The combined evidence suggests that Ardipithecus skeletal body size was nearly monomorphic, and less dimorphic than Australopithecus, as estimated from template bootstrapping (49). Most likely, Ardipithecus exhibited minimal skeletal body size dimorphism, similar to Pan, consistent with a male-bonded social system, most likely a primitive retention from the CLCA condition (31). With its subsequent commitment to terrestrial bipedality, Australopithecus probably enhanced
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female cooperation and group cohesion, thus potentially reducing female body size, whereas male size increased in response to predation pressure, probably elevated by expanding niche breadth. Postcranial biology and locomotion. Regardless of whether the Afar Ar. ramidus population represents a hominid relict or a lineal ancestor, this taxon’s biology resolves fundamental evolutionary questions persisting since Darwin. Its substantially primitive postcranial anatomy appears to signal a grade-based difference from later Australopithecus. The challenge of understanding its evolutionary and functional implications required a nontraditional approach. Without testable hypotheses of underlying genebased developmental mechanisms, many paleoanthropological analyses have been adaptationist (52) and/or purely numerically discriminatory. Therefore, wherever possible, in the accompanying postcranial papers (24–27) we restrict hypotheses to those that can be formulated consistent with putative selection acting on cascades of modular-based positional information, especially when these can be potentially grounded in known anabolic mechanisms. This approach is summarized elsewhere (53, 54) and in supporting online material text S1. The upper pelvis of Ar. ramidus presents a contrast to its primitive hand, foot, and limbs. The ilia are abbreviated superoinferiorly and sagittally oriented but broad mediolaterally, so much so that the anterior inferior iliac spine has become a separate growth site, as in all later hominids. The pubic symphyseal face is quite short. A slight sciatic notch is present, although ischial structure was similar to that of extant African apes. This suggests that pattern-formation shifts for bipedality were only partly realized in Ar. ramidus. These changes may have culminated a long period of facultative bipedality hinted at by isolated postcranial elements from the probable chronospecies Ar. kadabba (12) and other Late Miocene forms (13, 14). Paramount among the retained primitive characters of the Ar. ramidus hindlimb is a fully abductable first ray (hallux, or great toe), but in combination with elements of a robust plantar substructure that stabilized the foot during heeland toe-off. Although it was still a highly effective grasping organ, the foot of Ar. ramidus also maintained propulsive capacity long since abandoned by extant great apes (in which greater opposition between the hallux and lateral rays evolved, i.e., a more handlike conformation than in Ar. ramidus) (26). Other defining and notably primitive characters include a moderately elongate mid-tarsus, a robust lateral peroneal complex in which muscles of the lateral compartment performed substantial plantarflexion, and a primitive (flexion-resistant) geometric configuration of the lateral metatarsal bases. Thus, the Ar. ramidus foot is an amalgam of retained primitive characters as well as traits specialized for habitual
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bipedality, such as the expanded second metatarsal base that anchored plantarflexion during heel- and toe-off. Many of the foot’s primary adaptations to fulcrumation are probable retentions from the gorilla/chimpanzee/human last common ancestor (GLCA), but these have been eliminated in apes, presumably for vertical climbing. The ARA-VP-6/500 radius/tibia ratio is 0.95, as in generalized above-branch quadrupeds such as macaques and Proconsul (an Early Miocene ape) (27). Its intermembral index (the ratio of forelimb length to hindlimb length) is also similar to those of above-branch quadrupeds. These facts suggest that African apes experienced both forelimb elongation and hindlimb reduction, whereas hominid proportions remained largely unchanged until the dramatic forearm shortening and hindlimb elongation of Plio-Pleistocene Homo. These primitive proportions are consistent with virtually all other aspects of the Ar. ramidus skeleton. The inferred locomotor pattern combined both terrestrial bipedality and arboreal clambering in which much weight was supported on the palms. The hand phalanges are elongate relative to those of Proconsul, but metacarpals (Mc) 2 to 5 remained primitively short and lacked any corporal modeling or adaptations typical of knuckle-walking (24). Moreover, the virtually complete wrist of ARA-VP-6/500 (lacking only the pisiform) exhibits striking adaptations for midcarpal dorsiflexion (backward deflection of the dorsum of the hand), consistent with a highly advanced form of arboreal palmigrady. In addition, substantial metacarpal-phalangeal dorsiflexion is indicated both by moderate dorsal notching of the Mc2 to -5 heads and by marked palmar displacement of the capitate head. Together these must have permitted dorsiflexion of the wrist and hand to a degree unparalleled in great apes. The Ar. ramidus elbow joint provided full extension but lacks any characters diagnostic of habitual suspension. Ulnar withdrawal was complete and the thumb moderately robust, with indications of a distinct and fully functional flexor pollicis longus tendon. The hamate’s hamulus permitted substantial metacarpal motion for opposition against the first ray. The central joint complex (Mc2/Mc3/capitate/trapezoid) exhibits none of the complex angular relationships and marked syndesmotic reinforcement seen in extant apes. Together, these retained primitive characters, unlike their homologs in highly derived African apes, imply that the dominant locomotor pattern of the GLCA was arboreal palmigrady rather than vertical climbing and/or suspension (orthogrady). Another strong inference is that hominids have never knuckle-walked (26). The extraordinary forelimb of Ar. ramidus, in combination with its limb proportions and likely primitive early hominid lumbar column (55), casts new light on the evolution of the lower spine. The traditional interpretation has
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Research Articles RESEARCH ARTICLES been that the lumbar transverse processes became dorsally relocated as the lumbar column reduced in length. The data from Ar. ramidus imply that ulnar withdrawal was not a suspensory adaptation but was instead an enhancement of distal forelimb maneuverability that accompanied profound changes in the shoulder. Spinal column invagination appears to have been an integral part of thoracic restructuring to increase shoulder joint laterality, thereby enhancing forelimb mobility for advanced arboreal quadrupedalism, especially careful climbing and bridging. A still primitive deltoid complex in both Ar. ramidus and Asian ancestral apes (e.g., Sivapithecus) now becomes more understandable. A predominantly Sharpey’s fiber deltoid insertion can be viewed as a retention in abovebranch quadrupeds that only later became modified for suspension (separately) in extant African and Asian apes. The adoption of bipedality and its temporal association with progressive canine reduction and loss of functional honing now constitute the principal defining characters of Hominidae. The orthograde positional behaviors of hominids and apes were thus acquired in parallel, generated by early bipedal progression in the former and suspension and vertical climbing in the latter. Overall, Ar. ramidus demonstrates that the last common ancestors of humans and African apes were morphologically far more primitive than anticipated, exhibiting numerous characters reminiscent of Middle and Early Miocene hominoids. This reinforces what Huxley appreciated in 1860: “the stock whence two or more species have sprung, need in no respect be intermediate between those species” [(56), p. 568]. Ardipithecus and the great apes. Ar. ramidus illuminates several collateral aspects of hominoid evolution. Despite the demise of Ramapithecus as a putative hominid ancestor, at least one Eurasian Miocene ape, Ouranopithecus, has been suggested as being phyletically related to later African hominids (57), whereas another, Dryopithecus, is often considered an alternative sister taxon of the hominid and African ape clade (58). Ardipithecus effectively falsifies both hypotheses. Ar. ramidus lacks the derived characters of Ouranopithecus associated with postcanine enlargement and relative canine reduction while still providing a primitive morphological substrate for the emergence of Australopithecus. The new perspective that Ar. ramidus offers on hominoid postcranial evolution strongly suggests that Dryopithecus acquired forelimb adaptations to suspensory behaviors independently from African apes. Ar. ramidus suggests that these Eurasian forms were too derived to have been specially related to either the hominid or extant African ape clades. Moreover, the remarkably primitive postcranium of potential Pongo ancestors (e.g., Sivapithecus), coupled with what is now evidently widespread homoplasy in extant hominoids, suggests that the Pongo clade was established even before the first dispersal events of large-
bodied apes from Africa into Eurasia, shortly after docking of the Afro-Arabian and Eurasian plates at ~18 Ma (59). An additional implication of Ar. ramidus stems from its demonstration that remarkable functional and structural similarities in the postcrania of Pongo and the African apes have evolved in parallel, as have those of Pan and Gorilla (27). Until now, a myriad of characters shared among the extant African apes were presumed to have been present also in ancestral hominids (because they were presumed to have been the ancestral state) (60). However, it now appears that many of these putative shared primitive characteristics have evolved independently. This highlights the alacrity with which similar anatomical structures can emerge, most likely by analogous selection operating on homologous genomes. The same genetic pathways can be repeatedly and independently coopted, resulting in convergent adaptations (61). Recent work on gene expression demonstrates that there are also multiple pathways that can produce similar but independently derived anatomical structures (62). Work on deep homology shows that parallel evolution “must be considered a fact of life in the phylogenetic history of animals” [(63), p. 822]. This is also seen in more terminal branches; for example, during the past two million years of stickleback fish evolution (64). Such evolvability and parallelism are even suggested for the catarrhine dentition (65). Ar. ramidus reveals an excellent example of this phenomenon within the African ape-hominid clade by demonstrating the striking reoccurrence of syndesmotic fixation of the central joint complexes in hominoid wrists adapted to suspensory locomotion (including not only those of Pan and Gorilla but also those of Pongo and, partially, Dryopithecus). Such observations on very different evolutionary scales all caution against indiscriminant reliance on raw character states to assess phylogeny. A consideration of wider patterns of manifestations of such adaptive evolution, not only in character constellations but also in their evolutionary context, may be needed to tease apart homology and homoplasy. A far more complete fossil record will be needed to accomplish such a goal. Such considerations also bear on current estimates of the antiquity of the divergence between the human and chimpanzee clades. Many such estimates, suggesting striking recency, have become widely accepted because of the presumed homology of human and African ape
morphologies (60). This obtains despite the recognition that broad assumptions about both the regularity of molecular change and the reliability of calibration dates required to establish such rates have strong limitations (66, 67). The homoplasy now demonstrated for hominoids by Ar. ramidus provides fair warning with respect to such chronologies, especially those currently used to calibrate other divergence events, including the split times of New and Old World monkeys, hylobatids, and the orangutan. The sparseness of the primate fossil record affecting these estimates is now compounded by the dangers posed by convergences perceived as homologies. Such difficulties are further exacerbated by newly recognized complexities in estimating quantitative degrees of genetic separation (66–68). In effect, there is now no a priori reason to presume that human-chimpanzee split times are especially recent, and the fossil evidence is now fully compatible with older chimpanzee-human divergence dates [7 to 10 Ma (12, 69)] than those currently in vogue (70). Hominid phylogenetics. The expanded Ar. ramidus sample allows more detailed consideration of early hominid phylogenetics. The placement of Ardipithecus relative to later hominids can be approached by using modern and Miocene apes as the outgroup. An earlier cladistic study of this kind concluded that Ar. ramidus was the sister taxon of all later hominids (71). A more recent assessment of Ar. ramidus dental characters came to the same conclusion (7). In these analyses, a suite of derived features and character complexes exclusively aligning Ar. ramidus with Australopithecus was identified, but these were based on comparatively limited anatomical elements. The Ar. ramidus characters reported here, combined with those from Gona (36), allow a more complete analysis that clarifies the relationships among early hominid taxa. Parsimony-based cladistic analyses are useful in deciphering relationships within the hominid family tree, despite their shortcomings (72, 73). The distribution of characters identified in Table 1 clearly shows that Ar. ramidus is derived relative to all known Late Miocene fossils attributed to the hominid clade. The earlier and more primitive probable chronospecies Ar. kadabba is found in 5.5- to 5.7-million-year-old deposits a mere 22 km west of Aramis, consistent with local (and perhaps regional) phyletic evolution. Its limited known elements are similar to those of other Late Miocene hominids in Kenya and Chad (12–14).
Table 1. (See pages 82 and 83.) The assembly of shared derived characters among early hominid taxa. Late Miocene and early Pliocene fossils now allow the strong inference of some character states (primitive, in blue) in the last common ancestor shared by chimpanzees and humans. Many other characters (not shown here) of extant apes were once considered primitive but are now shown to be derived and specific to those lineages. Late Miocene fossils from Ethiopia, Kenya, and Chad share some derived characters (in yellow) with all later hominids. The Ar. ramidus sample reported here shows a mixture of primitive and derived characters consistent with its phylogenetic and chronological placement. Phylogenetic implications are in Fig. 5. (An Excel version of this table is available in the supporting online material.)
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Ardipithecus Ardipithecusramidus ramidus
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Ardipithecusramidus ramidus Ardipithecus Comparatively few features of Ar. ramidus are derived relative to these earlier hominids, although many body parts of the latter are still unrepresented. There are no apparent features sufficiently unique to warrant the exclusion of Ar.
ramidus as being ancestral to Australopithecus (74), and a greatly expanded set of shared derived characters now links Ar. ramidus with later members of the hominid clade. Table 1 identifies some of the most important. This pattern robustly falsi-
Fig. 5. Geographic and temporal sparsity of early hominid fossils. Colored windows represent presently available samples. Specific and subspecific relationships are currently impossible to resolve because of limited available data. Depicted species lineages are gray “bundles” that comprise sampled and hypothetical subspecific (populational; demic) “cords,” each with continuity through time and reticulating with adjacent populations through gene flow. The slice at ~6 Ma reveals the two known (red) samples of Late Miocene hominids (Chad and Kenya), schematized here for simplicity within the same bundle, pending additional evidence (12). Au. afarensis is (so far) sampled in the Ethiopian, Kenyan, Tanzanian, and Chadian (hidden behind the bundle) regions. The Ethiopian Afar region has yielded four named, time-successive taxa, including Ar. ramidus (yellow star). The close chronological and geographic proximity of Ar. ramidus and Au. anamensis within the Middle Awash stratigraphic succession can be accommodated in different stratophenetic arrangements, each with different predictions about future fossil discoveries. Hypothesis 1 interprets all known evidence to represent a species lineage evolving phyletically across its entire range. Hypothesis 2 depicts the same evidence in an Ardipithecus-toAustralopithecus transition (speciation) occurring between ~4.5 and ~4.2 Ma in a regional (or local) group of populations that might have included either or both the Afar and Turkana rifts. Hypothesis 3 accommodates the same evidence to an alternative, much earlier peripheral allopatric “rectangular” speciation model (cladogenesis through microevolution accumulated in a peripheral isolate population, becoming reproductively separated). Other possibilities exist, but at the present time, none of these hypotheses can be falsified based on the available evidence. To choose among them will require more fossil evidence, including well-documented transitions in multiple geographic locales. See the text [and (7)] for details.
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fies earlier assessments that the Aramis fossils represent an ancestral chimpanzee (13, 75). These results are suggestive of a cohesive hominid evolutionary grade preceding Australopithecus (currently >6.0 to 4.2 Ma). By priority, the name Ardipithecus may encompass other named genera at this adaptive plateau (12, 15). The question of whether Ar. ramidus is ancestral to later hominids is moot for some cladists because they consider ancestors inherently unrecognizable and therefore recognize only sister taxa (76). The fossils reported here make it even more obvious that Ar. ramidus is the cladistic sister to Australopithecus/Homo because it shares primitive characters with earlier hominids and apes but at the same time exhibits many important derived characters that are shared exclusively only with later hominids (Table 1). Species-level phylogenetics are more difficult to discern given the sparse geographic and temporal distribution of available fossils (Fig. 5). Primitive characters seen in Ar. ramidus persist most markedly in its apparent (but still poorly sampled) sister species Au. anamensis and, to a lesser degree, in Au. afarensis. The known dental and mandibular remains of Au. anamensis are temporally and morphologically intermediate between those of Ar. ramidus and Au. afarensis, with variation that overlaps in both directions. Its constellation of primitive and derived features of the mandible, CP3 complex, lower dm1 (lower first deciduous molar), and postcanine dentition lends support to the hypothesis of an evolutionary sequence of Ar. ramidus → Au. anamensis → Au. afarensis (7, 8, 77). Circumstantial evidence supporting this hypothesis is the temporal and geographic position of Ar. ramidus directly below the first known appearance of Au. anamensis within the Middle Awash succession. Here, these taxa are stratigraphically superimposed in the same succession, separated by ~80 vertical meters representing ~200,000 to 300,000 years (7). Au. afarensis appears later in the same sequence [3.4 Ma, at Maka (53)]. Therefore, at one end of a spectrum of phylogenetic possibilities, Ar. ramidus may have been directly ancestral to the more derived chronospecies pair Au. anamensis → Au. afarensis across the full (still unknown, presumably African) species range (7, 8, 77) (Fig. 5A). Although Au. afarensis is well represented in craniodental remains and postcrania, its apparent earlier chronospecies Au. anamensis is still woefully underrepresented in both, and because Ar. ramidus is so far known only from limited time horizons and locations, its last appearance, date, and potential relationship to these later taxa are still indeterminate. Given the dramatic differences in postcranial anatomy seen in later Australopithecus and hinted at in known Au. anamensis, it seems likely that a major adaptive shift marked the Ardipithecus-to-Australopithecus transition (whenever and wherever the transition might have occurred and whatever its population dynamics). This transition may not have occurred through
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Research Articles RESEARCH ARTICLES pan-specific phyletic evolution (Fig. 5A). Figure 5 presents two other phylogenetic hypotheses that are also, at present, impossible to falsify. If diagnostic contemporary fossils of Au. anamensis are someday found in rocks of >4.4 Ma, the hypothesis that the Afar population of Ar. ramidus is the phyletic ancestor of Au. anamensis (Fig. 5A, B) would be falsified. In such an eventuality, Aramis Ar. ramidus would represent a persisting relict population of the mother species (Fig. 5C). Given the lack of relevant fossils, it is currently impossible to determine whether there was a geologically rapid phyletic transition between Ardipithecus and Australopithecus in the Middle Awash or elsewhere. Nevertheless, the morphological and ecological transition between these two adaptive plateaus is now discernible. Ardipithecus and Australopithecus. For Darwin and Huxley, the basic order in which human anatomies, physiologies, and behaviors were assembled through time was unknown— indeed unknowable—without an adequate fossil record. They were forced to employ extant ape proxies instead. The latter are now shown to be derived in ways unrelated to the evolution of hominids. The Aramis fossils help clarify the origin of the hominid clade (27, 31), and reveal some paleobiological dimensions of the first hominid adaptive plateau (Ardipithecus). The primitive characters of Ar. ramidus simultaneously provide a new perspective on the evolutionary novelties of Australopithecus. Even in the wake of the Aramis and Gona discoveries, the morphological envelopes, phylogenetic relationships, and evolutionary dynamics of early hominid species remain incompletely understood (Fig. 5). However, the paleobiology of Ar. ramidus—even when viewed through its geographically and temporally restricted Afar samples—now reveals that the basal hominid adaptive plateau comprised facultatively bipedal primates with small brains, reduced nonhoning canines, unspecialized postcanine dentitions, and arboreally competent limb skeletons. Their ecological niche(s) were probably more restricted— and their geographic distribution(s) possibly smaller and more disjunct—than those of later hominid species and genera. The derived postcranial elements of Australopithecus provide a strong contrast to their more primitive homologs in Ardipithecus (78). Relative to the generalized anatomy of the latter, the highly evolved specializations of the foot, ankle, knee, pelvis, wrist, and hand of Au. afarensis (79–81) indicate that this species lineage had largely abandoned locomotion in the arboreal canopy (and its resources). Given the strong selection predicted to have been associated with the emergence of new ranging and feeding patterns in Australopithecus, the transition from Ardipithecus to Australopithecus could have been rapid, and anatomically particularly so in hindlimb structure. The forelimb
(especially the hand) was probably under less intensive selection. It is possible that modification of general cis-regulatory pathways may have generated the striking and novel morphology of the hindlimb, especially the foot, because the autopod seems to be the most morphologically compliant to such mechanisms of modification. The dentognathic shifts could have been more gradational, whatever the mode of phylogenesis. Homo and Australopithecus are the only primates with nongrasping feet, and this particular transformation was probably far-reaching, with consequences for key behavioral constancies in higher primates related to arboreal feeding and nesting. Without stabilizing selection for Ardipithecus-like arboreal capacities involving slow and careful climbing, the foot, pelvis, and thigh would have experienced directional selection to optimize bipedal locomotion during prolonged walking (also in more limited running bouts). With expanded ranging and social adaptations associated with terrestrial feeding in increasingly open environments, the transition could have been profound, but probably rapid, and therefore difficult to probe paleontologically. One possible dynamic of an Ardipithecusto-Australopithecus transition would have involved microevolution within a deme or regional group of demes. Being more ecologically flexible, the derived, potentially speciated populations would have undergone rapid range expansion, perhaps even encountering relict Ardipithecus populations. Unfortunately, the phylogeographic details remain obscure given the poor spatial and temporal resolution of the current fossil record (Fig. 5). This provides a strong incentive for pursuing that record by actively increasing sampling of sediments from different African basins with dates between ~5 and ~3.5 Ma. Currently, Australopithecus appears relatively abruptly in the fossil record at about 4.2 Ma. Relative to Ar. ramidus, available early Australopithecus is now revealed to have been highly derived: a committed biped with slightly enlarged brain, a nongrasping arched foot, further derived canines, substantially specialized postcanine teeth with thick molar enamel, and expanded ecological tolerances and geographic ranges. It is widely recognized that this is the adaptive plateau antecedent to Homo, which is now definable as the third such major adaptive shift in human evolution. Commitment to the terrestrial ranging behaviors of Australopithecus well before the Pleistocene appear to have catalyzed the emergence of what must have been even more highly specialized social and ecological behaviors remarkably elaborated in descendant Homo— the ultimate global primate generalist. Conclusions. Besides hominids, the only apes to escape post-Miocene extinction persist today as relict species, their modern distributions centered in forested refugia. The markedly primitive Ar. ramidus indicates that no modern ape is a realistic proxy for characterizing early hominid
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evolution—whether social or locomotor—as appreciated by Huxley. Rather, Ar. ramidus reveals that the last common ancestor that we share with chimpanzees (CLCA) was probably a palmigrade quadrupedal arboreal climber/clamberer that lacked specializations for suspension, vertical climbing, or knuckle-walking (24–27). It probably retained a generalized incisal/postcanine dentition associated with an omnivorous/frugivorous diet less specialized than that of extant great apes (22, 23). The CLCA probably also combined moderate canine dimorphism with minimal skull and body size dimorphism (22, 23), most likely associated with relatively weak male-male agonism in a male philopatric social system (22, 23, 31). Ardipithecus reveals the first hominid adaptive plateau after the CLCA. It combined facultative terrestrial bipedality (25, 26) in a woodland habitat (28–30) with retained arboreal capabilities inherited from the CLCA (24–27). This knowledge of Ar. ramidus provides us, for the first time, with the paleobiological substrate for the emergence of the subsequent Australopithecus and Homo adaptive phases of human evolution. Perhaps the most critical single implication of Ar. ramidus is its reaffirmation of Darwin’s appreciation: Humans did not evolve from chimpanzees but rather through a series of progenitors starting from a distant common ancestor that once occupied the ancient forests of the African Miocene. References and Notes
1. C. Darwin, The Descent of Man, and Selection in Relation to Sex (John Murray, London, 1871). 2. We here consider Hominidae to include modern humans and all taxa phylogenetically closer to humans than to Pan (common chimpanzee and bonobo), that is, all taxa that postdate the split between the lineage leading to modern humans and the lineage that led to extant chimpanzees. 3. T. H. Huxley, Evidence as to Man’s Place in Nature (London, 1863). 4. V. M. Sarich, A. C. Wilson, Proc. Natl. Acad. Sci. U.S.A. 58, 142 (1967). 5. D. C. Johanson, M. Taieb, Y. Coppens, Am. J. Phys. Anthropol. 57, 373 (1982). 6. M. D. Leakey et al., Nature 262, 460 (1976). 7. T. D. White et al., Nature 440, 883 (2006). 8. W. H. Kimbel et al., J. Hum. Evol. 51, 134 (2006). 9. G. WoldeGabriel et al., Nature 371, 330 (1994). 10. T. D. White, G. Suwa, B. Asfaw, Nature 371, 306 (1994). 11. Y. Haile-Selassie, Nature 412, 178 (2001). 12. Y. Haile-Selassie, G. Suwa, T. D. White, in Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia, Y. Haile-Selassie, G. WoldeGabriel, Eds. (University of California, Berkeley, CA, 2009), pp. 159–236. 13. B. Senut et al., Comptes Rendus de l’Academie des Sciences, Series IIA: Earth and Planetary Science 332, 137 (2001). 14. M. Brunet et al., Nature 418, 145 (2002). 15. Y. Haile-Selassie, G. Suwa, T. D. White, Science 303, 1503 (2004). 16. J. Moore, in Great Ape Societies, W. C. McGrew et al., Eds. (Cambridge Univ. Press, Cambridge, 1996), pp. 275–292. 17. B. G. Richmond, D. R. Begun, D. S. Strait, Yearb. Phys. Anthropol. 44, 70 (2001). 18. R. Wrangham, D. Pilbeam, in All Apes Great and Small, Volume 1: African Apes, B. Galdikas et al., Eds. (Kluwer Academic/Plenum, New York, 2001), pp. 5–17. 19. J. T. Stern, R. L. Susman, Am. J. Phys. Anthropol. 60, 279 (1983).
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Ardipithecusramidus ramidus Ardipithecus 20. J. T. Stern, Evol. Anthropol. 9, 113 (2000). 21. B. Latimer, in Origines de la Bipedie chez les Hominides, B. Senut, Y. Coppens, Eds. (Editions CNRS, Paris, 1991), pp. 169–176. 22. G. Suwa et al., Science 326, 69 (2009). 23. G. Suwa et al., Science 326, 68 (2009). 24. C. O. Lovejoy et al., Science 326, 70 (2009). 25. C. O. Lovejoy et al., Science 326, 71 (2009). 26. C. O. Lovejoy et al., Science 326, 72 (2009). 27. C. O. Lovejoy et al., Science 326, 73 (2009). 28. G. WoldeGabriel et al., Science 326, 65 (2009). 29. A. Louchart et al., Science 326, 66 (2009). 30. T. D. White et al., Science 326, 67 (2009). 31. C. O. Lovejoy, Science 326, 74 (2009). 32. H. Gilbert, B. Asfaw (Eds.), Homo erectus: Pleistocene Evidence from the Middle Awash, Ethiopia (Univ. California Press, Berkeley, CA, 2008). 33. Y. Haile-Selassie, G. WoldeGabriel (Eds.), Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia (Univ. California Press, Berkeley, California, 2009). 34. P. R. Renne, G. WoldeGabriel, W. K. Hart, G. Heiken, T. D. White, Geol. Soc. Am. Bull. 111, 869 (1999). 35. In 1994, the Middle Awash project instituted “crawls” of sedimentary outcrop between the GATC and DABT to collect all available fossil material. Crawls were generally upslope in direction, done by teams of 5 to 15 collectors who crawled the surface on hands and knees, shoulder to shoulder, collecting all fossilized biological materials between a prescribed pair of taut nylon cords. Surfaces were repeatedly collected with this technique, invariably resulting in successively depressed specimen recovery numbers in subsequent field seasons. 36. S. Semaw et al., Nature 433, 301 (2005). 37. No surface or in situ fragments of the ARA-VP-6/500 specimen are duplicate anatomical elements. Only 7.3% of 136 total pieces (table S2) were surface recoveries at the excavation site. All other pieces were excavated in situ. Preservation is identical across the entire recovered set. There is no evidence of multiple maturational ages among the 136 pieces, and many of them conjoin. Given the close stratigraphic and spatial association (Fig. 2), and given no evidence of any other individual from the carefully excavated spatiostratigraphic envelope, we conclude that the parts of the ARA-VP-6/500 specimen represent a single individual’s disarticulated skeleton. 38. S. Elton, J. Anat. 212, 377 (2008). 39. A. K. Behrensmeyer, Paleobiology 8, 211 (1981). 40. S. M. Kidwell, K. W. Flessa, Annu. Rev. Earth Planet. Sci. 24, 433 (1996). 41. D. Western, A. K. Behrensmeyer, Science 324, 1061 (2009). 42. R. Pik, B. Marty, J. Carignan, J. Lavé, Earth Planet. Sci. Lett. 215, 73 (2003). 43. A. V. Fedorov et al., Science 312, 1485 (2006). 44. T. D. White, G. Suwa, B. Asfaw, Nature 375, 88 (1995). 45. A. Hill, S. Ward, Yearb. Phys. Anthropol. 31, 49 (1987). 46. M. G. Leakey, J. M. Harris, Eds., Lothagam: The Dawn of Humanity in Eastern Africa (Columbia Univ. Press, New York).
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47. J. Kappelman et al., Nature 376, 558 (1995). 48. T. D. White, in The Paleobiological Revolution: Essays on the Growth of Modern Paleontology, D. Sepkoski, M. Ruse, Eds. (Univ. of Chicago Press, Chicago, 2009), pp. 121–148. 49. P. L. Reno, R. S. Meindl, M. A. McCollum, C. O. Lovejoy, Proc. Natl. Acad. Sci. U.S.A. 100, 9404 (2003). 50. M. Brunet et al., Nature 434, 752 (2005). 51. B. Wood, Nature 418, 133 (2002). 52. S. J. Gould, R. C. Lewontin, Proc. R. Soc. London Ser. B. 205, 147 (1979). 53. C. O. Lovejoy, R. S. Meindl, J. C. Ohman, K. G. Heiple, T. D. White, Am. J. Phys. Anthropol. 119, 97 (2002). 54. C. O. Lovejoy, M. J. Cohn, T. D. White, Proc. Natl. Acad. Sci. U.S.A. 96, 13247 (1999). 55. M. A. McCollum et al., J. Exp. Zool. B Mol. Dev. Evol. 312, published online 17 August 2009; 10.1002/jez.b.21316. 56. T. H. Huxley, Westminster Rev. 73, 541 (1860). 57. L. de Bonis, G. D. Koufos, Evol. Anthropol. 3, 75 (1994). 58. D. R. Begun, Anthropol. Sci. 113, 53 (2005). 59. J. Palfy et al., Earth Planet. Sci. Lett. 258, 160 (2007). 60. D. Pilbeam, N. Young, C. R. Palevol 3, 305 (2004). 61. D. S. Stern, V. Orgogozo, Science 323, 746 (2009). 62. M. D. Shapiro, M. A. Bell, D. M. Kingsley, Proc. Natl. Acad. Sci. U.S.A. 103, 13753 (2006). 63. N. Shubin, C. Tabin, S. Carroll, Nature 457, 818 (2009). 64. P. F. Colosimo et al., Science 307, 1928 (2005). 65. L. Hlusko, G. Suwa, R. T. Kono, M. C. Mahaney, Am. J. Phys. Anthropol. 124, 223 (2004). 66. M. J. F. Pulquerio, R. A. Nichols, Trends Ecol. Evol. 22, 180 (2007). 67. N. Elango, J. W. Thomas, S. V. Yi, Proc. Natl. Acad. Sci. U.S.A. 103, 1370 (2006). 68. R. J. Britten, Proc. Natl. Acad. Sci. U.S.A. 99, 13633 (2002). 69. G. Suwa, R. T. Kono, S. Katoh, B. Asfaw, Y. Beyene, Nature 448, 921 (2007). 70. N. Patterson, D. J. Richter, S. Gnerre, E. S. Lander, D. Reich, Nature 441, 1103 (2006). 71. D. S. Strait, F. E. Grine, J. Hum. Evol. 47, 399 (2004). 72. E. Trinkaus, Am. J. Phys. Anthropol. 83, 1 (1990). 73. For example, it has been noted that these methods fail to accurately resolve relationships of modern hominoid species without sufficient intermediate forms from a fossil record (71). 74. Enamel thickness of Ar. ramidus molars ranges largely from what would traditionally be termed “intermediate thin” to “intermediate thick” categories. Lacking the derived thickness pattern of Pan, it forms a suitable ancestral condition for later Australopithecus. The ubiquitous single-rooted lower fourth premolar (P4) in known Aramis and Gona Ar. ramidus is notable, but this is also a known variation of Au. anamensis and A. afarensis. Judging from the clear dominance of double-rooted lower P4’s in Au. afarensis (and thereafter an increasing robusticity of the roots themselves in Australopithecus), either there was selection for larger, more complex premolar root systems or such morphologies emerged as pleiotropy of postcanine enhancement.
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75. 76. 77. 78.
79. 80. 81. 82. 83.
Without such selection, Ar. ramidus as a species probably contained regional populations that varied in premolar root number (22). B. Senut, M. Pickford, C. R. Palevol. 3, 265 (2004). H. Gee, Deep Time: Cladistics, the Revolution in Evolution (Free Press, London, 1999). C. V. Ward, A. C. Walker, M. G. Leakey, Evol. Anthropol. 7, 197 (1999). We use genera to express both phyletic proximity and circumscribed adaptive systems, with ecobehavioral and morphological conditions being integral parts of the latter. This use employs the broadly defined genus Australopithecus, without recognizing the now commonly used Paranthropus (82). This is because both “robust” and “nonrobust” Australopithecus species are characterized by a commonly derived heavy masticatory apparatus (albeit to differing degrees), and also because we cannot—even to this day—be certain that the “robust” species are monophyletic. C. O. Lovejoy, Gait Posture 21, 95 (2005). C. O. Lovejoy, Gait Posture 21, 13 (2005). C. O. Lovejoy, Gait Posture 25, 325 (2007). T. D. White, in The Primate Fossil Record, W. Hartwig, Ed. (Cambridge Univ. Press, Cambridge), pp. 407–417. For funding, we thank NSF (this material is based on work supported by grants 8210897, 9318698, 9512534, 9632389, 9729060, 9727519, 9910344, and 0321893 HOMINID-RHOI), the Institute of Geophysics and Planetary Physics of the University of California at Los Alamos National Laboratory (LANL), and the Japan Society for the Promotion of Science. D. Clark and C. Howell inspired this effort and conducted laboratory and field research. We thank the coauthors of the companion papers (22-30), with special thanks to the ARA-VP-6/500 and -7/2 excavation teams, including A. Amzaye, the Alisera Afar Clan, Lu Baka, A. Bears, D. Brill, J. M. Carretero, S. Cornero, D. DeGusta, A. Defleur, A. Dessie, G. Fule, A. Getty, H. Gilbert, E. Güleç, G. Kadir, B. Latimer, D. Pennington, A. Sevim, S. Simpson, D. Trachewsky, and S. Yoseph. G. Curtis, J. DeHeinzelin, and G. Heiken provided field geological support. D. Helgren, D. DeGusta, L. Hlusko, and H. Gilbert provided insightful suggestions and advice. We thank H. Gilbert, K. Brudvik, L. Bach, D. Paul, B. Daniels, and D. Brill for illustrations; G. Richards and A. Mleczko for imaging; the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; and the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers who contributed directly to the research efforts and results.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/64/DC1 SOM Text Tables S1 and S2 References 4 May 2009; accepted 8 September 2009 10.1126/science.1175802
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Research Articles RESEARCH ARTICLES
The Geological, Isotopic, Botanical, Invertebrate, and Lower Vertebrate Surroundings of Ardipithecus ramidus Giday WoldeGabriel,1* Stanley H. Ambrose,2 Doris Barboni,3 Raymonde Bonnefille,3 Laurent Bremond,4 Brian Currie,5 David DeGusta,6 William K. Hart,5 Alison M. Murray,7 Paul R. Renne,8 M. C. Jolly-Saad,9 Kathlyn M. Stewart,10 Tim D. White11* Sediments containing Ardipithecus ramidus were deposited 4.4 million years ago on an alluvial floodplain in Ethiopia’s western Afar rift. The Lower Aramis Member hominid-bearing unit, now exposed across a >9-kilometer structural arc, is sandwiched between two volcanic tuffs that have nearly identical 40Ar/39Ar ages. Geological data presented here, along with floral, invertebrate, and vertebrate paleontological and taphonomic evidence associated with the hominids, suggest that they occupied a wooded biotope over the western three-fourths of the paleotransect. Phytoliths and oxygen and carbon stable isotopes of pedogenic carbonates provide evidence of humid cool woodlands with a grassy substrate.
A
rdipithecus ramidus and abundant associated faunal and floral fossils were recovered from sedimentary rocks in the Central Awash Complex (CAC) of the Middle Awash study area. The CAC is a complexly faulted dome centered 25 km east of the western rift margin, Afar, Ethiopia. Today, 300 m of strata deposited between 5.6 and 3.9 million years ago (Ma) are exposed in the CAC (1). The hominidbearing Lower Aramis Member of the Sagantole Formation lies midway in this stratigraphic succession and crops out along an erosional arc >9 km across, extending from the Ounda Sagantole drainage in the southeast to Aramis Locality 6 in the north, and to Kuseralee Locality 2 to the southwest (Fig. 1). Here, we describe regional and local geology, and present isotopic, paleobotanical, invertebrate, and lower vertebrate fossil evidence that illuminates local conditions at the time the vertebrate fossils were deposited. Geology. The Aramis Member directly overlies the Gàala (“Camel”) Tuff Complex (GATC), 1
Earth Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USA. 2Department of Anthropology, University of Illinois, Urbana, IL 61801, USA. 3 CEREGE (UMR6635 CNRS/Université Aix-Marseille), BP80, F-13545 Aix-en-Provence Cedex 4, France. 4Center for BioArchaeology and Ecology (UMR5059 CNRS/Université Montpellier 2/EPHE), Institut de Botanique, F-34090 Montpellier, France. 5Department of Geology, Miami University, Oxford, OH 45056, USA. 6Department of Anthropology, Stanford University, Stanford, CA 94305, USA. 7Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada. 8Berkeley Geochronology Center, 2455 Ridge Road, Berkeley, CA 94709, USA, and Department of Earth and Planetary Science, University of California, Berkeley, CA 94720, USA. 9Université Paris-Ouest La Défense, Centre Henri Elhaï, 200 Avenue de la République, 92001 Nanterre, France. 10 Paleobiology, Canadian Museum of Nature, Ottawa, Ontario K1P 6P4, Canada. 11Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA. *To whom correspondence should be addressed. E-mail:
[email protected] (T.D.W.);
[email protected] (G.W.)
which has a 40Ar/39Ar age of 4.419 T 0.068 Ma (2, 3). This vitric tuff is 0.5 to 2 m thick and is rich in pumice and crystals. The Aramis Member includes light salmon (hue 5YR) to deep redbrown silt, clay, and sand of variable thickness and induration, deposited on a floodplain. These strata show a general increase in thickness toward the east, and they range from an average of 3 m up to 6 m. They are overlain by the Daam Aatu (“Baboon”) Basaltic Tuff (DABT), which has a 40 Ar/39Ar age of 4.416 T 0.031 Ma (1). We define the Lower Aramis Member as the entirety of both tuffs and all sediments between them. A patchwork of variably fossiliferous localities along the outcrop arc has yielded a combined total of more than 6000 individually cataloged vertebrate fossils between the widespread volcanic marker horizons. The vertebrate assemblages are in close association with sedimentological and structural information, botanical and invertebrate fossils, and oxygen and carbon isotopic data on pedogenic carbonates in soil horizons. Integration of these data allows reconstruction of the physical and biological aspects of the depositional setting. The Middle Awash was a persistent sedimentary basin during the Pliocene (4). The basin axis during deposition of the entire Aramis Member was southeast of the Ardipithecus localities, as evidenced by deltaic and lake margin deposits generally disposed to the southeast, in the direction of paleocurrent orientations and erosional features. Active volcanic centers of the CAC were located to the south (1). Paleoenvironmental data and structural reconstructions suggest that the overall elevation may have been greater than today’s ~600 m, although kinematic models are equivocal (5, 6). The lower tuff (GATC) is underlain by a widespread cobble conglomerate. In the central part of the exposure arc, fossiliferous Lower
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Aramis Member sediments comprise predominantly massive and bioturbated silty clays deposited primarily on a low-relief floodplain far from the main river channel(s). Reworked GATC pumices and glass are present locally, but evidence of channels is limited to rare sandstone lenses generally situated below the fossiliferous strata. Massive (<1.5 m thick), predominantly micritic carbonate horizons and nodules representing groundwater and pedogenic deposits pinch out laterally within clayey silts. These are also locally fossiliferous. Carbonate deposits in some localities contain characteristic features of tufas (7), such as fossil gastropods and other invertebrates, abundant and uncrushed calcite-replaced vegetation, vertebrate remains, and eggshells (guinea-fowl size). These suggest that the carbonate horizons generally formed at or near the landscape surface. Evidence of spring activity includes several 1-m-wide banded travertine deposits associated with faults. A porous microcrystalline carbonate with dense concentrations of calcite isomorphs of plant parts forms a broad, low dome just north of ARA-VP-6. However, in almost all sections excavated for isotopic, phytolith, and pollen analysis, the carbonates lack diagnostic features of tufas. Their micritic textures and the presence of terrestrial soil invertebrate faunal activity (such as dung beetle brood burrows) suggest that the carbonate horizons are derived from groundwater carbonate that generally formed at or near the landscape surface in seasonally saturated soils near springs (fig. S1). Paleosols in the Lower Aramis Member are primarily protosols and calcisols (8) and are most strongly developed just below the DABT. Protosols are 10 to 200 cm thick, with massive to single-grain structure and abundant root structures. Calcisols are 50 to 100 cm thick and contain subsurface horizons (Bk) displaying massive to angular blocky ped structures, weakly developed argillic cutans, and small (<5 mm across) calcareous nodules and tubules. The best-developed calcisols are present directly below the DABT. These nodules are most abundant to the north and may imply that it was slightly drier there. Sections at the southeast end of the exposure arc show weaker soil development, perhaps implying deposition in a predominantly wetter, more axial environment. The DABT is poorly consolidated. The lower third (~15 to 20 cm) of the unit is composed of bedded and laminated gray basaltic glass lapilli and scoria. Given the geometry of its basal contact and lack of underlying incision, we interpret the DABT to have fallen across a dominantly lowrelief landscape. Reworked clasts of the DABT are seen in only a few small shallow channels. The presence of paleosols and minor channels before deposition of the DABT indicates that sedimentation was intermittent and that streams only slightly incised this part of the basin. Sediments immediately overlying the DABT near
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Ardipithecusramidus ramidus Ardipithecus WOBT
DABT
GATC
Silt
Burrows
Sandy silt
Sand (massive)
Sand (cross-
Silt loam
Root marks Root casts (carbonate)
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Isotope sample
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Granular loam
Daam Aatu Basaltic Tuff
Clay loam
Gàala Vitric Tuff Complex bedded)
Carbonate δ13C (‰)
Carbonate δ18O (‰)
Fig. 1. Satellite image of the ~9-km erosional arc exposing the Ardipithecus-bearing GATC-DABT horizon of the Central Awash Complex of the Middle Awash study area, Ethiopia. Isotopic data are shown. Values in the eastern sample sites indicate slightly more open habitat (where primate fossils were not found), a finding consistent with the macrobotanical and paleontological evidence.
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Research Articles RESEARCH ARTICLES the ARA-VP-1 (TS), ARA-VP-7, and ARA-VP10 localities contain massive to weak, blocky, root-marked protosols overlain by alternating massive clayey silt and fine, well-sorted sand with tubular, subvertical 1- to 2-cm burrows. These features indicate that the water table was high and that the floodplain was aggrading more rapidly after deposition of the tuff, in accordance with faunal evidence that more aquatic and waterdependent mammals were more abundant above the DABT. The time span represented by the fossiliferous sediments of the Lower Aramis Member (between the two tuffs) is difficult to ascertain. The dates for the two tephras are statistically indistinguishable, the difference between them only 0.003 T 0.075 million years at 68% confidence. Thus, the dates suggest that, most probably, this interval represents a few thousand to perhaps at most 100,000 years. Paleosols in similar aggrading distal floodplain environments often indicate geologically short time spans. The fossil assemblages collected from between the two tuffs are consistent with environmental stability during the interval, and no evolutionary trends are evident (9). On the basis of analogous settings, these sediments probably represent deposition within 100 to 10,000 years (10) and their paleontological contents would qualify as a “withinhabitat time-averaged assemblage” (11). The depositional environment of the Ar. ramidus fossils in the CAC differs somewhat
from that of penecontemporaneous Gona fossils ~70 km to the northwest. The Gona conspecifics were recovered in mixed-habitat faunas along the western basin margin where lake deposits interfinger with small fluvial channels or lap onto active basaltic cones and flows (12). Stable isotopes. To further elaborate the conditions surrounding deposition of the hominid remains between the two tuffs, we analyzed carbon and oxygen isotopes (13, 14) from paleosol carbonate, as well as carbon isotopes from associated organic matter (Fig. 1, figs. S1 to S3, and tables S1 and S2) (15). Plants using the C3 photosynthetic pathway (such as trees, shrubs, and most herbaceous dicots; shaded forest understory; and cold-adapted tropical alpine and highlatitude grasses) have average d13C values of –26.5 per mil (‰). Tropical savanna grasses using the C4 pathway have average d13C values of –12.5‰. Decomposing plant organic matter labels the soil with a similar isotopic composition (16). Disseminated organic carbon is present in trace amounts in ancient soils formed on volcanic parent materials, mainly in the allophane clay fraction (17), and in carbonate nodules (18). Trace amounts of organic carbon contamination, mainly from C3-based petroleum products introduced after excavation, can substantially lower the d13C values of soils formed in paleoenvironments with C4 plant biomass. We are confident that the procedures used to minimize contamination (table S2) (15) permit accurate reconstruc-
tion of the Aramis Member plant biomass isotopic composition. Soil carbonate d13C values are typically enriched by 14 to 17‰ relative to those of organic matter (19). Lower Aramis Member organic d13C values range from –21‰ to –15‰, and carbonate d13C values range from –6.5‰ to –0.5‰ (table S1). The mean difference between carbonate and included disseminated organic matter d13C values (D13C) is 13.8‰ and the median is 14.3‰. This is within the range expected for well-preserved paleosols (19). Oxygen isotope ratios of pedogenic carbonate nodules reflect those of soil water. The isotopic composition of meteoric waters is controlled by polar ice volume, altitude, temperature, humidity, and evapotranspiration (20–22). Preferential evaporation of isotopically “light” water (H216O) leads to isotopic enrichment of remaining water in near-surface soils (20). Pedogenic carbonate d18O values are thus highest in hot, arid habitats and at low latitudes and altitudes (14, 16). These data reflect woodland to grassy woodland savanna floral habitats with 30% to 70% C4 plants. Carbonate d13C and d18O values increase axially from west to east across this outcrop arc (Fig. 1). These data are consistent with sedimentological, taphonomic, paleobotanical, and paleontological indicators in suggesting more open, exposed, probably grass-dominated habitats for the localities at the eastern pole of the erosional arc of localities (toward the paleo-depocenter)
Fig. 2. Fossilized botanical remains from the Lower Aramis Member. Wood and seeds are ubiquitous at the Ardipithecus-bearing localities of the Lower Aramis Member. (A) Silica bodies (phytoliths). The bilobate (Bi) and polylobate (Po) types are from grasses (Poaceae); the globular echinate (GE) is from palms (Palmae). Scale bar, 10 mm. (B) Fossil wood. Scale bar, 2 cm. (C) Tangential microscopic section: general view showing disposition of rays of fossil wood specimen from ARA-VP-6, identified as the fig tree Ficoxylon sp. Scale bar, 108 mm. (D) Fossilized Celtis (hackberry) seeds. Scale bar, 2 cm.
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Ardipithecusramidus ramidus Ardipithecus (9, 23). None of the primate fossils, micromammals, birds, or macrobotanical remains were found in the 2.5-km stretch of Lower Aramis sediment outcrops southeast of the easternmost Ardipithecusbearing locality (SAG-VP-7). Paleobotany. Many carbonate horizons between the two tuffs contain abundant calcitereplaced wood and endocarps (Fig. 2). In the noncemented sediments, these macrobotanical remains are typically decalcified and sometimes appear during excavation as white streaks or manganese stains. The ubiquitous fossil wood generally lacks the internal structure needed to achieve reliable taxonomic identification, except for one specimen attributed to the fig Ficoxylon. Endocarps of hackberry fruits attributed to Celtis sp. (24) are well preserved and abundant, but there is an inherent preservational bias because these are easily fossilized (25, 26). Therefore, these trees cannot be assumed to have dominated the vegetation. Celtis trees are tolerant of a wide range of environmental conditions; their immature leaves are eaten by chimpanzees (27). We analyzed a variety of silt, clays, and carbonate samples (including splits of the isotopic samples) for pollen, but found none. However, a few grains were extracted from sediment within the ARA-VP-1/401 mandible, as well as from carbonate matrix encasing seeds and two coprolites from ARA-VP-6. The ARA-VP-6 grains are attributed to Myrica (n = 6), Borassus/ Hyphaene (n = 2), Poaceae grass (n = 4), and Cyperaceae (n = 2), and the ARA-VP-1 grains to Borassus/Hyphaene (n = 2). Myrica, Celtis, and palm tree pollen was recovered both below and above the Lower Aramis Member, and these trees
were part of the arboreal vegetation in the region between 4 and 5 Ma. Contemporaneous pollen data recovered from marine sediment deposited in the Gulf of Aden indicate that these trees were widespread and are associated with other components of today’s afromontane flora (28). Given the paucity of pollen, we extracted and analyzed phytoliths in the same samples (Fig. 2, fig. S4, and table S3) (15). Phytoliths produced by grasses (Poaceae) differ in shape and size from those produced by other plants, including woody dicotyledons (most trees and shrubs) and palms (29). Their abundance, relative to the abundance of globular phytoliths from woody dicots and palms, has been used to estimate tree cover on the basis of reference assemblages in modern soils (30). We recovered and recognized 96 phytolith types from 38 samples from the strata between the two tuffs. Types included globular ones typical of palms [globular echinate (31)], woody dicotyledons [globular granulate and smooth, produced by trees and shrubs (32)], grass silica short cells (64 different types), grass bulliform and hair cells, and some rare sclerids and tracheids. The relative abundance of globular phytoliths over grass phytoliths suggests an open grassland southeast of SAG-VP-7, with a maximum tree cover of <40%. West of SAG-VP-7, an estimated maximum tree cover of ~65% is suggested by some samples at KUS-VP-2, ARAVP-10, and ARA-VP-1 (TS). On the basis of the geology, phytoliths, fossils, and isotopic data, we infer that the local Pliocene vegetation included abundant palms and trees or shrubs as well as grasses (as would be characteristic of semi-deciduous woodlands
C
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and open forests for at least part of the year). Palms were present at all localities over the 9-km outcrop arc but were probably most abundant (despite potential overrepresentation) near the ARA-VP-1 and SAG-VP-7 localities. There is no evidence for lowland humid Guineo-Congolian rainforest, subdesertic arid vegetation, or highland C-3 Pooideae grasses (15) in the Lower Aramis Member or from younger or older sediments of the CAC. Evidence for Celtis, Myrica, and palm trees fits well with the presence of a groundwater-supported grassy woodland to forest. Invertebrate fossils. The invertebrate fauna of the GATC-DABT Ar. ramidus–bearing biotope (especially ARA-VP-1 and -6) includes fossilized insect larvae, dung beetle broodballs and nests, diverse gastropods, millipedes, and a small centipede (Fig. 3). The millipedes belong to Spirostreptida, a large order common in a wide variety of modern African habitats from savanna to forests. Pupal cases (calcite-replaced inclusions weathered from carbonate) are common, but taxonomic identification has not proven possible. Dung beetle broodballs from the Lower Aramis Member average 3 to 5 cm in diameter and have walls 5 to 7 mm thick. Up to 15 of these have been found together in chambers excavated into host deposits (fig. S1). Rare larger balls up to 7 cm in diameter indicate a larger species. Dung beetles exist wherever large mammals occur in Africa (33). Terrestrial gastropods are useful indicators of vegetation patterns, rainfall, altitude, and temperature (34). Their fragile shells do not withstand hydraulic transport well, so given their embedding fine-grain sediment of the Lower Aramis
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Fig. 3. Fossilized invertebrate remains and traces from the Lower Aramis Member. (A) Gastropods: ARA-VP-6 Maizania sp. (B) Gastropods: ARA-VP-6 Limicolaria sp. (C) Millipedes: ARA-VP-1. (D) Larvae: ARA-VP-6. (E) ARA-VP-6 centipede. (F) Dung beetle broodballs and nest, ARA-VP-6. Scale bar, 5 cm.
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Research RESEARCHArticles ARTICLES Member, the overall land snail assemblage can be considered to be locally derived (35). The presence of millipedes, insect cocoons, and solitary bee brood cells reinforces this conclusion. The most common gastropod (34 of 40 identified specimens) is Maizania from the M. hildebrandti group, followed by Limicolaria sp. (n = 5), and a single specimen of Chlamydarion cf. hians. This Aramis land snail assemblage resembles that of modern groundwater forests, such as the Kibwezi in Kenya (34). This lowland forest in a regionally semi-arid area thrives because it has a high water table, an analogy consistent with geological evidence from the Lower Aramis Member. Before poaching, its larger mammal composition appears to have been structured analogously to the similarly primate-rich Aramis assemblage. Lower vertebrates. Of 275 identified Lower Aramis Member fish specimens, the dominant genus is the catfish Clarias (n = 175), followed by Barbus (n = 20) and the family Cichlidae (n = 21). These are shallow-water fish, the former capable of tolerating highly deoxygenated waters and a wide temperature range. The giant terrestrial tortoise Geochelonia is present, along with Pelusios (African mud turtle or hinged terrapin), Cyclanorbinae (flapshell softshell turtle), and Pelomedusa (African helmeted turtle). Crocodiles are present and represented by scutes and teeth indistinguishable from those of extant Nile crocodiles. Remains of lizards, snakes, and frogs were recovered, particularly at the ARA-VP-6 microfauna quarry. The Lacertilia sample includes representatives of Varanidae (cf. Varanus) and Iguanidae (cf. chameleons, among others). The Serpentes sample includes at least cf. Pythoninae. Given the marked differences in habitat preferences typically seen even within genera of lizards and snakes, their use in paleoecological reconstruction is limited. Chelonian, crocodylian, and osteichthyan skeletal elements are readily recognizable even when highly fragmentary, so their abundance (number of identified specimens) in a fossil assemblage is almost always inflated relative to their ecological abundance. Even so, these taxa are rare in the Lower Aramis Member vertebrate assemblage relative to other Middle Awash strata and other Pliocene hominid localities (except Laetoli). Most of these aquatic species presumably appeared episodically on the Aramis floodplain during times of over-bank flooding, although it is possible that some fish represent raptor meals—an interpretation supported by the
lack of articulated elements of these taxa at Ardipithecus localities. The relatively thin Lower Aramis Member stratigraphic interval, exposed in an erosional 9-km arc of localities between the rift margin to the west and the basin axis to the east, provides a paleotransect through a 4.4-Ma Pliocene landscape. The largely aggradational plain centered at Aramis and adjacent to the low northern slopes of the emerging CAC was subject to alluvial flooding that embedded a rich faunal and floral community containing Ardipithecus. Evidence of wooded environment is present and seems to have prevailed during this interval across the Ardipithecus-bearing localities that constitute the western three-fourths of this transect (9, 23). The demonstrable co-occurrence of elements of a wooded biotope—including large and small mammals, birds, soil isotopes, gastropods, and micro- and macrobotanical remains—suggests that this floodplain, and the community it supported, constituted a wooded biotope rather than that of a grassland savanna in the localities that contain Ardipithecus. References and Notes 1. P. R. Renne, G. WoldeGabriel, W. K. Hart, G. Heiken, T. D. White, Geol. Soc. Am. Bull. 111, 869 (1999). 2. G. WoldeGabriel et al., Nature 371, 330 (1994). 3. T. D. White et al., Nature 440, 883 (2006). 4. Y. Haile-Selassie, G. WoldeGabriel, Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia (Univ. of California Press, Berkeley, 2009). 5. M. Hailemichael, J. Aronson, S. Savin, M. Tevesz, J. Carter, Palaeogeogr. Palaeoclimatol. Palaeoecol. 186, 81 (2002). 6. T. F. Redfield, W. H. Wheeler, M. Often, Earth Planet. Sci. Lett. 216, 383 (2003). 7. T. D. Ford, H. M. Pedley, Earth Sci. Rev. 41, 117 (1996). 8. G. H. Mack, W. C. James, H. C. Monger, Geol. Soc. Am. Bull. 105, 129 (1993). 9. T. D. White et al., Science 326, 67 (2009). 10. A. K. Behrensmeyer, Paleobiology 8, 211 (1982). 11. S. M. Kidwell, K. W. Flessa, Annu. Rev. Earth Planet. Sci. 24, 433 (1996). 12. J. Quade et al., Geol. Soc. Am. Spec. Pap. 446 (2009). 13. S. H. Ambrose, N. E. Sikes, Science 253, 1402 (1991). 14. T. E. Cerling, in Palaeoweathering, Palaeosurfaces and Related Continental Deposits (Special Publication of the International Association of Sedimentologists), M. Thiry, R. Simon-Coincon, Eds. (Blackwell, Oxford, 1999), pp. 43–60. 15. See supporting material on Science Online. 16. T. W. Boutton et al., Geoderma 82, 5 (1998). 17. A. Chadwick, L. A. Derry, P. M. Vitousek, B. J. Hubert, L. O. Hedin, Nature 397, 491 (1999). 18. M. E. Morgan, J. D. Kingston, B. D. Marino, Nature 367, 162 (1994). 19. T. E. Cerling, Earth Planet. Sci. Lett. 71, 229 (1984). 20. H. Craig, Science 133, 1833 (1961).
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21. J. R. Gat, in Handbook of Environmental Isotope Geochemistry, Vol. 1, P. Fritz, J. Ch. Fontes, Eds. (Elsevier, Amsterdam, 1980), pp. 21–47. 22. G. W. Darling, A. H. Bath, J. J. Gibson, K. Rozanski, in Isotopes in Paleoenvironmental Research, M. J. Leng, Ed. (Springer, Dordrecht, Netherlands, 2005), pp. 1–66. 23. A. Louchart et al., Science 326, 66 (2009). 24. An earlier paper on Aramis (2) attributed these endocarps to Canthium on the basis of identifications by the late R. Dechamps of Belgium. Subsequent work by R.B. revised the identification. 25. G. J. Retallack, J. Hum. Evol. 29, 53 (1995). 26. A. H. Jahren, M. L. Gabel, R. Amundson, Palaeogeogr. Palaeoclimatol. Palaeoecol. 138, 259 (1998). 27. R. W. Wrangham, M. E. Rogers, G. Ibasuta, Afr. J. Ecol. 31, 49 (1993). 28. R. Bonnefille, R. Potts, F. Chalié, D. Jolly, O. Peyron, Proc. Natl. Acad. Sci. U.S.A. 101, 12125 (2004). 29. D. R. Piperno, Phytolith Analysis: An Archaeological and Geological Perspective (Academic Press, San Diego, CA, 1988). 30. D. Barboni, L. Bremond, R. Bonnefille, Palaeogeogr. Palaeoclimatol. Palaeoecol. 246, 454 (2007). 31. F. Runge, Rev. Palaeobot. Palynol. 107, 23 (1999). 32. G. Scurfield, C. A. Anderson, E. R. Segnit, Aust. J. Bot. 22, 211 (1974). 33. I. Hanski, Y. Cambefort, Eds., Dung Beetle Ecology (Princeton Univ. Press, Princeton, NJ, 1991). 34. M. Pickford, J. Afr. Earth Sci. 20, 167 (1995). 35. Sparse contaminant lacustrine gastropod taxa are attributable to recent transport of bioclastic sandstone blocks from younger outcrops to the GATC-DABT package by local people building houses, and via construction of the ARA-VP-6/500 marker platform. 36. Supported by NSF grants 8210897, 9318698, 9512534, 9632389, 9910344, and 0321893 HOMINID-RHOI; the Institute of Geophysics and Planetary Physics of the University of California at Los Alamos National Laboratory (LANL); and the Philip and Elaina Hampton Fund for Faculty International Initiatives at Miami University. The Earth and Environmental Sciences Division Electron Microprobe laboratory at LANL assisted with access and use. We thank G. Curtis for fieldwork, insight, and inspiration; M. Pickford, H. Hutchinson, and W. Shear for gastropod, chelonian, and millipede identifications, respectively; M. Buchet and X. Prasad for pollen preparations and microscopic observations; M. Dupéron-Laudouaneix and J. Dupéron for identification of fossil wood; K. Brudvik and H. Gilbert for illustrations; J. Quade, N. Levin, and S. Semaw for discussion and comparative data; the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; and the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the research efforts.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/65/DC1 SOM Text Figs. S1 to S4 Tables S1 to S3 References 4 May 2009; accepted 14 August 2009 10.1126/science.1175817
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Ardipithecusramidus ramidus Ardipithecus
Taphonomic, Avian, and Small-Vertebrate Indicators of Ardipithecus ramidus Habitat Antoine Louchart,1 Henry Wesselman,2 Robert J. Blumenschine,3 Leslea J. Hlusko,4 Jackson K. Njau,4 Michael T. Black,5 Mesfin Asnake,6 Tim D. White4* Thousands of vertebrate specimens were systematically collected from the stratigraphic interval containing Ardipithecus ramidus. The carcasses of larger mammals were heavily ravaged by carnivores. Nearly 10,000 small-mammal remains appear to be derived primarily from decomposed owl pellets. The rich avifauna includes at least 29 species, mostly nonaquatic forms. Modern analogs of the most abundant birds and of a variety of rodents are associated with mesic woodland environments distant from large water bodies. These findings support inferences from associated geological, isotopic, invertebrate, and large-vertebrate assemblages. The combined results suggest that Ar. ramidus occupied a wooded Pliocene habitat.
I
n an effort to characterize the environment inhabited by Ardipithecus ramidus, between 1994 and 2000 we repeatedly collected fossils from the surface of all known hominidbearing exposures of the 4.4 million-year-old Lower Aramis Member (1). All fossils encountered in systematic “crawls” (2), excavations, and two quarries were collected; this avoided biases introduced by selective collection, a practice that can confound ecological analysis (3). Most of the recovered macrofaunal specimens (approximately 135,000 fossils from mammalian families in which most species exceed 5 kg in adult body weight) were pieces of bone or tooth that could not be taxonomically identified below the family level (Fig. 1). Most were long bone shaft splinters, and many teeth were represented by less than half of a crown. These less identifiable specimens were pooled into locality-specific bulk samples (such as “bulk equid dental” and “bulk mammal bone” from ARA-VP-6). The other >6000 collected specimens from this interval were taxonomically more precisely identifiable and were assigned individual numbers (such as ARA-VP-6/1356). These 1
Iziko South African Museum, Natural History Department, Cenozoic Palaeontology Collections, Box 61, Cape Town 8000, South Africa; and Institut de Génomique Fonctionnelle de Lyon, Team “Evo-devo of vertebrate dentition,” Ecole Normale Supérieure de Lyon, Université Lyon 1, CNRS, INRA, 46 Allée d’Italie, 69964, Cedex 07, Lyon, France. 2Post Office Box 369, Captain Cook, HI, 96704, USA. 3Center for Human Evolutionary Studies, Department of Anthropology, Rutgers University, 131 George Street, New Brunswick, NJ 08901-1414, USA. 4Human Evolution Research Center and Department of Integrative Biology, University of California, Berkeley, 3010 Valley Life Sciences Building, Berkeley, CA, 94720, USA. 5Phoebe A. Hearst Museum of Anthropology, 103 Kroeber Hall, Number 3712, University of California, Berkeley, CA 94720-3712, USA. 6 Ministry of Mines and Energy, Post Office Box 486, Addis Ababa, Ethiopia. *To whom correspondence should be addressed. E-mail:
[email protected]
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specimens represent mammals ranging in size from shrews to proboscideans (2). Taphonomy. Crania, horn core fragments, and postcranial elements identifiable to family level are rare in the total Lower Aramis Member collection. For example, not a single cranium, or even partial cranium, is present among 733 cataloged tragelaphine bovid specimens. Bovid postcranial samples include just 6 proximal metapodials, 17 distal metapodials, 7 calcanei, 19 astragali, 84 phalanges, and 8 distal humeri. Only a few mammals are represented by associated elements, the most complete being the primarily in situ ARAVP-6/500 Ar. ramidus skeleton (1). Fossils from larger mammals show no rounding or abrasion associated with hydraulic transport. This is consistent with the sedimentology of the deposits (1), as well as with the abundance and preservation of small specimens. The assemblages have therefore not been watertransported or -sorted. Surface exfoliation from subaerial weathering and chemical corrosion has obscured the original surface of some pieces and varies by locality. Only 66 of 157 limb bone shaft fragments retain original surfaces adequate for confident identification of perimortem modifications in the most affected bulk bone collection from an Ardipithecus-bearing sublocality (ARAVP-1 SHF). In the more representative bulk sample quantitatively analyzed for this variable (ARA-VP-1 SRG), 40 of 64 specimens had good surface preservation. Fragments from smaller taxa tend to show less weathering across all localities where present, suggesting more rapid burial. Where assessed on preserved original surfaces, limb bone shaft fragments from large mammals display a wide range of marks (Fig. 1). Tooth marking by mammalian carnivores is evident in 21 of 24 bulk bone samples from different localities (each sample typically containing hundreds of specimens). Tooth marks attributable to crocodiles (4) are rare, and were found in only three
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of nine bulk samples assessed. Rodent gnawing (mouse- to porcupine-sized) and insect-derived marks are present in all bulk samples. Root etching is extremely rare. The paucity of trampling marks corresponds to a lack of sand in the substrate (1). Although raptors can account for over 80% of deaths in some modern primate assemblages (5), the distinctive signature of such predation is missing from the cercopithecid assemblage. Instead, the damage and breakage patterns are more consistent with a mammalian carnivore [supporting online material text S1]. A full demographic range is represented, and it is likely that the cercopithecid assemblage is attritional, with heavy postmortem ravaging by carnivores (6, 7). This pattern also holds for the bovid remains. Large mammal carnivorans represent the dominant agent of perimortem bone breakage, as evidenced by the ubiquity of ancient spiral fractures. There are high rates of tooth marking on limb bone fragments (47 to 75% in three bulk assemblages quantitatively assessed; n = 155 specimens) and tooth notching of bone fragment edges (27% of tooth-marked pieces; n = 30). Proportions of limb bone shaft fragments with tooth marks and/or tooth notches are within ranges produced by modern spotted hyaenas, which have been observed to deflesh and extract all marrow while consuming whole limbs (8, 9). There is nearly complete destruction of limb bone ends (98% in one bulk assemblage assessed quantitatively; n = 166). Digestive etching by stomach acids is rare but widespread (including a hominid molar exemplar). This pattern of destruction parallels that seen in instances of complete marrow consumption by modern spotted hyaenas. The hyaenids Ikelohyaena abronia and cf. Crocuta cf. dietrichi, as well as the ursid Agriotherium and four suid taxa are likely suspects for the destruction of the larger bones. The canid Eucyon was also present. Degreased, subaerial, pre-fossilization fragmentation appears to have been relatively insignificant. Postfossilization fracture resulting from breakage upon erosional exposure is ubiquitous (between 33 and 63% of limb bone shaft fragments examined). The overall Ardipithecus-bearing locality and sublocality assemblages indicate that the competition for large mammal carcasses must have been intense. Abundant shaft fragments, rare epiphyseal portions, and the extremely low representation of axial postcrania as compared to those of the appendicular and craniodental skeletons, combined with the high tooth-marking rates, suggest that the Aramis ecosystem may have matched highly competitive modern settings such as Ngorongoro Crater (10). The rarity of late-stage weathering damage characterized by deep cracking and exfoliation (<3% of total specimens at stages 4 and 5) suggests that exposure to subaerial conditions before burial was brief and/ or buffered by tree cover and/or leaf litter. Exceptions to this taphonomic pattern associated with Ardipithecus are the SAG-VP-1 and
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Research RESEARCHArticles ARTICLES Fig. 1. Bone modification of medium and large mammalian remains from the Lower Aramis Member. The central panel shows limb bone shaft splinters that are ubiquitous in the assemblage and were collected by the thousands during the 100% recovery operation. Scale bar, 2 cm. (A) Termite damage. (B) Inner conchoidal scars from carnivore gnawing. (C) Carnivore tooth marks on an Ardipithecus mandible corpus. (D) Stomach acid etching on an artiodactyl phalanx and bone splinter of a mediumsized mammal. (E) Carnivore tooth punctures. (F) Gnawing damage by a small-to-medium carnivore on cercopithecoid limb bones. (G) Similar damage on an Ardipithecus metacarpal. (H) Damage from gnawing by a small rodent on a largemammal limb bone shaft fragment.
SAG-VP-3 localities, 0.5 and 2.0 km southeast of the easternmost Ar. ramidus occurrence. Here, different assemblage composition (table S1) and modification signatures are present. Micromammals, birds, and primates are absent from the Lower Aramis inter-tuff horizon within these spatially extensive but faunally depauperate localities (n = 5 and 3 identified specimens, respectively). Sublocalities with the most surface bone were circumscribed within each of these localities, and fossils were collected by identical methods for comparison with the faunally richer Ardipithecus-bearing localities to the northwest. The resulting assemblages are dominated by poorly preserved (highly weathered) remains of large, mostly aquatic animals, which is consistent with their more axial location in the
depositional basin (as evidenced by structural and sedimentological considerations) (1). Small mammals. Micromammals and birds closely related to extant taxa (and therefore presumed to be ecologically sensitive indicators) are found at all Ardipithecus-bearing localities (table S1). However, the large majority of these primarily small fossils (both individually cataloged and pooled bulk samples) were recovered by water-sieving at two widely separated quarries. The more productive quarry (located <100 m from the ARA-VP-6/500 partial Ar. ramidus skeleton) yielded about 10,000 total specimens. Of these, more than 1000 are micromammal teeth or jaw fragments, or small bird fragments identifiable at or below the ordinal level. In con-
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trast to the intensive destruction of large-mammal bones described above, micromammal and small avian postcrania are well preserved and abundant in these quarry assemblages. All microvertebrate remains from the two quarries were analyzed taphonomically [according to the protocol in (11)]. The dense concentration of remains, consistently high-quality preservation, abundant postcranial elements, and mostly intact jaws suggest that these small mammals were protected from trampling and sunlight. Thus, they probably experienced no postmortem transport, beyond perhaps bioturbation and/or emplacement in dessication cracks during alluvial flooding (based on the in situ vertical alignment of many rodent limb bones in the alluvial silty clay in both quarries).
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Ardipithecusramidus ramidus Ardipithecus
Fig. 2. Relative abundance of avian and small-mammal taxa. For each bird taxon, the pie slice and first number apply to the number of identified specimens (n = 263); the second (in parentheses) is the minimum number of individuals The lack of digestive traces on micromammal molars (0.9%, all in the “slightest” category), the low percentage and degree of such traces on incisors (10.7%; 9.9% in the “slightest” category), and the avian assemblage composition (Fig. 2) combine to suggest that many of the microvertebrate remains may have been disaggregated from barn owl (Tyto) pellets (11). Aside from one strigid specimen, Tyto sp. nov. is the only owl recorded at Aramis and is relatively abundant. Barn owls are well-known micromammal accumulators that produce the lowest levels of digestion and modification among avian predators. Their pellets are known to provide a sample of the micromammal fauna within several kilometers of the roost (11, 12), but the assemblages they create may be biased by prey availability and vulnerability. The Aramis collection (Fig. 2) includes up to 20 new species among a total of 32 small-mammal genera within the orders Insectivora (two families), Chiroptera (five families), Hyracoidea (one family), Rodentia (six families), Lagomorpha (one family) and Carnivora (one family) (2). These taxa indicate that the drainage basin contained a variety of biotopes, but the distribution of fossils and sediments implies that the Ardipithecus-bearing locales were wetter. Drier environments were present at some distance (1, 13). Fossils of the porcupine Atherurus, the murid Oenomys, and the emballonurid Taphozous found at Ardipithecus-bearing localities suggest that forests and/or well-developed mesic woodlands were at least locally present in the paleodrainage basin. Such flora, supported by a high water table or high rainfall due to a higher altitude (1), may have graded into deciduous woodlands. Other associated woodland animals
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represented in the overall sample. For small mammals, the numbers apply to the number of identified specimens only (n = 1127), but closely reflect the minimum number of individuals because only craniodental specimens are included.
include the shrews Crocidura, Myosorex, and Suncus; the bats Rousettus and possibly Hipposideros; the porcupine Xenohystrix; the mice Dendromus, Praomys, and Mus; and the dwarf mongoose Helogale. The existence of mesic settings is supported by the strong presence of the Asiatic murid Golunda (~13%), whose contemporary species G. ellioti is today typically found in thickets and bush on densely vegetated plains. The absence of the cane rat Thryonomys suggests that local suitable aquatic environments were absent, although it is also missing from the more aquatic, primate-free assemblages to the southeast of Aramis. The absence of small hyracoids and galagos is notable and unexplained. The murid Uranomys is abundant, large and small species together representing 44% of smallmammal specimens. In association with Praomys (10%), the two genera constitute about 50% of the micromammalian specimens. Today, Uranomys is almost always found in abundance and in association with Praomys in two biotopes: (i) Borassus palm savanna characterized by a wet Hyparrhenia grassland with dense thickets, and (ii) Mbuga mesic grassland characterized by dense, long grasses (14). Combined with the taphonomic findings, this numerical predominance may reflect predator bias, because barn owls would be expected to have focused their predation in open islands of palm-thicket grassland within the larger woodland setting, as indicated by the many “wooded-habitat” mammalian and avian indicator taxa. Rarer species in the Ardipithecus-bearing assemblages indicate that more xeric and open savanna woodlands were regionally present. These include the bats Rhinolophus and Cardioderma, the squirrel Xerus, the gerbil Tatera, the
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mice Acomys and Saidomys, and the rat Arvicanthis. Still dryer scrub or even arid steppe settings must have also been present (and probably sampled by avian predators), as rarely attested to by the hare Lepus, the hedgehog Atelerix, and the bat Coleura. The Lower Aramis Member localities are today at an elevation of about 600 m, but Tachyoryctes and Myosorex have contemporary counterparts typically found at higher altitudes, in mesic montane forests and uplands. Birds. Rich avifauna (Fig. 2 and table S2) provides additional understanding of the Aramis environment. The 370 cataloged specimens comprise a minimum of 29 different taxa representing at least 16 families in 13 orders. Most taxa are terrestrial rather than aquatic (the latter make up only 3.8% of identified specimens). Small taxa such as doves, lovebirds, mousebirds, passerines, and the swift are abundant. These were mostly recovered from the two quarries and are interpreted as deriving from owl pellets. Open-country taxa such as two bustards (Otididae) and the quail Coturnix sp. are exceedingly rare. Waterfowl are rare and include ?Platalea (ibis or spoonbill, n = 1 identified specimen), Anatidae (geese and ducks, n = 9), and Anhinga (darter, n = 1). These indicate the presence of open water, presumably a river or lake distal to the focus of deposition. In addition to the barn owl, we recovered fossils of the diurnal predators Aquila (eagle, n = 11) and smaller raptors (the size of hawks or kites). These prefer to hunt in open or ecotonal conditions and presumably roosted in tall emergent trees (15). The Aramis galliform assemblage (35% of identified specimens) is dominated by the abundant ecological indicator species Pavo sp., a peafowl (n = 39), signaling forested conditions (16). The lovebirds Agapornis (n = 88) the parrot
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Research Articles RESEARCH ARTICLES Poicephalus sp. (n = 1), and guineafowl ?Guttera sp. (n = 2) are known from woodlands and forests, ranging into wooded savanna. Collectively, the large-mammal taphonomy of Ardipithecus-bearing localities indicates a landscape where carcasses were almost always rapidly and intensively ravaged and the resulting fragments soon buried without transport. The small-mammal and avian assemblages combine with other geological and paleontological data to indicate that mesic woodlands dominated the Ardipithecusbearing landscape 4.4 million years ago. References and Notes 1. 2. 3. 4. 5.
G. WoldeGabriel et al., Science 326, 65 (2009). T. D. White et al., Science 326, 64 (2009). D. F. Su, T. Harrison, J. Hum. Evol. 55, 672 (2008). J. K. Njau, R. J. Blumenschine, J. Hum. Evol. 50, 142 (2006). W. J. Sanders, J. Trapani, J. C. Mitani, J. Hum. Evol. 44, 87 (2003).
6. There is no evidence that Ar. ramidus was in any way involved with this carnivory, but there is also no evidence with which to exclude this possibility. 7. T. D. White, N. Toth, in Breathing Life into Fossils, T. Pickering, K. Schick, N. Toth, Eds. (Stone Age Press, Gosport, IN, 2007), pp. 281–296. 8. R. J. Blumenschine, J. Archaeol. Sci. 15, 483 (1988). 9. R. J. Blumenschine, J. Hum. Evol. 29, 21 (1995). 10. R. J. Blumenschine, J. Hum. Evol. 18, 345 (1989). 11. P. Andrews, Owls, Caves and Fossils. Predation, Preservation and Accumulation of Small Mammal Bones in Caves, with an Analysis of the Pleistocene Cave Faunas from Westbury-sub-Mendip, Somerset, UK (Natural History Museum Publications, London, 1990). 12. R. L. Lyman, R. J. Lyman, Intl. J. Osteoarchaeol. 13, 150 (2003). 13. T. D. White et al., Science 326, 67 (2009). 14. L. Herwig, thesis, Universiteit Antwerpen, Antwerp, Belgium (1992). 15. W. J. Sanders, J. Trapani, J. C. Mitani, J. Hum. Evol. 44, 87 (2003). 16. A. Louchart, S. Afr. J. Sci. 99, 368 (2003).
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17. For funding, we thank the U.S. NSF (this material is based on work supported by grant nos. 8210897, 9318698, 9512534, 9632389, 9910344, and 0321893 HOMINIDRHOI) and the Institute of Geophysics and Planetary Physics of the University of California at Los Alamos National Laboratory. We thank L. Bach and J. Carrier for smallmammal and bird sketches, H. Gilbert for photographic illustration, K. Brudvik, and D. DeGusta for editorial assistance; the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; and the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the research efforts.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/66/DC1 SOM Text Tables S1 and S2 References 4 May 2009; accepted 18 August 2009 10.1126/science.1175823
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Ardipithecus ramidus
Macrovertebrate Paleontology and the Pliocene Habitat of Ardipithecus ramidus Tim D. White,1* Stanley H. Ambrose,2 Gen Suwa,3 Denise F. Su,4 David DeGusta,5 Raymond L. Bernor,6,7 Jean-Renaud Boisserie,8,9 Michel Brunet,10 Eric Delson,11,12 Stephen Frost,13 Nuria Garcia,14 Ioannis X. Giaourtsakis,15 Yohannes Haile-Selassie,16 F. Clark Howell,17† Thomas Lehmann,18 Andossa Likius,19 Cesur Pehlevan,20 Haruo Saegusa,21 Gina Semprebon,22 Mark Teaford,23 Elisabeth Vrba24 A diverse assemblage of large mammals is spatially and stratigraphically associated with Ardipithecus ramidus at Aramis. The most common species are tragelaphine antelope and colobine monkeys. Analyses of their postcranial remains situate them in a closed habitat. Assessment of dental mesowear, microwear, and stable isotopes from these and a wider range of abundant associated larger mammals indicates that the local habitat at Aramis was predominantly woodland. The Ar. ramidus enamel isotope values indicate a minimal C4 vegetation component in its diet (plants using the C4 photosynthetic pathway), which is consistent with predominantly forest/woodland feeding. Although the Early Pliocene Afar included a range of environments, and the local environment at Aramis and its vicinity ranged from forests to wooded grasslands, the integration of available physical and biological evidence establishes Ar. ramidus as a denizen of the closed habitats along this continuum.
C
ircumscribing the ecological habitat of the earliest hominids is crucial for understanding their origins, evolution, and adaptations. Evidence integrated from a variety of independent geological and paleontological sources (1–3) help to place Ardipithecus ramidus in its regional and local Pliocene environmental settings. Here, we assess fossils of the larger vertebrates (mammalian families in which most species exceed 5 kg adult body weight) to reveal characteristics of their diets, water use, and habitat preferences. At Aramis 4.4 Ma (million years ago), predominantly terrestrial plants, invertebrates, and vertebrates were buried relatively rapidly on a low-relief aggrading floodplain, away from perennially moving water capable of displacing most remains (2, 3). Collection bias was avoided by a systematic 100% collection strategy (1). Therefore, the large mammal assemblage spatially associated with Ardipithecus in the Lower Aramis Member allows for relatively robust and precise environmental inference compared with many other hominid-bearing occurrences. The assemblage was carnivore-ravaged and is consequently dominated by bone and dental fragments (3). It represents an attritionally derived fauna collected between two widespread marker tuffs that are today exposed along an extended erosional arc (2, 3). The larger mammal fossil assemblage (4) comprises 3837 individually cataloged specimens assigned to 42 species (6 of them newly discovered), in 34 genera of 16 families (1, 5), across a wide body size range (Fig. 1A). Many of the sampled taxa provide evidence for the evolution of African vertebrates.
We consider ecological habitat to mean the biological and physical setting normally and regularly inhabited by a particular species. Our floral definitions follow the United Nations Educational, Scientific, and Cultural Organization (UNESCO) classification of African vegetation (6). Forests have continuous stands of trees with overlapping crowns, forming a closed, often multistory canopy 10 to 50 m high; the sparse ground layer usually lacks grasses. Forests grade into closed woodlands, which have less continuous canopies and poorly developed grass layers. Woodlands have trees with canopy heights of 8 to 20 m; their crowns cover at least 40% of the land surface but do not overlap extensively. Woodland ground layer always includes heliophilous (sun-loving, C4) grasses, herbs/forbs, and incomplete small tree and shrub understories. Scrub woodland has a canopy height less than 8 m, intermediate between woodland and bushland. As proportions of bushes, shrubs, and grasses increase, woodlands grade into bushland/thickets or wooded grasslands. Reconstructing the Aramis biotope. Reconstructing an ancient environment based on vertebrate macrofossils is often imprecise (7). Even assemblages from a single stratigraphic interval may sample thousands of years and thus represent artificial amalgamations of different biotopes shifting on the landscape through time. Even in a geologically isochronous assemblage, animals from different habitats may be mixed by moving water or by a moving lake or river margin. Ecological fidelity can be further biased through unsystematic paleontological recovery, for example, when only more complete, identifiable, and/or rare specimens are collected.
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Consequently, most early hominid-bearing open-air fossil assemblages conflate multiple biotopes (7). Under such circumstances, it is not surprising that many Pliocene hominid habitats have been referred to as a “mosaic” or “a changing mosaic of habitats” (8). Such characterizations risk confusing noise for signal and local for regional environment, particularly for collection-biased assemblages lacking temporal and spatial resolution. Initial assessment of the fauna associated with Ar. ramidus indicated “a closed, wooded” environment (9), an inference subsequently misquoted as “forest” (10). This interpretation was criticized on the basis that colobine monkeys and tragelaphine bovids might be unreliable indicators (11, 12). Taxonomic abundance. Several aspects of Lower Aramis Member larger mammal assemblage abundance data constitute strong indicators of ancient biofacies and biotope (13). The locality-specific subassemblages are remarkably 1 Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA. 2Department of Anthropology, University of Illinois, 607 South Matthews Avenue, Urbana, IL 61801, USA. 3The University Museum, University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. 4 Department of Anthropology, Bryn Mawr College, Bryn Mawr, PA 19010–2889, USA. 5Department of Anthropology, Stanford University, Stanford, CA 94305–2034. 6National Science Foundation, Sedimentary Geology and Paleobiology Program, Arlington, VA 22230, USA. 7College of Medicine, Department of Anatomy, Laboratory of Evolutionary Biology, Howard University, 520 W Street, Washington, DC 20059, USA. 8Paléobiodiversité et Paléoenvironnements, UMR CNRS 5143, USM 0203, Muséum national d’histoire naturelle, 8 rue Buffon, CP 38, 75231 Paris cedex 05, France. 9Institut de paléoprimatologie et paléontologie humaine, évolution et paléoenvironnements, UMR CNRS 6046, Université de Poitiers, 40 avenue du Recteur-Pineau, 86022 Poitiers cedex, France. 10Collège de France, Chaire de Paléontologie humaine, 3 Rue d’Ulm, F-75231 Paris cedex 05, France. 11Department of Anthropology, Lehman College, City University of New York, Bronx, NY 10468, USA. 12Department of Vertebrate Paleontology, American Museum of Natural History, New York, NY 10024, USA. 13Department of Anthropology, University of Oregon, Eugene, OR, 97403– 1218, USA. 14Departamento Paleontología, Universidad Complutense de Madrid y Centro de Evolución y Comportamiento Humanos, ISCIII, C/ Sinesio Delgado 4, Pabellón 14, 28029 Madrid, Spain. 15Ludwig-Maximilians-University of Munich, Department of Geo- and Environmental Sciences, Section of Paleontology, Richard-Wagner-Strasse 10, D-80333 Munich, Germany. 16Department of Physical Anthropology, Cleveland Museum of Natural History, 1 Wade Oval Drive, Cleveland, OH 44106, USA. 17Human Evolution Research Center and Department of Anthropology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA. 18Senckenberg Forschungsinstitut, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany. 19Département de Paléontologie, Université de N’Djamena, BP 1117, N’Djamena, Chad. 20University of Yuzuncu Yil, Department of Anthropology, Faculty of Science and Letters, Zeve Yerlesimi 65080 Van, Turkey. 21Institute of Natural and Environmental Sciences, University of Hyogo, Yayoigaoka, Sanda 669-1546, Japan. 22Science and Mathematics, Bay Path College, 588 Longmeadow Street, Longmeadow, MA 01106, USA. 23Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, 1830 East Monument Street, Room 303, Baltimore, MD 21205, USA. 24Department of Geology and Geophysics, Yale University, New Haven, CT 06520, USA.
*To whom correspondence should be addressed. E-mail:
[email protected] †Deceased
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Ardipithecus ramidus consistent in their taphonomy and taxonomy across the ~7 km distance from the easternmost (SAG-VP-7) to westernmost (KUS-VP-2) Ar. ramidus localities (3). Contemporaneous localities between the two tuffs farther south of the modern Sagantole drainage (SAG-VP-1 and -3, at the southeastern paleotransect pole) are relatively impoverished. They lack this diverse and abundant mammal assemblage and contain no tragelaphines, no monkeys, no fossil wood or seeds, no birds, no micromammals, and no Ardipithecus (table S1). Complementary structural, taphonomic, and isotopic data from localities on this pole of the paleotransect suggest a more open landscape that supported more crocodilians, turtles, and hippopotamids, presumably associated with water-marginal settings more axial in the drainage basin (2, 3).
Research Articles Relative and absolute abundance measures for the large mammals in our collections from the Ardipithecus-bearing Lower Aramis Member localities were assessed by the number of identified specimens (NISP) (n = 1930) and the minimum number of individuals (MNI) based on teeth (n = 330). Proboscideans, giraffids, and hippopotamids are rare (Fig. 1, B and C). The rhinos Ceratotherium efficax and Diceros are represented by few specimens (NISP 6 and 1, MNI 4 and 1, respectively). Unlike most other waterside Plio-Pleistocene assemblages, rhinos are more abundant than hippos at Aramis. The dental mesowear pattern and occlusal morphology of Pliocene Ceratotherium efficax suggest that it was predominantly a grazer but ate less abrasive forage with respect to its highly specialized Pleistocene and extant descendant Ceratotherium simum. The
morphological and functional properties of the recovered Diceros sp. molars are similar to those of the extant browsing Diceros bicornis. Equids are rare. One, Eurygnathohippus sp. nov., is distinguished by its distal limb, which is adapted to open-country running. Its elongatenarrow snout with parabolic symphysis suggests adaptation to selective feeding. The teeth of this equid bear a low-blunt cusp morphology reflecting habitual grazing. Large carnivores and aardvarks are rare, in keeping with their trophic level (as in most other eastern African PlioPleistocene assemblages). Ardipithecus ramidus is represented at Aramis and environs by >110 cataloged specimens representing a minimum number of 36 individuals [14 by upper second molar (M2) count] in the Lower Aramis Member. These numbers are rel-
Fig. 1. Aramis large mammals. (A) Size range illustrated by astragali. The Lower Aramis Member contains a wide range of mammalian taxa, illustrated by this image. Top left, Rhinocerotidae; middle left, Ardipithecus ramidus (ARA-VP-6/500); lower left, small bovid. Included are other artiodactyls, carnivores, and rodents. (B) Relative abundance of larger mammal taxa at Aramis based on dental MNI. (C) Dental NISP based on dental individuals whose tooth crowns are more than half complete. The NISP value reflects all collected specimens identified to the taxon and excludes bulk specimens (tooth crowns less than half complete). Associated dental specimens are counted as one. The MNI values use permanent molars segregated into upper and lower first, second, and third molars, respectively. Numbers for each taxon vary between NISP and MNI, but the relative proportions hold similar. Tragelaphine bovids and cercopithecid monkeys dominate, accounting for more than half of the assemblage, however counted.
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atively low compared with many of the other macrovertebrate fossil species we collected. This rarity is consistent with that observed for hominids in other well-known vertebrate assemblages (7). Kuseracolobus aramisi and Pliopapio alemui are ubiquitous in the assemblage, accounting for 30% of both the larger mammal NISP and MNI. The colobine is numerically dominant within nearly all of the localities, and
overall by a ratio of 1.4 to Pliopapio (colobinae NISP:cercopithecinae NISP). It is slightly larger (12 kg female, 18 kg male) than this papionin (8.5 kg, 12 kg) based on dental regressions (14). Extant colobines exhibit strong preferences for arboreal habitats; extinct African taxa range from fully arboreal to highly terrestrial (15). Bovids and primates, particularly tragelaphines and cercopithecids, dominate the larger mammal
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Fig. 2. Aramis taxonomic abundance. (A) Comparison between the relative abundance (dental) of bovid taxa at Aramis and other Plio-Pleistocene sites (21, 23, 45). The bovid fauna at Aramis is markedly different due to the dominance of tragelaphines. All frequencies are based on NISP, except for Hadar, which is based on MNI. (B) Within-site comparison of the relative abundances of bovids and cerocopithecids. Among Lower Aramis Member localities, SAG-VP-7 has relatively lower abundances of cercopithecids and higher abundances of alcelaphines and reduncines, potentially indicative of ecotonal conditions at this easternmost locality of the Ardipithecus distribution. www.sciencemag.org
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assemblage based on taxonomically diagnostic craniodental elements (Fig. 1). Together, these taxa account for more than half of the larger mammal specimens, whether counted by NISP or dental MNI. Both cercopithecid and bovid assemblages appear to be attritional and were ravaged heavily by carnivores after death (3). Bovids help illuminate the local Aramis environment of the Ardipithecus-bearing localities. One useful index is the relative abundance of grazing versus browsing taxa, which can indicate the presence of open or closed conditions, respectively (16–19). The most ecologically sensitive of these taxa include grazing, open-habitat tribes such as Alcelaphini and Hippotragini versus the primarily browsing Tragelaphini or the riparian-associated Reduncini. Reduncine bovids commonly dominate in African Plio-Pleistocene faunal assemblages (Fig. 2), in keeping with fluviatile, swampy, or lake marginal depositional conditions. Whether counted by NISP or dental MNI, Tragelaphus (whose modern congeners are associated with wooded habitats) (20) is the numerically dominant Aramis bovid, comprising 85% (NISP) of the bovid assemblage (Fig. 1), followed by Aepyceros (whose modern form favors grassy woodland to wooded grassland environments). In contrast, alcelaphine and reduncine bovids that are plentiful at other Plio-Pleistocene sites are rare at Aramis, accounting for a mere 1% (NISP) and 4% (MNI) of all bovids. Aramis is unlike any other known African fossil assemblages in that Tragelaphus dominates the ungulates. (20–23) (Fig. 2). Alcelaphines and reduncines were found at slightly higher frequencies at locality SAG-VP-7 at the eastern end of the Ardipithecus distribution (although tragelaphines and aepycerotines still dominate there). This subtle difference between SAG-VP-7 and other more westerly hominidbearing localities is also indicated by cercopithecid abundance. SAG-VP-7 has relatively fewer cercopithecids and more alcelaphine and reduncine bovids (Fig. 2), potentially signaling that this easternmost Ardipithecus locality was a transition zone between two biotopes. Functional morphology. Taxon-based approaches to the inference of paleohabitats are usually restricted to using identifiable craniodental remains and assume that habitat preference persists through evolutionary time. Another approach is to evaluate the anatomy of fossils with respect to its implications for functional adaptations. These methods presume that mammals exhibit skeletal and dental adaptations for locomotion and feeding that correlate with their preferred environment (24). Samples of extant taxa are used to quantify the relations between skeletal/dental traits and environmental variables, with the results then applied to fossil forms (25). Here, we evaluate the “ecomorphology” of the most common large mammals at Aramis, the bovids and cercopithecid monkeys. For the Aramis bovids, we evaluated the astragali and
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phalanges (25, 26) because other elements that can be revealing (metapodials and femora) were not preserved in sufficient numbers. We used a four-habitat grouping scheme (26) (SOM text S1). Of the 11 available intact bovid astragali with statistically significant habitat predictions (accuracy >95%), 10 are classified as “forest” and one as “heavy cover.” This is a clear signal, since these methods typically produce more varied habitat predictions when applied to fossil samples (27, 28). To lessen possible biases introduced by confining the analysis to specimens sufficiently complete for measurement, we also examined nonmetric traits of the phalanges and classified the entire astragali/phalangeal sample by morphotype (SOM text S1, tables S2 and S3, and fig. S1). These results independently support the conclusion from metric prediction that these animals inhabited a “forest” (in the analytical, not floral, sense). As with bovids, cercopithecid postcranial features are routinely posited to indicate locomotion (29–31). However, systematic studies of large samples of extant taxa are generally lacking. We therefore consider most proposed correlations between cercopithecoid anatomy and locomotor mode to be of unknown reliability, pending additional study. Even so, the elbow is clearly a key joint for distinguishing between arboreal and terrestrial primate locomotion. Of 10 available Aramis cercopithecoid distal humeri, 9 are clearly consistent with “arboreal” substrate, whereas only one is consistent with “terrestrial” substrate based on current criteria. Of 9 proximal ulnae, all are Fig. 3. Mesowear analysis results for the second molar paracone apex of fossil ungulates. Cusp shape was scored qualitatively as sharp, rounded, or blunt. The relative difference in height between tooth cusp apices and intercusp valleys (occlusal relief) was qualitatively scored as either high or low (large or small distance between cusp apex and intercusp valley, respectively). Histograms show the results on the mesowear variables measured (i.e., the percentages of sharp versus rounded versus blunt cusp shapes and the percentages of high versus low occlusal relief).
arboreal. There was no clear evidence of terrestrial adaptation in 18 proximal radii. Hence, based on current criteria, there is clear evidence of arboreal locomotor adaptations, and a paucity of terrestrial indicators, in the overwhelming majority of the Aramis cercopithecoid postcranial sample (SOM text S2). Dental wear. The morphology, occlusal wear, and stable isotope composition of dental remains also reveal the diet—and, indirectly, habitat preferences—of some Aramis mammals. Differences in mesowear can distinguish among extant browsers, grazers, and mixed feeders (32). The Aramis neotragines, Giraffa, and Tragelaphus cluster with extant browsers (Fig. 3 and table S3), whereas Aepyceros falls between extant mixed feeders and nonextreme grazers. Rare Aramis alcelaphines cluster with nonextreme grazers, whereas the rare bovine and equid fossils are closest to extant coarser grass grazers. The high cusps and colobine-like morphology of Pliopapio alemui (tall molars with high relief and little basal flare) suggest that the two Aramis monkey taxa had similar diets. We sampled a mixed set of colobine and cercopithecine molars for a blind test of microwear. No significant differences were found between the two taxa. Microwear on the Aramis monkey molars is consistent with both frugivory and folivory but not hard object feeding. A diet of soft (but perhaps tough) foods would be typical of colobines, and the same may have been the case for the papionin (33). Enamel isotopes. The carbon isotopic composition of a mammal’s tooth enamel reflects the
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relative contributions of grass, trees, and shrubs to its diets. Oxygen isotopes can reveal the degree that a species lives in, or consumes, water from different sources (34). We sampled tooth enamel bioapatite from 177 specimens encompassing a wide range of mammalian taxa within the Ar. ramidus–bearing unit (Fig. 4, SOM text S3, and table S4). These were analyzed blind to taxon. Carbon isotopic ratios for grazers are high, whereas those for mixed feeders, browsers, and forest floor feeders decrease systematically (SOM text S4). Oxygen isotope vales are low for water-dependent species such as carnivores and hippos in wet riparian habitats and higher for water-independent browsers and open dryhabitat species. In the Ardipithecus-bearing Lower Aramis Member assemblage, the aquatic carnivore Enhydriodon (an otter) has the lowest d18O of all species. Conversely, the ursid Agriotherium (a bear) has the highest carnivore d18O, consistent with anatomical evidence for an omnivorous diet (35). Among herbivores, giraffids (Giraffa and Sivatherium) have the highest d18O and lowest d13C values, whereas grazing equids (Eurygnathohippus), alcelaphines, bovines, hippotragines, and rhinocerotids show the converse. Among primates, Kuseracolobus has higher d18O and lower d13C than Pliopapio, which resembles the difference between modern folivorous Colobini and more omnivorous Papionini (36, 37). The carbon isotopic composition of four of five Ardipithecus ramidus individuals is close to
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prey contributed more to their diet compared to their modern congeners in grazer-dominated open savanna environments (37). This is congruent with the numerical dominance of browsing tragelaphines and accords with other evidence for the dominance of woodlands in the 4.4 Ma local environment occupied by Ardipithecus (2, 3). A small number of rare grazing species—mainly equids, alcelaphines, hippotragines, and some impala, rhino, and bovines—have high d13C and d18O, indicating that they fed on waterstressed C4 plants in drier, open environments (41). These taxa comprise a small portion of the overall assemblage. The large range of d18O, particularly the large difference (9.6‰) between water-independent (evaporation-sensitive) Giraffidae (Giraffa and Sivatherium) and water-dependent (evaporationinsensitive) Hippopotamidae, suggests a mean annual evaporative water deficit of ~1500 mm (41). Therefore, Aramis was a generally dry woodland setting far from riparian environments. Enamel isotopes of these taxa from nearby penecontemporary sites at Gona (42) (SOM text S3 and fig. S2) have a d18O difference of only 4.6‰, reflecting an annual water deficit of ~500 mm
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Meteoric/surface Closed/humid, 18Odrinking water depleted leaf water
that of Pliopapio, reflecting diets that included small amounts of 13C-enriched plants and/or animals that fed on such plants. Ardipithecus consumed slightly more of these resources than modern savanna woodland chimpanzees (38) but substantially less than later Plio-Pleistocene hominids (39, 40). The fifth individual has a d13C value of –8.5 per mil (‰), which is closer to, though still lower than, the means for Australopithecus africanus, Au. robustus, and early Homo (39, 40). Slightly lower d18O compared with Pliopapio and Kuseracolobus suggests that Ardipithecus obtained more water from fruits, bulbs, tubers, animals, and/or surface sources. The isotopic composition of the Aramis mammals between the two tuffs (Fig. 4 and table S4) conforms broadly to patterns expected for their modern congeners across the forest-woodlandsavanna spectrum (37, 38) in the East African rift and is consistent with other early Pliocene assemblages (39, 40). Relatively low primate, giraffid, tragelaphine, and Deinotherium d13C values indicate that small patches of closed canopy forests were present, although woodlands to wooded grasslands probably dominated. Low d13C values for hyaenids suggest that browsing
Anancus (g, wi) Deinotherium (b, wd) Elephantidae (g, wd) Hyaenidae (c, wd) Agriotherium (c/o, wd) Enhydriodon (c, wd) Kuseracolobus aramisi (b, wi) Pliopapio alemui (b/o, wd?) Ardipithecus ramidus (b/o, wd?)
Fig. 4. Carbon and oxygen isotopic composition of mammal tooth enamel from the Lower Aramis Member of the Sagantole Formation in the Middle Awash Valley. (A) Individual d13C and d18O values plotted by taxon. (B) Bivariate means T1 SD. See SOM text S3 for methods and interpretations, table S3 for raw data and statistics, and fig. S1 for comparison with species also occurring in roughly contemporaneous deposits at Gona (42). Food and drinking habits are inferred from closest living relatives and from carbon and oxygen isotope ratios. b, browser (C3 feeder); m, mixed grazer/browser (C3 and C4 feeder); g, grazer (mainly C4 grasses); wi, water-independent (evaporation-sensitive) (41) or obtaining substantial amounts of water from green leaves; wd, water-dependent (evaporation-insensitive) (41), relying on drinking water when plant leaves are dry; c, carnivore; o, omnivore, including diets with leaves fruit, tubers, roots, flowers (all predominantly C3), seeds, fungi, and vertebrate and invertebrate animal matter. Diets, water use, and habitat preferences of species of extinct genera and families are indicated in italics because they are more intrinsically uncertain. Interpretations are described and justified in detail in SOM text S3. www.sciencemag.org
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(41). Consistently lower oxygen isotope ratios support geological evidence that Gona was close to permanent water (43), but higher carbon isotope ratios for all Gona browsers are inconsistent with greater water availability (SOM text S3). Other ecological approaches. An approach to deducing ancient environment is to first assign each mammal taxon in a fossil assemblage to an ecological category (usually based on diet and locomotion) and then compare the proportions of these categories in the fossil sample to a range of similarly categorized extant communities (44, 45). This approach uses only the presence or absence of taxa, so it is subject to taxonomic and taphonomic biases involving small samples and mixing. Furthermore, the results are often of low resolution because biased local fossil assemblages are compared to variably recorded modern communities that pool multiple habitats (21). Ardipithecus ramidus was previously interpreted as inhabiting a woodland or dry forest based on a preliminary Aramis faunal list (about 10% of the sample now available) (46). Although the full faunal list produces results consistent with this finding, these results are not highly robust because the data broadly overlap among distinct environments (e.g., open, riparian, medium-density, and closed woodland) (47). Other measures of abundance also provide information on the trophic structure of mammalian community represented by the Ardipithecusbearing Lower Aramis Member. Although there are many grazing and carnivorous species (Fig. 5), these taxa are rare (48), so a strict presence/ absence evaluation distorts the ecological signal. When measures of relative abundance (NISP and MNI) are included, along with direct information on trophic levels from the stable isotope and mesowear results, a different picture emerges. These combined data show that the large mammal biomass at Aramis was dominated by browsers and frugivores (including frugivorous animals that consume leaves as a substantial part of their diet). It is unlikely that a plethora of mammals dependent on browse and fruit would have been able to subsist in an environment without abundant trees, the presence of which is witnessed by fossil pollen as well as abundant seeds, wood, phytoliths, and rhizoliths (2). Hominid habitat. Establishing habitat (as opposed to general environment) is crucial for illuminating the paleobiology of any fossil species, including hominids. On the basis of mixed fossil faunas, it has been previously proposed that “early hominids were apparently not restricted to a narrow range of habitats.” [(8), p. 571]. However, this raises the question of whether the hominids actually occupied a wide range of habitats or whether taphonomic processes and sampling biases have mixed hominid remains with those of species from biotopes that hominids rarely, if ever, frequented. Many fossil assemblages simply do not preserve the necessary temporal and spatial resolution needed to determine whether hominids preferred the riverine forest, lake margin,
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Fig. 5. Trophic ecovariable distributions by faunal list, dental NISP, and dental MNI. Comparisons of the Aramis trophic structure based on the faunal list versus specimen-level, dental relative abundance data as measured by NISP and MNI. Grazing and carnivorous species are abundant in the faunal list– based trophic structure, whereas browsers and frugivores dominate when NISP and MNI data are incorporated. B, browser; G, grazer; MF, mixed feeder; FG, fresh grass grazer; Fg, Frugivore (includes fruit and leaves); C, carnivorous; I, insectivorous; O, omnivorous; RT, root and tuber. bushland, savanna, and/or woodland habitats demonstrably available within a few kilometers of most depositional loci within rift valley settings. For example, Ardipithecus ramidus has also been found at Gona, about 70 km to the north of Aramis, in a valley margin environment where lake deposits interfingered with small fluvial channels or lapped onto basaltic cones and flows (43). At Gona, the dominance of C3 plants indicated by paleosol isotopes contrasts with the C4 plant signal in many associated ungulate grazers (indicated by enamel isotopic data). Levin et al. thus concluded that Ardipithecus “...may have inhabited a variety of landscapes and was not as ecologically restricted as previous studies suggest” [(42), p. 232]. The Gona paleontological and isotopic data show only that a range of habitats was present, and the attribution of Ardipithecus to any particular set of the available biotopes is problematical in this mixed assemblage (49). Fish, birds, browsers, horses, and hominids are all frequently found in a single mixed fossil assemblage in a fluviatile or near-shore deposit. This does not mean that the fish were arboreal or that horses were aquatic. Neither do such data mean that the hominids exploited all potentially available habitats. The Lower Aramis Member deposits provide fossil samples that evidence a range of environments in the region at 4.4 Ma (2, 3). However, the consistent association of Ar. ramidus with a particular fauna and flora in deposits between SAG-VP-7 and KUS-VP-2 suggests its persistent occupation of a woodland with patches of forest across the paleolandscape (2, 3). Ardipithecus
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has not been found in the apparently more open settings to the southeast. There is no evidence of any taphonomic bias related to Ardipithecus that might produce this pattern (3) and no evidence of any other spatial or stratigraphic clustering within the 4.4 Ma Lower Aramis Member interval. Based on a range of independent methods for inferring habitat-based large samples of consilient spatial, geological, and biological evidence generated from diverse sources, we therefore conclude that at Aramis, Ar. ramidus resided and usually died in a wooded biotope that included closed through grassy woodlands and patches of true forest [sensu (6)]. There is no evidence to associate this hominid with more open wooded grasslands or grassland savanna. Isotopic data indicate that the Ar. ramidus diet was predominantly forest- to woodland-based. This interpretation is consistent with evidence of the dental and skeletal biology of this primate (1). The ecological context of 4.4 Ma Aramis hominids, combined with their absence or extreme rarity at Late Miocene and Early Pliocene sites, suggest that the anatomy and behavior of the earliest hominids did not evolve in response to open savanna or mosaic settings. Rather, this clade appears to have originated within more closed habitats favored by these peculiar primates until the origin of Australopithecus, and perhaps even beyond (50). References and Notes
1. T. D. White et al., Science 326, 64 (2009). 2. G. WoldeGabriel et al., Science 326, 65 (2009). 3. A. Louchart et al., Science 326, 66 (2009).
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4. This assemblage is the one co-occurring with Ardipithecus and excludes the small contemporary samples of fossils from the more easterly localities of SAG-VP-1 and -3; see (2, 3) and table S1 for details. 5. Included in the larger mammal subassemblage analyzed here are the following taxa: Artiodactyla, Perissodactyla, Proboscidea, Primates, Carnivora (except Viverridae), and Tubulidentata. 6. F. White, The Vegetation of Africa, Natural Resources Research, Vol. 20. (United Nations Scientific and Cultural Organization, Paris, 1983). 7. T. White, in Evolutionary History of the Robust Australopithecines, F. Grine, Ed. (Aldine de Gruyter, New York, 1988), pp. 449–483. 8. M. G. Leakey, C. S. Feibel, I. McDougall, A. Walker, Nature 376, 565 (1995). 9. G. WoldeGabriel et al., Nature 371, 330 (1994). 10. N. E. Sikes, B. A. Wood, Evol. Anthropol. 4, 155 (1995). 11. B. R. Benefit, in African Biogeography, Climate Change, and Human Evolution, T. Bromage, F. Schrenk, Eds. (Oxford Univ. Press, New York, 1999), pp. 172–188. 12. M. G. Leakey, in African Biogeography, Climate Change, and Human Evolution, T. Bromage, F. Schrenk, Eds. (Oxford Univ. Press, New York, 1999), pp. 271–275. 13. Taphonomic and curatorial biases inevitably compromise quantitative interpretations of any assemblage, including Aramis. For example, a single hominid canine may break into only a few identifiable fragments, whereas one elephantid’s tusk or molar can shatter into thousands of identifiable fragments. Simple comparisons of fragment abundance can therefore be misleading. Our abundance data take these potential problems into account (see Fig. 1 for details). 14. S. R. Frost, Am. Mus. Novit. 3350, 1 (2001). 15. J. F. Oates, A. G. Davies, E. Delson, in Colobine Monkeys: Their Ecology, Behaviour, and Evolution, A. G. Davies, J. F. Oates, Eds. (Cambridge Univ. Press, Cambridge, 1994) pp. 45–74. 16. P. Shipman, J. Harris, in Evolutionary History of the Robust Australopithecines, F. Grine, Ed. (Aldine de Gruyter, New York, 1988), pp. 343–381. 17. E. S. Vrba, in Fossils in the Making, A. Behrensmeyer, A. P. Hill, Eds. (Univ. of Chicago Press, Chicago, 1980), pp. 247–271. 18. R. Bobe, G. G. Eck, Paleobiology 27, 1 (2001). 19. G. Suwa et al., J. Vert. Paleontol. 23, 901 (2003). 20. The Aramis Tragelaphus cf. moroitu has a body size close to that of the living nyala (T. angasii) and is likely a direct descendent of the T. moroitu recorded from the Mio-Pliocene of Asa Koma and Kuseralee. 21. D. Su, thesis, New York University (2005). 22. R. Bobe, J. Arid Environ. 66, 564 (2006). 23. K. E. Reed, J. Hum. Evol. 54, 743 (2008). 24. H. A. Hespenheide, Annu. Rev. Ecol. Syst. 4, 213 (1973). 25. D. DeGusta, E. S. Vrba, J. Archaeol. Sci. 30, 1009 (2003). 26. D. DeGusta, E. S. Vrba, J. Archaeol. Sci. 32, 1099 (2005). 27. Y. Haile-Selassie et al., Geobios 37, 536 (2004). 28. L. J. Hlusko, Y. Haile-Selassie, D. DeGusta, Kirtlandia 56, 163 (2007). 29. J. G. Fleagle, Yearb. Phys. Anthropol. 20, 440 (1976). 30. H. B. Krentz, in Theropithecus, N. Jablonski, Ed. (Cambridge Univ. Press, Cambridge, 1993), pp. 383–422. 31. S. Elton, Folia Primatol. (Basel) 73, 252 (2002). 32. M. Fortelius, N. Solounias, Am. Mus. Novit. 3301, 1 (2000). 33. Crushing and shearing areas of 10 cercopithecoid molars yielded surfaces that could be included in this analysis. Surface images were made using an SEM at ×500 magnification, and microwear features were collected using the “Microwear” software (v. 2.2, 1996). Microwear features included relatively few pits, with narrow pits and scratches. The microwear on the molars of the Aramis monkeys is consistent with both frugivory and folivory, but they were not routinely feeding on hard objects. A diet of soft, but perhaps tough, foods would be typical of colobines, and the same might be true for the papionin, which has tall molars with a large amount of
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43.
relief and has a low level of basal flare in comparison with other papionins. T. E. Cerling, J. M. Harris, Oecologia 120, 347 (1999). B. Sorkin, Hist. Biol. 18, 1 (2006). M. L. Carter, thesis, University of Chicago (2001). S. H. Ambrose, M. J. DeNiro, Oecologia 69, 395 (1986). M. Sponheimer et al., J. Hum. Evol. 51, 128 (2006). M. Sponheimer, J. A. Lee-Thorp, in Handbook of Paleoanthropology, W. Henke, I. Tattersall, Eds. (Springer, Berlin, 2007) pp. 555–585. N. J. Van Der Merwe, F. T. Masao, M. K. Bamford, S. Afr. J. Sci. 104, 153 (2008). N. E. Levin, T. E. Cerling, B. H. Passey, J. M. Harris, J. R. Ehleringer, Proc. Natl. Acad. Sci. U.S.A. 103, 11201 (2006). N. E. Levin, S. W. Simpson, J. Quade, T. E. Cerling, S. R. Frost, in The Geology of Early Humans in the Horn of Africa, J. Quade, J. Wynn, Eds. (Geological Society of America Special Papers, 2008), vol. 446, pp. 215–234. J. Quade et al., in The Geology of Early Humans in the Horn of Africa, J. Quade, J. Wynn, Eds. (Geological Society of America Special Papers, 2008), vol. 446, pp. 1–31.
RESEARCH ARTICLES 44. P. J. Andrews, J. M. Lord, E. M. Nesbit Evans, Biol. J. Linn. Soc. Lond. 11, 177 (1979). 45. K. Kovarovic, P. Andrews, L. Aiello, J. Hum. Evol. 43, 395 (2002). 46. P. Andrews, L. Humphrey, in African Biogeography, Climate Change, and Human Evolution, T. Bromage, F. Schrenk, Eds. (Oxford Univ. Press, New York, 1999), pp. 282–300. 47. Our analysis also raised numerous questions about the assumptions and procedures underlying such efforts. 48. For example, there are 12 “grazing” taxa compared to only 5 “browsing” taxa, but the former are represented by only 152 specimens, whereas the latter are represented by 758 (NISP). 49. It is evident that in most rift-valley depositional settings, a variety of environments would almost always have been available to hominids. Of primary interest is determining whether any one of these environments was the preferred habitat of these primates. Mixed assemblages cannot usually do this. 50. T. D. White et al., Nature 440, 883 (2006). 51. Supported by NSF (grants SBR-82-10897, 93-18698, 9512534, 96-32389, 99-10344, and 03-21893 HOMINID-
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RHOI; and grant SBR 98-71480 for mass spectrometry instrumentation at the Environmental Isotope Paleobiogeochemistry Laboratory) and the Japan Society for the Promotion of Science (G.S. and H.S.). We thank L. Bach, H. Gilbert, and K. Brudvik for illustrations; the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; and the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the data.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/67/DC1 SOM Text Figs. S1 and S2 Tables S1 to S5 References 4 May 2009; accepted 14 August 2009 10.1126/science.1175822
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The Ardipithecus ramidus Skull and Its Implications for Hominid Origins Gen Suwa,1* Berhane Asfaw,2 Reiko T. Kono,3 Daisuke Kubo,4 C. Owen Lovejoy,5 Tim D. White6 The highly fragmented and distorted skull of the adult skeleton ARA-VP-6/500 includes most of the dentition and preserves substantial parts of the face, vault, and base. Anatomical comparisons and micro–computed tomography–based analysis of this and other remains reveal pre-Australopithecus hominid craniofacial morphology and structure. The Ardipithecus ramidus skull exhibits a small endocranial capacity (300 to 350 cubic centimeters), small cranial size relative to body size, considerable midfacial projection, and a lack of modern African ape–like extreme lower facial prognathism. Its short posterior cranial base differs from that of both Pan troglodytes and P. paniscus. Ar. ramidus lacks the broad, anteriorly situated zygomaxillary facial skeleton developed in later Australopithecus. This combination of features is apparently shared by Sahelanthropus, showing that the Mio-Pliocene hominid cranium differed substantially from those of both extant apes and Australopithecus.
T
he first fossil of Australopithecus, a partial child’s skull found in 1924 at Taung, South Africa, was reported by R. A. Dart to combine an ape-like cranial capacity with distinctive hominid features such as weak facial prognathism, small anterior deciduous teeth, and an anteriorly situated foramen magnum (1). Since then, diverse Plio-Pleistocene cranial fossils have been recovered, primarily in southern and eastern Africa, establishing a widely recognized Australopithecus grade of evolution (2–6). Australopithecus crania exhibit small, chimpanzee-to-gorilla–sized cranial capacities, distinct cranial base flexion, and varying degrees of postcanine megadonty with associated craniofacial/vault morphologies (2–5, 7–10). The derivation of the genus Homo from Pliocene Australopithecus is probable (11), whereas the pre-Pliocene ancestry of Australopithecus has been elusive. Until now, the only substantial specimen to shed any light on pre-Australopithecus hominid cranial evolution was that of Sahelanthropus tchadensis from Chad (12). Discovered in 2001, this Late Miocene cranium [specimen TM 26601-060-1; estimated at 6.0 to 7.0 million years ago (Ma)] combines a cranial capacity smaller than Australopithecus with a long and low neurocranium, an anteriorly extended upper face
surmounted by a massive supraorbital torus with no post-toral sulcus, and a lower face less prognathic than those of either chimpanzees or gorillas (12–14). The posterior vault and cranial base are described as resembling post–3.5 Ma Pliocene Australopithecus (12–14). However, the hominid status of S. tchadensis has been challenged; some opined that it exhibits a surprisingly evolved face (15), whereas others have
suggested it to be a gorilla ancestor or some other ape (16, 17). We report here the skull of Ardipithecus ramidus recovered from Aramis, Ethiopia, as a part of the ARA-VP-6/500 skeleton (18). Together with other key Aramis specimens, including the ARA-VP-1/500 temporal/occipital portion (19), these fossils constitute the first substantial cranial remains of a pre-Australopithecus hominid directly associated with extensive postcranial remains (18). The Ar. ramidus postcranium indicates both substantial arboreal capability and an intermediate form of terrestrial bipedality that preceded the more fully established Australopithecus condition (20–23). The revelation of a primitive pre-Austalopithecus locomotor grade raises substantial interest in establishing the major features of the Ardipithecus cranium. Did Ar. ramidus share any of the derived hominid features seen in Australopithecus, or did it exhibit a skull more like those of extant African apes? What are its implications with respect to the controversies surrounding the hominid status of Sahelanthropus? We seek answers to these questions by comparing the Aramis fossils to Australopithecus, Sahelanthropus, and extant African apes, and we offer new hypotheses about cranial evolution in the hominid and African ape clades. The ARA-VP-6/500 skull. The ARA-VP-6/ 500 skull comprises most of the vault, parts of the base, much of the right face, the left Fig. 1. The fragmented skull of ARA-VP-6/500. (Upper panel) Identifiable pieces of the skull after limited refitting for digital and physical molding. (Lower panel) (A) ARA-VP-6/500-032, (B) micro-CT rendered image of the same, with cross-sectional locations of (C) and (D) indicated. Arrowheads in (A) denote the positions of (C) and (D).
1 The University Museum, the University of Tokyo, Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan. 2Rift Valley Research Service, Post Office Box 5717, Addis Ababa, Ethiopia. 3 Department of Anthropology, National Museum of Nature and Science, Hyakunincho, Shinjuku-ku, Tokyo, 169-0073, Japan. 4Department of Biological Sciences, Graduate School of Science, the University of Tokyo, Tokyo, 113-0033, Japan. 5 Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44240–0001, USA. 6 Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA.
*To whom correspondence should be addressed. E-mail:
[email protected]
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Ardipithecus ramidus mandibular corpus, and most of the teeth (Fig. 1 and fig. S1). These elements were scattered widely across the excavation area (18). Many were partially disintegrated by the silty clay sediment, and major structures were fragmentary and variably distorted. Each was stabilized in the field, transported within its encasing sediment via plaster jacket, and later extracted from matrix under a binocular microscope. The extracted pieces preserve contiguous bone from lambdoidal suture to face, but distortion prevented correct alignments (24). The largest intact element is most of the relatively well-preserved left parietal portion. It was collapsed into the vault space such that cranial height was reduced to ~35 mm (Fig. 1). There has been excessive fragmentation and/or damage to the temporal and occipital portions. Individual pieces are so friable and soft that edge cleaning would have risked serious damage and loss of conjoint surface morphology. Therefore, major pieces were molded and otherwise left largely as recovered. Restoration was undertaken independently using casts (Berkeley, CA) and digital data (Tokyo, Japan). In December 2003, we used high-resolution micro–computed tomography (CT) to scan the original fossils. We then segmented the representations of the better-preserved parts into 64 separate polygon shells. Using these digital models, we corrected the positions and alignments of each individual piece (24) (Fig. 2). We then added the digital model of the better-preserved ARA-VP-1/500 temporal/occipital fossil (19) (scaled to 92% size) to complete the ARA-VP-6/ 500–based reconstruction of the Ar. ramidus cranium (25). The descriptions and comparisons that follow initially outline key features observed directly on the individually preserved fossils and then extend these to an analysis of the digital reconstruction. Basion position and basicranial length. In our initial evaluation of Ar. ramidus (19), we noted the anterior position of the foramen magnum relative to lateral basicranial structures and interpreted this as a derived condition shared with later hominids. However, the utility of our observations has been questioned (26, 27). Here, we re-evaluate basion position and its importance in Ar. ramidus, using the newly available micro-CT data. These data allow high-resolution, three-dimensional wholesurface topographic assessment (Fig. 3). To minimize influences of orientation, we evaluated basion position in the basioccipital plane (Fig. 3) and confined our analysis to landmarks located inferiorly on the cranial base (i.e., excluding porion) (28). In ARA-VP-1/500, our digital methods yield a basion position 1.3 mm posterior to the center of the carotid foramen. Previous workers have cautioned that because bonobos tend to have an anteriorly positioned foramen magnum (29), anterior placement of the basion might be primitive and therefore not a derived hominid feature (27). Thus, we com-
RESEARCH ARTICLES pared basion position of Ar. ramidus with that of both Pan troglodytes and P. paniscus (24), as well as with Plio-Pleistocene Australopithecus. We found that although P. paniscus (mean 6.4 mm, n = 28 specimens) does have a slightly shorter basion-to-bicarotid distance than P. troglodytes (mean 7.3 mm, n = 20), this difference was not statistically significant. Furthermore, both species exhibit almost identical relative values when scaled by size (bicarotid breadth) (Fig. 3). Basion position of Australopithecus overlaps minimally with the two Pan species (Fig. 3 and
Fig. 2. Digital representations of the Ar. ramidus cranium and mandible. (A to D) The ARA-VP-6/500 and downscaled ARA-VP-1/500 composite reconstruction in inferior, superior, lateral, and anterior views (in Frankfurt horizontal orientation). (E) Individual pieces of the digital reconstruction in different colors. Note the steep clivus plane intersecting the cranial vault on the frontal squama (as in Sts 5 and not apes). (F and G) Lateral and superior views of the ARA-VP-1/401 mandible (cast). (H and I) Lateral and superior views of the ARA-VP-6/500 left mandibular corpus with dentition.
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fig. S2). In Plio-Pleistocene hominids, the basion is situated from ~0 to 5 mm posterior to the carotid foramen (30). This distance is generally <10% of bicarotid breadth, whereas the same index is >10% in both species of Pan. ARA-VP1/500 lies at the extreme lower end of the hominid range and is clearly distinct from Pan (31). Sahelanthropus also shares the hominid condition. On the basis of published information and our own observations of the original fossil with allowance for the effects of taphonomic damage, the basion was probably positioned
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Ardipithecus ramidus slightly posterior to the bicarotid chord, as in the hominids examined here. We also evaluated distance from the basion to the bi-foramen ovale (basi-ovale) chord as an alternative measure of posterior basicranial length (32) (figs. S3 and S4). Regression analysis in Pan shows a proportional relation between basi-ovale distance and basioccipital length. This relation also holds for Australopithecus. Therefore, basi-ovale distance can be used as a proxy for basioccipital length. Although ARA-VP-1/500 does not preserve the foramen ovale itself, the internal lateral wall of the foramen spinosum is preserved (Fig. 3), which permits a reasonable estimate of basi-ovale distance (24). Ar. ramidus falls squarely within the hominid range (fig. S4). Although bonobos exhibit an absolutely shorter basi-ovale distance than do common chimpanzees throughout growth, this length relative to bicarotid breadth differs comparatively little between the corresponding age groups of the two species or among their growth periods (fig. S4). Thus, the wide and short posterior cranial base of Ar. ramidus and Plio-Pleistocene hominids is not part of a continuum seen in modern ape morphology, but rather appears to reflect reorganization of the cranial base, most likely manifested early in ontogeny. Analysis of juvenile Australopithecus crania will allow a test of this prediction. Though differences in posterior cranial base lengths and proportions are seen in the two Pan
Research Articles species, they show an even greater difference in their anterior cranial base lengths. Exocranially, this is reflected, for example, in metrics such as the distance from the foramen ovale to pterygopalatine fossa (fig. S5) and endocranially in the length of the planum sphenoideum (33). The morphological effects of these differences are a particularly elongate nasopharyngeal region with anterior placement of the palate and the entire dental arcade in P. troglodytes (fig. S6). Hence, the cranial base and facial hafting pattern of P. troglodytes appears highly derived relative to both P. paniscus and Ar. ramidus. The Ar. ramidus face and vault: basic morphology. The ARA-VP-6/500-115 maxilla exhibits a superoinferiorly short face and weak prognathism compared with the common chimpanzee. Its overall structure resembles that of Sahelanthropus, although it is smaller in size and proportionately shorter superoinferiorly. The preserved incisor alveoli and the size of its isolated roots/partial crowns indicates weak subnasal prognathism compared with both the common chimpanzee and the smaller-faced bonobo. This reflects the lack of incisor hypertrophy in Ar. ramidus (34). Facial topography from the infraorbital plane to the nasal aperture suggests that it had a short but projecting muzzle, considerably more primitive than the flatter-faced Plio-Pleistocene Australopithecus or the gracilized face of small Homo specimens such as KNM-ER 1813. The zygomatic root of the
Fig. 3. Basion position in ARA-VP-1/500. (A) Basal view (basioccipital plane horizontal). The two pieces were positioned by applying criteria of symmetry to the well-preserved basioccipital surface and by mirror imaging and determining overall best fit of the right and left sides (24). Metric landmarks (shown by red squares) are the basion, carotid foramen, and lateral margin of foramen spinosum (hidden). Two lines are drawn, depicting the sagittal plane (vertical line) and the bicarotid foramen chord (horizontal line). (B) Box plot of the basion-tobicarotid chord distance scaled by bicarotid breadth (24). The Australopithecus specimens measured were as follows: Sts 5, Sts 19, MLD 37/38 (casts of Au. africanus); KNM-WT 17000 (Au. aethiopicus); and O.H. 5 (cast), KNM-ER 406, KNM-ER 407 (Au. boisei) (see fig. S2 for individual values). (C) Anterior view showing segmented internal ear. The validity of the bilateral placements was evaluated by examining semicircular canal asymmetry, which was confirmed to be slight and within ranges observed in humans (57, 58). Radii of the semicircular canals were measured as in (59) and were found comparable to the modern ape and Australopithecus conditions (60).
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maxilla (anterior face) is placed above the upper first molar (M1), more posterior than is typical of Pliocene Australopithecus, but more anterior than is seen modally in bonobos and common chimpanzees. This reflects a less prognathic face compared with Pan and probably represents the primitive condition for both hominids and African apes. A similar zygomatic root location is found in many Miocene apes (e.g., Kenyapithecus, Nacholapithecus, Sivapithecus, Dryopithecus, Pierolapithecus, and Ouranopithecus). The ARA-VP-6/500-115 maxilla exhibits a small but distinct upper second incisor/canine diastema (reportedly absent in Sahelanthropus and variable in Au. afarensis). Dental-arcade shape is observable in the ARA-VP-6/500 restoration and the ARA-VP-1/401 mandible (from an older presumed female) (Fig. 2). The mandible exhibits some primitive features, as well as some derived features shared with early Australopithecus. Although the canine-to-postcanine tooth row is straight in ARA-VP-6/500 [as it is in Au. anamensis (KNM-KP 29281) (35, 36) and some Au. afarensis (10)], the better-preserved ARA-VP-1/401 mandible exhibits an anteromedial position of the lower canine relative to lower third premolar, as in most Au. afarensis. However, the worn lower canine of ARA-VP-1/401 projects above both the postcanine occlusal and incisal planes, indicating that it was not incorporated into the functional incisive row, thus differing from Australopithecus (37).
(D) Close-up of basioccipital showing a horizontal plane passing through the midbasioccpital point (24). Note the approximate symmetry of the basioccipital surface [1.5 times the scale of (A), (C), and (E)]. (E) Oblique basal view showing the three landmarks (the basion, carotid foramen, and lateral margin of foramen spinosum). The latter was used in alternative measures of cranial base length (24) (see text and figs. S3 and S4 for further details and discussion). Scale bar, 20 mm; common to (A), (C), and (E). VOL 326
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Fig. 4. Major structural features (24) of the Ar. ramidus cranium (ARA-VP-6/500–based reconstruction). (A) Upper facial projection: ratio of porion-to-nasion radius by porionto-prosthion radius. S. tchadensis (14); Australopithecus includes Sts 5 (this study), Sts 71 (9), and O.H. 5 (14); KNMER 1813 from CT scan of cast (this study). The Ar. ramidus value is 0.73. (B) Midfacial projection: ratio of porion-tonasal aperture radius by average of porion-to-orbitale and porion-to-zygomatic root radii. Australopithecus is Sts 5 (this study); KNM-ER 1813 from CT scan of cast (this study). The Ar. ramidus value is 1.23. (C) Facial mask index: maximum zygomatic breadth at orbital plane divided by biorbital breadth across ectoconchion. S. tchadensis (14); Australopithecus includes A.L. 444-2, Sts 5, Sts 71, SK 48, TM 1517, O.H. 5, KNM-ER 406, KNM-ER 732, KNM-ER 13750, and KNM-WT 17000 (10). The Ar. ramidus value is 1.20. (D) Overlap index: ratio of projected glenoid tubercle-toprosthion length to projected zygomaxillare-to-distal M3 distance. Australopithecus includes A.L. 444-2, Sts 5, Sts 71, SK 48, SK 52, TM 1517, O.H. 5, KNM-ER 406, KNM-ER 732, and KNM-WT 17000 (10). The Ar. ramidus value is 0.26. (E) Subnasal alveolar prognathism: ratio of porion-to-prosthion radius by porion-to-nasal aperture radius. Australopithecus is Sts 5 (this study); KNM-ER 1813 from CT scan of cast (this study). The Ar. ramidus value is 1.23. (F) Relative upper facial breadth: bi-frontomalare temporale breadth divided by cube root of cranial capacity. S. tchadensis (13); Australopithecus is divided into nonrobusts (A.L. 444-2, Sts 5, Sts 71, and Stw 505) and robusts (O.H.5, KNM-ER 13750, and KNM-ER 23000); data for these and KNM-ER 1813 compiled from (9, 10, 47, 61). The Ar. ramidus value is 15.4. (G) Relative palatal length: projected palate (or dental row) length divided by cube root of cranial capacity. Australopithecus is divided into nonrobusts (A.L. 444-2, Sts 5, and Sts 71) and robusts (O.H. 5 and KNM-WT 17000); data for these and KNM-ER 1813 compiled from (10). The Ar. ramidus value is 9.1. (H) Relative bi-glenoid breadth: biexternal glenoid tubercle breadth divided by cube root of cranial capacity. S. tchadensis [estimated from (13)]; Australopithecus divided into nonrobusts (A.L. 444-2, Sts 5, and MLD 37/38) and robusts (O.H. 5, KNM-ER 13750, KNMER 23000, and KNM-WT 17000); data for these and KNM-ER 1813 compiled from (10). The Ar. ramidus value is 15.8. See SOM materials and methods (24) for further details.
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Ardipithecus ramidus In mandibular corpus morphology, ARA-VP1/401 exhibits a posteriorly receding symphysis and lateral corpus proportions resembling Au. anamensis rather than Pan. However, compared with Au. anamensis, both ARA-VP-1/401 and ARA-VP-6/500 exhibit a less inflated mandibular corpus, accompanied by extensive lateral hollowing and high posterior placement of the ramus root. The Ar. ramidus mandible is similar to those of Sahelanthropus and Ar. kadabba in corpus dimensions (12, 38, 39), ramus root position and development, and circum mid-corpus height placement of the anterosuperiorly exiting mental foramen. The Ar. ramidus supraorbital torus is represented by a small but informative segment of the ARA-VP-6/500 frontal bone. The torus is vertically 6 mm thick at about mid-orbital position, a location commonly thinnest in African apes. It is equivalent to the thinnest end of the P. troglodytes range (40). Although there is considerable individual variation and overlap of ranges in torus thickness between the sexes of modern apes (12, 17), the thin supraorbital torus of ARA-VP6/500 suggests that this individual was female, supporting our sex assignment on the basis of canine size (34). Concavity behind the torus is slight, indicating the absence of Gorilla- or Pan-like post-toral sulci. The lateral wall of the frontal sinus is exposed on the medial break of
Research Articles the preserved supratoral region. Thus, the presence of a sizeable frontal sinus is shared with both Pan and Gorilla. The frontozygomatic region lateral to the orbit of the Ar. ramidus cranium is wide and rugose, comparable to robust individuals of P. troglodytes, and distinctively more robust than in the bonobo. The temporal line turns posteriorly at about mid-orbital position, comparable to Sahelanthropus, and well within the wide P. troglodytes range of variation. The superior temporal line then runs largely anteroposteriorly for the length of the parietal portion (right and left lines separated by ~25 mm) and crosses the lambdoidal suture. The crushed occipital region does not allow for comprehensive evaluation of compound temporal/nuchal crest configuration, but a small compound crest is preserved laterally on the left side. Such a crest is variably expressed in both male and female P. troglodytes but is typically absent in bonobos (both sexes). A similar crest is commonly seen in Au. afarensis (10). In summary, the facial bones of ARA-VP-6/ 500 suggest that prognathism is weaker than in Pan, but that the masticatory complex is more developed than in bonobos, consistent with the larger Ar. ramidus postcanine dentition (34). The ARA-VP-6/500 face is markedly short superoinferiorly, but modern ape data (10, 41, 42)
Fig. 5. Natural log-log plot of total cranial length against cranial capacity (24). Least-squares regression lines for the catarrhine subsets are fitted. African apes are Gorilla gorilla, P. troglodytes troglodytes, P. t. schweinfurth, and P. paniscus. Although P. t. schweinfurthi has a smaller body size, it has a larger ECC and cranial length than P. t. troglodytes. Bonobos have small skull size relative to ECC. Ar. ramidus (large red filled star) is plotted using the ARA-VP-6/500 body weight of ~50 kg (23) and a rough total cranial length estimate of 162.5 mm (fig. S7 and table S1). The boxed range of Ar. ramidus is depicted with a wide ECC range of 280 to 350 cm3. Possible skull length dispersion is depicted for a hypothetical situation in which ARA-VP-6/500 represents a small-skulled individual (within-sex correlation between body size and skull size is expected to be weak); most individuals may have had a larger skull size. The upper Ar. ramidus plots represent two SD positions using chimpanzee levels of variation as a model. The plotted Ar. ramidus range corresponds to approximately half of the species range of P. troglodytes, so its actual range of variation was greater. S. tchadensis (TM 266-01-60-1, large red unfilled star) is plotted from data in (13). See figs. S8 and S9 for further details.
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show that such facial features are highly variable within sexes and species. Hence, we do not consider its short face to be a species character of Ar. ramidus. The Ar. ramidus cranium: overall structure and comparisons. Digital restoration of the ARAVP-6/500 cranium enables further observation and quantitative evaluation of its craniofacial architecture (24) (Figs. 2 and 4, fig. S7, and table S1). The Ar. ramidus cranium shares enhanced relative upper facial projection (Fig. 4A) with Sahelanthropus (14) and later Pliocene hominids. However, the ape-like projecting midfacial muzzle of the Sahelanthropus/Ardipithecus face clearly differs from that of Australopithecus and early Homo, as shown metrically in Fig. 4B. The Ardipithecus cranium also lacks the suite of derived masticatory features characteristic of later Australopithecus (2–5, 7–11, 43–47). We compared two such parameters, one of them explicitly examined in Sahelanthropus (14). Relative to biorbital breadth, maximum midfacial-zygomatic breadth at the orbital plane is considerably enhanced in Australopithecus (facial mask index, Fig. 4C) (10). Another measure, the overlap index (Fig. 4D), reflects the extent of anteroposterior overlap between the anterior-most limit of the origin of masseter and the postcanine tooth row (10, 43). In this measure, Ar. ramidus overlaps with Gorilla and the least derived end of the Australopithecus range. Comparisons of Ar. ramidus and Australopithecus with the two extant Pan species reveal distinct cranial structures characteristic of each species. A pronounced feature of P. troglodytes is its elongate nasopharyngeal region and long anterior cranial base (see earlier in text). Associated morphological correlates include an anteroposteriorly elongate temporal fossa and infratemporal crest, as well as an anteriorly extended glenoid and preglenoid plane (48). The entire lower face/dentition is anteriorly displaced, an inference supported by morphological details such as the configuration of the posterior alveolar process. The P. troglodytes post-M3 maxillary tuberosity tends to be anteroposteriorly long, thereby adding to evidence for anterior displacement of the entire dental arcade relative to the pterygoid plates. The combined effect is an extremely prognathic lower face (Fig. 4E and fig. S6). We hypothesize that these craniofacial structures are highly derived but are not dietary adaptations; instead they are related to canine enlargement (34), perhaps in association with enhanced gape and/or increased aggression in P. troglodytes. Although most of these details cannot yet be directly observed in the Ar. ramidus cranium, it appears that such specializations were lacking. This is inferred from features such as the anteroposteriorly short glenoid and the ARA-VP6/500–based reconstruction with an anteroposteriorly short temporal fossa as in P. paniscus and G. gorilla. The bonobo shares a long premaxilla and large incisors with the common chimpanzee, but
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Ardipithecus ramidus lacks the extreme features of the latter. Instead, the bonobo cranium appears uniquely derived in its particularly small face and jaws (Fig. 4, F to H) (compared with both P. troglodytes and Ar. ramidus). This structural pattern is consilient with the hypothesized size reduction of the entire bonobo dentition (34). The gorilla cranium is almost certainly derived in exhibiting an extreme anteriorly and inferiorly developed lower face [analytical results of (13, 14)]. These and other facial and jaw features of the gorilla, some paralleling the Australopithecus condition (Fig. 4, C, G, and H), are best interpreted as the combined effects of allometry (large absolute size) and functional adaptations to herbivory. Cranial capacity, scaling, and cranial base flexion. Because the endocranial surface of the frontal pole region is preserved in ARA-VP6/500, we were able to estimate cranial capacity from internal calvarial dimensions (length, breadth, and height). Multiple regressions based on modern African apes (total n = 18, sexbalanced samples of P. troglodytes, P. pansicus and G. gorilla) yield an estimate of 300 T 10 cm3, with a larger range of 280 to 350 cm3 if we account for uncertainty that stems from combining ARA-VP-6/500 and the scaled ARA-VP-1/500 temporal/occipital portion (24). This small cranial capacity is comparable with that of female Pan (fig. S8). Extending the Ar. ramidus reconstruction to include a rough approximation of total cranial length (fig. S7 and table S1) allows for a comparison of cranial size (maximum cranial length) with body size (fig. S9). Because subfamily level trends have been reported among catarrhines in relative endocranial volume (49), we also examined total skull length in relation to endocranial capacity (ECC). In addition to some colobines (in particular, Presbytis sensu stricto), atelines, hylobatids, and Pan, Ar. ramidus has the smallest relative cranial length among large-bodied anthropoids [as judged from regressions of cranial length on endocranial volume (Fig. 5)]. Because maximum cranial length controlled for endocranial volume must largely reflect facial and nuchal size, the results suggest a particularly gracile head in the ARA-VP-6/500 individual (50). At the same time, our scaling analysis shows that postcranially dimorphic species tend to exhibit a large cranial size relative to that of the endocranium, as well as a large degree of cranial size dimorphism. In this context, it is instructive that Ar. ramidus shares its relatively small cranial size with taxa that are weakly dimorphic both cranially and postcranially. Despite its small cranial capacity, there is tantalizing evidence for advanced cranial base flexion in Ar. ramidus. This is seen from the steep orientation of its clivus, which directly reflects midsagittal flexion (figs. S10 and S11). However, because bonobos and Australopithecus overlap in measures of cranial base flexion (33, 41, 51), it is uncertain whether Ar. ramidus represents a primitive condition shared with bonobos or a
RESEARCH ARTICLES more Australopithecus-like flexion involving the planum sphenoideum and/or greater orbital kyphosis (52). The Sahelanthropus and Ardipithecus crania securely associate a relatively short basicranium with small cranial capacity. The hominid basicranial pattern and associated morphologies [such as foramen magnum orientation (24)] are widely held to be related to bipedality and upright posture (12, 13), despite a lack of empirical evidence to clearly support a functionally based correlation (52, 53). The Ar. ramidus cranium raises the alternative possibility that early hominid cranial base flexion was associated with neural reorganization that was already present in Sahelanthropus/Ardipithecus, as suggested for Pliocene Australopithecus (1, 54, 55). Such a hypothetical supposition is in part testable by both future fossil finds and by anticipated advances in our understanding of genomic expression patterns pertaining to brain function, structure, and morphogenesis. Conclusions. Micro-CT–based evaluations of the Ar. ramidus cranial base confirm a derived basicranium of Ar. ramidus shared by both Sahelanthropus and Australopithecus. Our comparative analyses of P. troglodytes and P. paniscus suggest that this probably reflects basicranial organization unique to the hominid clade. The digitally reconstructed Ar. ramidus skull further allows a variety of inferences about African ape and hominid evolution. Cranial capacity of preAustralopithecus hominids (as represented by Ar. ramidus and S. tchadensis) was probably slightly smaller than that of Australopithecus and also more comparable to Pan. The Ar. ramidus skull (and that of S. tchadensis) lacked the masticatory specializations of later Australopithecus, consistent with the dental evidence for an omnivore/frugivore niche lacking emphasis on hard and/or abrasive diets. Finally, comparisons of Ar. ramidus and extant African apes suggest that each is unique in aspects of its cranial anatomy. In particular, the common chimpanzee appears derived in its forwardly placed lower facial skeleton, possibly associated with increased aggression, whereas the bonobo is characterized by a secondary reduction of facial size. Ar. ramidus and Sahelanthropus lack these specialized morphologies of Pan and constitute the probable ancestral morphotype of Pliocene Australopithecus. References and Notes
1. R. A. Dart, Nature 115, 195 (1925). 2. J. T. Robinson, Am. J. Phys. Anthropol. 12, 181 (1954). 3. P. V. T. Tobias, Olduvai Gorge Vol. 2, The Cranium and Maxillary Dentition of Australopithecus (Zinjanthropus) boisei (Cambridge Univ. Press, Cambridge, 1967). 4. B. Wood, N. Richmond, J. Anat. 197, 19 (2000). 5. T. D. White, in The Primate Fossil Record, W. C. Hartwig, Ed. (Cambridge Univ. Press, Cambridge, 2002), pp. 407–417. 6. Here we follow the taxonomy and phylogenetic scheme summarized in (5), which subsumes Paranthropus within the broadly defined genus Australopithecus. This is in part because monophyly of robust Australopithecus (Au. aethiopicus, Au, robustus, Au. boisei) is inconclusive,
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7. 8. 9. 10.
11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25.
26. 27. 28.
29. 30.
absent stratophenetic tests in South Africa (5, 56). We recognize seven species of Australopithecus spanning ~4.2 to ~1.3 Ma [the three “robust” species/chronospecies and Au. anamensis, Au. afarensis, Au. africanus, and Au. garhi (most of the latter also considered chronospecies)], as well as a single variable lineage of early Homo predating Homo erectus (56). We interpret a considerable amount of the observed metric and morphological variation to reflect temporal (phyletic evolutionary) and geographic differentiation (5). Others recognize more than 10 species in four or more genera of separate putative clades. T. D. White, D. C. Johanson, W. H. Kimbel, S. Afr. J. Sci. 77, 445 (1981). M. C. Dean, B. A. Wood, Am. J. Phys. Anthropol. 59, 157 (1982). B. Wood, Koobi Fora Research Project Volume 4: Hominid Cranial Remains (Clarendon, Oxford, 1991). W. H. Kimbel, Y. Rak, D. C. Johanson, Eds., The Skull of Australopithecus afarensis (Oxford Univ. Press, New York, 2004). B. Asfaw et al., Science 284, 629 (1999). M. Brunet et al., Nature 418, 145 (2002). C. P. E. Zollikofer et al., Nature 434, 755 (2005). F. Guy et al., Proc. Natl. Acad. Sci. U.S.A. 102, 18836 (2005). B. Wood, Nature 418, 133 (2002). B. Senut, M. Pickford, C. R. Palevol 3, 265 (2004). M. H. Wolpoff, J. Hawks, B. Senut, M. Pickford, J. Ahern, Paleoanthropology 2006, 36 (2006). T. D. White et al., Science 326, 64 (2009). T. D. White, G. Suwa, B. Asfaw, Nature 371, 306 (1994). C. O. Lovejoy et al., Science 326, 70 (2009) C. O. Lovejoy et al., Science 326, 71 (2009). C. O. Lovejoy et al., Science 326, 72 (2009). C. O. Lovejoy et al., Science 326, 73 (2009). Materials and methods are available as supporting material on Science Online. Adding the scaled ARA-VP-1/500 temporal/occipital portion to the ARA-VP-6/500 cranial reconstruction is justified by general similarities in the major parts preserved in both specimens (basioccipital, glenoid, and zygomatic root areas) (24). M. S. Schaefer, Am. J. Phys. Anthropol. 110, 467 (1999). J. C. M. Ahern, Am. J. Phys. Anthropol. 127, 267 (2005). We initially reported that, in Ar. ramidus, the bicarotid chord intersects the basion (19). Subsequently, the Sahelanthropus cranium was similarly described as having a basion intersected by the bicarotid chord and “touched” by the biporion line (12). The latter depends on cranial orientation, which was not specified in that publication. Other workers measured the basion-tobiporion (or basion-to-bicarotid) distance, either by projection in standard (Frankfurt horizontal) orientation (27) or by direct measurement in basal view (26). Differences between and within methods are potentially large when biporion or bitympanic chords are used, due to the vertical offset of these landmarks from the basion. An additional difficulty arises in evaluating fragmentary fossils that are rarely complete enough to apply methods relying on standard orientations. We therefore opted to measure the basion-to-bicarotid distance in locally determined basilar orientation (24). S. A. Luboga, B. A. Wood, Am. J. Phys. Anthropol. 81, 67 (1990). Earlier studies of Australopithecus external basicranial shape (8) combined radiographic and direct caliper measures, apparently without due regard to the potential effects of orientation in such metric evaluations. These results suggested an extreme anterior position of the basion in robust Australopithecus crania, but not in A. africanus. However, this dichotomy was not replicated in a more recent study (27) that examined the basion-tobicarotid chord distance in Frankfurt horizontal projection. Our own results also failed to reveal clear differences in basion position between Au. africanus and eastern African robust Australopithecus (fig. S2). Rather, all Australopithecus taxa appear broadly comparable in their positions of the basion, which is consistently located slightly posterior to the carotid foramina.
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Ardipithecus ramidus 31. We agree with previous workers (26, 27) that, relative to the basion, the carotid foramen is more anteriorly situated in modern humans than in Plio-Pleistocene hominids. Thus, considerable overlap in range of variation occurs between chimpanzees and humans in measures such as basion-to-biporion or basion-to-bicarotid distances (26, 27). However, modern human and chimpanzee cranial bases differ considerably in overall structure, and the importance of isolated metrics must be considered carefully. We observe that jugular and carotid sizes are much larger in humans than in apes or MioPliocene hominids and that this directly affects measures of basion position. Larger jugular and carotid size almost certainly stems from allometric enlargement of the cranial vascular system in extremely encephalized Homo. Thus, overlap in parameters such as the basion-to-bicarotid chord between humans and chimpanzees has little consequence in evaluating and interpreting Ar. ramidus. 32. Following Guy et al. (14), we term the pre- and postchordal portions of the cranial base the anterior and posterior cranial base, respectively. 33. R. C. McCarthy, J. Hum. Evol. 40, 41 (2001). 34. G. Suwa et al., Science 326, 69 (2009). 35. C. V. Ward, M. G. Leakey, A. Walker, J. Hum. Evol. 41, 255 (2001). 36. W. H. Kimbel et al., J. Hum. Evol. 51, 134 (2006). 37. T. D. White, G. Suwa, S. Simpson, B. Asfaw, Am. J. Phys. Anthropol. 111, 45 (2000). 38. M. Brunet et al., Nature 434, 752 (2005). 39. Y. Haile-Selassie, G. Suwa, T. D. White, in Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash Valley, Y. Haile-Selassie, G. WoldeGabriel, Eds. (Univ. of California Press, Berkeley, CA, 2009), pp. 159–236. 40. Equivalent measures of mid-torus thickness were taken on a random subset of the P. troglodytes sample of the cranial base analysis (24) with the following results:
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42. 43. 44. 45. 46. 47. 48. 49. 50. 51. 52. 53. 54. 55. 56. 57. 58.
males (n = 5), mean 8.4 mm, range 6.4 to 12.1 mm; females (n = 6), mean 6.5 mm, range 5.0 to 8.2 mm. Guy et al. (14) report size-standardized values of midtorus thickness of the S. tchadensis cranium. This can be converted to an absolute mid-torus thickness of 13.8 mm. R. Fenart, R. Deblock, Pan paniscus et Pan troglodytes Craniométrie. Ann. Mus. Roy. Afrique Centr. Ser. IN-8: no. 204 (Royal Museum for Central Africa, Tervuren, Belgium, 1973). J. M. Plavcan, J. Hum. Evol. 42, 579 (2002). Y. Rak, The Australopithecine Face (Academic Press, New York, 1983). W. H. Kimbel, T. D. White, D. C. Johanson, Am. J. Phys. Anthropol. 64, 337 (1984). A. Walker, R. E. Leakey, J. M. Harris, F. H. Brown, Nature 322, 517 (1986). G. Suwa et al., Nature 389, 489 (1997). C. A. Lockwood, P. V. Tobias, J. Hum. Evol. 36, 637 (1999). C. A. Lockwood, J. M. Lynch, W. H. Kimbel, J. Anat. 201, 447 (2002). K. Isler et al., J. Hum. Evol. 55, 967 (2008). Both small ECC and small relative cranial length provide additional support to our inference that ARA-VP-6/500 is a female (18, 34). F. Spoor, S. Afr. J. Sci. 93, 182 (1997). C. Ross, M. Henneberg, Am. J. Phys. Anthropol. 98, 575 (1995). J. Biegert, in Classification and Human Evolution, S. L. Washburn, Ed. (Aldine, Chicago, 1963), pp. 116–145. R. L. Holloway, Nature 303, 420 (1983). R. L. Holloway, R. J. Clarke, P. V. Tobias, C. R. Palevol 3, 287 (2004). G. Suwa, T. D. White, F. C. Howell, Am. J. Phys. Anthropol. 101, 247 (1996). G. Suwa, J. Anthrop. Soc. Nippon 89, 303 (1981). M. Caix, G. Outrequin, Anat. Clin. 1, 259 (1979).
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59. F. Spoor et al., Proc. Natl. Acad. Sci. U.S.A. 104, 10808 (2007). 60. F. Spoor, F. Zonneveld, Yearb. Phys. Anthropol. 41, 211 (1998). 61. B. Brown, A. Walker, C. V. Ward, R. E. Leakey, Am. J. Phys. Anthropol. 91, 137 (1993). 62. We thank NSF (this material is based on work supported by grants SBR-82-10897, 93-18698, 95-12534, 9632389, 99-10344, and 03-21893 HOMINID-RHOI) and the Japan Society for the Promotion of Science (grant 11691176, 16405016, 17207017, and 21255005) for funding; the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the data; H. Gilbert for graphics assistance for Figs. 1 and 2; and the following institutions and staff for access to comparative materials: National Museum of Ethiopia, National Museums of Kenya, Transvaal Museum South Africa, Cleveland Museum of Natural History, Royal Museum for Central Africa Tervuren, Naturalis Leiden, the University of California at Berkeley Human Evolution Research Center, and the Department of Zoology of the National Museum of Nature and Science Tokyo. We also thank M. Brunet, F. Guy, M. Plavcan, M. Ponce de León, and C. Zollikofer for cooperation with comparative data.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/68/DC1 Materials and Methods Figs. S1 to S11 Table S1 References 4 May 2009; accepted 31 August 2009 10.1126/science.1175825
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Ardipithecusramidus ramidus Ardipithecus
Paleobiological Implications of the Ardipithecus ramidus Dentition Gen Suwa,1* Reiko T. Kono,2 Scott W. Simpson,3 Berhane Asfaw,4 C. Owen Lovejoy,5 Tim D. White6 The Middle Awash Ardipithecus ramidus sample comprises over 145 teeth, including associated maxillary and mandibular sets. These help reveal the earliest stages of human evolution. Ar. ramidus lacks the postcanine megadontia of Australopithecus. Its molars have thinner enamel and are functionally less durable than those of Australopithecus but lack the derived Pan pattern of thin occlusal enamel associated with ripe-fruit frugivory. The Ar. ramidus dental morphology and wear pattern are consistent with a partially terrestrial, omnivorous/frugivorous niche. Analyses show that the ARA-VP-6/500 skeleton is female and that Ar. ramidus was nearly monomorphic in canine size and shape. The canine/lower third premolar complex indicates a reduction of canine size and honing capacity early in hominid evolution, possibly driven by selection targeted on the male upper canine.
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ossilized teeth typically represent the most abundant and best preserved remains of hominids and other primates. They provide crucial evidence on variation, phylogenetic relationships, development, and dietary adaptations. Furthermore, because canines function as weapons in interindividual aggression in most anthropoid species, they additionally inform aspects of social structure and behavior. We have now recovered and analyzed a sample of 145 non-antimeric tooth crowns comprising 62 cataloged dentition-bearing specimens of Ardipithecus ramidus from the Lower Aramis Member of the Sagantole Formation, about five times more than previously reported (1, 2) (Fig. 1 and table S1). All permanent tooth positions are represented, with a minimum of 14 individuals for both the upper canine and upper second molar (M2) positions. Excluding antimeres, 101 teeth have measurable crown diameters. In addition, seven Ar. ramidus specimens with teeth have been described from Gona (3). These are broadly comparable to their Aramis counterparts in size, proportions, and morphology but slightly extend the smaller end of the species range in some mandibular crown diameters. The major morphological characteristics of the Ar. ramidus dentition have been outlined in previous studies of Aramis and Gona fos1
The University Museum, the University of Tokyo, Hongo, Bunkyo-ku, Tokyo, 113-0033 Japan. 2Department of Anthropology, National Museum of Nature and Science, Hyakunincho, Shinjuku-ku, Tokyo, 169-0073 Japan. 3Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106–4930, USA. 4Rift Valley Research Service, Post Office Box 5717, Addis Ababa, Ethiopia. 5Department of Anthropology, Division of Biomedical Sciences, Kent State University, Kent, OH 44240–0001, USA. 6Human Evolution Research Center and Department of Integrative Biology, 3101 VLSB, University of California Berkeley, Berkeley, CA 94720, USA. *To whom correspondence should be addressed. E-mail:
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sils (1, 3, 4). Comparisons of Ar. ramidus with Late Miocene hominids (Ar. kadabba, Orrorin tugenensis, and Sahelanthropus tchadensis) have identified slight but distinct differences, particularly in the canine (4–6). Other subtle features of incisors and postcanine teeth have been noted as phylogenetic or taxonomic distinctions (5–10). However, the most recent and comprehensive evaluation of the available Late Miocene materials concluded that these differences are minor compared with extant ape (and later hominid) genus-level variation and that both Ar. ramidus and Ar. kadabba dentitions exhibit phenetic similarities with early Australopithecus (4). The expanded Ar. ramidus sample of the present study allows a more definitive phylogenetic placement of Ar. ramidus relative to the more primitive Ar. kadabba and the more derived Au. anamensis and Au. afarensis (11). Here, we focus on the paleobiological aspects of the Ar. ramidus dentition, including variation, size, and scaling, probable dietary niche, and canine/lower third premolar (C/P3) complex evolution and its behavioral implications. We also address the alleged phylogenetic importance (7) of enamel thickness in Ar. ramidus (1). This is now made possible by the more comprehensive dental collection that includes key associated dental sets. Crown size, proportions, and variation. The Ar. ramidus dentition is approximately chimpanzee-sized (fig. S1 and tables S2 to S4). Mean canine size is comparable to that of female Pan troglodytes, although the incisors are smaller. Upper and lower first molars (M1s) are P. troglodytes–sized but tend to be buccolingually broader (figs. S1 to S3). The second and third molars (M2s and M3s) are both absolutely and relatively larger (figs. S1 and S4 to S6). Postcanine size and proportions of Ar. ramidus are similar to those of Ar. kadabba and other ~ 6.0-million-year-old forms (O. tugenensis and S. tchadensis) (4–10), as well as to many Mio-
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cene hominoids (although Miocene ape lower molars tend to be buccolingually narrower) (fig. S3). Variation within the Aramis dental sample is low. In modern anthropoids, the coefficient of variation (CV) is lowest in M1 and M2, with single-sex and mixed-sex values usually ranging from about 3.5 to 6.5 (12–14). At Aramis, Ar. ramidus upper and lower M1s and M2s are less variable (CVs ranging from 2.5 to 5.6) than those of Australopithecus afarensis and Au. anamensis (table S2). However, these Australopithecus samples represent multiple sites and span a much greater time than the Aramis fossils (11). The low variation seen in Aramis Ar. ramidus probably reflects spatially and temporally restricted sampling and low postcanine sexual dimorphism as in Pan (15) (table S5). The Aramis postcanine dentition is also morphologically more homogenous than known Australopithecus species samples. For example, the six relatively well-preserved M1s (Fig. 1) differ little in features otherwise known to vary widely within hominid and modern hominoid species (16, 17), including Carabelli’s expression, occlusal crest development, and hypocone lingual bulge. This suggests that the Aramis Ar. ramidus collection samples regional demes or local populations with persistent idiosyncratic tendencies. The ubiquitous occurrence of single rooted lower fourth premolars (P4) (now seen in eight non-antimeric Aramis P4s) suggests increased frequency of otherwise rare variants from genetic drift, absent substantial selection for larger and/or more complicated root systems (18). Because this anatomy is shared with Gona Ar. ramidus (3), it appears characteristic of this regional population. Morphology and evolution of the C/P3 complex. The C/P3 complex of anthropoids has behavioral and evolutionary importance because canine size and function are directly linked to male reproductive success (19). Therefore, clarifying the tempo and mode of the evolution of the C/P3 complex, from hominid emergence through its early evolution, is important. Not counting antimeres, 23 upper and lower canines from 21 Ar. ramidus individuals are now known from Aramis. Three more have been described from Gona (3), and seven from the ~ 6.0million-year-old Ar. kadabba, O. tugenensis, and S. tchadensis (4–10). There are no examples of a distinctly large male morphotype in any of these collections (Fig. 1 and figs. S7 and S8), suggesting that canine sexual dimorphism was minimal in Mio-Pliocene hominids. In basal crown dimensions, Ar. ramidus canine/postcanine size ratios overlap extensively with those of modern and Miocene female apes (fig. S9). Absolute and relative canine heights are also comparable to those of modern female apes, although canine height appears exaggerated in P. troglodytes [Fig. 1; figs. S8, S10, and S11; and supporting online material (SOM) text S1].
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Research Articles RESEARCH ARTICLES Canine shape of Ar. ramidus is either comparable to female apes or more derived toward Australopithecus (11) (Fig. 1 and figs. S12 and
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S13). The upper canine (UC) is clearly derived in Ar. ramidus, because it has a diamond-shaped lateral crown profile with elevated and/or flar-
Fig. 1. Representative examples of the Aramis Ardipithecus ramidus dentition. (A) Occlusal view micro-CT– based alignment of ARA-VP-1/300: top, maxillary dentition; bottom, mandibular dentition. The betterpreserved side was scanned and mirror-imaged to form these composites. (B) ARA-VP-1/300 in buccal view: top, right maxillary dentition (mirrored); bottom, left mandibular dentition. (C) Comparison of canine morphology (micro-CT–based renderings). Top row, lingual view of upper canines, from left to right: male P. troglodytes (cast), female P. troglodytes (cast), Ar. kadabba ASK-VP-3/400, Ar. ramidus ARA-VP-6/1, Au. afarensis L.H. 6 (cast), Au. afarensis A.L. 333x-3 (cast, mirrored). Lower rows, distolingual view of lower canines, main row from left to right: male P. troglodytes (cast), female P. troglodytes (cast), Ar. kadabba (STD-VP-2/61), Ar. ramidus ARA-VP-1/300, Au. africanus Sts 50 (mirrored), Au. africanus Sts 51. Lowest two specimens are ape lower canines with hominid-like features: left, P. paniscus (cast); right, Ouranopithecus macedoniensis RLP-55 (cast). The Ar. ramidus upper canine is highly derived, with a diamond-shaped crown with elevated crown shoulders. The lower canine tends to retain aspects of primitive ape features. Further details are given in the SOM figures and SOM text S1. (D) M1 morphology (micro-CT–based renderings) showing relatively little morphological variation among the Aramis individuals. Top row left, ARA-VP-1/300 (mirrored); right, ARA-VP-1/1818. Middle row left, ARA-VP-1/3288; right, ARA-VP-6/500. Bottom row left, ARA-VP-6/502 (mirrored); right, KUS-VP-2/154. (E and F) Box plot of upper canine maximum diameter and labial height (in mm). Ar. ramidus includes Aramis and published Gona materials (2). The ~6-million-year-old hominids are represented by Ar. kadabba (ASK-VP-3/400) and O. tugenensis (BAR 1425'00) (7). Symbols give central 50% range (box), range (vertical line) and outliers. See SOM figures and text S1 for additional plots and details. www.sciencemag.org
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ing crown shoulders (n = 5 from Aramis and n = 1 from Gona) [this study and (3, 4, 6)]. However, the lower canine (LC) retained much more of the morphology of the female ape condition (4, 5) (Fig. 1, figs. S11 to S13, and SOM text S1). A hominid-like incisiform LC morphology (high mesial shoulder, developed distal crest terminating at a distinct distal tubercle) is seen in some female apes (e.g., Ouranopithecus and P. paniscus), whereas the LCs of Ar. kadabba and Ar. ramidus tend to be conservative, exhibiting a strong distolingual ridge and faint distal crest, typical of the interlocking ape C/P3 complex (4) (Fig. 1 and SOM text S1). The Ar. ramidus P3 is represented by seven observable crowns, ranging from obliquely elongate to transversely broad (1) (fig. S14). The Ar. ramidus P3 is relatively smaller than that of Pan and typically not as asymmetric or elongate in occlusal view (figs. S15 and S16). In these respects, the Ar. ramidus P3 is comparable to those of Au. anamensis and Au. afarensis. However, Ar. ramidus is more primitive than Australopithecus in retaining a proportionately higher P3 crown (fig. S16). It appears that there was a decrease of P3 size from the ancestral ape to Ar. ramidus conditions, but this reduction was greater in basal crown dimensions than in crown height (SOM text S1). In Ar. ramidus, the combined effect of (i) reduced canine size and projection and (ii) reduced size and mesiobuccal extension of the P3 results in the absence of upper canine honing (defined as distolingual wear of the UC against the mesiobuccal P3 face, cutting into the lingual UC crown face and resulting in a sharpened distolabial enamel edge). Instead, apical wear in Ar. ramidus commences early and thereafter expands as wear progresses. None of the known UCs or P3s exhibits evidence of honing (fig. S14). However, both upper and lower canines project beyond the postcanine occlusal plane before heavy wear, resulting in steep and beveled wear slopes, as also seen in examples of Au. afarensis and Au. anamensis (1, 4, 20). Two Ar. ramidus specimens provide associated maxillary and mandibular dentitions with minimal canine wear. One is almost certainly female (ARA-VP-6/500), and the other is a probable male (ARA-VP-1/300) (see below). Both individuals possess a UC with a shorter crown height than the associated LC (>10% difference in ARA-VP-1/300) (21). In contrast in most anthropoid species, the UC is greater in height than the LC (fig. S17), a condition exaggerated in males of dimorphic species (over 50% in some papionins). Although less extreme in extant great apes (22), the UC still exceeds LC crown height by up to ~20% (fig. S18). In modest samples of modern great ape canines with little to no wear, we found no instances of LC height exceeding that of the UC (25 males and 27 females). This pattern of relative UC and LC height in Ar. ramidus appears unique among anthropoids and indicates differential reduction
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Ardipithecusramidus ramidus Ardipithecus of the UC in hominids. The UC < LC height relation is retained in modern humans. Morphological changes in the series Ar. kadabba–Ar. ramidus–early Australopithecus support the hypothesis of selection-induced UC reduction. As detailed above, the UC is clearly derived in Ar. ramidus, whereas the LC tends to retain the primitive female apelike condition. Au. anamensis, geologically younger than Ar. ramidus but older than Au. afarensis, exhibits a polymorphic condition represented by both primitive and advanced LC morphologies (4, 20) (SOM text S1). The more incisiform morphology becomes universal in Au. afarensis and later hominids. Furthermore, compared with both male and female apes, Ar. ramidus exhibits a small UC crown (both basal diameter and height) relative to apico-cervical root length, more so than the LC (figs. S19 and S20). This observation provides further support to the interpretation that the UC crown was differentially reduced (SOM text S1). A broader comparison of Ar. ramidus with extant and Miocene apes illuminates aspects of C/P3 complex evolution. Compared with cercopithecoids, hominoids tend to have smaller P3s with less extensive honing (fig. S15). Compared with other modern and Miocene apes, both species of Pan appear to show P3 reduction. The P3 of Ar. ramidus is even smaller, suggesting further reduction of the C/P3 complex from an ancestral ape condition. At first sight, the comparatively small P3 size in Pan appears paradoxical, because among the modern great apes both male and female P. troglodytes have relatively large and tall canines (figs. S9 and S10 and SOM text S1). However, this apparent paradox is removed by a broader perspective on tooth and body size proportions. Both Pan species share with atelines and Presbytis (sensu stricto) small postcanine size relative to body size (Fig. 2, figs. S21 and S22, and SOM text S2), low postcanine dimorphism,
and low to moderate canine size dimorphism (figs. S23 to S25). Conversely, papionins exhibit the opposite condition: large postcanines, large canines, and extreme dimorphism. We therefore hypothesize that the basal Pan condition was characterized by a somewhat reduced C/P3 complex as part of a generally small dentition relative to body size and that the canines were secondarily enhanced leading to modern P. troglodytes. The ARA-VP-6/500 skeleton and sexual dimorphism. Of the 21 individuals with canines, ARA-VP-6/500 has UC and LC that are strikingly small; its UC ranks either 12th or 13th (of 13), and its LC ranks seventh (of eight) in size (table S6). However, postcranially, ARA-VP-6/ 500 is a large individual with an estimated body weight of ~50 kg (23). Was ARA-VP-6/500 a small-canined male or a large-bodied female? We began our evaluation of ARA-VP-6/500 (24) by estimating the degree of dimorphism in the Ar. ramidus canine (SOM text S3). Even in modern humans, the canine is metrically the most dimorphic tooth. Mean basal crown diameter of human male canines is about 4 to 9% larger than that in females (table S5). Our analysis indicates that Ar. ramidus was probably only marginally more dimorphic than modern humans (tables S6 to S9 and SOM text S3), with a probable range of 10 to 15% dimorphism (in canine mean crown diameter). This is substantially less dimorphic than modern great apes, whose male canines (mean crown diameter) are larger than those of females by 19 to 47%. On the basis of the above dimorphism estimate, the probability of a male having canines as small as those of ARA-VP-6/500 can be evaluated by bootstrapping (2). Assuming 12% dimorphism in mean canine size (table S8), the probability that ARA-VP-6/500 is a male is <0.03 (if the UC is ranked 12th of 13) or <0.005 (if ranked 13th) (table S9 and SOM text S4). We conclude that ARA-VP-6/500 is a large-bodied
Fig. 2. Size and scaling of the Ardipithecus ramidus dentition. Natural log-log scatter diagram of relative upper canine height (y axis) against relative postcanine length (x axis): left, females; right, males. Both axes represent size free variables (residuals) derived from scaling tooth size against body size across a wide range of anthropoids (2). A value of zero represents the average female catarrhine condition. Positive and negative residuals represent relatively large and small tooth sizes, respectively. The diagonal line indicates the direction of equivalent canine and postcanine proportions independent of size. The five great ape taxa plotted are from left to right: P. paniscus, P. t. troglodytes, P. t. schweinfurthi, Gorilla gorilla, and Pongo pygmaeus. Ar. ramidus is plotted by using mean postcanine size and canine crown heights of probable female (ARA-VP-6/500) and male (ARA-VP-1/300) individuals. A hypothetical female
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female, a conclusion also corroborated by cranial anatomy (25). This shows that skeletal size dimorphism in Ar. ramidus must have been slight (11), as is the case in both species of Pan (26, 27). The ARA-VP-6/500 skeleton and dimorphism estimates allow us to place the Ar. ramidus dentition within a broader comparative framework. Scaling analyses (2) show that the UC of Ar. ramidus was relatively small in both sexes (fig. S22 and SOM text S2). In particular, male UC height of Ar. ramidus is estimated to be close to that of female P. paniscus and Brachyteles and to be much lower than that of male P. paniscus (which has the least projecting male canine among extant catarrhines) (Fig. 2). Canine development and function. In cercopithecoids with highly dimorphic canines, canine eruption is typically delayed in males, beginning after the age of eruption in females (28) and apparently corresponding with species-specific patterns of body size growth spurts (29–31). Once male canine eruption is initiated, it then proceeds at a higher rate than in females, but it can still last for several years depending on species (31). As a consequence, males attain full canine eruption as they approach or achieve adult body size, both of which are necessary for reproductive success (19). Sexually distinct patterns of canine eruption in relation to body size growth have yet to be well documented in modern great apes but appear to broadly share the cercopithecoid pattern described above (28, 32–34). Initiation of canine eruption in P. troglodytes differs by about 1.5 to 2 years between the sexes (35). In males of both P. troglodytes and P. paniscus, full canine eruption appears to coincide broadly with M3 eruption (observations of skeletal materials), with polymorphism in the eruption sequence of the two teeth. By contrast in females of both species, full canine eruption is attained before M3 eruption.
body weight of 45 kg or 50 kg was used (right and left stars, respectively). Ar. ramidus is shown to have small postcanine tooth sizes, similar to those of Ateles, Presbytis sensu stricto, and Pan. Relative canine height of Ar. ramidus is lower than that of the smallest-canined nonhuman anthropoids, P. paniscus and Brachyteles arachnoides. See SOM text S2 for further details. SCIENCE
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Research Articles RESEARCH ARTICLES The relative timing of canine eruption in Ar. ramidus is revealed by two juveniles. The ARAVP-6/1 holotype, a probable male (table S6), includes an unworn UC whose perikymata count is 193, higher than that in Au. africanus/afarensis (maximum 134, n = 4) (36) and lower than those in small samples of female P. troglodytes and Gorilla (minimum 204, n = 10) (37). The ARAVP-6/1 UC crown formation time was 4.29 or 4.82 years, depending on estimates of enamel formation periodicity (fig. S26). This is a comparatively short formation time, around the minimum reported for modern female apes (38). The eruption pattern of a second individual, ARA-VP-1/300, can be assessed from the presence or absence of wear facets and/or polish. The ARA-VP-1/300 canines were just completing eruption, its M2s were worn occlusally, and its unerupted M3 crowns were barely complete (Fig. 1 and fig. S27). Compared with extant apes, both its UC and LC development are advanced relative to M2 and M3 (fig. S28) (39). The combined morphological and developmental evidence suggests that selection for delayed canine eruption had been relaxed in Ar. ramidus. We hypothesize that canine prominence had ceased to function as an important visual signal in male competitive contexts. Tooth size and diet. We consider relative incisor and postcanine sizes to be potentially useful in inferring dietary adaptations, although consistent patterns across primates have not been obtained (40). In particular, postcanine megadontia has been considered a defining feature of Australopithecus (41). We evaluated incisor and molar sizes of Ar. ramidus in comparison to those of Pan and Australopithecus. Among anthropoids, Pan and Pongo are unique in having large incisors relative to both postcanine and body size, a condition not shared by Ar. ramidus (fig. S29). This suggests that Ar. ramidus was not as inten-
sive a frugivore as are Pan and Pongo, incisor length probably being functionally related to removal of fruit exocarp (42) and/or feeding behavior such as wadging. Although the M1 area, normalized by individual postcranial metrics, lies well within the range of extant chimpanzees, the total postcanine area of ARA-VP-6/500 falls between Pongo and P. troglodytes (Fig. 3). Ar. ramidus is not only less megadont than Pongo and Au. afarensis but, together with Pan, Ateles, and some Presbytis species, lies at the small end of the range of variation of large-bodied anthropoids (fig. S30). The most megadont anthropoids include robust Australopithecus, such as Au. boisei, as well as papionins and Alouatta. Ouranopithecus was probably as megadont as Australopithecus species, whereas Dryopithecus and Pierolapithecus probably had relative postcanine sizes closer to Ar. ramidus and thus better approximate the dentition–to–body size relationship of the last common ancestor of humans and chimpanzees. We conclude that Ar. ramidus was substantially less megadont than Australopithecus. Molar structure and enamel thickness. Molar structure, enamel thickness, and tooth wear further illuminate dietary adaptation in Ar. ramidus. Compared with the distinct occlusal structure of the molars of each of the modern ape species (see below), Ardipithecus occlusal morphology is more generalized, with low, bunodont cusps and moderate to strong basal crown flare. Such morphology also characterizes Australopithecus as well as a diversity of Miocene apes (43). Gorilla molars have much more salient occlusal topography and enhanced shearing crests. Pan molars are characterized by broad, capacious occlusal basins flanked by moderately tall cusps, effective in crushing relatively soft, fluidal mesocarp while retaining the ability to process more fibrous herbaceous materials (Fig. 4) (44, 45). These features are ac-
Fig. 3. Relative postcanine dental size in Ar. ramidus. Postcanine size is compared directly in reference to associated postcranial elements; x axis is natural log of the size variable (body size proxy) of Lovejoy et al. (23), derived from four metrics of the talus and five metrics of the capitate; y axis is natural log of the square root of the sum of calculated areas (mesiodistal length multiplied by buccolingual breadth) of lower M1 (left) and lower P4 to M3 (right). A, Ar. ramidus ARA-VP-6/500; L, Au. afarensis A.L. 288-1; c, Pan troglodytes troglodytes; g, Gorilla gorilla gorilla; o, Pongo pygmaeus (males blue, females red). www.sciencemag.org
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centuated in Pan by the characteristically thin enamel of its occlusal basin (45, 46). To further elucidate molar structure and dietary adaptations of Ar. ramidus, particularly in comparison with Pan and Australopithecus, we used micro–computed tomography (micro-CT) to study molar enamel thickness and underlying crown structures (2). Although the weak contrast of fossil enamel and dentin makes micro-CT– based evaluations difficult, we were able to assess several Ar. ramidus molars with this method. These and analyses of CT sections and natural fracture data (2) indicate that Ar. ramidus enamel is considerably thinner than that of Australopithecus but not as thin as in Pan [as originally reported in (1)] (Fig. 4 and figs. S31 and S32). Of particular importance is that Ar. ramidus molars do not exhibit enamel distribution patterns characteristic of P. troglodytes and P. paniscus. Both Pan species have similar crown structure and enamel distribution patterns (Fig. 4), although P. paniscus molars exhibit a higher cuspal topography, perhaps related to greater reliance on fibrous food (46, 47). Ar. ramidus lacks the thin occlusal fovea enamel of Pan and in this regard is similar to both Australopithecus and Miocene forms such as Dryopithecus (Fig. 4). The Pan condition is most likely derived, probably associated with an increased reliance on highercanopy ripe fruit feeding. Despite the generalized molar structure common to both Ar. ramidus and Australopithecus, the adaptive difference between the two is expressed by enamel tissue volume, which we consider to broadly track net resistance to abrasion. Modern ape species exhibit a near-isometric relation between molar durability (measured as volume of enamel tissue available for wear per unit occlusal area) and tooth size, despite diverse dietary preferences and crown anatomy (Fig. 4). Ar. ramidus falls near this isometric continuum, but Australopithecus does not. Australopithecus molars achieve greater functional durability from increased enamel volume. Au. boisei occupies an extreme position distant from the modern ape baseline. Thus, both tooth size and enamel thickness and volume suggest a substantial adaptive shift from Ardipithecus to Australopithecus. This is further expressed in molar macroand microscopic wear patterns. In contrast to Australopithecus, Ar. ramidus molars did not wear flat but instead retained stronger buccolingual wear slopes. The Aramis Ar. ramidus dentition also exhibits consistently weak M1 to M3 wear gradients (48). Microwear of the Ar. ramidus molars tends to differ from that of Au. afarensis, the latter characterized by a dominance of buccolingually oriented scratches (49). In contrast, the Ar. ramidus molars tend to exhibit finer and more randomly oriented striae (fig. S33). Collectively, the wear evidence suggests that Ar. ramidus consumed a less abrasive diet and engaged in less masticatory grinding than Australopithecus.
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Ardipithecusramidus ramidus Ardipithecus Enamel thickness and phylogenetic implications. Since the initial description of Ar. ramidus as a new species of Hominidae (1), its relatively thin molar enamel has been a focus of attention. Some authors have suggested that its thin enamel might be a shared derived feature with Pan (7). The fuller study of molar enamel thickness and patterns outlined above establishes the
following: (i) Although Ar. ramidus enamel is thinner than that of Australopithecus, it is not as thin as Pan’s; (ii) the thin enamel of Pan molars can be considered a part of a structural adaptation to ripe fruit frugivory (46) and therefore differs from the Ar. ramidus condition. Furthermore, the distinct internal structure of Pan molars seems lacking in Ar. kadabba, O. tugenensis, and S.
Fig. 4. Enamel thickness and distribution patterns in Ar. ramidus. Left panels: micro-CT–based visualizations of maxillary first molars in arbitrary size. (A) Outer enamel surface; (B) enamel thickness in absolute thickness scale superimposed on topographic contours; (C) enamel thickness in relative scale to facilitate comparison of pattern. The molars [labeled in (A)] are as follows: 1 and 5, Au. africanus Sts 24 (mirrored) and Sts 57; 2, Dryopithecus brancoi; 6, Ar. ramidus ARA-VP-1/3288; 3, Pan troglodytes; 4, Pan paniscus; 7, Gorilla gorilla; 8, Pongo pygmaeus. The Pan species share a broad occlusal basin and thin occlusal enamel. Both Ar. ramidus and D. brancoi are thinner-enameled than Australopithecus but share with Australopithecus a generalized distribution pattern. (D) Maximum lateral enamel thickness, showing that Ar. ramidus enamel is thicker than those of
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tchadensis (4, 8, 10). Hence, the Pan condition is best considered derived relative to the ancestral and early hominid conditions. Conclusions. Multiple lines of morphological evidence suggest that Ar. ramidus was a generalized omnivore and frugivore that did not rely heavily on either ripe fruits (as in Pan or Pongo), fibrous plant foods (as in Gorilla), or hard and
Pan and D. brancoi and thinner than that of Australopithecus species. Horizontal line is median; box margins are central 50% range. (E) Ratio of occlusal (volume/surface area) to lateral (average linear) enamel thicknesses, showing that Pan is unique in its distinctly thin occlusal enamel. (F) Molar durability (enamel volume per unit occlusal view crown area) plotted against projected occlusal view crown area. An isometric line (slope of 0.5) is fitted through the centroid of the three measured Ar. ramidus molars. The least squares regression (y = 0.418x− 1.806) of the combined modern ape sample is also shown. This slope does not differ significantly from isometry. Ar. ramidus and D. brancoi are close to, and Australopithecus species considerably above, the regression line, indicating greater enamel volume available for wear in Australopithecus molars. See (2) for further details. SCIENCE
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Research Articles RESEARCH ARTICLES tough food items (as in Pongo or Australopithecus). Ar. ramidus also lacked adaptations to abrasive feeding environments (unlike Australopithecus). These inferences are corroborated by the isotopic analysis of enamel, which indicates that Ar. ramidus predominantly consumed (~85 to 90%) C3 plant sources in woodland habitats and small patches of forest (50), thus differing from both savanna woodland-dwelling chimpanzees (>90% C3) and Australopithecus spp. (>30% C4) (51). Conversely, extant Pan and Gorilla, each with its distinctive dental morphology, are best considered derived in their dietary and dental adaptations. This is consistent with the Ar. ramidus postcranial evidence and its interpretations (11, 23) and strengthens the hypothesis that dental and locomotor specializations evolved independently in each extant great ape genus. This implies that considerable adaptive novelty was necessary to escape extinction in the Late Miocene forest and woodland environments. These analyses also inform the social behavior of Ar. ramidus and its ancestors. The dental evidence leads to the hypothesis that the last common ancestors of African apes and hominids were characterized by relatively low levels of canine, postcanine, and body size dimorphism. These were probably the anatomical correlates of comparatively weak amounts of male-male competition, perhaps associated with male philopatry and a tendency for male-female codominance as seen in P. paniscus and ateline species (52, 53). From this ancestral condition, we hypothesize that the P. troglodytes lineage secondarily enhanced its canine weaponry in both sexes, whereas a general size reduction of the dentition and cranium (25) occurred in the P. paniscus lineage. This suggests that the excessively aggressive intermale and intergroup behavior seen in modern P. troglodytes is unique to that lineage and that this derived condition compromises the living chimpanzee as a behavioral model for the ancestral hominid condition. The same may be the case with Gorilla, whose social system may be a part of an adaptation involving large body size, a specialized diet, and marked sexual dimorphism. In the hominid precursors of Ar. ramidus, the predominant and cardinal evolutionary innovations of the dentition were reduction of male canine size and minimization of its visual prominence. The Ar. ramidus dental evidence suggests that this occurred as a consequence of selection for a less projecting and threatening male upper canine. The fossils now available suggest that male canine reduction was well underway by 6 million years ago and continued into the Pliocene. Further fossils will illuminate the tempo and mode of evolution before 6 million years ago. References and Notes
5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.
16. 17. 18.
19. 20. 21.
22. 23. 24.
25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 36. 37. 38. 39.
1. T. D. White, G. Suwa, B. Asfaw, Nature 371, 306 (1994). 2. Materials and methods are available as supporting material on Science Online. 3. S. Semaw et al., Nature 433, 301 (2005). 4. Y. Haile-Selassie, G. Suwa, T. D. White, in Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash
40. 41. 42. 43.
Valley, Y. Haile-Selassie, G. WoldeGabriel, Eds. (Univ. California Press, Berkeley, 2009), pp. 159–236. Y. Haile-Selassie, Nature 412, 178 (2001). Y. Haile-Selassie, G. Suwa, T. D. White, Science 303, 1503 (2004). B. Senut et al., C. R. Acad. Sci. Paris 332, 137 (2001). M. Pickford, B. Senut, Anthropol. Sci. 113, 95 (2005). M. Brunet et al., Nature 418, 145 (2002). M. Brunet et al., Nature 434, 752 (2005). T. D. White et al., Science 326, 64 (2009). P. D. Gingerich, M. J. Schoeninger, Am. J. Phys. Anthropol. 51, 457 (1979). D. A. Cope, in Species, Species Concepts, and Primate Evolution, W. H. Kimbel, L. B. Martin, Eds. (Plenum, New York, 1993), pp. 211–237. J. M. Plavcan, thesis, Duke University (1990). Mean postcanine size in one of two subspecies of the common chimpanzee that we examined (P. troglodytes schweinfurthi) is marginally greater in females. Pan paniscus and P. troglodytes both have postcanine teeth with size dimorphism weaker than in modern humans (table S5). D. C. Johanson, thesis, Univ. of Chicago (1974). W. G. Kinzey, in The Pygmy Chimpanzee: Evolutionary Biology and Behavior, R. L. Susman, Ed. (Plenum, New York, 1984), pp. 65–88. Premolar root number and morphologies are known to be polymorphic, with single rooted P4s known in both Au. anamensis (KNM-ER 22683) and Au. afarensis (MAK-VP-1/12) (54, 55). S. R. Leigh, J. M. Setchell, M. Charpentier, L. A. Knapp, E. J. Wickings, J. Hum. Evol. 55, 75 (2008). T. D. White et al., Nature 440, 883 (2006). ARA-VP-1/300 UC and LC heights are 14.5 and 16.6 mm, respectively. Reasonable estimates of crown height of the ARA-VP-6/500 UC and LC are 13 to 13.5 mm and 14.4 mm, respectively. J. Kelley, Am. J. Phys. Anthropol. 96, 365 (1995). C. O. Lovejoy, G. Suwa, S. W. Simpson, J. Matternes, T. D. White, Science 326, 73 (2009). Our analysis for determining ARA-VP-6/500 sex consists of several steps detailed in (2) and SOM text S3. Although Ar. ramidus canines for which standard crown dimensions could be measured are limited, by comparing preserved portions, almost all can be ranked in terms of size. We therefore simulated probabilities of obtaining size ranks in model populations with set amounts of dimorphism in basal crown diameters. G. Suwa et al., Science 326, 68 (2009). P. L. Reno, R. S. Meindl, M. A. McCollum, C. O. Lovejoy, Proc. Natl. Acad. Sci. U.S.A. 100, 9404 (2003). H. M. McHenry, Hum. Evol. 1, 149 (1986). B. H. Smith, T. L. Crummett, C. L. Brandt, Yearb. Phys. Anthropol. 37, 177 (1994). S. R. Leigh, B. T. Shea, Am. J. Phys. Anthropol. 101, 455 (1996). Y. Hamada, S. Hayakawa, J. Suzuki, S. Ohkura, Primates 40, 439 (1999). S. R. Leigh, J. M. Setchell, L. S. Buchanan, Am. J. Phys. Anthropol. 127, 296 (2005). K. L. Kuykendall, Am. J. Phys. Anthropol. 99, 135 (1996). S. R. Leigh, B. T. Shea, Am. J. Phys. Anthropol. 99, 43 (1996). Y. Hamada, T. Udono, Am. J. Phys. Anthropol. 118, 268 (2002). G. C. Conroy, C. J. Mahoney, Am. J. Phys. Anthropol. 86, 243 (1991). M. C. Dean, D. J. Reid, in Dental Morphology 2001, A. Brook, Ed. (Sheffield Academic Press, Sheffield, UK, 2001), pp. 135–149. M. C. Dean, D. J. Reid, Am. J. Phys. Anthropol. 116, 209 (2001). G. T. Schwartz, C. Dean, Am. J. Phys. Anthropol. 115, 269 (2001). S. W. Simpson, C. O. Lovejoy, R. S. Meindl, Am. J. Phys. Anthropol. 87, 29 (1992). C. J. Vinyard, J. Hanna, J. Hum. Evol. 49, 241 (2005). H. M. McHenry, Am. J. Phys. Anthropol. 64, 297 (1984). P. W. Lucas, P. J. Constantino, B. A. Wood, J. Anat. 212, 486 (2008). Many Miocene apes generally considered more advanced than Proconsul have molars with less expansive cingular
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44. 45. 46. 47. 48.
49. 50. 51. 52. 53. 54. 55. 56.
structures. Such species, when they simultaneously lack distinct modifications of occlusal structure, all exhibit a common bunodont hominoid molar morphology. Such Miocene apes with this largely generalized molar morphology include Griphopithecus, Kenyapithecus, Equatorius, Nacholapithecus, Chororapithecus, Nakalipithecus, Dryopithecus, Pierolapithecus, Sivapithecus, Ankarapithecus, and Ouranopithecus. Slight differences in central tendencies in overall crown shape, occlusal cresting, accessory cuspules, and enamel thickness are used to distinguish among some of these taxa, but individual variation is high and specific distinctions are not necessarily clear on a specimen-by-specimen basis. One feature that seems to separate Late Miocene hominids, Ar. ramidus, and Australopithecus sp., on the one hand, and the Middle and Late Miocene apes, on the other, is the lack of a well-developed and distinct protoconule in the upper molars of hominids. This condition is also shared by both genera of extant African apes and may be characteristic of the African ape and human clade. E. Vogel et al., J. Hum. Evol. 55, 60 (2008). R. T. Kono, Anthropol. Sci. 112, 121 (2004). R. T. Kono, G. Suwa, Bull. Natl. Mus. Nat. Sci. Ser. D. 34, 1 (2008). R. K. Malenky, R. W. Wrangham, Am. J. Primatol. 32, 1 (1994). Two of five available Ar. ramidus individual molar rows show comparable dentine exposure at all three molar positions. The remaining three individuals show either weak or no clear gradients between adjacent molar pairs. In contrast to Australopithecus, both Ar. ramidus and Ar. kadabba molars exhibit deep dentine exposures suggestive of erosive rather than abrasive wear (4). F. E. Grine, P. S. Ungar, M. F. Teaford, S. El-Zaatari, J. Hum. Evol. 51, 297 (2006). T. D. White et al., Science 326, 67 (2009). M. Sponheimer et al., J. Hum. Evol. 51, 128 (2006). A. D. Di Fiore, R. C. Fleischer, Int. J. Primatol. 26, 1137 (2005). C. J. Campbell, Ed., Spider Monkeys: Behavior, Ecology and Evolution of the Genus Ateles (Cambridge Univ. Press, Cambridge, 2008). T. D. White, G. Suwa, S. Simpson, B. Asfaw, Am. J. Phys. Anthropol. 111, 45 (2000). E. D. Shields, Am. J. Phys. Anthropol. 128, 299 (2005). For funding, we thank NSF (grant nos. 8210897, 9318698, 9512534, 9632389, 9727519, 9729060, 9910344, and 0321893 HOMINID-RHOI) and the Japan Society for the Promotion of Science (grant nos. 11640708, 11691176, 14540657, 16405016, 16770187, 17207017, 19207019, 19770215, and 21255005); the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the data; the institutions and staff of National Museum of Ethiopia, National Museums of Kenya, Transvaal Museum South Africa, Cleveland Museum of Natural History, Royal Museum of Central Africa Tervuren, Naturalis Leiden, and the Department of Zoology of the National Museum of Nature and Science (Tokyo) for access to comparative materials; H. Gilbert for graphics work on Fig. 1; D. DeGusta and L. Hlusko for editorial assistance; R. Bernor, L. de Bonis, M. Brunet, M. C. Dean, B. Engesser, F. Guy, E. Heizmann, W. Liu, S. Moya-Sola, M. Plavcan, D. Reid, S. Semaw, and J. F. Thackeray for cooperation with comparative data and fossils; and T. Tanijiri, M. Chubachi, D. Kubo, S. Matsukawa, M. Ozaki, H. Fukase, S. Mizushima, and A. Saso for analytical and graphics assistance.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/69/DC1 Materials and Methods SOM Text Figs. S1 to S33 Tables S1 to S9 References 4 May 2009; accepted 18 August 2009 10.1126/science.1175824
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Ardipithecusramidus ramidus Ardipithecus
Careful Climbing in the Miocene: The Forelimbs of Ardipithecus ramidus and Humans Are Primitive C. Owen Lovejoy,1* Scott W. Simpson,2 Tim D. White,3* Berhane Asfaw,4 Gen Suwa5 The Ardipithecus ramidus hand and wrist exhibit none of the derived mechanisms that restrict motion in extant great apes and are reminiscent of those of Miocene apes, such as Proconsul. The capitate head is more palmar than in all other known hominoids, permitting extreme midcarpal dorsiflexion. Ar. ramidus and all later hominids lack the carpometacarpal articular and ligamentous specializations of extant apes. Manual proportions are unlike those of any extant ape. Metacarpals 2 through 5 are relatively short, lacking any morphological traits associable with knuckle-walking. Humeral and ulnar characters are primitive and like those of later hominids. The Ar. ramidus forelimb complex implies palmigrady during bridging and careful climbing and exhibits none of the adaptations to vertical climbing, forelimb suspension, and knuckle-walking that are seen in extant African apes.
T
he grasping hand is a hallmark of all primates (1), and elaborated forelimb flexibility characterizes all extant hominoids. Hands have played a central role in human evolution and perhaps even in the emergence of higher cognition (2). Although we no longer use our hands in locomotion, our ancestors must have. Chimpanzees, which knuckle-walk and vertically climb, have long fingers compared to their thumbs. Gorilla proportions are similar but less extreme. Did our ancestors also knuckle-walk and adapt to vertical climbing and suspension as the modern African apes have, or did our anatomy emerge directly from a more generalized Miocene ancestor, as some mid-20th century anatomists argued (3)? Answers to these central questions are now provided by Ardipithecus ramidus. The Aramis Ar. ramidus sample includes all bones of the forelimb except for the pisiform and some terminal phalanges (4). Of particular importance are ARA-VP-7/2, a forelimb skeleton, and ARA-VP-6/500, a partial skeleton preserving a lower arm and most of both hands (Fig. 1). We describe here the salient aspects of the taxon’s forelimb anatomy and their implications for hominid evolution. These and other data (5–7) show that Ar. ramidus was both terrestrially bipedal and arboreally capable. 1
Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44240-0001, USA. 2Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106-4930, USA. 3Human Evolution Research Center, and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA. 4Rift Valley Research Service, Post Office Box 5717, Addis Ababa, Ethiopia. 5The University Museum, the University of Tokyo, Hongo, Bunkyo-ku, Tokyo 1130033, Japan. *To whom correspondence should be addressed. E-mail:
[email protected] (C.O.L.);
[email protected] (T.D.W.)
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Medial metacarpus and phalanges. The medial metacarpals (Mc2 to Mc5) of Ar. ramidus are short (figs. S1 and S2 and table S1) compared with those of African apes. Their heads lack any traits associated with knuckle-walking, such as prominent ridges and/or grooves (Fig. 2 and fig. S3). Ar. ramidus metacarpal heads exhibit marked, proximally located, dorsal invaginations that are associated with their metacarpophalangeal (MP) joint’s collateral ligaments (reflecting routine hyperdorsiflexion at this joint), as do those of some Old and New World monkeys and some Miocene hominoids (8–10), including Proconsul [reviewed in (11)]. Such constrictions have become minimal in all extant hominoids but for different functional reasons (see below) (Fig. 2 and figs. S4 and S5). Ar. ramidus also lacks the expansion of the metacarpal heads that is typical of knuckle-walking apes (Fig. 2 and figs. S4 to S6). The basal articulation of the Ar. ramidus Mc5 is cylindrical/condyloid. Its articular surface extends onto the dorsum of the bone (Fig. 2), as it does in Australopithecus afarensis (12, 13), Homo sapiens, Proconsul heseloni (14–17), Pierolapithecus catalaunicus, Equatorius africanus, and papionins [this study; see also (10)]. It is entirely unlike the immobilized, noncondylar, planar homolog in Pongo, Pan, and Dryopithecus laietanus. Some Gorilla Mc5-hamate joints are sufficiently compliant to allow energy dissipation via their soft tissues, but they are too angular at their base to permit substantial motion without cavitation. In contrast, the dorsal prolongation of the Ar. ramidus Mc5 surface appears to have permitted a greater range of flexion and extension than in any extant hominoid (>20° extension and >25° flexion from a neutral position; Fig. 2). This may reflect selective modification of underlying positional information (type 1) (18) and/or chondral modeling (type 4).
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The mating surfaces for the Mc4 and Mc5 bases on the Ar. ramidus hamulus lack the angled and distopalmarly extending facets that are present in Pan, Pongo, and (to a lesser degree) Gorilla. These are additional reflections of restricted mobility and increased rigidity of the Mc4- and Mc5-hamate joints in these apes. The hamate’s primitive state (a hamulus still permitting substantial Mc5-hamate dorsiflexion) in Sivapithecus parvada (19), Oreopithecus bambolii, Proconsul sp. (14–17), and E. africanus [(10), this study] implies that a more rigid hamatemetacarpal articulation emerged in parallel between early ancestors of African apes and Pongo. This rigidity was therefore unrelated to knuckle-walking and may have emerged only in large-bodied suspensory forms. Mobility in the Mc5-hamate joint, as seen in Ar. ramidus, facilitates and/or reflects compliance of the palm with the substrate during palmigrady, as well as providing hypothenar opposition to the first ray during grasping (20). The latter proved to be a pivotal exaptation for extractive foraging and eventually tool using and making in both Australopithecus (21) and Homo, but especially in the latter. The Ar. ramidus phalanges of rays 2 to 5 (figs. S7 to S15 and table S2) are shorter than those of Pan but longer than those of Gorilla, relative to body size. However, because of elongation of the medial metacarpus in African apes, phalangeal-to-metacarpal length ratios in Ar. ramidus are more similar to those of Old World monkeys (figs. S8 and S14). Manual/ pedal phalangeal length ratios are similar in Ar. ramidus, Pan, and Gorilla and are substantially higher than those in Proconsul (fig. S15). The first ray. Unlike in apes, the Ar. ramidus first ray is relatively large and robust (Fig. 1, figs. S16 to S22, and tables S1 to S3). The Mc1 base flares outward with a prominent attachment for the abductor pollicis longus muscle, as in all later hominids. In both size and proportions, its head is robust and dorsally expanded, with welldefined and asymmetric sesamoid grooves as in Homo but in distinction to Pan or Gorilla. The ARA-VP-6/500 Mc1/Mc5 length ratio is close to that of Proconsul and exceeds those of extant African apes, largely reflecting elongation of the medial metacarpus in the latter (fig. S17). The first ray’s terminal phalanx exhibits a symmetrically constructed, rugose insertion gable (22, 23) for the flexor pollicis longus (Fig. 1, inset), in contrast to African apes in which this muscle’s tendon is reduced or absent (3). The first ray’s carpometacarpal, MP, and interphalangeal joints are also somewhat larger and more humanlike in shape than those of African apes, suggesting greater thenar mobility and/or possibly greater loading during ontogeny [that is, types 1 and/or 4 (18)]. The trapezium’s tuberosity is large and projects toward the palm (Fig. 3), deepening the adjacent groove for the flexor carpi radialis tendon.
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Research Articles RESEARCH ARTICLES The central joint complex and midcarpal joint. Ar. ramidus provides pivotal evidence about the natural history of the immobile (24) or fixed unit (25) of the hand (trapezoid/capitate/ proximal Mc2 and Mc3) that we refer to as the central joint complex (CJC). Most previous analyses have presumed a modern apelike antecedent of the human CJC, without due regard for the key anatomy described below. Ar. ramidus shows that CJC anatomy is pivotal to understanding the evolution of the hominoid hand.
A suite of derived structures stabilizes the CJC in extant great apes. These can be summarized as follows: (i) the palmar portion of the lateral (radial) side of the capitate has been extended distally to create a novel capitate-Mc2 facet that now allows the Mc2 to act as a buttress against rotation in the CJC (Figs. 3 to 5), and (ii) the lateral portion of the capitate’s dorsodistal surface has been withdrawn proximally. These novel articular geometries have resulted in a CJC with a complex polyaxial interface; the dorsal
Fig. 1. Digitally rendered composite hand of ARA-VP-6/500 in palmar view. Lateral (bottom left), dorsal (bottom center), and medial (bottom right) views are also shown. All carpals except for the trapezium are from the left side. The trapezium, Mc2, and some phalanges have been mirror-imaged. The first ray’s proximal phalanx is from ARA-VP-7/2 and has been size-adjusted based on estimated Mc4 length (7) in the two specimens (estimated in ARA-VP-6/500). Intermediate and terminal phalanges are provisionally allocated to position and side only, except for ARA-VP-6/500-049, a pollical terminal (inset; cast). Note its clearly marked insertion gable for the flexor pollicis longus as in modern humans. Imagery is based on computed tomography (CT) scans taken at 150-mm voxel resolution by a peripheral quantitative computed tomography (pQCT) XCT-Research SA+ instrument (Stratek, Pforzheim, Germany), and processed by use of software Analyze 6.0 (Mayo Clinic, Rochester, MN) and Rapidform 2004/2006 (Inus Technology, Seoul, South Korea). 2 OCTOBER 2009
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portions of their joint surfaces are angled opposite to their palmar portions (Fig. 5H), creating a partial screw effect. This morphology has several extraordinary advantages. The partial screw effect (26) provides a route for cartilage-sparing energy dissipation during loading. In palmar view (Fig. 5H), it can be seen that external axial rotation of the Mc3 upon the capitate causes distention of the joint, which can then be resisted by tension in greatly hypertrophied carpometacarpal ligaments. However, the Mc2 and Mc3 cannot rotate (from a neutral position) in the opposite direction, because such internal rotation is now blocked by the capitate; that is, by the position of the capitate’s palmar process, which has displaced the (less stable) trapezoid and abuts against the Mc2. Finally, the overall proximodorsal-todistopalmar angulation of the Mc3-capitate interface converts any dorsopalmar shear to tension. Thus, dorsopalmar shear and torsion acting in the CJC are both resisted by the greatly enlarged and axially disposed carpometacarpal ligaments (see below and Figs. 3 to 5). The topographically complex (polyaxial) and heavily buttressed African ape CJCs increase rigidity and permit energy dissipation during suspension (Figs. 3 to 5) and vertical climbing (27), and possibly during knuckle-walking. The CJC of Ar. ramidus is very different. It exhibits the simple, planar joint interface shared with some Old World monkeys and Proconsul sp. (14–17), in which all four CJC elements meet one another at nearly a single dorsopalmar axis (Figs. 3 and 5). This configuration is less competent to restrict torsion and dorsopalmar shear within the CJC, because it can only resist rotation and/or shear via its slight subchondral surface undulations, whose relative translation only minimally distends the joint. The configuration of CJC joint geometry can be assessed visually (fig. S23) and by two metrics: angulation of the capitate’s hamate facet relative to the long axis of the Mc3 (fig. S23) and mediolateral angulation of the Mc3-capitate joint’s dorsal surface relative to the Mc3 shaft’s axis (figs. S24 and S25). Whereas both metrics record minimal angulation in palmigrade taxa, such as Papio and Ar. ramidus, both are elevated in Pan and Gorilla. However, angulation of this joint is also present in Homo. In the latter, it may have been associated with transfer of the styloid anlage (28) from the capitate to the Mc3, because the transfer had not yet occurred in Ar. ramidus, which also did not yet exhibit any angulation (it is actually slightly negative). Thus, the transfer may have either been directly associated with the introduction of Mc3 ulnar deviation or, alternatively, a pleiotropic consequence of changes in pattern formation underlying it. But it seems quite probable that the introduction of this angulation was to enhance the opposition of the medial rays with the hypertrophied thumb (29). The development of axial ligaments and their attachment patterns is also an integral part of the
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Ardipithecusramidus ramidus Ardipithecus above CJC functional morphology. In extant great apes, massive centrally located carpometacarpal ligaments pass through deep notches in the capitate and hamate to attach to Mc2 to Mc4 (Figs. 3 to 5). Thickening of these CJC ligaments, as indicated by substantial expansion of their passageways from capitate to Mc2 and Mc3, has occurred in virtually all hominoids engaged in suspension, including Pongo, Pan, and Gorilla. Osteologically, such thickening is expressed as isolation of dorsal and palmar intermetacarpal articular facets separated by deep cylindrical grooves. Whereas D. laietanus exhibits the extant great ape condition, similar capitate and Mc base notching is entirely absent in Proconsul, Ar.
ramidus, Australopithecus, and Homo, reflecting the absence of similarly robust carpometacarpal ligaments in these taxa. The CJC’s primitive state in Ar. ramidus strongly suggests that the earliest hominids and their immediate ancestors did not engage in habitual suspension or vertical climbing. The proximal part of the Ar. ramidus capitate also differs from all known hominoid homologs. Its head and neck lie more palmar to the bone’s corpus (Fig. 4), and the head’s dorsal articular surface blends distally into a broad dorsal depression that accommodates the distal edges of the scaphoid and lunate during midcarpal joint dorsiflexion (30). In knuckle-walking African
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Fig. 2. Metacarpus of Ar. ramidus. (A to D) Left Mc4s of a modern human (CMNH-HT-1617), ARA-VP-7/2-G, and a chimpanzee (CMNH-B1708). Views include medial, proximal, dorsal, and distal. Note the very large notch on the lateral side of the base of the Pan specimen for transmission of its carpometacarpal ligament (a much smaller notch is present in the Ar. ramidus specimen) and the deep knuckle-walking sulcus on the head’s dorsum (see also fig. S3). The latter is absent in hominids. (E to H) Equivalent views of the left Mc5 of the same extant individuals and ARA-VP-6/500-036. The basal articular surface of the Ar. ramidus Mc5 is cylindrical and is continued well onto the shaft’s dorsum, unlike either of the other specimens. Its form is almost identical to its homolog in Equatorius africanus. The Pan surface is virtually flat and nonmobile. (I) Mc1s of the same extant individuals (Pan, top left; Homo, top right), and two Ar. ramidus [ARA-VP-6/1638 (bottom right) and ARA-VP-6/500-015 (bottom left)]. Note the very broad Mc1 sellar bases in the hominids, demonstrating that palmar grasping is the probable antecedent condition for extant African apes and humans. This may have been lost in conjunction with apparent first-ray involution in apes (71, 72). Scale bar, 2 cm.
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apes, the capitate head’s surface usually bears a subchondral tidemark recording maximum dorsiflexion of the scaphoid, which engages only a portion of the capitate’s dorsal surface (Figs. 3 and 4) (31–33). In Ar. ramidus, the scaphoid’s distal articular margin is deeply concave. Here, dorsiflexion did not terminate on the capitate head, but continued onto the dorsal surface of the capitate’s anatomical neck (Figs. 3 and 4). In Ar. ramidus, the scaphoid completely engulfed the head and thus entered hyperdorsiflexion, greatly enhancing its capacity for palmigrady at the midcarpal joint. The palm of Ar. ramidus is made relatively narrow by the dominance of its spherical lunate but mostly by its markedly narrow trapezoid (Fig. 3). The capitate head’s palmar (and thereby eccentric) location may have limited midcarpal rotation in Ar. ramidus. However, its symmetric lunate, narrow trapezoid (figs. S26 to S29 and table S3), and more laterally facing scaphoid may have allowed greater compensatory radiocarpal axial rotation, and possibly greater radial deviation (see below), than in extant African apes and humans (in which the capitate’s head is broad and less spherical). These changes appear to have occurred independently in humans for palmar grasping and in Pan and Gorilla for vertical climbing and knuckle-walking. If so, they have caused conflation of the functional and evolutionary history of the midcarpal joint [see, for example, (32, 33)]. Ar. ramidus establishes that the null hypothesis for evolution of the human hand must be that hominids have never had modern apelike CJCs or their attendant behaviors, in contrast to previous assumptions (32–34). Alteration of the primitive CJC in later hominids has been largely restricted to the following: (i) dorsal elevation of the capitate head; (ii) broadening of the capitate and trapezoid (for greater palmar span) (Fig. 3, figs. S28 and S29, and table S3); (iii) reduction of the surface relief in the Mc3capitate joint (thereby permitting greater kinematic compliance, probably initiated after the elimination of the forelimb from weight-bearing locomotion); and (iv) transfer of the os styloideum element from the capitate to the Mc3 (28, 29). Au. afarensis exhibits a more humanlike, albeit intermediate, condition. It shows evidence of all but the fourth of these shifts, each of which presumably facilitated nonlocomotor palmar grasping. The much-discussed lateral orientation of the capitate’s Mc2 and Mc3 facets [see review in (35)] in later hominids is probably now best viewed as a collateral pleiotropic effect [type 2A (18)] of mediolateral expansion of the radial wrist associated with increased thenar size and robusticity, because both the trapezium and trapezoid are enlarged in Homo as compared with Ar. ramidus. The only possible kinematic significance of these minor variations of the capitate [that is, palmar cupping (24)] is most likely a consequence of cartilage modeling during on-
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Research Articles RESEARCH ARTICLES togeny (type 4) or is simply inconsequential inherent variation (type 2B and/or 5). The capitate’s Mc2 and Mc3 angles are close to 90° in both Ar. ramidus and Au. anamensis (35). This
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Fig. 3. Articulated wrists (left sides) of hominoids (no pisiform) in maximum dorsiflexion. (A) Pan (CMNH-B1708); (B) ARA-VP-6/500 (casts; the trapezium of ARA-VP-6/500 is a rapid prototyping model based on CT scan of the contralateral side); (C) Homo (CMNH-HT-1617). (Top row) Lateral view (Mc3 surface of capitate is vertical). The scaphoid’s radial surface faces dorsolaterally in ARA-VP6/500. It faces slightly more proximal in Homo, but demonstrably more so in Pan. Its more limited articular extent in Pan allows enlarged radioscaphoid ligaments, which insert into its nonarticular area (see text, Fig. 4F, and fig. S30). (Second row) Dorsal view aligned with the capitate-hamate joint plane made vertical. The ARA-VP-6/500 scaphoid completely engulfs the capitate’s head, advancing into a furrow formed between its articular neck and the proximal surface of the trapezoid. That of Pan articulates only with the more proximally directed capitate head. Both extant taxa have substantial mediolateral wrist expansion for palmar grasping in Homo and for knuckle-walking in Pan. Distally, there is a large styloid element on the ARA-VP-6/500 capitate [see text and (28)]. It has been transferred to the Mc3 in Homo, leaving behind a broad V-shaped recess. (Third row) Proximal view (plane of the capitate’s Mc3 surface is vertical). The more proximally oriented radial surface of Pan is obvious, although that of Homo also faces less medially than that of Ar. ramidus (note the lunate’s subchondral tidemark of maximum dorsiflexion superiorly as a slight dorsal ridge in Pan). (Fourth row) Distal view (the capitate-trapezoid joint plane is vertical). The capitate-trapezoid axis is simple in ARA-VP-6/500, whereas it has become medially concave in Homo, either facilitating or reflecting compliance within the carpus for palmar grasping. The distal carpal row is generally broadened in Homo. In Pan, the capitate’s palmar portion has been extended distally, and large notches allow transit of its massive carpometacarpal ligaments (absent in hominids). Its hamate is broadened, with a more distally projecting and mediolaterally expanded hamulus. The distal face of the ARA-VP-6/500 capitate is a simple plane interrupted only by transverse palmar and dorsal furrows; its trapezoid is mediolaterally slender, whereas it has been mediolaterally expanded in Homo and Pan. Note the unusually large styloid element in Ar. ramidus [text and (28)]. 2 OCTOBER 2009
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In retrospect, it appears that subsequent to their last common ancestor with hominids, the Gorilla clade (and sometime thereafter the chimpanzee clade) faced an adaptive conundrum. Palmar conformity to substrates (primitive and retained in Ar. ramidus) is obviously beneficial to climbing. However, this imparts risk of injury to the hand from insufficient joint integrity and energy dissipation mechanisms that are apparently required during vertical climbing, suspension, and/or knuckle-walking. Only Pan appears to have eliminated substantial joint mobility in the Mc4- and Mc5-hamate joints entirely, but both African apes have evolved a sophisticated stabilizing mechanism in their CJCs. Scaphoid morphology, ulnar retraction, and radiocarpal joint. The scaphoid of Ar. ramidus differs substantially from those of Old World monkeys, Proconsul, and other Miocene apes not only by the fusion of the os centrale, but by the elongation of its tuberosity and palmar deflection of its distal facet(s) for the trapezium and trapezoid (Fig. 3). These changes probably accompanied deepening of the carpal tunnel on the ulnar side of the wrist to prevent flexor tendon bowstringing by distal prolongation and increased prominence of the hamulus. Because the ulna was withdrawn to permit greater adduction, there was apparently a general deepening of the wrist’s proximal transverse arch (25). This was probably also present in Pierolapithecus at ~12.5 million years ago (Ma) (36). Fusion of the os centrale may have been a collateral consequence [nonselected pleiotropic effect; type 2B (18)] of this reorganization. If so, ulnar retraction must have occurred independently in the ancestors of the hominid–African ape clade and Pierolapithecus, because the latter retained a separate os centrale (36). None of these advanced characters is present in Sivapithecus. Pongo also exhibits a form of ulnar retraction, but scaphoid–os centrale fusion is only rarely seen. Moreover, unlike the extant African apes, Pongo also exhibits substantial midcarpal rotation (37). In extant African apes, the radiocarpal joint experiences large collision loads during knucklewalking. These are shared by the radiolunate and radioscaphoid articulations and account for a less proximodistal orientation of the scaphoid in African apes as compared with those of orangutans and Ar. ramidus. A markedly rugose and heavily buttressed scaphoid tubercle receives the hypertrophied styloscaphoid ligament in knuckle-walking apes, which restricts dorsiflexion that is imposed by ground reaction force (GRF) (38) and thereby maintains joint integrity and potentially contributes to the dissipation of collision forces. In addition, the ligamentous attachment area on the scaphoid’s dorsum for the dorsal radiocarpal ligaments (that is, its nonarticular area; Figs. 3 and 4) is also enlarged in these apes. The Ar. ramidus scaphoid is unlike its African ape counterpart. Its nonarticular area is narrower,
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Ardipithecusramidus ramidus Ardipithecus and its tuberosity is of small caliber, elongate, and relatively gracile, exhibiting virtually no expansion where it joins the bone’s corpus. It would therefore be poorly suited to sustain large loads applied to its tuberosity by the styloscaphoid ligament. In humans, the scaphoid has been further reorganized to accommodate an enlarged trapezium. Ar. ramidus is near the mean of modern humans in an index reflecting the scaphoid’s potential to sustain GRF (fig. S30), confirming that the Ar. ramidus scaphoid lacks evidence of high-impact loading.
The Ar. ramidus lunate lies directly proximal to the head of the capitate, which accounts for its more spherical form than in humans or extant African apes. Lunate-hamate contact during dorsiflexion was minimal in Ar. ramidus, as in Old World monkeys, Proconsul (16), and humans (Fig. 3), whereas substantial lunate-hamate contact in Pan and Gorilla appears to be derived by capitate head expansion and scaphoid reorientation, probably in response to the collision loading of knuckle-walking, because Pongo lacks these features.
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Fig. 4. Hominoid capitates and scaphoids. (A to E) Left capitate. Top, lateral (radial) view; bottom, distal capitate surfaces. (A) Pan (CMNH-B1718); (B) Homo (KSU-02234); (C) Au. afarensis [A.L. 333-40 (reversed)]; (D) Ar. ramidus (ARA-VP-7/2F); (E) Ar. ramidus (ARA-VP-6/500-058). (Bottom row) Hominid Mc3 surfaces exhibit only shallow dorsal and palmar transverse furrows. In Pan, the palmar capitate surface extends distally (toward the viewer), providing a buttress against the Mc2 [angled arrow in (A)] (see also Fig. 5H) that prevents Mc3-capitate rotation. Angled white arrows point to broad, shallow, nonblocking Mc2 facets in hominids. The Homo and Au. afarensis capitates are mediolaterally expanded by a beveled Mc2 surface (dotted lines); it is much narrower in Ar. ramidus. A white asterisk marks a subchondral defect on (B) of no functional significance. The styloid element is marked by a black asterisk in each specimen except the human, in which it is instead fused to the Mc3 (Figs. 3 and 5). (Top row) Vertical arrow in (A) points to a large carpometacarpal ligament canal (as does horizontal arrow in bottom row). Hominids exhibit only uninterrupted cartilage surfaces. The Ar. ramidus capitate head is palmar, permitting marked dorsiflexion (see also Fig. 3). The head is more dorsal in apes and intermediate in Australopithecus and Homo. In Pan, the edge of the capitate’s scaphoid articular surface is sharply delimited (horizontal arrow). In Au. afarensis and Homo, the head and neck blend imperceptibly, but a subchondral tidemark indicates maximum dorsiflexion (horizontal arrows). (F to H) Left scaphoids, trapezoid/trapezium surface faces superior; tuberosity is to the right, and the radial surface faces down to the left. (F) Pan (CMNH-1718), (G) Homo (KSU-12202), and (H) ARA-VP-6/500-062. Pan scaphoids often exhibit much shallower capitate notches (if present) (white asterisks) than hominids. Human scaphoid notch depth varies, but it is not typically as great as in Ar. ramidus (n = 2; the human scaphoid notch shown is exceptionally deep). (I) Location of the capitate head in Ar. ramidus [for method, see (73)]. Scale bar, 2 cm.
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Lunate position in Ar. ramidus also accounts for the previously unexplained lunate/scaphoid facet area ratios on the distal radius of Australopithecus, which exceed those of both humans and extant African apes (table S4). However, it is now clear that scaphoid reorientation occurred in African apes for knuckle-walking and independently in humans for increased palmar span. The similar ratio in Ardipithecus and Australopithecus therefore represents the primitive condition for both hominid and extant African apes. In summary, the hand of Ar. ramidus appears almost entirely primitive relative to the anatomical specializations seen in extant apes (for example, metacarpal elongation, elaboration of CJC articulations and ligaments, novel capitate geometry, reorientation of the scaphoid’s radial surface, enlargement of the radioscaphoid ligament, relative diminution of the first ray, etc.). Ar. ramidus establishes that these changes in the ape hand are independent specializations for arboreal access and terrestrial travel (vertical climbing, forelimb suspension, knuckle-walking) and were apparently never established in hominids, which retained a more generalized, substrateconforming, grasping hand. Radius and ulna. The Ar. ramidus sample includes a complete radius [ARA-VP-6/500-039; although damaged, its length is largely preserved (7)] and a second intact distal radius (ARA-VP7/2-B). Both exhibit greater distal articular surface angulation relative to the shaft axis than do those other early hominids [as previously reported (39)], which is consistent with the scaphoid’s more laterally facing radial facet (Fig. 3). This is now clearly identifiable as a primitive character, as previously surmised (35), and is not an adaptation to knuckle-walking [contrary to (40)]. Moreover, Ar. ramidus indicates that the radiocarpal joints of African apes and humans have become broadened mediolaterally in parallel, presumably for knucklewalking in the African apes and as a consequence of elaboration of the pollex for tool-using or -making and/or for extractive foraging in hominids. Scaphoid expansion and palmar broadening almost certainly underlie reduced radiocarpal joint angulation in later humans. Morphometrically based suppositions attributing these various characters to a history of knuckle-walking (40) or suspension in Australopithecus have been critiqued previously on theoretical grounds (41) and are now moot, because anatomical evidence indicates that Ar. ramidus was never reliant on either. The proximal ulna exhibits substantial differences among extant hominoids (42, 43). Some Miocene hominoid ulnae, as well as those of colobines, generally exhibit both long olecranons and anteriorly facing trochlear notches, a combination that is consistent with pronograde above-branch quadrupedality. Two proximal ulnae (ARA-VP-6/500-051 and ARA-VP-7/2-C) were recovered at Aramis and show that the trochlear notch in Ar. ramidus faces anteriorly (table S5 and figs. S31 and S32). A cranially oriented trochlear notch with a retroflexed olec-
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Research Articles RESEARCH ARTICLES Fig. 5. (A to D) Schematic of the articular geometry of the left CJC in hominoids. (A) Primitive planar condition of the CMc2 and CMc3 joints as seen in Ar. ramidus (and Homo). (B) The primitive CJC cannot resist shear or torsion (pronation/supination) except by distention by joint surface irregularities. (C) In African apes, the palmar capitate is insinuated distally into the interface between the Mc2 and Mc3, blocking CJC rotation (asterisk). (D) Dorsal schematic view of the Mc3-capitate portion of the CJC shown in (C). The dorsal and palmar portions of the capitate-Mc3 joint are oriented oppositely, creating a screw mechanism. Supination (26) of the Mc3 results in joint distention resisted by its hypertrophied carpometacarpal ligaments (red springs) (the location and lateral orientation of the capitate’s Mc2 facet are indicated by ⊥). (E to H) Medial, dorsal, lateral, and palmar views of an exploded right CMc3 joint in Pan CMNH-B1758. An asterisk indicates ranon, as in African apes, enhances the triceps moment arm in full elbow extension. A more anteriorly facing notch favors triceps leverage at mid-flexion (42). Although a substantially foreshortened olecranon is shared among hominids, Pan, and Gorilla, as well as with other middle and late Miocene hominoids that exhibit ulnar withdrawal at the wrist, a proximally oriented trochlear notch must be reflective of habitual suspension, because it is also found in Pongo. Retroflexion of the trochlear notch has, until now, been regarded as primitive, because the last common ancestor was presumed to have been adapted to some form of suspension. Instead, we conclude that an anteriorly facing notch is primitive, associated with an adaptation to careful climbing and bridging (44). Its presence in Ar. ramidus further supports the hypothesis that hominids have never been adapted to either suspension or vertical climbing and that human and ape proximal ulnar morphology converged for different reasons. The data for Ar. ramidus are consistent with arguments that early hominid ulnar morphology might reflect substantial manipulative skills (42), and that early hominids might have been involved in activities such as extractive foraging. In any case, ulnar morphology is congruent with transarticular force being generally greatest in full extension in both humans and great apes: during suspension in Pongo, suspension and knuckle-walking in extant African apes, and myriad possible manipulative activities unrelated to locomotion in hominids. Another ulnar character in extant African apes, here termed the “flexor expansion,” is a typically prominent, proximomedial enlargement adjacent to the posterior subcutaneous surface of the olecranon. This is created by the latter’s juncture with a markedly deep excavation of the proximal-most origin of the deep digital flexor (fig. S33). When the ulna is
the capitate’s palmar Mc2 facet, and red springs/arrows the carpometacarpal ligaments. The dorsal surface of each bone is angled opposite its palmar surface. This causes distention within the joint whenever it is supinated from a neutral (anatomical) position.
viewed anteriorly, this medial projection reaches great prominence only in African apes (45) and is not present in Ar. ramidus. It probably reflects the expansion of the mesenchymal territory of the flexor muscles’ enthesis. This flexor expansion is derived and uniquely associable with knuckle-walking based on the role of the digital flexors (eccentric contraction and/or passive tension in their connective tissue capsules) and the enlarged relative muscle mass in Pan and Gorilla (38), as well as the tubercle’s absence in orangutans and all hominids, including Ar. ramidus. The hypertrophy in extant African apes may have also been accompanied by myological reorganization in the forearm that resulted in gracilization or loss of the flexor pollicis longus tendon’s attachment on the first ray. Humerus. The Ar. ramidus humerus sample includes a well-preserved proximal humerus with shaft (ARA-VP-7/2-A), a well-preserved humerus shaft (ARA-VP-1/4) (39) (fig. S34), and multiple distal humeral shafts lacking most or all of their distal articular surfaces (total n = 7). Distal humeral morphology is largely conserved among hominoids, which vary only minimally in a variety of minor phenetic characters associated with full extension at the elbow (46), including a deep zona conoidea with a posteriorly extended lateral wall and a spherical capitulum with a short radius of curvature. Both are present in Ar. ramidus (ARA-VP-7/2-A) (47). The Ar. ramidus proximal humerus (39) exhibits equally typical hominid characters, including an elliptical head and shallow bicipital groove (48). It exhibits only minimal torsion (fig. S34). The deltopectoral crest of ARA-VP-1/4 is elevated and rugose (39). The common assumption that this reflects differentially powerful arm musculature can be rejected for two reasons. First, the morphotype is shared among mod-
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ern humans, cercopithecoids, P. heseloni (14), Sivapithecus indicus (49), Ar. ramidus, and Au. afarensis. Second, the crest is consistently less developed in apes and virtually absent in brachiating gibbons. It is therefore a trait dictated primarily by positional information rather than loading (type 1 and/or 2) (18, 50, 51). A rugose deltoid crest is clearly primitive (52), retained in hominids but substantially modified in suspensory, vertical-climbing, and knucklewalking apes—an observation made more than 75 years ago (53). A possible explanation of crest reduction in apes is that it reflects increased intermuscular fusion, as has occurred in gibbons (54), which also use suspension and exhibit almost no deltopectoral cortical surface manifestations. Deltopectoral morphology may therefore serve as a key indicator of locomotor habitus in other fossil hominoids. Conclusions. The forelimb has played a definitive role in most chronicles of human evolution since Huxley’s and Keith’s original accounts (55, 56). Most recent narratives of its anatomical and behavioral evolution have emphasized a heritage of suspensory locomotion, vertical climbing, and knuckle-walking in the common ancestors that humans shared with extant African apes. Encouraged by human and chimpanzee genetic similarity and cladistic analyses, such views have come to dominate recent explications of early hominid evolution (27, 40), although alternative interpretations based on classical comparative anatomy have long differed (3, 57, 58). Ar. ramidus now permits resolution of these controversies. It indicates that, although cranially, dentally, and postcranially substantially more primitive than Australopithecus, these known Late Miocene to Early Pliocene hominids probably all lacked the numerous, apparently derived, forelimb features of extant African apes. The most probable hypothesis to explain these observations is that hominids never passed through adaptive stages
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Ardipithecusramidus ramidus Ardipithecus that relied on suspension, vertical climbing, or knuckle-walking. Further fossil remains from the Late Miocene, including those before and after the African ape–hominid phyletic divergences, will test this hypothesis derived from our analysis of Ar. ramidus. References and Notes
1. G. Mivart, Proc. Zool. Soc. London 1873, 484 (1873). 2. C. Darwin, The Descent of Man, and Selection in Relation to Sex (John Murray, London, 1871). 3. W. L. Straus Jr., Q. Rev. Biol. 24, 200 (1949). 4. T. D. White et al., Science 326, 64 (2009). 5. C. O. Lovejoy, G. Suwa, L. Spurlock, B. Asfaw, T. D. White, Science 326, 71 (2009). 6. C. O. Lovejoy, B. Latimer, G. Suwa, B. Asfaw, T. D. White, Science 326, 72 (2009). 7. C. O. Lovejoy, G. Suwa, S. W. Simpson, J. H. Matternes, T. D. White, Science 326, 73 (2009). 8. D. R. Begun, J. Hum. Evol. 24, 373 (1993). 9. D. R. Begun, M. F. Teaford, A. Walker, J. Hum. Evol. 26, 89 (1994). 10. S. Ward, B. Brown, A. Hill, J. Kelley, W. Downs, Science 285, 1382 (1999). 11. S. Almecija, D. M. Alba, S. Moya-Sola, M. Kohler, Proc. Biol. Sci. 274, 2375 (2007). 12. M. E. Bush, C. O. Lovejoy, D. C. Johanson, Y. Coppens, Am. J. Phys. Anthropol. 57, 651 (1982). 13. Apparently stemming from (33), the morphology of the Mc5-hamate joint in Au. afarensis has been mischaracterized. Its Mc5-hamate joint is fundamentally similar in both structure and function to that of H. sapiens, save for the effects of the latter’s dramatic palmar rotation of the hamulus. The original observations of these specimens were that the four preserved Mc5 bases were “convex” (that is, condyloid) and lacked “true articulation with the hamulus” [(12), p. 659]. Thus, the statement that it “is obvious that the bases of the fourth and fifth metacarpals articulated with the hamate [in afarensis] as in Pan” [(33), p. 178] is unsubstantiated and incorrect. 14. J. R. Napier, P. R. Davis, Fossil Mammals of Africa No. 16 (British Museum of Natural History, London, 1959). 15. K. C. Beard, M. F. Teaford, A. Walker, Folia Primatol. (Basel) 47, 97 (1986). 16. K. C. Beard, M. F. Teaford, A. Walker, in Hands of Primates, H. Preuschoft, D. J. Chivers, Eds. (SpringerVerlag, Vienna, 1993), p. 387. 17. A. C. Walker, M. Pickford, in New Interpretations of Ape and Human Ancestry, R. L. Ciochon, R. S. Corruccini, Eds. (Plenum, New York, 1983) p. 325. 18. The trait nomenclature system used here is taken from (50, 59) and is briefly as follows [for more complete explanations, see (4)]. Type 1: traits whose morphogenesis is the direct consequence of pattern formation; usually (but not always) subjected to direct selection. Type 2: traits that are genetic but are pleiotropic to, or result from, hitchhiking on type 1 traits and are not themselves subject to selection. 2A: Parent type 1 is inferred to be under selection; its secondary effects are not. 2B: Neither parent trait nor its derivative is inferred to be under selection (rare). Type 3: resulting from a systemic growth factor. Type 4: epigenetic consequence of osteochondral remodeling and/or response to environmental stimuli; that is, not heritable but useful in interpreting behavior. Type 5: developmentally similar to type 4, but functionally uninformative. 19. C. F. Spoor, P. Y. Sondaar, S. T. Hussain, J. Hum. Evol. 21, 413 (1991). 20. Whereas the digits of apes have an “astonishing interdigital versatility” not seen in humans, only humans have an entirely independent flexor pollicis longus combined with specialized “digital pairing” of flexor tendons 3 and 4 and 2 and 5. These provide the uniquely human “cylindrical grip,” which we regard as the likely selective target of changes in the hands of early hominids; that is, “palmar grasping.” In humans, digits 2 and 3 oppose the expanded tip of the thumb, and 4 and 5 the thenar eminence, providing afferent/efferent
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21. 22. 23. 24. 25. 26.
27. 28.
29.
30.
31.
32. 33. 34. 35. 36. 37.
“information on shape, consistency, and surface qualities” [(60), p. 331]. That the necessary proportional and neural changes were eventually achieved in Homo is adequate evidence that although obviously still lacking in the hands of Au. afarensis, early recognizable manual changes in this taxon (for example, an increase in palmar breadth and greater length of ray 1) indicate a selective target of hand function similar to that eventually achieved in Homo. B. Asfaw et al., Science 284, 629 (1999). M. W. Marzke, M. M. Shrewsbury, J. Hum. Evol. 51, 213 (2006). M. M. Shrewsbury, M. W. Marzke, R. L. Linscheid, S. P. Reece, Am. J. Phys. Anthropol. 121, 30 (2003). F. J. Bejjani, J. M. F. Landsmeer, in Basic Biomechanics of the Musculoskeletal System, M. Nordin, V. H. Frankel, Eds. (Lea & Febiger, Philadelphia, 1989), p. 275. M. Baratz, A. D. Watson, J. E. Imbriglia, Orthopaedic Surgery: The Essentials (Thieme, New York, 1999). A “screw”-type ligament tensing mechanism must be unidirectional, because any opposite rotation could potentially cause cartilage damage by shear generated during compression. This is prevented by the novel abutment of the capitate’s palmar process against the medial face of the Mc2. J. G. Fleagle et al., Symp. Zool. Soc. London 48, 359 (1981). The styloid process of the human Mc3 is almost certainly the result of embryogenetic transfer of a styloid anlaga from the capitate to the Mc3. A separate os styloideum is frequently found in humans or is adherent to the capitate or trapezoid [total: 6% of cases (61)]. Indeed, an os styloideum is so frequently encountered that it was at one time considered the “ninth carpal” (62). Mobility in the Mc4- and Mc5-hamate joints has been further enhanced in humans by palmar angulation of the hamulus, presumably after a long period of freedom from the selective rigors of locomotion. Moreover, ulnar angulation of the medial metacarpals cannot have the same importance in apes as in humans, because the African ape first ray has undergone involution rather than hypertrophy. The capitate of P. heseloni shows a slight depression that may foreshadow the eventually dramatic relocation of the head that is present in Ar. ramidus [see especially (15, 16)]. Capitate waisting has been argued to facilitate midcarpal locking and to be a suspensory adaptation in apes [and early hominids (32, 33)]. Frictionless synovial diarthroses promote motion, and joints do not normally lock because it is hazardous to their structure (41). In most joints, stability is instead almost entirely the responsibility of ligaments and soft tissues [contractile and connective tissue (noncontractile) components of the joint’s surrounding muscles (63)]. If these did not arrest motion at and near full midcarpal dorsiflexion (64), the capitate’s precipitous distal expansion would habitually strain the scaphoid-lunate syndesmosis, leading to its deterioration and instability. We agree with recent observations that midcarpal structures differ substantially in Gorilla and Pan (65); however, knuckle-walking functions assigned to minor surface topographic fluctuations of the scaphoid, capitate, and hamate reflect only the ontogenetic interplay of cartilage modeling, positional information, and the stabilizing soft tissues surrounding these joints. Mere concavities (or ridges) on synovial surfaces are almost never able to restrict motion and are more likely to merely reflect its limits as dictated by the joint’s surrounding soft tissues (63). These features reflect the joint’s likely kinematics, but little about its kinetics. O. J. Lewis, Nature 230, 577 (1971). O. J. Lewis, Functional Morphology of the Evolving Hand and Foot (Clarendon Press, Oxford, 1989). M. G. Leakey, C. S. Feibel, I. McDougall, C. Ward, A. Walker, Nature 393, 62 (1998). C. V. Ward, M. G. Leakey, A. Walker, J. Hum. Evol. 41, 255 (2001). S. Moya-Sola, M. Kohler, D. M. Alba, I. Casanovas-Vilar, J. Galindo, Science 306, 1339 (2004). F. A. J. Jenkins, J. Zool. Soc. London 48, 429 (1981).
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38. R. H. Tuttle, thesis, University of California, Berkeley, CA (1965). 39. T. D. White, G. Suwa, B. Asfaw, Nature 371, 306 (1994). 40. B. G. Richmond, D. S. Strait, Nature 404, 382 (2000). 41. C. O. Lovejoy, K. G. Heiple, R. S. Meindl, Nature 410, 325 (2001). 42. M. S. Drapeau, C. V. Ward, W. H. Kimbel, D. C. Johanson, Y. Rak, J. Hum. Evol. 48, 593 (2005). 43. M. S. Drapeau, Am. J. Phys. Anthropol. 124, 297 (2004). 44. M. Cartmill, K. Milton, Am. J. Phys. Anthropol. 47, 249 (1977). 45. L. C. Aiello, B. Wood, C. Key, M. Lewis, Am. J. Phys. Anthropol. 109, 89 (1999). 46. This is expected given the following: (i) advanced antebrachial anatomy with full ulnar withdrawal (32, 33, 44) and pronation/supination were already present in Pierolapithecus at ~12.5 Ma (36), and (ii) the primary differences in elbow morphology take place in the ulna, rather than the humerus. A parallel relationship occurs in the joint’s hindlimb counterpart: The femur contains most functional information about kinematic behavior in the knee; the tibia relatively little. 47. Some have argued that functionally and phylogenetically meaningful distinctions can be made among Pliocene hominid humeri, and that the Kanapoi distal humerus has affinities with Homo (66), whereas other Pliocene materials of Australopithecus and Ar. ramidus represent primitive hominid or ape branches cladistically outside of Orrorin (66, 67). However, two morphometric studies of Pliocene hominid distal humeri (68, 69) have independently confirmed our visual assessments that these humeri cannot be segregated into meaningful morphotypes, thus leaving no quantifiable basis for such assertions. 48. M. Pickford, D. C. Johanson, C. O. Lovejoy, T. D. White, J. L. Aronson, Am. J. Phys. Anthropol. 60, 337 (1983). 49. J. Kelley, in The Primate Fossil Record, W. C. Hartwig, Ed. (Cambridge Univ. Press, Cambridge, 2002), pp. 369–384. 50. C. O. Lovejoy, M. J. Cohn, in Development, Growth, and Evolution, P. O’Higgens, M. J. Cohn, Eds. (Academic Press, London, 2000), pp. 41–55. 51. A. Zumwalt, J. Exp. Biol. 209, 444 (2006). 52. B. Benefit, M. McCrossin, Annu. Rev. Anthropol. 24, 237 (1995). 53. “A comparison with the humerus of the anthropoid [apes] shows that the Sinanthropus humerus is as different from it as the humerus of modern man. Not in one single feature does Sinanthropus reveal a true anthropoid character . . . [T]he deltoid tuberosity . . . is very poorly developed in all three great apes. . . . It is, therefore, all the more surprising that the tuberosity is very pronounced in [Macaca and Cynocephalus]. . . . If, therefore, the peculiar shape of the deltoid tuberosity in the Sinanthropus humerus is to be interpreted as a simian character, it is one that must be traced back to a pre-anthropoid stage” [(70), p. 60]. 54. A. B. Howell, W. H. Straus, Proc. U. S. Natl. Mus. 80, 1 (1938). 55. T. H. Huxley, Evidence As to Man’s Place in Nature (Williams & Norgate, London, 1863). 56. A. Keith, Br. Med. J. 1, 788 (1912). 57. A. H. Schultz, Q. Rev. Biol. 11, 259 (1936). 58. Straus observed that “[t]here can be no reasonable doubt that a long thumb (relative to the other fingers) is a generalized pithecoid character, or that its marked relative reduction in such animals as the anthropoids, some of the Semnopithecinae, and certain platyrrhines, is an extreme specialization correlated with addiction to brachiation” (3). He observed that human thumb musculature is probably primitive because of the following: (i) “a morphologically complete and functional long flexor to the thumb . . . is normally absent in orangs, and present in less than half of African apes but is constant in prosimians, platyrrhines . . . Cercopithecinae, the Hylobatidae, and man” [(3), p. 87]; and (ii) “The short, intrinsic, volar muscles of the thumb [which are either weakly developed or absent in the apes] are regularly welldeveloped in man, the Hylobatidae, the Old World monkeys (except Colobus), the New World monkeys (except Ateles), and the prosimians” [(3), p. 87].
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Research RESEARCHArticles ARTICLES 59. C. O. Lovejoy, R. S. Meindl, J. C. Ohman, K. G. Heiple, T. D. White, Am. J. Phys. Anthropol. 119, 97 (2002). 60. J. M. F. Landsmeer, in Hands of Primates, H. Preuschoft, D. J. Chivers, Eds. (Springer-Verlag, Vienna, Austria, 1993), pp. 323–333. 61. R. O’Rahilly, J. Bone Jt. Surg. 35-A, 626 (1953). 62. E. A. Zimmer, S. P. Wilk, Borderlands of the Normal and Early Pathologic in Skeletal Roentgenology (Grune & Stratton, New York, 1968). 63. A. H. Burstein, T. W. Wright, Fundamentals of Orthopaedic Biomechanics (Williams & Wilkins, Baltimore, 1994). 64. W. L. Straus, Am. J. Phys. Anthropol. 27, 199 (1940). 65. T. L. Kivell, D. Schmitt, Proc. Natl. Acad. Sci. U.S.A. 106, 14241 (2009). 66. B. Senut, S. Afr. J. Sci. 92, 165 (1996). 67. B. Senut et al., Sci. Paris. 332, 137 (2001). 68. M. R. Lague, W. L. Jungers, Am. J. Phys. Anthropol. 101, 401 (1996). 69. A. M. Bacon, Am. J. Phys. Anthropol. 111, 479 (2000). 70. F. Weidenreich, Palaeontologia Sinica, Whole Series No. 116; New Series D, No. 5 (Geological Survey of China, Peking, China, 1941).
71. C. O. Lovejoy, M. J. Cohn, T. D. White, Proc. Natl. Acad. Sci. U.S.A. 96, 13247 (1999). 72. P. L. Reno et al., J. Exp. Zool. B Mol. Dev. Evol. 310, 240 (2008). 73. Photographs were taken normal to the capitate’s lateral surface, and a vertical tangent was inscribed along the palmar and dorsal surfaces of its Mc3 facet. Three perpendiculars were then erected to this vertical tangent: (i) a horizontal tangent (at the bottom) to the most palmar point on the capitate; (ii) a horizontal tangent at the top to the most dorsal point on the capitate, and (iii) a horizontal tangent to the dorsalmost point on the articular surface of the capitate head. The distance between tangents ii and iii was then normalized by the total distance between tangents i and ii. 74. Supported by NSF (this material is based on work supported by grant numbers 8210897, 9318698, 9512534, 9632389, 9729060, 9910344, and 0321893 HOMINID-RHOI), and the Japan Society for the Promotion of Science. We thank the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; the Afar Regional
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Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the data; the following institutions and staff for access to comparative materials: National Museum of Ethiopia, National Museums of Kenya, Transvaal Museum South Africa, Cleveland Museum of Natural History, Royal Museum of Central Africa Tervuren, and the University of California at Berkeley Human Evolution Research Center; D. Kubo and H. Fukase for assistance in computerized tomography scanning and R. T. Kono for the rapid prototyping model; R. Meindl for statistical advice and assistance; P. L. Reno, M. A. Serrat, M. A. McCollum, M. Selby, A. Ruth, L. Jellema, D. DeGusta, and B. A. Rosenman for aid in data collection and exceptionally helpful discussions; and K. Brudvik, H. Gilbert, and J. Carlson for figure preparation.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/70/DC1 Figs. S1 to S34 Tables S1 to S5 References 4 May 2009; accepted 18 August 2009 10.1126/science.1175827
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The Pelvis and Femur of Ardipithecus ramidus: The Emergence of Upright Walking C. Owen Lovejoy,1* Gen Suwa,2 Linda Spurlock,3 Berhane Asfaw,4 Tim D. White5 The femur and pelvis of Ardipithecus ramidus have characters indicative of both upright bipedal walking and movement in trees. Consequently, bipedality in Ar. ramidus was more primitive than in later Australopithecus. Compared with monkeys and Early Miocene apes such as Proconsul, the ilium in Ar. ramidus is mediolaterally expanded, and its sacroiliac joint is located more posteriorly. These changes are shared with some Middle and Late Miocene apes as well as with African apes and later hominids. However, in contrast to extant apes, bipedality in Ar. ramidus was facilitated by craniocaudal shortening of the ilium and enhanced lordotic recurvature of the lower spine. Given the predominant absence of derived traits in other skeletal regions of Ar. ramidus, including the forelimb, these adaptations were probably acquired shortly after divergence from our last common ancestor with chimpanzees. They therefore bear little or no functional relationship to the highly derived suspension, vertical climbing, knuckle-walking, and facultative bipedality of extant African apes.
T
he hominid pelvis is among the most distinct osteological complexes of primates. Its distinctiveness derives from the configuration of its superior portion that maintains balance on a single limb during upright walking. These changes are not shared with apes. Therefore, comparison of the pelvis and hip among fossil and extant hominids and apes is critical for reconstructing the evolutionary steps leading to upright walking in humans versus the knucklewalking and vertical climbing practiced by our nearest ape relatives. An almost complete but damaged left hip (os coxa), a portion of the right ilium, and a distal sacral fragment were recovered from the Aramis Ardipithecus ramidus partial skeleton (ARA-VP6/500) (1). The os coxa’s overall form is preserved despite postmortem distortions of varying magnitude, most notably the fragmentation, separation, and translation of cranial and caudal portions of the acetabulum (Fig. 1). The recovered os coxa is fragmented, distorted, friable, and inseparable from internal matrix, preventing restoration by standard methods (2–4). To aid our analysis, we made a reconstruction by using anatomical and high-resolution tomographic rapid prototyping models. We iteratively adjusted various surface metrics to verify them against the original fossil. Multiple permutations of this pro1
Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44242–0001, USA. The University Museum, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. 3Cleveland Museum of Natural History, Cleveland, OH 44106–4930, USA. 4Rift Valley Research Service, Post Office Box 5717, Addis Ababa, Ethiopia. 5 Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California at Berkeley, Berkeley, CA 94720, USA. 2
*To whom correspondence should be addressed. E-mail:
[email protected]
cess produced a model that conformed to all major undistorted linear measurements of the original fossil (Figs. 1 and 2 and figs. S1 to S3). The superior portion of the iliac blade was bent anteromedially postmortem, eliminating its original lateral flare. This has been adjusted in the model. The natural curvature of the superior pubic ramus is preserved despite its fragmentation into three sections. These sections were reassembled to form the upper portion of the ischiopubic region. The position of the ischiopubic ramus was restored on this basis. All of our descriptions of the features and linear measurements of the hip and femur are independent of this reconstruction, which was used as a three-dimensional heuristic aid (5). Acetabular size and some angles are, by necessity, approximations. We provide probable ranges of likely original values where appropriate. The majority of the sacrum was not preserved. In reconstructions of the entire pelvis, however, the distance separating the two auricular surfaces is also indicated by the length and angulation of the arcuate line and plane of the pubic surface. The former can be well approximated from the fossil, and the latter is intact. Nevertheless, the exact biacetabular breadth remains unknown as do, therefore, the exact dimensions of the three primary pelvic planes. The ilium, ischium, and pubis. The Ar. ramidus ilium is dramatically mediolaterally broad as in all post-Miocene hominoids, especially Symphalangus, Gorilla, Australopithecus, and Homo (6). Its iliac fossa is largely intact, from the anterior margin of its auricular surface to the well-preserved anterior iliac margin. Here, a prominent anterior inferior iliac spine (AIIS) maintains an intact relationship to the superior acetabular wall (Fig. 1). As in later hominids, the ilium is laterally flared for relocation of the anterior gluteals and has a forward sweeping anterior superior iliac spine (ASIS).
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The anterosuperior edge of the ilium is fractured and lacks an intact crest. On the basis of the form of the bone in both apes and humans, we estimated that it would have extended only about 1 cm superior to its broken edge. A further extension would improve the role of the abductor lever arm during upright gait. We based the anterosuperior projection of the ASIS on the wellpreserved AIIS and their typical relationship in hominoids. We therefore regard its position in Figs. 1 and 2 and figs. S1 to S3 to be close to that of the original, although it may have terminated less superiorly than reconstructed here. The protuberant and anteriorly positioned AIIS is associated with a broad, short, and sagittally disposed iliac isthmus. We define the isthmus as the constricted inferior portion of the iliac blade immediately superior to the acetabulum (Figs. 1 and 2 and fig. S3). These features are shared with later hominids, but in both modern and Early Miocene apes and monkeys the isthmus is markedly elongate, and the greater sciatic notch (GSN) angle is more obtuse (Fig. 3B). The Ar. ramidus GSN is intermediate between its counterpart in modern apes and those of later fossil hominids (Fig. 3C and fig. S4). In stark contrast to its distinctly hominid ilium, the preserved Ar. ramidus ischium is like that of African apes. Although the ischial tuberosity is not preserved, the ischium is intact from its typical concave surface flare just superior to the tuberosity to the inferior border of the acetabulum (Fig. 1). Even this minimum preserved length of the superior ischial ramus is substantially longer than any known Australopithecus example (Fig. 3D) (7). The pubis preserves an intact, superoinferiorly elongate body. However, the outline of the pubic symphyseal face is similar to that of Homo and A.L. 288.-1 and unlike its extreme dorsoventral elongation in African apes (Fig. 3A). This more ovoid shape may be a collateral pleiotropic manifestation [Type 2A effect (8)] of the shortened iliac isthmus and elongated superior pubic ramus, especially in A.L. 288-1 (which exhibits both an unusually broad pubic face and greatly elongated pubic rami) (Fig. 3A) (7). Pelvic form and function. Anthropoid pelvic form is highly conserved, and major proportions are therefore similar from Old World monkeys (cercopithecoids) to Proconsul (9, 10). However, features shared by all demonstrate that the last common ancestor of Gorilla, Pan, and Homo (hereafter the GLCA) must have exhibited two substantial modifications of the anthropoid pattern, both largely occurring in the coronal plane (10): (i) a lateral expansion of the iliac fossa and crest (fig. S5) and (ii) a corresponding reduction in the retroauricular region or pars sacralis of the ilium (fig. S6) (10). Both of these changes appear to be present in some other hominoid ilia, those of Dryopithecus brancoi (11) and Oreopithecus bambolii (12), but apparently are absent in Proconsul and Nacholapithecus (13). The breadth of the ilium appears to scale with body mass and
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Fig. 1. Original and reconstructed os coxa of ARA-VP-6/500. (Left) Anterolateral and anteromedial views of the original, with a close-up of the AIIS. (Middle) CT scans of same views, except the bottom view is a close-up of the pubic symphyseal face, preserved in its entirety but damaged at its inferior extremity. It is like later hominids in its dorsoventral height and ovoid outline. (Right) Anterolateral and anteromedial views of the reconstructed os coxa (11th permutation) and of the entire pelvis using mirror reconstruction and a conjectural sacrum. Various permutations were attempted with respect to sacral breadth; the solution shown provides presumed functional minimal inlet and outlet dimensions for a hominoid of this individual’s body size (Fig. 2 and figs. S1 to S3). (Middle) Arrows in the CT images indicate major areas of distortion corrected by reconstruction. The entire iliac blade was bent anteromedially (single yellow arrow) (additional and corrective data were provided by right iliac fragment). Two green arrows indicate primary foci of subduction of three largely intact segments of the superior pubic ramus; obvious overlapping allowed accurate restoration of original length (compare with reconstruction). The acetabulum was separated into two halves (total height of the exploded acetabulum is indicated by white arrows), with substantial intervening matrix infill. This separation greatly elongates its unrestored appearance. The two halves were recompressed on the basis of a calculated rim circumference obtained through the summation of individual segments (a range of probable values is presented in discussions of metric parameters). Two red arrows mark the inferior edge of the intact acetabular rim and the superior edge of the (missing) surface of the ischial tuberosity. These provide a minimum ischial length. Various additional dimensions were corrected by means of surface metrics. The breadth of the iliac fossa was intact from the AIIS to the lateral edge of the auricular surface; the degree of individual fragment separation was assessable from surface observation and CT scan data as indicated. Areas of particular anatomical importance include the protuberant sigmoid AIIS and sagittally oriented iliac isthmus, typical of later hominids, and the notably short, ovoid, pubic symphyseal face. Major metrics and angles are provided in Fig. 3. CT scans were taken at 300-mm voxel resolution on the University Museum, the University of Tokyo, micro-CT system [TX-225 Actis (Tesco, Tokyo)] and processed with the software Analyze 6.0 (Mayo Clinic, Rochester, MN) and Rapidform 2004/2006 (Inus Technology, Seoul).
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may reflect a relatively greater gut volume in larger anthropoids involved in frugivory and/or mid-gut folivory (14). The reduction of the pars sacralis (the portion posterior to the iliac fossa/ auricular surface boundary), however, was clearly not a simple product of body size but rather a collateral manifestation (pleiotropic but of selective importance; type 2A) (8) of thoracic vertebral column invagination associated with posterolateral reorientation of the scapular glenoid (15, 16). The African ape pelvis has also undergone dramatic craniocaudal differentiation. However, unlike the changes in the iliac fossa and crest breadth, the morphology of the Ar. ramidus pelvis implies that these changes in craniocaudal dimensions evolved after the last common ancestor of the African apes and hominids. Pan and Gorilla show slight positive allometry of maximum iliac height (17) as compared with Proconsul (fig. S7). Gorilla appears to have isometrically increased the height of the lower ilium versus its dimensions in Proconsul (fig. S8, lower iliac height). In Pan, the lower ilium is extended cranially, principally by elongation of the iliac isthmus. This elongation, at least in Pan, is but one element of global change in ape pelvic morphology, in which reduction of the lumbar column and narrowing of the sacral alae (fig. S9) have constricted and dorsally extended lumbar-iliac contact in the sagittal plane (fig. S10, the trans-iliac space). This entraps the caudal lumbar (or lumbars). In combination with reduced vertebral height and fewer lumbar vertebrae (18), this effectively eliminates any thoracopelvic mobility in African apes (table S1) (7) and appears to be an adaptation to vertical climbing and/or suspension. There is no evidence of any difference in the relative height of the lower ilium between Proconsul and ARA-VP-6/500 (fig. S8). However, the pelvis of ARA-VP-6/500 shows that the lower lumbars were not entrapped as in great apes but were clearly free for anteroposterior curvature (lordosis) (figs. S9 to S11). This is because the posterior ilium and pars sacralis did not extend sufficiently superior to have restricted the most caudal lumbar. Given that early hominids most likely had six lumbars, and other manifestly primitive characters (7, 15, 16, 18), it seems probable that hominids either quickly reversed or never experienced any tendency for the sacral narrowing seen in extant great apes. A capacity for posturally dependent lower lumbar orientation was a key adaptation to bipedality, an inference made almost a century ago (19). The inferred freedom of the lowermost lumbar (or lumbars) in Ar. ramidus, coupled with broadening and more sagittal orientation of the iliac isthmus (fig. S4), would have permitted both lordosis and anterior extension of the lesser gluteals for pelvic stabilization during upright walking (15, 16). These changes, in conjunction with retention of a long lumbar column and a lowered iliac crest [that is, a reduced maximum iliac height (fig. S7)], enhanced lordosis. Lordosis can be situationally achieved by cercopithecoids
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Ardipithecus ramidus (20) (and presumably in Proconsul), even though Old World monkey ilia typically entrap the most caudal lumbar vertebra. Lordosis has been entirely eliminated in the African apes. The form and size of the AIIS in ARA-VP6/500, as well as its projection anterior to the acetabular margin, indicate that this structure had already begun to appear and mature via a novel physis. Isolation of the AIIS as a separate growth center, which is unique to hominids (21), was probably a consequence of its increased separation from the original iliac portion of the acetabular chondroepiphysis. This is because much of iliac broadening must occur at the triradial epiphysis (as well as the posterior iliac crest). An analogous phenomenon occurs in mammals with elongate femoral necks, in which accelerated growth in the region separating the presumptive greater trochanter and femoral head isolates these structures before separate ossification of each epiphysis (22). The emergence of a novel AIIS center of ossification, as seen in ARA-VP-6/500, attests to global modification of the entire pelvis. This is also demonstrated by the abbreviated craniocaudal
RESEARCH ARTICLES length of the pubic symphyseal face (Figs. 1, 2, and 3A). The anteroventral pubic surface is surmounted by a rugose pectineal line that is continuous with the nonperiosteal attachments of abductor brevis and gracilis muscles. This is a derived character in human females [the ventral arc (23)]. It is only rarely present in great apes. There is no lateral displacement of this feature in Ar. ramidus as there is in human females (and partially in A.L. 288-1). The systematic reduction of overall craniocaudal pelvic height would have lowered the trunk’s center of mass and shortened its moment arm during single support. This would at least partially compensate for retention of the long lumbar column required for anterior lordotic shift of the center of mass during bipedality. Any deletion of thoracic vertebra would also lower the center of mass. Flexibility in its positioning probably maintained ample hind-limb mobility during arboreal climbing and clambering, albeit with considerable attendant risk of lower-back injury. Given retention by Ar. ramidus of multiple primitive skeletal characters (15, 16, 24, 25), its
Fig. 2. CT comparison of ARA-VP-6/500 (left) os coxa reconstruction (11th permutation) and A.L. 288-1 (right) restoration. Reconstruction of ARA-VP-6/500 was achieved by means of sculptural modeling on the basis of numerous dimensions and contours preserved on the original fossil (Fig. 1). The sacrum is largely conjectural because only its lower portion was recovered, but four segments are likely (18). The enlarged A.L. 288-1 (115% of actual size) and ARA-VP-6/500 images have been aligned on their acetabulae. The green scale square (lower left) is 180 mm on a side. The broad sacral alae of ARA-VP-6/500 are probably because African ape sacra have almost certainly been narrowed since the GLCA (figs. S10 and S11). A novel ossification center for the AIIS and a substantial reduction in the height of the iliac isthmus are derived characters present in both hominids. Length of the ischia was reconstructed on the basis of the position of the ischial spine, shape of the obturator foramen, and (most importantly) the length of an intact surface transect from the lower edge of the acetabulum to the dorsal edge of the (missing) ischial tuber (Fig. 1). The acetabulum was preserved in two separated portions (Fig. 1). Together, they suggest a diameter of 36 to 42 mm. Spatial orientation was made on an assumption of vertical alignment of the pubic tubercle and ASIS, although the primitive form of this pelvis suggests that lumbar lordosis during terrestrial bipedality was partially situational and that the superior pelvis may have been angled less anteriorly during arboreal clambering. There is a dramatic reduction of lower pelvic length and robusticity in A.L. 288-1. www.sciencemag.org
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exceptionally derived ilium is striking. It implies an early adaptation to habitual terrestrial bipedality before any increase in the lumbar entrapment seen in the African apes, but after the lateral iliac expansion shared with them. This is consistent with the hypothesis that vertebral column invagination (its anterior transpositioning into the thorax and abdomen) was a primary morphogenetic mechanism underlying scapulohumeral reorganization for greater forelimb flexibility during arboreal clambering and bridging. If this is correct, then the extensive reorganization of the column in hominoids was not originally an adaptation to suspensory locomotion or vertical climbing (15, 16, 24–27). Comparisons of the ossa coxae of Ar. ramidus and Au. afarensis demonstrate the latter’s modifications for habitual bipedality following abandonment of arboreal locomotion (Figs. 2 and 3C and figs. S1 to S3). In general, Au. afarensis demonstrates even greater global craniocaudal abbreviation of its entire pelvis, and an accompanying increase in platypelloidy via elongation of the pubic rami anteriorly, and deepening of the greater sciatic notch and probable expansion of alar breadth posteriorly (7). Such changes appear morphogenetically coordinated and therefore were also likely expressed partially in Ar. ramidus, although the actual dimensions of its sacrum remain unknown. This view receives independent support from the remarkable pelvic stasis seen between A.L. 288-1 and the much more recent [0.9 to 1.4 million years ago (Ma); post-Au. afarensis] Busidima pelvis (BSN49/P27) (28). The functional importance of platypelloidy in Au. afarensis has been widely debated. Viewed now from the perspective of its ancestral state, however, it appears likely to have been a consequence of establishing mobility of the L6/S1 joint as a permanent character. The ancestral morphology presumably involved situationally dependent lordosis (during terrestrial upright walking) for gluteal stabilization during the stance phase. Platypelloidy may also have enhanced gut volume, although a trunk length with six lumbars may have been sufficient. The reduction of lateral iliac flare and more posterior placement of the iliac cristal tubercle in Homo therefore probably reflect an ontogenetic predisposition for lumbar lordosis with (i) reduction in lower lumbar positional lability (permitting a reduction from six to five lumbars) after complete abandonment of arboreal activity and (ii) optimization of birth-canal geometry (4). The femur. Two partial proximal femora were recovered at Aramis (Fig. 4). That of the partial skeleton (ARA-VP-6/500-5) preserves most of the shaft but is damaged by extensive expanding matrix distortion (29). A second (ARA-VP-1/701) is in good condition. Although neither preserves a head, neck, or greater trochanter, in conjunction with the os coxa they are informative with respect to the evolution of the gluteus maximus muscle (hereafter simply the maximus). The African ape posterolateral femoral shaft regularly exhibits a distomedially displaced in-
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Ardipithecus ramidus sertion for the maximus. This is separated from a more superior attachment of the vastus lateralis [to whose tendon, however, the maximus is normally fused (30)] by an elevated boss on the shaft [defined as the lateral spiral pilaster (31)]. The femora of Au. afarensis and subsequent hominids exhibit a strikingly different morphotype that in-
Research Articles cludes a trochanter tertius that surmounts a rugose hypotrochanteric fossa (31, 32). Both structures are clearly associated with hypertrophy of the maximus’ ascending tendon, which inserts directly into the lateral aspect of the femur (30). It had been thought that the lateral spiral pilaster of apes was primitive (31) and that the
A
B
C
D
Fig. 3. Some geometric and anatomical traits of the ossa coxae of hominids and African apes. (A) Maximum breadth of the pubic symphyseal face normalized by its length. The shortened condition in ARAVP-6/500 may reflect an abbreviation of overall pelvic height. The extreme value for A.L. 288-1 is largely due to the great breadth of its pubic symphyseal face; this might also be a type 2 (8) effect of this specimen’s greatly elongate superior pubic ramus. Metrics are from originals. Pan-Homo differences are highly significant (n = 15 specimens each taxon; P < 0.0001; two-tailed t test). Boxes represent 25th and 75th percentiles, vertical lines represent 5th and 95th percentiles, and the transverse lines are medians. Values between 1.5 and 3 box lengths from the upper or lower boundaries of a box are shown as open circles (asterisks indicate more than three box lengths). (B) Angle made by two chords connecting three landmarks on the ilium: from the superomost point on the auricular surface to the ASIS and from the auricular surface to the AIIS. The angle between these chords was directly measured with a modified goniometer. Maximum value shown for ARA-VP-6/500 represents the most superior location of the ASIS as described in the text and used in the model (Fig. 2); the lower value would obtain if the ASIS were less protuberant. There is a more elongate ilium (more obtuse angle) in Pan as compared with Gorilla (P < 0.001; two-tailed t test). The overlap of higher possible values in ARA-VP-6/500 with those of Gorilla, and the intermediate values in A.L. 288-1 and STS-14, at least partially reflect ASIS elongation and lateral iliac flare for increased lordosis. The exceptionally high values for Proconsul reflect both its extremely tall ilium and the precipitous anterior tilt of its auricular surface. Pan-Homo differences are highly significant (n = 15 specimens each taxon; P < 0.0001; two-tailed t test). (C) Angle made by two chords connecting three landmarks on the ilium: from the acetabular center to the caudalmost point on the auricular surface and from the acetabular center to the ischial spine (fig. S4). A third chord was measured (auricular surface to the ischial spine), and the angle was determined trigonometrically. All early hominids lie within the human range because all have a greatly shortened iliac isthmus. The isthmus in Pan is significantly longer than that of Gorilla (P < 0.0001; two-tailed t test). The angle for ARA-VP-6/500 was estimated from reconstruction. Pan-Homo differences are highly significant (n = 15 specimens each taxon; P < 0.0001; two-tailed t test). (D) Minimum ischial length (from inferior acetabular border to juncture of the ischial body and tuberosity surface) normalized by acetabular diameter. Two values for ARA-VP-6/500 bracket possible extremes for the acetabular diameter. Pan-Homo differences are highly significant (n = 15 specimens each taxon; P < 0.0001; two-tailed t test).
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hominid morphotype was derived. The femur of Ar. ramidus shows that this inference was incorrect. African ape femora never exhibit a third trochanter or hypotrochanteric fossa, whereas ARA-VP-1/701 exhibits obvious homologs to both. Moreover, the femur of Proconsul, millions of years older than Ar. ramidus, exhibits a strong gluteal tuberosity immediately inferior to its greater trochanter, as do those of Nacholapithecus (13) and Dryopithecus (33). In ARA-VP-1/701, the medial border of an obvious hypotrochanteric fossa homolog converges with the spiral line to form a markedly rugose, elevated plane on the posterior femoral surface, but their further course is lost to fracture. A similar morphology is visible on the ARA-VP-6/500 specimen. A broad linea of low relief is also clearly present in ASI-VP-5/154, assigned to Au. anamensis (34). Its morphology is reminiscent of that of A.L. 288-1, in which the linea is still notably broad, but contrasts with that of MAK-VP1/1, which is more modern in form at 3.4 Ma (31). Because most of the length of the ASI-VP5/154 shaft is preserved, its moderately elevated linea (~11.5 mm in breadth) is distinct and imparts a prismatic cross section at midshaft. Specimen BAR-1002'00 (Orrorin tugenensis) (35) presents obvious homologs to these structures. Moreover, both BAR-1002'00 and ASI-VP-5/154 exhibit an obvious homolog to the third trochanter, and neither shows any evidence of a lateral spiral pilaster. African ape morphology can therefore now be interpreted as derived and probably a consequence of global alterations of their hip and lower back for suspensory locomotion. Further narrowing of their iliac cleft from its state in Proconsul must have also relocated their maximus insertion more distomedially as well and caused increased separation from its previous position adjacent to that of the vastus lateralis, a hiatus now filled in African ape femora by the lateral spiral pilaster. This has eliminated any evidence of the otherwise ubiquitous Miocene morphotype. The disappearance of any homolog of the hypotrochanteric fossa and third trochanter in extant apes suggests a possible change in muscle and/or enthesis architecture, although fascicle length does not appear to differ substantially in the gluteals of humans and apes (36). In contrast, the gluteal complex in Ar. ramidus remains anterolaterally displaced as in Proconsul and Orrorin and still unlike its more posteromedial position in most Australopithecus (Fig. 4) (31). Such medial translation of the maximus insertion is probably a consequence of hypertrophy of the quadriceps at the expense of the hamstrings (31). Indeed, the combination of a broad, ape-like, expansive ischial tuberosity and broad proto-linea aspera in Ar. ramidus suggests that the hamstring/ quadriceps exchange had not yet achieved its modern proportions, although some expansion of the maximus was probably present given the substantial restructuring of the ilium and trans-iliac space. In contrast, most Australopithecus specimens [such
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Ardipithecus ramidus as MAK-VP-1/1, A.L. 333w-40, and A.L. 333110) (31)] had marked elevation and narrowing of a true linea aspera that is typical of later hominids (37, 38). The thorax. The thorax of ARA-VP-6/500 is represented by a partial first rib, several associated crushed ribs, and a thoracic vertebral arch. A thoracic arch from a second individual was also recovered (ARA-VP-6/1001). Both vertebrae lack centra, so the angulations of their rib facets and their implications for vertebral column invagination (39) cannot be determined. It has recently become common wisdom that early hominids had a funnel-shaped thorax. However, this supposition stems from a reconstruction of A.L. 288-1 (40) that relied on (i) an ilium left uncorrected for extensive postmortem fracture of its retroauricular portion (a defect that exaggerates lower thoracic breadth) (41), (ii) a highly fragmentary thorax, and (iii) the presumption of a short-backed, great ape–like, ancestral morphology. Because dramatic forelimb elongation, hindlimb abbreviation, and lower thoracic rigidity are seen together in all three great apes, relative constriction of their upper thorax is probably a modification accompanying these advanced adaptations to suspension and/or vertical climbing. Ardipithecus reveals, however, that earliest hom-
RESEARCH ARTICLES inids did not regularly engage in these behaviors (15, 16) and that an elongated iliac isthmus and narrowed trans-iliac space are African ape specializations that negate the lordosis required for effective transitional upright walking. Nearly 30 years have now passed since the observation that the human serratus anterior “lacks the specializations associated with suspensory behavior in large bodied, broad-chested nonhuman primates [suggesting] descent from a small ape with a thoracic shape similar to atelines.” (42). This seems particularly prescient given a recent examination of thoracic form in primates (43), which demonstrates that Ateles (also highly skilled at suspension) nevertheless lacks many other great ape-like adaptations, including a funnel-shaped thorax. It follows that this unique thoracic form is likely to emerge only as an element accompanying these other extensive great ape specializations for suspension and vertical climbing. It is therefore unlikely to have ever been present in early hominids. Confirmation of this inference, however, will require additional fossil evidence. The pelvis, femur, and preserved thoracic elements of Ar. ramidus establish that adaptations to upright walking in these regions were well established by 4.4 Ma, despite retention of a capacity for substantial arboreal locomotion. Ar. ramidus
thus now provides evidence on the long-sought locomotor transition from arboreal life to habitual terrestrial bipedality. This evidence suggests that the transition took place in the absence of any of the characters that today substantially restrict upright walking in extant apes (particularly lumbar column abbreviation, trans-iliac space narrowing, and approximation of iliac crest and thorax, and the muscles that traverse this gap). As a consequence, explications of the emergence of bipedality based on observations made of African ape locomotion no longer constitute a useful paradigm. References and Notes 1. 2. 3. 4. 5.
6.
7. 8.
9. 10. 11. 12. 13. 14. 15. 16. 17. 18.
Fig. 4. Lateral and posterior CT scan surface renders of (A) MAK-VP-1/1 (Au. afarensis, cast) and (B) ARAVP-1/701 (Ar. ramidus, original). Specimens have been aligned by their lesser trochanters. The preserved portion of the ARA-VP-1/701 shaft is sufficient to demonstrate the absence of a lateral spiral pilaster and the presence of a distinct rugose insertion area for the gluteus maximus that is homologous to the true hypotrochanteric fossa present in MAK-VP-1/1 (arrows indicate the third trochanter; brackets indicate hypotrochanteric fossae). In ARA-VP-1/701, this area is more laterally placed, as in other early hominid femora, including BAR-1002'00. The more posterior position of this insertion in MAK-VP-1/1 is almost certainly associated with decreased sagittal iliac orientation in Au. afarensis, a consequence of further posterior pelvic broadening and increased lateral iliac flare (fig. S1). None of these early hominid specimens shows evidence of a lateral spiral pilaster, which is restricted to African ape femora. www.sciencemag.org
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19. 20. 21. 22. 23. 24. 25. 26.
T. D. White, G. Suwa, B. Asfaw, Nature 375, 88 (1995). C. O. Lovejoy, Am. J. Phys. Anthropol. 50, 413 (1979). D. C. Johanson et al., Am. J. Phys. Anthropol. 57, 403 (1982). R. G. Tague, C. O. Lovejoy, J. Hum. Evol. 15, 237 (1986). In order to facilitate our examination, we also reconstructed the innominate of KNM-RU 13142 D (fig. S4). Our reconstruction does not differ substantially from that drawn by its original descriptor (17) but facilitated some three-dimensional comparisons. “The marked difference between the pelvis of Hylobates and that of Symphalangus syndactylus is ...apparent... [demonstrating] that the siamang has already a pelvis of typical anthropoid ape character, particularly in regard to the broad ilium with its prominent ASIS, whereas the pelves of the gibbons have not yet departed so far from the more primitive condition of catarrhine monkeys” [(44) p. 350]. C. O. Lovejoy, Gait Posture 21, 95 (2005). The trait nomenclature system used here is taken from (31) and is briefly as follows [for more complete explanations see (24)]. Type 1 indicates traits whose morphogenesis is the direct consequence of pattern formation, usually (but not always) subject to direct selection. Type 2 indicates traits that are genetic but are pleiotropic to or result from hitchhiking on type 1 traits and are not themselves subject to selection [2A indicates a parent type 1 is inferred to be under selection; its secondary effects are not; 2B indicates neither parent trait nor derivative is inferred to be under selection (and is rare)]. Type 3 indicates a result from a systemic growth factor. Type 4 indicates an epigenetic consequence of osteochondral remodeling and/or response to environmental stimuli, not heritable but useful in interpreting behavior. Type 5 is similar to type 4 but uninformative. C. V. Ward, A. Walker, M. F. Teaford, I. Odhiambo, Am. J. Phys. Anthropol. 90, 77 (1993). C. V. Ward, Am. J. Phys. Anthropol. 92, 291 (1993). C. V. Ward, Am. J. Phys. Anthropol. 135(S46), 218 (2008). T. Harrison, in Origine(s) de la Bipedie chez les Hominides, Y. Coppens, B. Senut,Eds. (CNRS, Paris, 1991), pp. 235–244. M. Nakatsukasa, Y. Kunimatsu, Evol. Anthropol. 18, 103 (2009). D. J. Chivers, C. M. Hladik, J. Morphol. 166, 337 (1980). C. O. Lovejoy et al., Science 326, 70 (2009). C. O. Lovejoy et al., Science 326, 73 (2009). C. V. Ward, thesis, Johns Hopkins (1991). M. A. McCollum et al., J. Exp. Zool. B Mol. Dev. Biol. 10.1002/jez.621316 (2009). W. L. Straus Jr., Am. J. Anat. 43, 403 (1929). M. Nakatsukasa, J. Anat. 204, 385 (2004). R. A. Dart, J. Palaeon. Soc. India 2, 73 (1957). M. A. Serrat, P. L. Reno, M. A. McCollum, R. S. Meindl, C. O. Lovejoy, J. Anat. 210, 249 (2007). L. C. Budinoff, R. G. Tague, Am. J. Phys. Anthropol. 82, 73 (1990). T. D. White et al., Science 326, 64 (2009). C. O. Lovejoy et al., Science 326, 72 (2009). M. Cartmill, K. Milton, Am. J. Phys. Anthropol. 47, 249 (1977).
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Ardipithecus ramidus 27. This is also consistent with substantial differences in the soft tissue configuration of the pelvic floor of extant humans and African apes. In African apes, the sphincter ani externus is hypertrophied. It serves as the primary urogenital floor, thus greatly exceeding its distribution in Old World monkeys. In humans, this muscle is instead reduced, and its function alternatively subsumed by hypertrophy of the transversus perinei profundus. “The simplest interpretation of this difference […is] that in the…[GLCA] the sphincter ani and the bulbocavernosus resembled those muscles in the…[Old World monkeys]” (45). Elftman was, of course, unaware of Proconsul pelvic structure at the time of his observation, but his conclusion was essentially that the GLCA’s pelvic floor had remained primitive, such as it presumably was in Early Miocene apes practicing above-branch quadrupedality and remaining underived for suspensory locomotion. 28. S. W. Simpson et al., Science 322, 1089 (2008). 29. T. D. White, Science 299, 1994 (2003). 30. J. T. Stern Jr., Am. J. Phys. Anthropol. 36, 315 (1972). 31. C. O. Lovejoy, R. S. Meindl, J. C. Ohman, K. G. Heiple, T. D. White, Am. J. Phys. Anthropol. 119, 97 (2002). 32. A. Hrdlička, Smithsonian Misc. Coll. 92, 1 (1934). 33. S. Moya-Sola et al., Am. J. Phys. Anthropol. 139, 126 (2009). 34. T. D. White et al., Nature 440, 883 (2006). 35. B. Senut et al., C. R. Acad. Sci. IIA Earth Planet. Sci. 332, 137 (2001). 36. R. C. Payne et al., J. Anat. 208, 709 (2006). 37. C. O. Lovejoy, Gait Posture 21, 113 (2005). 38. It has been suggested (via canonical variates analysis) that the Orrorin proximal femur “exhibits an Australopithecus-like bipedal morphology [that] evolved early in the hominin clade and persisted successfully for most of human evolutionary history” [(46) p. 1664]. However, BAR-1002’00 lacks a complete greater trochanter, making such a conclusion dependent on reconstruction. Our examination of both casts and
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39. 40. 41.
42. 43. 44. 45. 46. 47. 48.
originals leads us to agree that the specimen belongs to a bipedal hominid, but the femoral and pelvic evidence presented here demonstrate that (i) bipedality was not morphologically static from 6 to 2 Ma as claimed nor (ii) is there now any evidence for an “appreciable scansorial component” in the locomotor repertoire of Australopithecus. To the contrary, substantial arboreal behavior is now contraindicated by much of the postcranial anatomy that differentiates Ardipithecus and Australopithecus. B. Latimer, C. V. Ward, in The Nariokotome Homo erectus Skeleton, A. Walker, R. Leakey, Eds. (Harvard Univ. Press, Cambridge, 1993), pp. 266–293. P. Schmid, in Origine(s) de la Bipedie chez les Hominides., Y. Coppens, B. Senut, Eds. (CNRS, Paris, 1991), pp. 226–234. The retroauricular portion of the innominate of A.L. 288-1 was crushed postmortem, introducing a 90° angulation defect at its juncture with the iliac fossa. Failure to correct this defect results in extreme lateral extension of the ilium, making it Pan-like in three-dimensional disposition. Moreover, if uncorrected, the pubic symphyseal face fails to reach midline by several centimeters, once the broken but otherwise undistorted ischiopubic rami are restored. Compare figure 4 in (40) and figure 6 in (47) with figure 8 in (37). J. T. Stern Jr., J. P. Wells, W. L. Jungers, A. K. Vangor, Am. J. Phys. Anthropol. 52, 323 (1980). M. Kagaya, N. Ogihara, M. Nakatsukasa, Primates 49, 89 (2008). A. H. Schultz, Hum. Biol. 2, 303 (1930). H. O. Elftman, Am. J. Anat. 51, 307 (1932). B. G. Richmond, W. L. Jungers, Science 319, 1662 (2008). J. T. Stern Jr., R. L. Susman, Am. J. Phys. Anthropol. 60, 279 (1983). For funding, we thank NSF [this material is based on work supported by grants 8210897, 9318698, 9512534, 9632389, 9729060, 9910344, and 0321893
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HOMINID–Revealing Hominid Origins Initiative (RHOI)] and the Japan Society for the Promotion of Science. We thank the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation. We thank the Afar Regional Government, the Afar people of the Middle Awash, and many other field and laboratory workers for contributing directly to the data. We thank the following institutions and staff for access to comparative materials: National Museum of Ethiopia; National Museum of Natural History; Royal Museum of Central Africa Tervuren, and the Cleveland Museum of Natural History. We thank B. Senut and R. Eckhardt for access to the original specimen and casts of BAR-1002’00 and S. Moya-Sola and M. Kohler for access to multiple specimens in their care. We thank M. Brunet for comparative data and C.V. Ward for access to her large pelvic database which was used extensively in this analysis. We thank D. Kubo and H. Fukase for assistance in computed tomography (CT) scanning; R. Meindl for statistical advice and assistance; and M. A. McCollum, P. L. Reno, M. A. Serrat, M. Selby, D. DeGusta, A. Ruth, L. Jellema, S. W. Simpson, and B.A. Rosenman for aid in data collection and exceptionally helpful discussions. We thank H. Gilbert and J. Carlson for help with figures. We thank A. Sanford and A. Ademassu for the many generations of casts required to complete this study, R. T. Kono for the rapid prototyping models, and L. Gudz and E. Bailey for assistance with illustrations.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/71/DC1 Figs. S1 to S11 Table S1 References 4 May 2009; accepted 17 August 2009 10.1126/science.1175831
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Ardipithecusramidus ramidus Ardipithecus
Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus C. Owen Lovejoy,1 Bruce Latimer,2 Gen Suwa,3 Berhane Asfaw,4 Tim D. White5* Several elements of the Ardipithecus ramidus foot are preserved, primarily in the ARA-VP-6/500 partial skeleton. The foot has a widely abducent hallux, which was not propulsive during terrestrial bipedality. However, it lacks the highly derived tarsometatarsal laxity and inversion in extant African apes that provide maximum conformity to substrates during vertical climbing. Instead, it exhibits primitive characters that maintain plantar rigidity from foot-flat through toe-off, reminiscent of some Miocene apes and Old World monkeys. Moreover, the action of the fibularis longus muscle was more like its homolog in Old World monkeys than in African apes. Phalangeal lengths were most similar to those of Gorilla. The Ardipithecus gait pattern would thus have been unique among known primates. The last common ancestor of hominids and chimpanzees was therefore a careful climber that retained adaptations to above-branch plantigrady.
T
he modern human foot is unique among mammals because it exhibits a series of adaptations that allow it to dissipate kinetic energy during foot strike in walking and running (and thus preserve its structural integrity), and to then transform into a rigid lever for propulsion during toe-off. Until now, the natural history of these adaptations has been shrouded because Australopithecus already exhibits most of them. Ardipithecus ramidus (1) now reveals much more about their evolution. Well-preserved foot elements recovered from the Lower Aramis Member include a talus, medial and intermediate cuneiforms, cuboid, first, second, third, and fifth metatarsals, and several phalanges (2) (Fig. 1). Other Ar. ramidus foot elements are fragmentary and less informative. Here we describe these key foot elements, focusing on their implications for the locomotion of early hominids. Talus. Hominoid tali vary extensively, limiting their value for inferring locomotor habitus (3). Even so, a deep, anteromedially projecting cotylar fossa is frequently generated by habitual tibiotalar contact during extreme ankle dorsiflexion [cartilage modeling; type 4 (4)]. Such morphology is typical of extant African apes and some Miocene hominoid taxa [e.g., KNM-RU 2036 F (5)], but is only minimally expressed in ARA-VP-6/500-023 (Ar. ramidus) and A.L. 2881as (Au. afarensis) (6).
1
Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44240, USA. 2Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA. 3University Museum, University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. 4Rift Valley Research Service, P.O. Box 5717, Addis Ababa, Ethiopia. 5Human Evolution Research Center and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA. *To whom correspondence should be addressed. E-mail:
[email protected]
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Trochlear geometry, absent a calcaneus or distal tibia to provide talar orientation, does not specify foot placement (7), but several characters are possible correlates of talocrural and subtalar mobility. The talar axis angle (fig. S1) (7–9) is both remarkably low and minimally variable in Au. afarensis and other early hominids, consistent with their stereotypically pronounced knee valgus during terrestrial bipedality (10). By contrast, this angle in ARA-VP-6/500-023 lies within the ranges of quadrupedal primates (Table 1). In addition, the flexor hallucis longus groove on the posterior aspect of the talus is both substantially more angulated and more trapezoidal in form (i.e., its superior surface is broader than its inferior), indicating a much greater range of tendon obliquity during locomotion than in A.L. 288-1, in which the groove is both more vertical and more parallel-sided (8). Together, these suggest more knee rotation during stance phase than was likely the case in Au. afarensis (10), even though the Ardipithecus pelvis implies full extension of both the knee and hip during upright gait (11). A prominent tubercle marks the presence of an anterior talofibular ligament in ARAVP-6/500-023. This landmark is absent in African apes but is usually present in Homo sapiens. However, bony evidence of local joint capsule expansion is remarkably variable (12). Medial cuneiform and first metatarsal. ARAVP-6/500-088 is a medial cuneiform (Fig. 2). Although damaged, a portion of its proximal joint surface articulates with the intact intermediate cuneiform (ARA-VP-6/500-075). The firstray metatarsal (Mt1) (ARA-VP-6/500-089) is preserved for its entire length. Its superoproximal surface is intact. This allows direct examination of first-ray abducence (Fig. 2), which was substantial and similar to that shown by extant Pan. As in African apes, the proximal Mt1 facet exhibits substantial spiral concavity for conjunct rotation on the hemicylindrical medial cuneiform facet (13). The ARA-VP-6/500 proximal
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Mt1 base is therefore unlike its counterpart in Australopithecus, in which it is reniform and faces directly distally (14), indicating that it was permanently adducted [(15, 16); for a contrary view, see (17, 18)]. Cuboid. The human midtarsus is much longer than are those of extant African apes. Tarsal elongation increases lever arm length during toe-off (19–21). Elongation of the metatarsals would have also accomplished this goal, but would subject them to frequent midshaft fracture or failure of their tarsometatarsal joints [both are still common in modern humans, and their cause may be as simple as a misstep (22)]. It has been reasonably assumed that the human cuboid is highly derived from a more chimpanzee-like one for powerful plantarflexion during upright walking and running. Indeed, the eccentric placement of the modern human cuboid’s calcaneal process is uniquely derived for enhanced midfoot rigidity during plantarflexion (7, 9). The morphology of the African ape lateral midfoot contrasts greatly with that of humans. Their cuboids, naviculars, and lateral cuneiforms are greatly foreshortened. Associated soft tissues permit substantial laxity at their midtarsal and tarsometatarsal joints (9, 23–27). Such laxity facilitates plantar conformity to substrates during pedal grasping and vertical climbing (9, 28). However, it greatly compromises any plantarflexor torque about their metatarsal heads. The African ape cuboid’s facets for the fourth and fifth metatarsals (Mt4 and Mt5) are, in addition, mildly concave, permitting such potential motion (9, 23, 24). That such morphology is highly derived can be established by the midfoot morphology of Old World monkeys, which rely on plantarflexor torque during above-branch running and leaping—behaviors largely abandoned by great apes. When normalized for body size, the Old World monkey cuboid is longer than are those of African apes (Table 1 and fig. S2). It is therefore notable that the ARA-VP-6/500 cuboid is equally long (Fig. 3). Moreover, its Mt4 facet is sinusoidal (suggesting immobility), and its Mt5 facet is virtually flat (also suggesting immobility). Was Ar. ramidus morphology derived for bipedality from a shortened African ape-like midfoot, or was it primitive? Resolution of this important issue is provided by another character of the Ar. ramidus midfoot that also varies strikingly among extant taxa. The Ar. ramidus cuboid exhibits an expansive facet for an os peroneum: a large sesamoid in the fibularis longus (= peroneus longus) tendon (29, 30). An obvious homolog is virtually constant in humans and Old World monkeys, because both taxa exhibit a constant, prominent underlying articular facet (Fig. 3). However, the os peroneum is usually cartilaginous or only partially calcified in humans, which accounts for routine reports of its absence in radiographic surveys. Both the sesamoid
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Research Articles RESEARCH ARTICLES and its facet are absent in extant great apes (31). The fibularis longus, in whose tendon this ossicle resides, performs substantially different functions in Old World monkeys, African apes, and humans. In Old World monkeys, in addition to adducting the hallux, it is also poised to prevent laxity in the cuboid, Mt4, and Mt5 joints. The mass, location, and breadth of the muscle’s tendon [as judged from its contained os peroneum (Fig. 3)] suggest that it readily resists plantar cavitation of the tarsometatarsal joints, which would dissipate plantarflexor torque. In stark contrast, any supportive function in either African ape has been eliminated along with the os
peroneum, and these taxa exhibit substantial midtarsal laxity even during plantigrade propulsion (9, 23–27, 31). In humans, the fibularis longus tendon supports the longitudinal arch and controls pedal inversion, both critical to successful bipedality [reviewed in (7–9)]. Moreover, the human fibularis longus no longer resides in the cuboid’s prominent groove as it does in Old World monkeys and African apes. Instead, it (and its contained os peroneum) has become relocated more proximolaterally, outside and essentially perched above (in plantar view) the sometimes still-present cuboidal groove (32). The latter likely continues to be generated by retained
A
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Fig. 1. Digitally rendered composite foot of ARA-VP-6/500. (A) Plantar view. (B to D) Dorsal, medial, and anteromedial oblique views, respectively. Better-preserved elements from both sides were assembled as the left foot of Ar. ramidus. Mirror-imaged elements are the talus, cuboid, Mt2 shaft, and some phalanges. The intermediate and terminal phalanges are provisionally allocated to position and side. Note the anteroposteriorly strongly abducent first ray (Fig. 2), elongate cuboid (Fig. 3), and large os peroneal facet located more distolaterally than in Homo. Cuboids of African apes generally lack an os peroneum. Scale bars, 5 cm. Imagery is based on CT scans taken at 50- to 150-mm voxel resolution. 2 OCTOBER 2009
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elements of pattern formation that still underlie cuboid osteogenesis [genetically derived but selectively neutral; type 2B (4)] (33). These are not trivial anatomical shifts in African apes (elimination of the sesamoid) or humans (relocation of the tendon’s pathway). Elimination of the os peroneum in African apes, coupled with the marked anteroposterior shortening of their cuboid, causes the fibularis longus tendon to pass immediately behind and parallel to the axis of their cuboidometatarsal joints (9, 23, 24). This allows substantial plantar conformity to the substrate even during powerful grasping of the great toe by the fibularis longus. In contrast, translation of the tendon posteriorly in derived hominids, along with its new additional attachment to the medial cuneiform, reroutes the tendon’s course so that it crosses the plantar foot more obliquely, thereby improving resistance to flexion in the cuboidometatarsal and especially the cuneiform-metatarsal joints. Both the transverse and longitudinal arches increase the tendon’s moment arm to provide such resistance. Relocation of the os peroneum is thus a morphological signal of the presence of these arches. The elimination of any first-ray abduction in humans has allowed the os peroneum to vary substantially (and become merely cartilaginous), because most of the translation of the tendon has been eliminated by permanent adduction of the great toe. Ar. ramidus morphology is clearly primitive. Its fibularis longus tendon passed over an exceptionally broad, shallow facet underlying what must have been a relatively massive os peroneum similar in size to those of most Old World monkeys (Fig. 3). Its fibularis longus could thus both adduct the great toe and plantarflex the foot, but still aid, to some extent, in support of the cuboidometatarsal joints. Not until an abducent first ray was abandoned could the os peroneum then be relocated as it is in later hominids, thereby enhancing its supportive function. It is notable, therefore, that the os peroneum facet in OH-8 is highly derived in location and morphology (Fig. 3). Navicular. ARA-VP-6/503 is only a small fragment of navicular, but is sufficiently preserved to further illustrate the natural history of the hominid midfoot. Despite its fragmentary condition, it suggests a primitive anteroposterior length intermediate between its homologs in extant African apes and humans. This suggests that there has been substantial midtarsal abbreviation since the common ancestor of gorillas, chimpanzees, and humans (outlined in fig. S3), and subsequent elongation of the midtarsus during hominid evolution. Indeed, a substantial portion of measurable cuboidal elongation in humans can be attributed to proximal extension of its calcaneal process, which is now located more eccentrically to further stabilize the calcaneocuboid joint during toe-off (7). Although the Ar. ramidus cuboid’s calcaneal process is moderately elongate, it retained a primitive, more centroidal position.
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Ardipithecusramidus ramidus Ardipithecus A
G
80 60 40 20
Abduction Angle (degrees) 6/500
B
C
D
F
E
Fig. 2. First-ray abduction in Ar. ramidus. Abduction of the first ray is dependent on soft tissue structures operating about the joint, but can be readily inferred from preserved joint structure. (A) Dorsal view of female gorilla (CMNH-B1801) with Mt1 articulated with the medial and intermediate cuneiforms, showing maximum abduction without joint cavitation. (B) ARA-VP-6/500 articulated in a similar fashion (casts). Note that the two Mt1s differ in axial orientation. This difference may be a consequence of habitual bipedality in Ar. ramidus, which did not exhibit ape-like midtarsal laxity. Abduction is measured as the angle between a tangent to the distal surface of the intermediate cuneiform and the centroidal axis of the Mt1. It is 68° in ARA-VP-6/500. (C and D) CT rendering of ARA-VP-6/500 in similar (C) and exploded (D) views. (E) Approximate posterior, medial, and anterior views of the medial cuneiform. (F) Medial view in dorsoplantar orientation. Although its inferior portion has suffered extensive damage, its posterosuperior portion is intact and articulates perfectly between the intermediate cuneiform and the dorsoproximal joint surface of the Mt1. Note the intact posterior portion of the plateau-like projection of the medial cuneiform’s Mt1 facet distomedially. This is rare in Pan but occasional in Gorilla. Note the nonsubchondral isthmus [white arrow in (C)] separating the two articular facets on the dorsum of the Mt1. These likely record rotation of the proximal phalanx in the MP joint during grasping and terrestrial bipedality (see text). They are notably absent in Au. afarensis but usually present in African apes. Scale bars, 2 cm [(A) to (E)], 1 cm (F). (G) Abduction angle in ARA-VP-6/500, humans, and African apes [N = 15 each taxon; boxes show median, quartiles, and extreme cases in each taxon (asterisk indicates case >1.5 box lengths from quartile box boundary)].
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Lateral metatarsals. ARA-VP-6/1000 is a right Mt2 lacking its head and the plantar portion of its base (Fig. 4). However, both plantar cornua are preserved, thereby permitting reasonable reconstruction of its length. The base is large. The ratio of basal height as preserved (no reconstruction or estimation) to metatarsal length lies in the upper range of Homo (fig. S4). ARAVP-6/1000 exhibits only minimal longitudinal curvature (Fig. 4) but exhibits substantial shaft torsion, which orients it for opposition with the Mt1, as in extant African apes (fig. S5). ARA-VP6/500 lacks an intact Mt2, but its intermediate cuneiform also allows comparison of the joint’s dorsoplantar Mt2 facet height with an estimate of body size. This ratio lies near the upper limit of the human range and outside the ranges of the African apes (fig. S6), suggesting a similarly robust base size in ARA-VP-6/500. The Mt2’s large base is readily explicable in light of its role as the foot’s medial mainstay during bipedal toe-off. The dorsal edge of ARAVP-6/1000’s proximal joint surface exhibits paired chondral invaginations (Fig. 4) that are rare in the Mt2s of either gorillas or chimpanzees [one single (lateral) facet in N = 50]. These cannot reflect habitual contact with the intermediate cuneiform, as this would require impossible joint cavitation. Nor does the intermediate cuneiform of ARA-VP-6/500 or any other higher primate bear matching projections; there are, instead, slight corresponding invaginations of its dorsal surface as well. Each invagination of the Mt2’s dorsal surface lies just proximal to medial and lateral rugosities. In humans, these mark receipt of medial and lateral expansions of the joint’s dorsal capsule [(34); this study]. Habitual, intermittent pressure against these local tarsometatarsal joint expansions almost certainly induced the paired subchondral depressions in the Aramis bone’s dorsal surface. Their probable etiology [chondral modeling; type 4 (4)] is therefore informative. Substantial spiraling of the Mt2 shaft places the bone’s distal end into functional opposition to the Mt1 in African apes and would have done so in Ar. ramidus (35). Such torsion is most pronounced in the Mt2 because it lies adjacent to the hallux, and because Mt2 rotation is restricted by the mortising of its base between the medial cuneiform and lateral cuneiform/Mt3 laterally. The bases of the more lateral rays are less restricted and thus have (progressively) less prestructured torsion. The developmental biology of tendon and ligament attachments is complex (36), but a markedly rugose insertion likely signals substantial Sharpey fiber investment via pattern formation (37). This is especially the case for eutherian tarsometatarsal joints, which appear to have sacrificed their proximal metapodial growth plate to encourage a more rigid syndesmosis (38). The markedly rugose tarsometatarsal joint capsule in the Ar. ramidus Mt2 suggests that it was an adaptation [direct selection acting on
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Research Articles RESEARCH ARTICLES morphogenetic fields; type 1 (4)] to upright walking and running, absent any substantial loadsharing by a still abducent great toe. Moreover, the total morphological pattern of the Ar. ramidus foot suggests that it exhibited a noninverted footflat during midstance [i.e., unlike that of Pan (23–27)]. The primary terrestrial role of the hallux, as in apes, would have been for balance rather than for propulsion (but see below). Powerful fulcrumation occurred only on the lateral metatarsal heads in Ar. ramidus, especially that of the Mt2, whose role in humans remains especially prominent in bipedality even after having been reinforced by the addition of a permanently adducted Mt1. ARA-VP-6/505 is a virtually intact left Mt3 (Fig. 4). Its preserved head shows two particularly important characters. First, it exhibits dorsal doming in excess of African ape metatarsals. Second, a deep-angled gutter isolates the head
from the shaft at the dorsal epiphyseal junction. Although a similar gutter is also found in ape metatarsals, it is considerably shallower, consistent with substantially less loading and excursion during metatarsophalangeal joint (MP) dorsiflexion [cartilage modeling; type 4 (4)]. Moreover, in ARA-VP-6/505, the angle between the head’s dorsoplantar axis and the dorsoplantar axis of its base shows slight external torsion of the shaft, which would have optimized MP joint alignment during toe-off. This implies that growth plate loading during terrestrial bipedality predominated over that generated during grasping (i.e., it exhibits far less torsion than the Mt2, and also lacks the medial and lateral joint capsule compression facets present in ARA-VP-6/1000). The gutter also implies that loading during terrestrial bipedality was applied during substantial toe-out during and after heel-off, coupled with external rotation of the foot during late toe-off. Pro-
A
B
nounced doming is entirely absent in the ARAVP-6/500 Mt1, confirming that the first ray did not participate substantially in propulsion (fig. S12). Doming is present in the Au. afarensis Mt1, again implying terrestrial bipedality with a permanently adducted great toe. The shaft of the ARA-VP-6/505 Mt3 is only slightly curved (Fig. 4) and its base is well preserved, lacking only a minor portion of its superomedial corner. Its base morphology is remarkably similar to that of the human Mt3 in having a dorsoplantarly tall proximal articular surface (Fig. 4 and fig. S7). African ape Mt3 bases are instead regularly subdivided into distinct upper and lower portions by deep semicircular notches of their medial (for Mt2) and lateral (for Mt4) surfaces (Fig. 4 and Table 1). These serve as passageways and surfaces for tarsometatarsal and transverse intermetatarsal ligaments. The abbreviated dorsoplantar height and distinctly rhom-
F
C
Fig. 3. Natural history of the hominoid midfoot. (A) The os peroneum. This sesamoid (white arrow in a ligamentous preparation of Papio anubis) is a large and prominent inclusion in the fibularis longus tendon of Old World monkeys, residing on an appropriately D E large inferolateral facet of the cuboid. In Old World monkeys, the muscle inserts at the Mt1 base, acting as both plantarflexor and hallucal adductor. Because some flexion can occur at both the calcaneocuboid and tarsometatarsal joints during climbing and terrestrial walking (9, 23, 24, 27), the fibularis longus tendon also aids plantar rigidity during plantarflexion. (B to E) Plantar surfaces of hominoid cuboids. (B) Chimpanzee (CMNH-1726). In apes, the cuboid is anteroposteriorly short and the groove in which the fibularis longus tendon lies is narrow and deep, usually with high walls. It is converted to a retaining tunnel by a homolog of the human short plantar ligament (56–58). Ape cuboids essentially lack functional os peronei [they occasionally contain small, nonfunctional, chondral bodies (31)]. (C) ARA-VP6/500-081. In Ar. ramidus the surface medial to the facet over which the tendon must pass is rugose and subperiosteal, confirming that a laterally placed os peroneum elevated its travel on the facet. (D) Human (KSU-01206). (E) OH-8 (cast; reversed). In these later hominids, the fibularis longus no longer lies in the cuboidal groove, but is instead elevated above and posterior to it by the os peroneum residing on a facet located proximolateral on the groove’s proximal wall (white arrows) (32). Unlike Ar. ramidus, the fibularis longus inserts into the medial cuneiform and no longer adducts the first ray. Scale bar, 2 cm. (F) Natural log-log scatterplot of medial cuboid length and cube root of estimated body mass in extant anthropoids (42). A regression line (reduced major axis; y = 1.184x + 1.666; r = 0.836, N = 26) has been fitted to the combined cercopithecines and colobines. The most parsimonious interpretation of these data is that cuboid length in Ar. ramidus is primitive, and that the bone was elongated in later hominids (including elongation of its calcaneal process) but shortened in African apes in order to enhance hallucal grasping and plantar compliance to substrates during vertical climbing. The ranges and medians for a similar metric clarify these relationships in fig. S2. 2 OCTOBER 2009
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Ardipithecusramidus ramidus Ardipithecus boidal form of African ape Mt2 and Mt3 bases [direct selection acting on morphogenetic fields; type 1 (4)] permit more plantar conformity and tarsometatarsal laxity during grasping, consistent with recent observations that the midtarsal break combines motion at both the lateral tarsometatarsal and midtarsal joints (figs. S4 and S6 to S9) (9, 23, 24, 27). ARA-VP-6/505 lacks this distinctive central notching morphology. This presumably reflects retention of soft tissue structures similar to those of humans. These enhance midtarsal and tarsometatarsal bending resistance from foot-flat through toe-off, ultimately culminating in the emergence of the proximal part of the long plantar ligament, which is likely derived in humans (13, 33). These conclusions receive strong support from geometric analysis of joint surface section moduli of the Mt3 (figs. S8 and S9). Phalanges. Several proximal pedal phalanges from the lateral rays of Ar. ramidus preserve a base. Three are complete with proximal ends evincing clear, typically hominid dorsiflexive cants (figs. S10 and S11). Canting is more pronounced in modern humans as a consequence of the reduction of phalangeal curvature (39) (fig. S10) and abbreviation of the intermediate phalanx (figs. S12 and S13). Phalangeal shape ratios (40) are not particularly informative, but they do show that Ar. ramidus phalanges are moderately robust (i.e., like those of Pan and Proconsul and unlike those of Ateles or Hylobates), with moderately deep trochleas. Midshaft robusticity is similar to that in Pan, Proconsul, and most Old World monkeys. Manual/pedal phalangeal ratios are like those in extant hominoids and unlike those in Proconsul [for discussion see (40, 41)]. When complete phalanges from ray 4 of ARA-VP-6/500 are normalized by body size, their lengths fall near the Gorilla mean but below values in Pan, which may have therefore witnessed substantial phalangeal elongation since the last common ancestor of African apes and humans (fig. S13) [for further discussion, see (42)]. Pedal phalanges in Ar. ramidus are relatively shorter than those of New World monkeys
(regardless of locomotor pattern), orangutans, and gibbons. Phalangeal curvature is moderate to large. The included angle of ARA-VP-6/500-094, an intact proximal phalanx of the fourth pedal ray, is 58°. However, its base is substantially canted, which obscures its joint angulation in lateral view. Expansion of the apical tufts of the terminal phalanges is moderate. The first ray during terrestrial gait. The dorsal articular margin of the Mt1 head of ARAVP-6/500 preserves detailed evidence of how Ar. ramidus used its foot in some locomotor settings. Its dorsal surface bears two symmetrically placed and equal-sized V-shaped facets separated by a central nonarticular isthmus (Fig. 3). Each facet appears to have been generated by axial rotation of the ray’s proximal phalanx at its MP joint [cartilage modeling; type 4 (4)]. The Mt1’s dorsolateral facet was presumably generated during grasping by external rotation of both the Mt1 and its proximal phalanx, which would have brought the hallux into opposition with the lateral foot. The Mt1’s dorsomedial facet would then have been generated by internal rotation that occurred when the foot was emplaced on a terrestrial substrate with the first ray in substantial abduction (because it exhibits no doming; see above). This Ar. ramidus morphology is especially notable because of its remarkable symmetry. Although similar rotation facets occur regularly on the Mt1s of both Pan and Gorilla, they are most often asymmetrical and also appear to be generally deeper. In some Gorilla specimens, the medial facet is more prominent than the lateral, which suggests that during terrestrial locomotion, greater relative loads were imposed on its Mt1s than in Ar. ramidus. This would at first seem to be a paradox, because the African apes are not habitual bipeds. However, Ar. ramidus retained primitive features [a prominent os peroneum, substantial tarsometatarsal joint rigidity, a long midtarsus, and soft tissue characters that likely accompanied these (Table 2)] that allowed powerful plantarflexion
about its lateral metatarsal heads, including what must have been a substantial contribution by its peroneal compartment. The African apes, by contrast, have lost such capacity in favor of substantial midtarsal laxity. This has greatly compromised the plantarflexor impulse on their lateral metatarsal heads. Partial accommodation appears to be provided by occasional or even regular impulse by their Mt1 during terrestrial gait. The Mt1s of Australopithecus lack any evidence of comparable facets (15). This, and the prominent doming of their Mt1, now serve as further confirmation that the taxon lacked any first-ray abduction, and almost certainly exhibited a longitudinal arch—features that are consistent with their derived ankle morphology (8, 9, 15, 23, 24) and the Laetoli footprints (43). Interpretations and dynamics. Ar. ramidus is the only known hominid with an abducent great toe (15, 16, 44). Its foot, along with other postcranial elements, indicates that the Late Miocene hominid precursors of Ar. ramidus practiced mixed arboreal and terrestrial locomotion during which the lateral forefoot became extensively adapted to upright walking, even as the medial forefoot retained adaptations for arboreal exploitation. During the gait cycle, fibularis longus contraction would also have stabilized the proximal ankle joints. The moderate to strong talar declination of the angle between the trochlea and that of the ankle’s axis of rotation, in combination with clear evidence of abductor stabilization of the hip during stance phase (11), together suggest that the foot was placed near midline. The knee may have been in greater external rotation than is typical in human and Australopithecuslike (i.e., accentuated) valgus (10), with compensation by means of a more extensive range of knee rotation throughout stance phase. Ar. ramidus therefore may have lacked the consistently elevated bicondylar angle of Australopithecus. Ar. ramidus likely relied on situationally dependent lordosis to generate functional hip abduction (minimum pelvic tilt) during stance
Table 1. Talus, cuboid, Mt1, Mt5, and Mc5 (fifth metacarpal) metrics in Ar. ramidus and other anthropoids. Values in parentheses, except for the leftmost column, denote standard deviation. Taxon (N) Old World monkeys (27) New World monkeys (11) Homo (30) Australopithecus and early Homo (12) ARA-VP-6/500 Pan (26) Gorilla (29) Pongo (16)
Angle between trochlear axis and talocrural rotation axis (°)*
Max. cuboid length†/body size‡
Mt1/body size‡
Mc5/body size‡
Mt5/body size‡
Mc5/Mt5
13.2 (2.2)§
1.51 (0.13) 1.48 (0.12) 1.81 (0.10)
4.4 (0.40) 4.7 (0.22) 3.9 (0.18)
4.2 (0.30) 4.5 (0.85) 2.6 (0.17)
6.6 (0.43) 6.6 (0.14) 4.6 (0.13)
0.73 (0.07) 0.80 (0.06) 0.75 (0.04)
1.41 1.15 (0.06) 1.14 (0.08) 1.18 (0.16)
4.1 4.1 (0.31) 3.6 (0.25) 3.6 (0.22)
3.2 4.3 (0.26) 3.8 (0.24) 5.3 (0.39)
4.9 5.1 (0.07) 4.9 (0.10) 6.7 (0.11)
0.87 1.12 (0.07) 1.02 (0.03) 1.03 (0.05)
10.2 (2.3) 7.4 (1.4) 14.5¶ 15.5 (2.9) 17.8 (2.7)║ 18.4 (3.5)
*Data from (9); Australopithecus and early Homo sample is composed of Stw-102, Stw-363, Stw-486, Stw-88, TM-1517, A.L. 288-1, Omo323-76-898, KNM-ER 813, 1464, 1476, 5428, and OH-8. †In Homo this usually includes the calcaneal process. ‡Body size estimated as equal contributions of the geometric means of metrics of the wrist and talus (42). Old World monkey taxa include Papio, Mandrillus, Macaca, Trachypithecus, Semnopithecus, Colobus, Cercocebus, and Presbytis. New World monkey taxa are Ateles and Alouatta. §Old World monkey taxa for trochlear angle are from Papio (9). ¶See fig. S1. ║Data for Gorilla (9) are a weighted mean for both species.
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A
B
C
D
E
F
G
H
Fig. 4. Metatarsals of Ar. ramidus and extant hominoids, right Mt2 (top) and left Mt3 (bottom). (A) Enlarged CT rendering of dorsal surface of ARA-VP-6/1000. Facets interpreted to be induced by rotation of its base during toe-off and grasping are indicated by arrows. These facets are shown to the right in proximal view [provided to the right in all panels except (E)]. (B) Medial view of entire original specimen (photograph). Although the head is missing, both cornua are preserved, allowing reasonable estimation of original length. Areas of postmortem damage are indicated by hatching. (C) Mt2 of Pan (CMNH-B1718). Note distinctive notching for centrally located tarsometatarsal ligaments. Damage to this area in ARA-VP-6/1000 prevents interpretation of its complete basal form. (D) Modern human Mt2. Proximal surface is superoinferiorly elongate and lacks dorsal facets, consistent with adaptation to bipedality absent an abducent great toe. (E and F) Dorsal (CT) and lateral (photograph) views of ARA-VP-6/505, an Mt3. Hatching shows minor postmortem damage. (G and H) Mt3s of Pan and Homo specimens whose Mt2s are shown in (C) and (D). As is typical of the chimpanzee, the Mt3 shows bilateral notching, although it is not as pronounced in this specimen as in most. Note the striking similarity in the basal morphology of the two hominid Mt3 bases, which suggests that this morphology is likely primitive rather than derived, given the exceptionally great differences in locomotor behavior. CT methods: ARA-VP-6/ 1000, pQCT at 150 mm; ARA-VP-6/505, microCT at 80 mm. Scale bar, 2 cm. 2 OCTOBER 2009
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phase (11). Combined with the pedal characters described here, this suggests a form of primitive terrestrial bipedality in which the foot was emplaced at or only slightly lateral to midline, with the great toe typically in abduction (as often occurs in African apes) and the lateral forefoot in external rotation. Fulcrumation occurred along the oblique axis (fig. S12) and was obviously achieved by the triceps surae, likely substantially aided by a powerful and particularly robust fibularis longus. Balance before and during propulsion was achieved by the opposing actions of (i) a medially emplaced great toe, and (ii) plantarflexion by the fibularis longus, which would also tend to evert the foot. Thus, the lateral compartment must have been very powerful and central to its gait pattern. Indeed, the large os peroneum suggests that once the great toe was restrained by friction against the substrate, contraction of the fibularis longus could further enhance plantarflexion during heel-off through toe-off, while simultaneously maintaining rigidity in the midtarsal and tarsometatarsal joints and preventing inversion induced by substrate disconformities. At the same time, the symmetric rotary facets of the Mt1’s distal joint surface, induced by MP joint motion, suggest that any eversion was prevented by a broadly abducted first ray. Indeed, by the time of emergence of Au. afarensis, hominids had evolved substantially more advanced adaptations to bipedality than were present in Ardipithecus. In the former, the knee had become tibial dominant (10) with accentuated valgus (exceeding even that of modern humans). Hip abduction had been established with a human-like distribution of proximal femoral cortical and trabecular bone (45–47). Moreover, in all known subsequent hominids, the more posterior location and elevation of the os peroneum facet on the cuboid [direct selection acting on morphogenetic fields; type 1 (4)] signals the presence of longitudinal and transverse arches, and thereby the addition of the transverse axis of fulcrumation (fig. S12). The facet’s position in the OH-8 cuboid is virtually human, as is the length of its calcaneal process (Fig. 2). Doming and the simpler unnotched dorsal surface of the Mt1 head characterize both Au. afarensis (A.L. 333-21) (15, 48) and Au. africanus, confirming an immobile first ray with fundamentally human-like propulsion during toe-off (43). The feet of extant African apes are so prehensile that some early anatomists regarded them as hand homologies [reviewed and refuted in (49)]. Compared to the primitive condition of a long midtarsus as seen in taxa such as Proconsul (5), enhanced grasping required the abandonment of forceful plantarflexion on the lateral metatarsal heads in favor of increased plantar laxity at the midtarsal and tarsometatarsal joints. Primitive morphology was replaced by a shortened hindfoot and a talocrural joint modified for enhanced dorsiflexion and inversion. African apes eliminated the os peroneum, plantaris (50), and a
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Ardipithecusramidus ramidus Ardipithecus Table 2. Primitive and derived states of the foot in extant taxa. Extant state
Structure
Primitive*
Old World monkey
Chimpanzee
Gorilla
Human
Thick and dense Separate Fib. to toes 1, 3, 4 Tib. to toes 1, 2, (4), 5
43% 50% (diminutive if present) Minimal Separate Fib. to toes 1, 3, 4 Tib. to toes 2 and 5
Absent 29% (diminutive if present) Minimal Separate Fib. to toes 1, 3, 4 Tib. to toes 2 and 5
90% present Constant with novel medial head Thick and dense Fused Fib. to toes 1, 2, 3 Tib. to toes 2, 3, 4, 5
0.97 (29)
<0.04‡
<0.04‡
0.93+ (30)
Present but with inferior facets
86%§ No inferior facets
80%§ No inferior facets
Probably absent
Absent
Absent
Absent
Absent§ Usually no inferior facets Present
Absent
Absent
Present
Present
Absent
Plantaris (51) Quadratus plantae (51)
Present Present
Constant Constant
Plantar aponeurosis Structure and distribution of long tibial and fibular flexor tendons to digits 1 to 5 (51)† Frequency of an os peroneum‡ Central notching morphology of Mt3
Thick and dense Fused Fib. to toes 1, 2, 3, 4, 5 Tib. to toes 1, 2, 3, 4, 5
See discussions in (29, 30, 55) Present but with inferior facets
Posterior part of long plantar ligament Substantial abbreviation of cuboid length
*The term “primitive” here refers to underived in either African apes or hominids for locomotor patterns established after the last common ancestor of African apes and humans (vertical climbing, suspension, knuckle-walking in African apes, and terrestrial bipedality in hominids). †In humans, the long tibial flexor is termed the flexor digitorum longus and the long fibular flexor is termed the flexor hallucis longus. ‡Presence or absence of an os peroneum based on the presence or absence of an underlying functional facet (31). In samples of N = 25+ for Pan and Gorilla, one definite, human-like, facet was found in Pan [see (31)]. §Current study, N = 25 each taxon.
functional quadratus plantae (51). This character constellation (Table 2) suggests shifts in genes encoding regulatory and signaling molecules modifying fields underlying pedal structure (52). The human plantaris is hardly functional, but its retention and association with the plantar aponeurosis as in Old World monkeys (53) signals retention of primitive features from which specialized aspects [e.g., medial head of the quadratus plantae; posterior part of the long plantar ligament (33)] could have been readily derived under selection for advanced terrestrial bipedality. Hominid morphology has often been presumed to have evolved from ancestral morphotypes like those of extant African apes. Ar. ramidus now establishes that this was not the case. The hominid foot was instead derived from one substantially less specialized. References and Notes
1. T. D. White, G. Suwa, B. Asfaw, Nature 375, 88 (1995). 2. T. D. White et al., Science 326, 64 (2009). 3. C. O. Lovejoy, in Primate Morphology and Evolution, R. H. Tuttle, Ed. (Mouton, The Hague, 1975), pp. 291–326. 4. The trait nomenclature system used here is taken from (47, 54) and is briefly as follows [for more complete explanations, see (2)]. Type 1: traits whose morphogenesis is the direct consequence of pattern formation; usually (but not always) subject to direct selection. Type 2: traits that are genetic but are pleiotropic to, or result from hitchhiking on, type 1 traits and are not themselves subject to selection [2A: parent type 1 is inferred to be under selection but its secondary effects are not; 2B: neither parent trait nor derivative is inferred to be under selection (rare)]. Type 3: resulting from a systemic growth factor. Type 4: epigenetic consequence of osteochondral remodeling and/or response to environmental stimuli, i.e., not heritable but useful in interpreting behavior. Type 5: similar to type 4, but uninformative.
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5. A. C. Walker, M. Pickford, in New Interpretations of Ape and Human Ancestry, R. L. Ciochon, R. S. Corruccini, Eds. (Plenum, New York, 1983), pp. 325–413. 6. D. C. Johanson et al., Am. J. Phys. Anthropol. 57, 403 (1982). 7. V. T. Inman, The Joints of the Ankle (Williams and Wilkins, Baltimore, 1976). 8. B. Latimer, J. C. Ohman, C. O. Lovejoy, Am. J. Phys. Anthropol. 74, 155 (1987). 9. J. M. DeSilva, Proc. Natl. Acad. Sci. U.S.A. 106, 6567 (2009). 10. C. O. Lovejoy, Gait Posture 25, 325 (2007). 11. C. O. Lovejoy et al., Science 326, 71 (2009). 12. C. O. Lovejoy, K. G. Heiple, Nature 235, 175 (1972). 13. O. J. Lewis, Functional Morphology of the Evolving Hand and Foot (Clarendon, Oxford, 1989). 14. Schultz noted that the medial cuneiform-Mt1 joint is “directed more forward and less sidewise in the mountain gorilla than in the other apes” [(20), p. 395]. Our sample contained only “western” specimens (G. g. gorilla). 15. B. Latimer, C. O. Lovejoy, Am. J. Phys. Anthropol. 82, 125 (1990). 16. H. M. McHenry, A. L. Jones, J. Hum. Evol. 50, 534 (2006). 17. R. J. Clarke, P. V. Tobias, Science 269, 521 (1995). 18. K. D. Hunt, J. Hum. Evol. 26, 183 (1994). 19. A. H. Schultz, Symp. Zool. Soc. London 10, 199 (1963). 20. A. H. Schultz, Hum. Biol. 2, 303 (1930). 21. A. H. Schultz, Folia Primatol. 1, 150 (1963). 22. J. T. Campbell, L. C. Schon, in Orthopaedic Surgery: The Essentials, M. E. Baratz, A. D. Watson, J. E. Imbriglia, Eds. (Thieme, New York, 1999), pp. 591–614. 23. J. M. DeSilva, thesis, University of Michigan (2008). 24. J. M. DeSilva, Am. J. Phys. Anthropol. 10.1002/ ajpa.21140 (2009). 25. H. Elftman, J. Manter, Am. J. Phys. Anthropol. 20, 69 (1935). 26. H. Elftman, J. Manter, J. Anat. 70, 56 (1935). 27. E. Vereecke, K. D’Aout, D. De Clercq, L. Van Elsacker, P. Aerts, Am. J. Phys. Anthropol. 120, 373 (2003). 28. J. G. Fleagle et al., Symp. Zool. Soc. London 48, 359 (1981). 29. T. Manners-Smith, J. Anat. 42, 397 (1908). 30. J. M. Le Minor, J. Anat. 151, 85 (1987). 31. In two Pan specimens dissected for this paper, a small cartilage nodule (invisible upon x-ray) could be palpated within the tendon but had no effect on its caliber, nor was
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either accompanied by a facet. This accounts for reports by some earlier anatomists that the sesamoid is present in African apes (although it is clearly present in gibbons, which exhibit regular facets). A recent review (55) concluded an incidence of 2/11 for the os peroneum in apes from classical literature. However, this datum is likely unreliable, because many early authors did not inspect the tendon closely and typically reported its structure “as in humans,” whereas “the few anatomists who have explicitly looked for the [os peroneum] have noted its absence in Gorilla…, Pan troglodytes…, and…Pongo pygmaeus” [(30), p. 93]. Examination of the cuboid is the most reliable standard because a functional os peroneum cannot obtain without an underlying facet, just as the presence of a clearly functional facet assures the ossicle’s presence, whether or not it was calcified. In rare cases, a facet-like discoloration of the bottom of the fibularis longus groove in Pan can be seen. However, the depth and cylindrical nature of the groove make such facets (if in fact they supported an os peroneum during life) largely nonfunctional, and we here report only clearly functional facets. One such human-like facet was found in a Pan specimen in our survey. Interestingly, its associated Mt4 and Mt5 facets suggested hypermobility at these joints far in excess of other Pan specimens. This supports the argument that relocation of the tendon, as in humans, does in fact reduce general midtarsal mobility. 32. M. A. Edwards, Am. J. Anat. 42, 213 (1928). 33. In primates, a fascial sheet spans the plantar aspect of the foot from calcaneus to cuboid, lateral cuneiform, and lateral metatarsal bases, and underlies the fibularis longus tendon in its course to the first ray. In humans this sheet is described as two separate elements, the short and long plantar ligaments. However, in apes the fascial sheet bridges the cuboidal groove, transforming it into a tunnel confining the fibularis longus tendon (56, 57). Old World monkeys have a rough equivalent but retain an os peroneum lateral to the tunnel. In humans, the fibularis longus tendon lies outside (plantar to) the cuboidal groove, and the short plantar ligament terminates proximal to it. A second portion of the sheet, which lies plantar to the tendon, spans it and inserts distally on the lateral metatarsal bases. In humans this is distinguished as the long plantar ligament (57, 58). These human divisions of the plantar sheet are therefore likely derived (13).
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Research Articles RESEARCH ARTICLES 34. R. J. Terry, in Morris’ Human Anatomy, J. P. Schaeffer, Ed. (Blakiston, Philadelphia, 1942), pp. 266–376. 35. We base this simply on torsion of the bone’s diaphysis because its head was not preserved. We have not provided a numerical value because estimating the articular head’s dorsoplantar axis in near-adult (but still unfused) African ape Mt2 growth plates provides only a broadly reliable estimate of the exact angle between the proximal and distal joint axes when the (unfused) head is articulated on its growth plate. 36. X. Chen, C. Macica, A. Nasiri, S. Judex, A. E. Broadus, Bone 41, 752 (2007). 37. A. Zumwalt, J. Exp. Biol. 209, 444 (2006). 38. P. L. Reno, W. E. Horton Jr., R. M. Elsey, C. O. Lovejoy, J. Exp. Zool. B 308, 283 (2007). 39. Considerable debate has centered around the importance of phalangeal shaft curvature in Au. afarensis, largely with respect to its etiology. If developmentally plastic [cartilage modeling; type 4 (4)], then curvature may imply active grasping history. However, if a direct product (or pleiotropic effect) of positional information [types 1 or 2 (4)], then it can be moot with respect to phalangeal function in rapidly evolving species. The fact that curvature increases during maturation does not resolve this issue because increasing curvature during growth is as explicable by positional information as it is by hypothetical strain regimen(s). Current evidence, such as the phalangeal curvature in great ape fetuses, supports a type 1 status. An important element that has long been ignored is phalangeal morphology in Au. afarensis itself (A.L. 333-115); see fig. S11. 40. D. R. Begun, M. F. Teaford, A. Walker, J. Hum. Evol. 26, 89 (1994). 41. M. Nakatsukasa, Y. Kunimatsu, Y. Nakano, T. Takano, H. Ishida, Primates 44, 371 (2003). 42. C. O. Lovejoy et al., Science 326, 70 (2009). 43. T. D. White, G. Suwa, Am. J. Phys. Anthropol. 72, 485 (1987). 44. STW-573 (“Little Foot”) preserves a talus, navicular, medial cuneiform, and Mt1. Its first ray has been described as partially abducent (17, 18). Replacement of its talus and/or navicular with those of either a chimpanzee or human would have had no substantial effect on first-ray abducence; they are not informative. The higher primate medial cuneiform itself is not mobile
45. 46. 47. 48. 49. 50.
51. 52.
and is therefore equally uninformative, save for its Mt1 joint surface. This surface faces distally, is virtually flat, and is therefore immobile in STW-573. The claim that “the first metatarsal facet overflows from distal to proximal, as in apes” [see footnote 18 of (17)] is incorrect, and the dotted line drawn to indicate the proximal extent of the facet in their figure 3B is exaggerated. The joint surface of STW-573 is virtually identical to that of OH-8 and unlike that of any ape. This alone falsifies the contention that the specimen’s hallux was abducent. Indeed, the fibularis longus insertion of STW-573 is described as spanning both the medial cuneiform and Mt1 and therefore cannot have adducted the Mt1 even if it retained any mobility in the first tarsometatarsal joint. C. O. Lovejoy, Gait Posture 21, 95 (2005). C. O. Lovejoy, Gait Posture 21, 113 (2005). C. O. Lovejoy, R. S. Meindl, J. C. Ohman, K. G. Heiple, T. D. White, Am. J. Phys. Anthropol. 119, 97 (2002). C. V. Ward, Yearb. Phys. Anthropol. 119S-35, 185 (2002). T. H. Huxley, Evidence as to Man’s Place in Nature (Williams and Norgate, London, 1863). The plantaris is “normally present in prosimians, monkeys, and man, but is lacking in gibbons and gorillas, nearly all orang-utans, and a considerable percentage of chimpanzees” (53). W. L. Straus Jr., Q. Rev. Biol. 24, 200 (1949). Interpretation of structure frequency requires constant attention to the selective mechanism in play. Narrowly defined (i.e., named) anatomical structures (e.g., long and short plantar ligaments) emerge from mesenchymal fields, which are manifestations of their parent positional information. It is therefore field configuration that is the target of selection. Constant structures within a species (e.g., the Achilles’ tendon) suggest low field variance and intense stabilizing selection. Conversely, substantially reduced frequencies of a “named” tissue mass within a species (e.g., the quadratus plantae in Pan) signal the occurrence of underlying field shifts. These may emanate from selective encouragement of changes in target structures that share field commonality with the reduced structure, simple relaxation of selection, selection against the structure, or some combination of these.
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53. C. G. Hartman, W. L. Straus, The Anatomy of the Rhesus Monkey (Williams and Wilkins, Baltimore, ed. 1, 1933), pp. 1–383. 54. C. O. Lovejoy, M. J. Cohn, T. D. White, Proc. Natl. Acad. Sci. U.S.A. 96, 13247 (1999). 55. V. K. Sarin, G. M. Erickson, N. J. Giori, A. G. Bergman, D. R. Carter, Anat. Rec. 257, 174 (1999). 56. W. L. Straus Jr., Q. Rev. Biol. 5, 261 (1930). 57. D. N. Gomberg, J. Hum. Evol. 14, 553 (1985). 58. H. Gray, Gray’s Anatomy (Lea and Febiger, Philadelphia, ed. 26, 2008). 59. Supported by NSF grants 8210897, 9318698, 9512534, 9632389, 9729060, 9910344, and 0321893 HOMINIDRHOI, and by the Japan Society for the Promotion of Science. We thank the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation; the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the data; the National Museum of Ethiopia, National Museums of Kenya, Transvaal Museum South Africa, Cleveland Museum of Natural History, Royal Museum of Central Africa Tervuren for access to comparative materials; L. Spurlock and P. L. Reno for assistance with dissections and histology preparations; D. Kubo and H. Fukase for assistance in computed tomography (CT) scanning; C. Hernandez for calculation of section modulus data for Mohr’s Circle analyses; M. Brunet, C. V. Ward, and J. DeSilva for cooperation with comparative data; R. Meindl for statistical advice and assistance; J. DeSilva, P. L. Reno, M. A. Serrat, M. A. McCollum, M. Selby, A. Ruth, L. Jellema, S. W. Simpson, and B. A. Rosenman for aid in data collection and exceptionally helpful discussions; and H. Gilbert, J. Carlson, and K. Brudvik for figure preparation.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/72/DC1 Figs. S1 to S14 Tables S1 and S2 References 4 May 2009; accepted 14 August 2009 10.1126/science.1175832
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Ardipithecusramidus ramidus Ardipithecus
The Great Divides: Ardipithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes C. Owen Lovejoy,1* Gen Suwa,2* Scott W. Simpson,3 Jay H. Matternes,4 Tim D. White5 Genomic comparisons have established the chimpanzee and bonobo as our closest living relatives. However, the intricacies of gene regulation and expression caution against the use of these extant apes in deducing the anatomical structure of the last common ancestor that we shared with them. Evidence for this structure must therefore be sought from the fossil record. Until now, that record has provided few relevant data because available fossils were too recent or too incomplete. Evidence from Ardipithecus ramidus now suggests that the last common ancestor lacked the hand, foot, pelvic, vertebral, and limb structures and proportions specialized for suspension, vertical climbing, and knuckle-walking among extant African apes. If this hypothesis is correct, each extant African ape genus must have independently acquired these specializations from more generalized ancestors who still practiced careful arboreal climbing and bridging. African apes and hominids acquired advanced orthogrady in parallel. Hominoid spinal invagination is an embryogenetic mechanism that reoriented the shoulder girdle more laterally. It was unaccompanied by substantial lumbar spine abbreviation, an adaptation restricted to vertical climbing and/or suspension. The specialized locomotor anatomies and behaviors of chimpanzees and gorillas therefore constitute poor models for the origin and evolution of human bipedality.
T
homas Huxley published Evidence as to Man’s Place in Nature (1) only 4 years after Darwin’s On the Origin of Species. Its frontispiece featured a human skeleton and four suspensory adapted apes, each posed upright and each obviously more human-like than any pronograde Old World monkey. By century’s end, Keith was enumerating a cornucopia of characters in support of a brachiationist human past (2). Even our pericardial-diaphragmatic fusion, hepatic bare area, and colic mesenteries were interpreted as adaptations to orthogrady, evolved to tame a flailing gut in the arboreal canopy. Bipedality was simply habitual suspension brought to Earth (3). The “suspensory paradigm” for early hominid evolution was born. Challenges, however, were mounted. Straus enumerated disconcertingly primitive human features in “The Riddle of Man’s Ancestry” (4), and Schultz doubted that brachiation “… opened the way automatically for the erect posture of modern man” [(5), pp. 356–357]. Although withdrawal of the ulna from its primitive pisotriqetral recess was thought to be the sine qua non of suspension (6), a functional equivalent was dis1
Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44242–0001, USA. 2The University Museum, the University of Tokyo, Hongo, Bunkyoku, Tokyo 113-0033, Japan. 3Department of Anatomy, Case Western Reserve University School of Medicine, Cleveland, OH 44106–4930, USA. 44328 Ashford Lane, Fairfax, VA 22032, USA. 5Human Evolution Research Center, and Department of Integrative Biology, 3101 Valley Life Sciences, University of California at Berkeley, Berkeley, CA 94720, USA. *To whom correspondence should be addressed. E-mail:
[email protected] (C.O.L.);
[email protected] (G.S.)
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covered to have evolved in parallel in the wrists of never-suspensory lorisines (7). African ape knuckle-walking (8), considered by many too bizarre to have evolved independently in Gorilla and Pan, came to be viewed in light of emergent molecular phylogenetics (9) as a natural successor of suspensory locomotion—and by some as the almost-certain default engine of bipedality (10). A flood of morphometric analyses appeared to confirm arguments for knuckle-walking hominid ancestors [reviewed in (11)], even though hints of the behavior were also seen in captive orangutans (12). Knuckle-walking was surmised to be a natural consequence of irreversible modifications of the forelimb skeleton to facilitate advanced suspension and vertical climbing (11). It was thereby hypothesized to be an adaptive signal of the first two phases of a deterministic succession leading to bipedality: advanced suspension/vertical climbing → terrestriality/ knuckle-walking → bipedality. A compendium of observations of chimpanzees and bonobos performing upright stance and locomotion followed. Accumulating molecular biology propelled this troglodytian paradigm (conceived as a natural succession to its older, suspensory counterpart) to near-consensus. Chimpanzee-human protein homologies and DNA base sequence comparisons (9, 13–16) established Homo and Pan as likely sister clades [today further confirmed by comparative genomics (17, 18)]. The only question remaining seemed to be whether the bonobo or chimpanzee represented the best living proxy for the last common ancestor (19–22).
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The Chimpanzee model and Australopithecus. The discovery and recognition of the thenprimitive Australopithecus afarensis during the 1970s (23) pushed the hominid record back to 3.7 million years ago (Ma). Although its postcranium was recognized to harbor unusually sophisticated adaptations to bipedality [reviewed in (24)], a feature confirmed by human-like footprints at Laetoli (25, 26), many interpreted these fossils to represent the closing argument for the troglodytian paradigm [see, e.g., (27)]. Only the recovery of earlier, chimpanzee-like fossils from the Late Miocene seemed necessary to complete this scenario [even though newer Australopithecus fossils have led at least one discoverer to doubt a chimpanzee-like ancestry (28)]. Until now, the few available fossils of appropriate antiquity have remained largely uninformative (29–31). The Ardipithecus ramidus fossils from 4.4 Ma Ethiopia are obviously not old enough to represent the chimpanzee/human last common ancestor (CLCA; the older common ancestor of hominids and both Gorilla and Pan is hereafter the GLCA). However, their morphology differs substantially from that of Australopithecus. The Ar. ramidus fossils therefore provide novel insights into the anatomical structure of our elusive common ancestors with the African apes. For that reason, and because of its phylogenetic position as the sister taxon of later hominids (32), this species now provides opportunities to examine both the suspensory and troglodytian paradigms with greater clarity than has previously been possible. Here we first provide evidence of limb proportions, long considered to bear directly on such issues, and then review key aspects of the entire Ar. ramidus postcranium. Comparing the basic proportions and postcranial anatomy of Ar. ramidus (Fig. 1) with those of apes enables us to propose the most probable anatomies of the last common ancestors of Gorilla, Pan, and the earliest hominids. Much of the relevant information on Ar. ramidus is based on the partial skeleton from Aramis (32). Body mass. The geometric means of several metrics of the capitate and talus are strongly related to body mass in extant primates (correlation coefficient r = 0.97; fig. S1), and can be used to estimate body mass in ARA-VP-6/500, as well as in A.L. 288-1. Restricting the sample to large-bodied female hominoids predicts that ARA-VP-6/500 had a mass of about 51 kg. The metrics for A.L. 288-1 fall below those of all extant hominoids. We therefore used the female anthropoid regression to estimate the body mass of A.L. 288-1 (26 kg), which is consistent with previous estimates (33) (table S1). Based on several shared metrics, ARA-VP-7/2, a partial forelimb skeleton (32), was slightly smaller than ARA-VP-6/500 [supporting online material (SOM) Text S1]. Given the apparent minimum body size dimorphism of Ar. ramidus (32, 34), the predicted
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Research Articles RESEARCH ARTICLES body mass of ARA-VP-6/500 serves as a reasonable estimate for the general body mass of Ar. ramidus. Although ARA-VP-6/500 was one of the larger individuals of the Aramis sample (32), it was probably more representative of its species than was A.L. 288-1 [the latter clearly lies at the lower end of the Au. afarensis species range based on larger samples (35)]. Unfortunately, ARA-VP-6/500 tells us little about the body mass of the CLCA and GLCA because these predate Ar. ramidus by wide margins and may have still been primarily arboreal. The limited available (mostly dental and cranio-mandibular) samples indicate that the size of Late Miocene hominids (29–31) was similar to that of Ar.
ramidus (34), and estimated body weight for the 6 Ma Orrorin femoral remains is 30 to 50 kg (36). Although body mass in early Miocene forms appears to have varied greatly (37, 38), it is likely that the CLCA and GLCA were either equal to or smaller than Ar. ramidus, and possibly even substantially so. Only additional fossils can resolve this issue. Limb segment proportions. Radial, ulnar, and tibial lengths can be accurately determined for ARA-VP-6/500 (SOM Text S1). The specimen’s radius/tibia ratio (0.95; fig. S2) is similar to those of generalized above-branch quadrupeds such as the Old World monkey Macaca (0.90 to 0.94; table S2) and the Mio-
Fig. 1. Reconstructed frontal and lateral views of the skeleton of ARA-VP-6/500. Major long-bone lengths were determined directly from preserved skeletal elements (radius, tibia), by crural index (femur), by regression from adjacent elements (ulna), or by ratio and regression (humerus) from a marginally smaller forelimb skeleton (ARA-VP-7/2) via ratios of commonly preserved elements (SOM Text S1). All manual and pedal elements were drawn directly from casts. Pelvis was traced from frontal and lateral computer tomography (CT) scans of reconstructed pelvis (59). Vertebral column and thorax were based on six lumbars, 12 thoracics, and four sacrals (58). No attempt has been made to indicate failure of lateral fusion between the transverse processes of S4 and S5 [i.e., failure of complete closure of either of the fourth sacral foramina (the state preserved in both A.L. 288-1 and KNM-WT 15000)]. Such four-segment sacra may have been modal in Ar. ramidus, but the five-segment form shown here was also a likely variant of high frequency [for discussion, see (59)]. Pectoral girdle and thorax were based on preserved portions of clavicle, first rib, and common elements known in Au. afarensis. Skull and mandible were based on models generated by restoration of cranium using both CT/rapid prototyping and “cast-element-assembly” methods (79). Reconstruction by J. H. Matternes was based on full-scale (life-size) architectural drawings circulated among authors for multiple inspections and comments. Stature (bipedal) is estimated at 117 to 124 cm and body weight at 51 kg. [Illustrations: Copyright 2009, J. H. Matternes] www.sciencemag.org
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cene ape Proconsul heseloni (0.88 in KNM-RU 2036) (38). The ratio is unlike that of African apes (P. troglodytes, 1.11 T 0.04; Gorilla, 1.13 T 0.02) (39) and is, remarkably, 17 standard deviations below that of Pongo (1.47 T 0.03). The Ardipithecus skeleton’s nearly intact tibia allows estimation of femoral length because the crural index (CI: tibia length/femur length × 100) is highly conserved in African apes and humans (5, 40) (81 to 84; SOM Text S1). Tibial length in A.L. 288-1 can likewise be estimated from its effectively complete femur. Although no humerus was recovered for ARA-VP-6/500, one belonging to ARA-VP-7/2 is almost complete and can be used to estimate humerus length in ARAVP-6/500 by simple proportion of shared elements (SOM Text S1). The A.L. 288-1 humerus is intact, and its radius length was previously estimated by regression (41). These data allow calculation of the more familiar intermembral index (IMI; forelimb length/hindlimb length × 100). The IMIs of both specimens resemble those of Proconsul and Old World monkeys (table S3). ARA-VP-6/500 also allows interpolation of other key limb proportions. The brachial indices (BI: radius length/humerus length × 100) of Proconsul, Equatorius, A.L. 288-1, and ARAVP-6/500 are each within the observed range of Pan (fig. S3). It is therefore likely that the BI has remained largely unmodified since the GLCA, especially in light of the relationship of radius length to estimated body mass (fig. S4). In contrast, the BIs of Homo and Gorilla are both derived, albeit by obviously different routes (fig. S3). Humans have greatly shortened radii in conjunction with their novel antebrachial/manual proportions for grasping and manipulation [(41, 42) and see below]; Gorilla appears to have experienced both humeral elongation and possibly slight radial shortening (figs. S4 and S5), most likely to reduce joint stresses at the elbow imposed by the immense mass of adult males. The BIs of Pan and Ar. ramidus are similar (fig. S3), but Pan exhibits a much higher IMI (table S3). Therefore, both Pan and Gorilla have undergone forelimb elongation and hindlimb reduction since the GLCA (table S2 and figs. S4 to S6). The IMIs of hominids appear to have remained primitive until 2.5 Ma (41, 43). The relatively high BI of Pongo reflects its entirely different evolutionary history. Manual anatomy and proportions. Compared to estimated body size, the manual phalanges of Ar. ramidus and Gorilla are long relative to those of the Miocene ape Proconsul (fig. S7). They are relatively even more elongate in Pan, but dramatically abbreviated in Homo. These conclusions are supported by similar calculations using the means of observed body mass (table S3). There is no evidence that the manual phalanges of Au. afarensis were elongated relative to those of Ar. ramidus. In contrast to their manual phalanges, the posterior (medial) metacarpals 2 to 5 (Mc2-5) of Proconsul and ARA-VP-6/500 are substantially
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Ardipithecusramidus ramidus Ardipithecus shorter than are those of any extant ape (figs. S8 and S9). Viewed in the context of relative limb length patterns (see above), as well as the anatomical details of the hand (44), the short Mcs of Ar. ramidus strongly suggest that Pan and Gorilla independently acquired elongate Mcs as a part of an adaptation to vertical climbing and suspensory locomotion. Elongation of Mc2-5 in African apes demanded heightened resistance to torsion and consequent fixation of the carpometacarpal joints within the central joint complex (CJC) (44). The retention of the primitively short Mcs in Ar. ramidus suggests that the GLCA/CLCA also did not have elongate Mcs, and engaged in a form of above-branch quadrupedal locomotion involving deliberate bridging and careful climbing. We hypothesize that this was retained from Middle Miocene precursors of the GLCA. A retained short metacarpus would optimize palmar conformity to substrates, an adaptation later abandoned by extant African apes. The thumb metacarpal of ARA-VP-6/500 was more aptly proportioned for manual grasping than are those of extant apes (figs. S10 and S11) (44). In extant apes, elongation of the posterior (medial) metacarpus may have been achieved by increased expression of Hoxd11 or one of its targets, which do not affect the first ray (SOM Text S2) (42, 45). However, the Mc1 of apes does seem moderately less robust than that of Ar. ramidus, and its soft tissues have undergone substantial involution (4, 42). This suggests that some degree of down-regulation of Hoxd13 may have been responsible for elongation of the posterior (medial) metacarpus. Ar. ramidus greatly illuminates the natural history of the thumb in higher primates. Its robusticity in hominids, while certainly enhanced during the past 3 million years, is nevertheless at least partially primitive. In contrast, in taxa adapted to vertical climbing and suspension, lengthening of the palm has become so dominant as to eclipse some of the thumb’s function, a condition that has reached its apogee in Ateles and, to a lesser extent, large-bodied extant apes. These findings strongly suggest that the target of recently discovered major cis-regulatory modification of gene expression in the first ray (46) was not manual but pedal—it is the human hallux, not our largely primitive pollex, that is highly derived (47). Additional relevant hand anatomy leads to the same conclusions. Ar. ramidus is the only hominid fossil thus far recovered with a metacarpal head reminiscent of the metacarpophalangeal (MP) joint structure seen in many Miocene hominoids [such as Equatorius, Proconsul, Dryopithecus, and Pierolapithecus (48)]. The collateral ligament facets in these taxa colocate with deep symmetric invaginations of the metacarpal head’s dorsum. This morphology is typical of Old World monkeys and is thereby associable with substantial dorsiflexion of the MP joint, an obvious manifestation of their palmigrady. The
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trait is only moderately expressed in Oreopithecus. Modern human and orangutan MP joints are substantially less constricted, and neither taxon exhibits appreciable locomotor-related MP dorsiflexion. Constricted metacarpal head morphology appears to be primitive because it is still partially present in Ar. ramidus, albeit substantially reduced compared to early Miocene hominoids and Old World monkeys. Its retention suggests moderately frequent MP dorsiflexion, a finding consistent with the remarkable adaptations to palmigrady seen in the Ar. ramidus wrist [see below and (44)]. The metacarpal heads of knuckle-walking apes are also somewhat constricted by their collateral facets, but are heavily flattened and broadened to withstand excessive compression during dorsiflexion. Constriction by their collateral ligament facets is therefore only minimal. Moreover, the origins of their collateral ligaments have been substantially expanded volarly, presumably because such positioning improves their capacity to restrict abduction or adduction during MP dorsiflexion imposed by knuckle-walking. Joint flattening enhances cartilage contact and is likely at least partially a cartilage-modeling trait [cartilage modeling; Type 4 (49)]. Loss of MP dorsiflexion in Pongo is readily explicable by its extreme metacarpal and phalangeal elongation and curvature. These can safely be presumed to have eliminated any appreciable functional MP dorsiflexion. Modern humans lack any dorsiflexion because our hand plays no important role in locomotion. The trait is also absent in Au. afarensis, suggesting that either its hand no longer played any role in locomotion, or that such use no longer included an MP dorsiflexive component of palmigrady. The former seems far more likely, given the paramount adaptations to bipedality in the species’ lower limb (24, 50, 51). The primitive metacarpal head morphology within the overall primitive hand anatomy (44) of Ar. ramidus carries obvious implications for reconstruction of GLCA/CLCA locomotion. The unique combination of marked midcarpal mobility, ulnar withdrawal, and moderate MP dorsiflexion in Ar. ramidus, probably mostly primitive retentions, implies that the GLCA/CLCA locomotor pattern was also characterized by some form of arboreal palmigrade quadrupedality, unlike that in any extant descendant great ape. Finally, it is clear now that phalangeal length of Ar. ramidus is not related to suspensory locomotion, but instead reflects a more general grasping adaptation. This renders phalangeal length moot regarding the hypothesis that manual (or even pedal) phalangeal lengths are an active signal of suspensory locomotion in Au. afarensis [contra (52, 53)]. It is more probable that selection had not reduced their length in the younger species, and that such reduction did not occur until selection for tool-making became more intense later in the Pliocene (43, 54). Pedal proportions. Pedal phalangeal evolution appears to have closely paralleled its manual
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counterpart in each clade (compare figs. S7 and S12). However, pedal phalanges of African apes and hominids appear to have been substantially abbreviated, rather than elongated. Functional demands of terrestrial locomotion, perhaps similar to those acting on papionins (which also exhibit pedal phalangeal shortening), are a probable explanation. Pongo represents a marked contrast, with substantial pedal phalangeal elongation. It is thus reasonable to infer that the GLCA/CLCA’s pedal phalanges were longer than those of the partially terrestrial extant African apes and Ar. ramidus. The metatarsus of Ar. ramidus, chimpanzees, and gorillas presents a striking contrast to their metacarpus. Like the foot phalanges, the metatarsals also appear to have been universally shortened in all hominoids subsequent to Proconsul (figs. S13 and S14) (47). The basis of this universal shortening, however, is somewhat unclear, because tarsal evolution contrasts dramatically in hominids and African apes. The modern ape foot has obviously experienced functional reorganization into a more hand-like grasping organ. The Ar. ramidus foot did not. This suggests that substantial elements of a more leverbased, propulsive structure seen in taxa such as Proconsul and Old World Monkeys [robust plantar aponeurosis; retained quadratus plantae; robust peroneal complex (47)] were preserved in the GLCA/CLCA. These structures were sacrificed in both African ape clades to enhance pedal grasping for vertical climbing (55, 56). The moderate shortening of the metatarsus in Ar. ramidus and both African apes may therefore simply reflect negative allometry of metatarsal (Mt) lengths with an increase in body size. The human foot has been lengthened primarily by tarsal elongation (5, 47), presumably because of the likely high failure rate of metatarsal shafts during forceful fulcrumation. In summary, a comparison of the pedal proportions of Ar. ramidus and the extant African apes suggests that the GLCA/CLCA hindlimb remained dominant for body mass support during bridging and arboreal clambering, to the extent that it later proved permissive to bipedality in transitionally terrestrial hominids. Trunk structure. Knowledge of the role of selector genes in early vertebral column formation [especially the role of the Hox code on column differentiation (57, 58)] has advanced our ability to interpret the vertebral formulae of extant hominoids. It now appears that the modal number of lumbar vertebrae in Australopithecus was six, and that a four-segment sacrum was also probably common (57, 58). This axial formula is unlike that of any extant ape. Comparison of the axial columns of extant species further indicates that postoccipital somite number in the GLCA/CLCA was probably either 33 or 34, and that lumbar column reduction occurred independently in chimpanzees, bonobos, gorillas, and hominids. This probably resulted from either transformation of vertebral identities,
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Research Articles RESEARCH ARTICLES or a combination of such transformation and reduction in the number of somites contributing to the lumbosacral region (fig. S15). The most likely vertebral patterns for Ar. ramidus are therefore those also inferred for the GLCA/CLCA and Australopithecus. Pelvic structure indicates that Ar. ramidus retained a primitive spine. Its iliac and acetabular regions establish not only that it was habitually bipedal when terrestrial, but also that this was achieved by combining situational anterior pelvic tilt to accentuate substantial lordosis during upright walking (59). Such rotation placed the still partially primitive anterior gluteal musculature into a position of functional abduction for single support stabilization. In contrast to Ar. ramidus, Au. afarensis is known to have exhibited highly evolved mechanisms of hip abduction, confirmed by the distinctly stereotypic trabecular profile of its femoral neck (24). The Ar. ramidus pelvis retained other elements in common with extant African apes (and presumably the GLCA/CLCA). These include a long, expansive and rugose ischial region and shorter pubic rami (but not a long pubic corpus) (59). The species’ highly flexible lower lumbar column, coupled with its narrower interacetabular distance, still must have provided a moderately reflexive hindlimb for arboreal climbing. Not until hominids became habitually terrestrial bipeds with broad interacetabular distances, reduced and angulated ischial tuberosities (possibly indicating hamstring deceleration of the hindlimb at heel strike), and extremely shortened, flared, and broadened ilia did they then exchange such flexibility for the much more rigid constraints of lower-limb stabilization that characterize Australopithecus (50, 51). The combined pelvic and vertebral data imply that the morphological elements of extant great apes emerged separately rather than in concert. Vertebral column invagination and its associated gracilization of the retroauricular pelvic space preceded specialized iliac modification and the radical lumbar column shortening seen in the African apes (58). The ARA-VP-6/ 500 pelvis shows that hominid ilia shortened and broadened to establish permanent lumbar lordosis. African ape ilia were instead modified to increase abdominal stiffness. The posterior pelvic changes and pronounced lordosis in hominids subsequently promoted even more dramatic vertebral column invagination (60). This trend is eventually reflected in more dorsally oriented transverse processes of hominid thoracic vertebrae compared to those of apes (60). In extant apes, vertebral column invagination and shortening were acquired both independently and noncontemporaneously, the first being a deeply rooted embryogenetic mechanism that posterolateralized the pectoral girdle for a more lateralfacing glenoid; the second, an independent means of increasing abdominal rigidity. We hypothesize that hominids never participated in the second (SOM Text S3), having rather evolved
from a careful climber in which deliberate bridging placed no undue stress on the lower spine. Not until the ancestors of African apes embarked (separately) on their adaptations to vertical climbing and suspension did the lumbar spine undergo its dramatic reduction in length. The last common ancestors. Integration of the data and observations reviewed above allows us to hypothesize about the postcranial adaptations and locomotion of the GLCA and CLCA. The extensive array of highly distinctive specializations seen in modern Gorilla and Pan (in part shared with Pongo) indicates that these are derived features most likely related to vertical climbing and suspension. Not only does Ar. ramidus fail to exhibit these specialized modifications, it exhibits others (e.g., a palmar position of the capitate head that facilitates extreme dorsiflexion of the midcarpal joint rather than its limitation; a robust os peroneum complex limiting plantar conformity to substrates rather than its facilitation) that are effectively their functional opposites. The expression of some of these characters (e.g., capitate head position) is even more extreme than it is in either the Miocene apes preceding Ardipithecus or in Australopithecus that follows. It is therefore highly unlikely that Ar. ramidus descended from a Pan/Gorilla-like ancestor and then (re)evolved such extreme characters. Conversely, some other detailed differences in Pan and Gorilla structure [e.g., scapular form (61), iliac immobilization of lumbar vertebrae (58), appearance of a prepollex (62)] suggest that each of these ape clades independently acquired their anatomical adaptations to vertical climbing and/or suspension. Therefore, we hypothesize that Ar. ramidus retains much of the ancestral GLCA and CLCA character states, i.e., those that relate to abovebranch quadrupedality. In particular, contra Gorilla and Pan, the GLCA carpometacarpal, midcarpal, radiocarpal, and ulnotrochlear joints must have lacked notable adaptations to suspension and/or vertical climbing (44). The GLCA foot seems to have been only partially modified for manual-like grasping. Its hindlimb remained fully propulsive at its midtarsal and tarsometatarsal joints (47). Although its shoulder joint must have been fully lateralized, its lumbar column nevertheless was still long (58) (fig. S15). Its limb proportions were still primitive (see earlier). If body size was as large as in Ar. ramidus, it may have been too large for habitual, unrestricted above-branch quadrupedality, but this remains uncertain. Assuming considerable reliance on arboreal subsistence, it is likely that body mass did not exceed 35 to 60 kg [i.e., combined probable range of Ar. ramidus and 6 Ma Orrorin (36)]. The GLCA picture that emerges, therefore, is one of generalized, deliberate bridging with quadrupedal palmigrady and preference for largediameter substrates. This may have involved either suspension or vertical climbing, but without sufficient frequency to elicit morphological
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adaptations specific to these behaviors. It is likely that these hominoids ranged mostly in the lower canopy, and perhaps were even partially terrestrial. However, their mode of terrestrial locomotion remains unknown. The GLCA therefore represents a foundation for two adaptive paths. Gorilla and Pan independently specialized for both suspension and vertical climbing (and eventually knucklewalking). Gorillas might have acquired larger body size in relation to mixing higher-canopy frugivory with a more terrestrial herbaceous or folivorous dietary component. Lacking definitive fossil evidence, it is currently impossible to determine when the large body mass of Gorilla evolved, but it probably occurred in concert with its more herbaceous diet. The 10 Ma Chororapithecus, which shows incipient signs of Gorilla-like molar morphology (63), may be an early representative of the Gorilla clade. If so, then this clade’s shift toward increased body mass and terrestriality must have occurred early in its phyletic history. The other adaptive pathway retained palmar flexibility, with a short metacarpus that lacked notable syndesmotic restriction. This was combined with retention of an essentially rigid midtarsal joint that was insufficiently flexible to perform vertical climbing (55, 56), but was fully satisfactory for less specialized careful climbing, clambering, and bridging. This is the hypothesized structure of the CLCA, from which Pan would have evolved a greater reliance on vertical climbing and suspension than occurred in the Gorilla clade, never reaching as large a body size. In contrast to Pan, the forebears of Ar. ramidus early in the hominid clade must have relied increasingly on lower arboreal resources and terrestrial zones, without being dependent on higher-canopy resources (such as ripe fruits). From the comparative evidence now available from Ar. ramidus and Pan dental anatomy and isotopes, we posit that the chimpanzee clade increasingly developed a preference for (or dependency on) ripe fruit frugivory, whereas hominids retained a more primitive dental complex adequate for the range of transitional arboreal/ terrestrial resources (34). The likely K-selected demographic adaptation of all hominoids in a setting of almost certain competition with the surging Old World monkey radiation would have been a major factor (64, 65) driving such very different evolutionary trajectories of early African apes and hominids. The earliest fossil evidence for cercopithecid radiation (an early colobine) is now close to 10 Ma (66). A much better record of both fossil hominoids and cercopithecids from the late Middle to early Late Miocene is needed to clarify these suggested patterns of ape-cercopithecid evolution. Orthogrady, suspension, knuckle-walking, and bipedality. Ar. ramidus affords new insights into ape and hominid bauplan evolution
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Ardipithecusramidus ramidus Ardipithecus (Fig. 2 and Table 1). The most fundamental is the clear demonstration that the GLCA lacked the suspensory adaptations long recognized to be common to all extant apes. The chimpanzee and gorilla clades each independently increased their reliance on highercanopy resources, and modified characters originally associable with advanced bridging to those more useful in vertical climbing and suspension. These include an elongated posterior (medial) metacarpus, broadened radiocarpal joint with reduced midcarpal mobility, syndesmotically and morphologically buttressed carpometacarpal joints, expanded long antebrachial flexor tendons, a redistributed long pollical flexor tendon (to the elongated second ray), a modified enthesis for the deltopectoral complex, a retroflexed trochlear notch, elongate forelimbs (44), abbreviated hindlimbs, elimination of the os peroneum complex (47), lumbar column reduction (58), and iliac fixation of remaining lumbars [acquired by iliac elongation and sacral narrowing (58, 59)]. Viewed from the perspective of Ar. ramidus, all of these can now be visualized as having been acquired independently. All represent adaptations related directly to suspension, vertical climbing, and/or knuckle-walking. In African apes, terrestrial travel may have become the primary means of overcoming expanding canopy gaps. A return to partial terrestrial pronogrady would have necessitated compensatory energy-absorptive mechanisms to ameliorate ground reaction in heavily modified forelimbs (which would have suffered an increased risk of injury). Knuckle-walking filled this role because it promotes eccentric contraction and/or energy dissipation (and storage) in the wrist and digital flexors (especially their connective tissue components) during impact loading in a completely extended forelimb, without compromising the animal’s newly acquired adaptations to either suspension or vertical climbing (44). More elaborate mechanisms of negotiating gaps in trees (67) evolved separately in orangutans, in which both manual and pedal rays radically elongated, possibly to more effectively gather and assem-
Homo sapiens
Australopithecus afarensis*
ble multiple lianas necessary to negotiate such gaps. Thus, Ar. ramidus allows us to infer that GLCA anatomy was exaptive for suspension and vertical climbing. Early hominids continued to practice palmigrade, above-branch quadrupedal clambering. Ulnar retraction, common to both Pan and Gorilla, therefore appears to have emerged for forelimb flexibility as part of arboreal clambering and bridging before the GLCA (7), and not as an adaptation to suspension [as has been argued (6)]. Initialized in forms like Proconsul, the combination of enhanced forelimb flexibility and hindlimb propulsive dominance, without anatomical modifications for forelimb suspension, may have reached an apogee in the GLCA. These observations also conform to evidence available from the steadily increasing Miocene hominoid fossil record. European nearcontemporaries of the African CLCA to GLCA exhibited only various degrees of adaptation to suspension, suggesting a separate Miocene trend toward increasing forelimb dominance. At 12 Ma, Pierolapithecus had ulnar withdrawal and partial spinal invagination (68), but likely retained a long lumbar spine. Its hand lacked the degree of metacarpal or phalangeal elongation seen in extant apes. More recent Dryopithecus, which did display both an African ape-like CJC (44) and elongate metacarpals relative to body size, nevertheless retained palmigrady (68, 69). Suspensory locomotion was therefore likely independently derived (minimally) in Dryopithecus, Pan, and Gorilla (and certainly so in Pongo). Hypotheses that hominid ancestry included suspensory locomotion and vertical climbing (52, 53), as projected from electromyographic and kinematic analyses of living ape behavior, are now highly unlikely. From their beginning, accounts of human evolution relied on postural similarities between living humans and apes. The inference that habitual orthogrady was central to the origin of bipedality has been taken as largely self-evident (2, 70). Until now, no fossils of sufficient age
Ardipithecus ramidus*
Pan paniscus
Fig. 2. Branching diagram to illustrate cladistic relationships of extant hominoids. Branching order among the extant forms shown here is well established by molecular evidence. The two fossil forms are possible phyletic ancestors of the human
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and anatomical representation have been available for seriously testing these presumptions. Ar. ramidus requires comprehensive revision of such entrenched, traditional canons. Its anatomy makes clear that advanced orthogrady evolved in parallel in hominids and apes, just as it has in an array of other primates, both living and extinct [including prosimians such as Propithecus and Megaladapis, some ceboids, gibbons, and a variety of Miocene hominoids, especially Nacholapithecus (71), and Oreopithecus (72)]. The long-held view that dorsal transposition of the lumbar transverse processes onto their pedicles implies orthogrady is now falsified, because Ar. ramidus establishes that such relocation is a direct correlate of ventral invagination of the entire spinal column within a context of abovebranch quadrupedal palmigrady that established increased shoulder mobility for bridging and clambering (SOM Text S3). In hominids, from an above-branch quadrupedal ancestry, advanced orthogrady was the independent consequence of terrestrial bipedality made possible by a mobile lumbar spine and largely primitive limbs. It is sobering to consider one profound implication—if emergent hominids had actually become as adapted to suspension or vertical climbing as are living apes, neither bipedality nor its social correlates would likely have evolved. It is therefore ironic that these locomotor modes have played so prominent a role in explanations of bipedality. In retrospect, it seems clear that they would instead have likely prevented it (SOM Text S3). Conclusions. Ar. ramidus implies that African apes are adaptive cul-de-sacs rather than stages in human emergence. It also reveals an unanticipated and distinct locomotor bauplan for our last common ancestors with African apes, one based on careful climbing unpreserved in any extant form. Elaborate morphometric statistical procedures were the culmination of a 20thcentury trend toward objectivity, in which metrics came to be regarded as more informative than careful comparative anatomy—a trend accompanied by too many presumptions and too few
Pan troglodytes
Gorilla gorilla
Pongo pygmaeus
clade, but are shown here in a sister relationship to the extant forms. Circled numbers indicate evolutionary derivations, itemized in Table 1, hypothesized to have occurred on each lineage. [Illustrations: Copyright 2009, J. H. Matternes] SCIENCE
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Research Articles RESEARCH ARTICLES Table 1. Evolutionary derivations of various hominoid clades with fossil and modern representation. Numbers refer to circles on Fig. 2. 1. Basal node. An inferred generalized ancestor of the great ape clade, which lived probably more than 18 Ma. We infer this primate to have been an above-branch palmigrade, plantigrade quadruped, with generalized limb proportions, an anteriorly oriented pectoral girdle, and long lumbar vertebral column with transverse processes located ventrally on their bodies. It would have also been characterized by an extensive postauricular iliac region for a massive erector spinae, a long olecranon process, an anteriorly oriented trochlea, a capitate head located mid-body, and a primitive central joint complex in the wrist. It would have featured a full wrist mortise with pisotriquetral contact and a moderately long midtarsus for fulcrumation on its metatarsal heads. It was presumably tailless (80). 2. Orangutan clade. Dramatic elongation of entire forelimb, posterior (medial) metacarpus and phalanges, extreme elongation of posterior (lateral) metatarsus and phalanges but abbreviation of thigh and leg, partial involution of first pedal and manual rays. Abbreviation of lumbar vertebral column (average four elements) by means of sacralization of lumbar vertebrae, reduction in axial length by two segments, and craniocaudal shortening of lumbar centra (58). Entrapment of caudal-most lumbars by articulation with variable cranial extension of ilia and reduction in breadth of sacral alae. Invagination of spine with posterolateralization of pectoral girdle and reduction of deltopectoral crest. Retroflexion of trochlear notch, extreme abbreviation of olecranon process, and elevation of lateral margin of trochlea. Ulnar withdrawal with elimination of wrist mortise. Modification of central joint complex for torsional resistance during suspension. Frequent postnatal fusion of os centrale and scaphoid. 3. Extant African ape and hominid clade (GLCA). Minor abbreviation of midtarsal length, elongation of manual phalanges, and shortening of posterior (lateral) metatarsus. Invagination of spine with posterolateralization of pectoral girdle, mediolateral proportionality shift of sacroiliac region, craniocaudally shortened vertebral centra, and relocation of lumbar transverse processes to corporopedicular junction or onto pedicle. Abbreviation of olecranon and elevation of lateral margin of trochlea. Ulnar withdrawal with elimination of wrist mortise (i.e., loss of pisotriquetral contact) and deepening of carpal tunnel. Fusion of os centrale to scaphoid. 4. Gorilla clade. Elongation of forelimb (by disproportionate elongation of humerus) and abbreviation of hindlimb (global change in limb proportions), moderate elongation of posterior (medial) metacarpus, moderate shortening of manual phalanges. Abbreviation of lumbar vertebral column (average 3.5 elements) by means of sacralization of lumbars and reduction in axial length by one segment (58). Entrapment of most caudal lumbars by articulation with cranially extended ilia and reduction in breadth of sacral alae. Moderate increase in cranial orientation of scapular spine and glenoid plane, reduction of deltopectoral crest. Retroflexion of ulnar trochlear notch with attendant abbreviation of olecranon process, expansion of long digital flexor (emergence of “flexion tubercle” on ulna), subduction or gracilization of long flexor tendon of thumb to expanded long digital flexor, increased osseo-ligamentous resistance to torque in CJC via distal prolongation of the volar portion of the capitate with corresponding evacuation of the Mc3 base (creating a mediolateral block-to-joint rotation by novel abutment of Mc2 and Mc3), dorsalization and enlargement of capitate head, frequent formation of prepollex (62) on trapezium, anterior relocation of collateral ligament attachments of metacarpophalangeal joints (with simultaneous expansion of attachment facets on metacarpals), expansion of metacarpal heads, reduced capacity for dorsiflexion at midcarpal joint. Introduction of lateral spiral pilaster with loss of third trochanter, elimination of os peroneal complex and substantial shortening of midtarsus, especially proximodistal abbreviation of navicular and cuboid, and abbreviation of dorsoplantar dimensions of metatarsal bases. Gracilization of plantar aponeurosis with loss of plantaris and reduction/elimination of quadratus plantae. 5. Basal chimpanzee/bonobo clade. Elongation of forelimb and abbreviation of hindlimb (global change in limb proportions) but less extreme than in 4. Substantial elongation of posterior (medial) metacarpus and further elongation of manual phalanges. Chimpanzees exhibit higher intermembral index than bonobos and are probably derived in this regard. Abbreviation of lumbar vertebral column (three or four elements) by transformation of vertebral type and/or reduction in axial length by one segment [chimpanzees and bonobos differ substantially in number of axial elements, and bonobo is clearly primitive in this regard (58)]. Entrapment of most caudal lumbars by articulation with cranially extended ilia and reduction in breadth of sacral alae. Further immobilization by novel lumbo-inguinal ligaments (81). Elongation of iliac isthmus. Dramatic mediolateral narrowing of scapula, marked increase in cranial orientation of scapular spine and glenoid plane, reduction of deltopectoral crest (intermuscular fusion?). Retroflexion of ulnar trochlear notch with attendant abbreviation of olecranon process, expansion of long digital flexor (emergence of “flexion tubercle” on ulna), subduction or gracilization of long flexor tendon of thumb to expanded long digital flexor, increased osseo-ligamentous resistance to torque in CJC via distal prolongation of the volar portion of the capitate with corresponding evacuation of the Mc3 base (creating a mediolateral block to joint rotation by novel abutment of Mc2 and Mc3), dorsalization and enlargement of capitate head, elimination of mobility in hamate/Mc4/Mc5 joint, possible gracilization of Mc1, reduced capacity for dorsiflexion at midcarpal joint, reduction and anterior relocation of collateral ligament “grooves” of metacarpophalangeal joints (but expansion of attachment facets on metacarpals), expansion of metacarpal heads. Introduction of lateral spiral pilaster with loss of third trochanter, elimination of os peroneal complex and substantial shortening of midtarsus, especially proximodistal abbreviation of navicular and cuboid, abbreviation of dorsoplantar dimensions of metatarsal bases. Gracilization of plantar aponeurosis with loss of plantaris and reduction/elimination of quadratus plantae. 6. Hominid clade, Late Miocene. Substantial superoinferior abbreviation of iliac isthmus and pubic symphyseal body, increased sagittal orientation and mediolateral broadening of ilium with novel growth plate for anterior inferior iliac spine, introduction of slight (obtuse) greater sciatic notch, (inferred) facultative lumbar lordosis, probable broadening of sacral alae to free most caudal lumbar for lordosis. Possible increased size and robusticity of fibularis longus, increased robusticity of second metatarsal base/shaft and doming of dorsal metatarsal heads related to toe-off. 7. Hominid clade, Mid-Pliocene. Shortening of ischial length and angulation of ischial tuberosity, further mediolateral expansion of iliac fossa with introduction of substantial (acute) greater sciatic notch, further invagination of lumbar vertebral column and fixation of lordosis (no longer facultative). Reduction of thoracic column from 13 to 12 elements associated with reduction in axial length by one segment [or this occurred at 6 (58)]. Elongation of pubic rami and femoral neck. Posterior relocation of third trochanter and emergence of true hypotrochanteric fossa. Elevation of quadriceps attachments to form “true” linea aspera, signaling fundamental shift in knee extensor/hip extensor proportions conducive to primary propulsion by quadriceps. Probable emergence of tibial dominant knee and transverse tibial plafond (or these occurred at 6). Expansion of fibularis longus attachment to include markedly remodeled medial cuneiform and permanent adduction of great toe, elevation of sustentaculum tali to create mediolateral and longitudinal plantar arches, likely development of “spring ligament,” marked inflation of calcaneal tuber (with secondary introduction of distinct lateral plantar process) for energy absorption at heel strike, gracilization of second metatarsal base, relocation of fibularis longus tendon to more proximo-plantar location (with inferred attendant change in short and long plantar ligaments [see (47)] to support novel transverse arch during toe-off and foot-flat, introduction of “dual phase” metatarsofulcrumation (addition of transverse axis to oblique axis of fulcrumation). Dorsalization and expansion of capitate head and broadening of trapezoid for greater palmar span, slight reduction in dorsal mobility of Mc5/hamate joint, anterior relocation and near elimination of collateral ligament “grooves” for metacarpophalangeal joint. 8. Hominid clade, Plio-Pleistocene. Elongation of lower limb, global modification of pelvis to expand birth canal (late) including abbreviation of femoral neck and pubic rami. Reduction of modal lumbar column by one (from six to five typically by sacralization of most caudal lumbar). Slight reduction in glenoid angulation of scapula, increased robusticity of thumb, transfer of styloid body from capitate to third metacarpal, palmar rotation of hamulus, loss of growth plate from pisiform, increased robusticity of terminal phalangeal tufts in carpus. Substantial abbreviation of posterior metacarpus, antebrachium, and carpal phalanges. Substantial anteroposterior thickening of navicular and length and eccentricity of calcaneal process of cuboid. Increased robusticity of Mt1. Reduction in frequency of calcification of os peroneum, abbreviation of tarsal phalanges—especially intermediates.
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Ardipithecusramidus ramidus Ardipithecus fossils. Contemporary morphogenetics now show that organisms as diverse as sticklebacks and fruit flies can display remarkable parallel evolution merely because they share fundamentally similar genomic toolkits (73, 74). Knucklewalking in chimpanzees and gorillas appears now to be yet one more example of this phenomenon. In retrospect, it is impressive that the straightforward cogency of Schultz and the detailed dissections of Straus more accurately predicted the early course of human evolution than the more objective quantitative and technologically enhanced approaches heralded in the last quarter of the 20th century. Recent work in genetics and developmental biology has identified fundamental mechanisms by which morphological structures emerge during evolution. In the study of fossils, such insights have had their primary value as heuristic guides with which to construct and test hypotheses. Understanding the morphogenesis underlying profound shifts in the hominoid bauplan evidenced by Ar. ramidus may take years, perhaps even decades, but is likely to further transform our understanding of human natural history. Ardipithecus has thus illuminated not only our own ancestry, but also that of our closest living relatives. It therefore serves as further confirmation of Darwin’s prescience: that we are only one terminal twig in the tree of life, and that our own fossil record will provide revealing and unexpected insights into the evolutionary emergence not only of ourselves, but also of our closest neighbors in its crown. References and Notes
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20. R. Wrangham, D. Pilbeam, in All Apes Great and Small, vol. 1, African Apes, B. Galdikas et al., Eds. (Kluwer Academic/Plenum, New York, 2001), pp. 5–17. 21. W. C. McGrew, The Cultured Chimpanzee: Reflections on Cultural Primatology (Cambridge Univ. Press, Cambridge, 2004). 22. B. Wood, W. Lonergan, J. Anat. 212, 354 (2008). 23. D. C. Johanson, T. D. White, Science 203, 321 (1979). 24. C. O. Lovejoy, R. S. Meindl, J. C. Ohman, K. G. Heiple, T. D. White, Am. J. Phys. Anthropol. 119, 97 (2002). 25. M. D. Leakey, R. L. Hay, Nature 278, 317 (1979). 26. T. D. White, G. Suwa, Am. J. Phys. Anthropol. 72, 485 (1987). 27. J. T. Stern Jr., R. L. Susman, Am. J. Phys. Anthropol. 60, 279 (1983). 28. R. J. Clarke, S. Afr. J. Sci. 98, 523 (2002). 29. M. Brunet et al., Nature 418, 145 (2002). 30. B. Senut et al., C. R. Acad. Sci. IIA 332, 137 (2001). 31. Y. Haile-Selassie, Nature 412, 178 (2001). 32. T. D. White et al., Science 326, 64 (2009). 33. A. M. W. Porter, Int. J. Osteoarchaeol. 5, 203 (1995). 34. G. Suwa et al., Science 326, 69 (2009). 35. P. L. Reno, R. S. Meindl, M. A. McCollum, C. O. Lovejoy, J. Hum. Evol. 49, 279 (2005). 36. M. Nakatsukasa, M. Pickford, N. Egi, B. Senut, Primates 48, 171 (2007). 37. C. V. Ward, A. Walker, M. F. Teaford, I. Odhiambo, Am. J. Phys. Anthropol. 90, 77 (1993). 38. K. L. Rafferty, A. Walker, C. B. Ruff, M. D. Rose, P. J. Andrews, Am. J. Phys. Anthropol. 97, 391 (1995). 39. P. troglodytes and P. paniscus differ in a number of skeletal proportions and characters (75, 76). Our sample of Pan was limited to P. troglodytes, and our use of the genus nomen Pan herein refers only to P. troglodytes, except where otherwise noted. 40. W. L. Jungers, Nature 297, 676 (1982). 41. P. L. Reno et al., Curr. Anthropol. 46, 575 (2005). 42. P. L. Reno et al., J. Exp. Zool. B Mol. Dev. Evol. 310B, 240 (2008). 43. B. Asfaw et al., Science 284, 629 (1999). 44. C. O. Lovejoy et al., Science 326, 70 (2009). 45. G. P. Wagner, A. O. Vargas, Genome Biol. 9, 213 (2008). 46. S. Prabhakar et al., Science 321, 1346 (2008). 47. C. O. Lovejoy et al., Science 326, 72 (2009). 48. S. Almecija, D. M. Alba, S. Moya-Sola, M. Kohler, Proc. Biol. Sci. 274, 2375 (2007). 49. The trait nomenclature system used here is taken from (77, 78) and is briefly as follows [for more complete explanations, see (32)]. Type 1: traits whose morphogenesis is the direct consequence of pattern formation usually (but not always) subject to direct selection. Type 2: traits that are genetic but are pleiotropic to, or result from hitchhiking on, type 1 traits and are not themselves subject to selection [2A: parent type 1 is inferred to be under selection; its secondary effects are not; 2B: neither parent trait nor derivative is inferred to be under selection (rare)]. Type 3: resulting from a systemic growth factor. Type 4: epigenetic consequence of osteochondral remodeling and/or response to environmental stimuli, i.e., not heritable but useful in interpreting behavior. Type 5: developmentally similar to type 4, but functionally uninformative. 50. C. O. Lovejoy, Gait Posture 21, 113 (2005). 51. C. O. Lovejoy, Gait Posture 21, 95 (2005). 52. J. T. Stern Jr., Evol. Anthropol. 9, 113 (2000). 53. J. T. Stern Jr., R. Sussman, Am. J. Phys. Anthropol. 60, 279 (1983). 54. S. Semaw et al., Nature 385, 333 (1997). 55. J. M. DeSilva, thesis, Univ. of Michigan (2008). 56. J. M. DeSilva, Proc. Natl. Acad. Sci. U.S.A. 106, 6567 (2009). 57. D. Pilbeam, J. Exp. Zool. 302B, 241 (2004).
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58. M. A. McCollum et al., J. Exp. Zool. B Mol. Dev. Evol. 10.1002/jez.b.21316 (2009). 59. C. O. Lovejoy et al., Science 326, 71 (2009). 60. C. V. Ward, B. Latimer, Am. J. Phys. Anthropol. 34 (S12), 180 (1991). 61. Z. Alemseged et al., Nature 443, 296 (2006). 62. J. M. LeMinor, Acta Anat. (Basel) 150, 227 (1994). 63. G. Suwa, R. T. Kono, S. Katoh, B. Asfaw, Y. Beyene, Nature 448, 921 (2007). 64. C. O. Lovejoy, Science 211, 341 (1981). 65. P. Andrews, Cold Spring Harb. Symp. Quant. Biol. 51, 419 (1986). 66. Y. Kunimatsu et al., Proc. Natl. Acad. Sci. U.S.A. 104, 19220 (2007). 67. S. K. S. Thorpe, R. Holder, H. Crompton, Proc. Natl. Acad. Sci. U.S.A. 106, 12646 (2009). 68. S. Moya-Sola, M. Kohler, D. M. Alba, I. Casanovas-Vilar, J. Galindo, Science 306, 1339 (2004). 69. C. O. Lovejoy, Proc. Biol. Sci. 274, 2373 (2007). 70. J. T. Stern Jr., R. L. Susman, Am. J. Phys. Anthropol. 60, 279 (1983). 71. M. Nakatsukasa, Y. Kunimatsu, Evol. Anthropol. 18, 103 (2009). 72. T. Harrison, in Origine(s) de la Bipedie chez les Homindes (Editions du CNRS, Paris, 1991), pp. 235–244. 73. S. Carroll, J. K. Grenier, S. D. Weatherbee, From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design (Blackwell Science, Malden, MA, 2001). 74. M. D. Shapiro, M. A. Bell, D. M. Kingsley, Proc. Natl. Acad. Sci. U.S.A. 103, 13753 (2006). 75. A. L. Zihlman, D. L. Cramer, Folia Primatol. (Basel) 29, 86 (1978). 76. H. J. Coolidge, B. T. Shea, Primates 23, 245 (1982). 77. C. O. Lovejoy, R. S. Meindl, J. C. Ohman, K. G. Heiple, T. D. White, Am. J. Phys. Anthropol. 119, 97 (2002). 78. C. O. Lovejoy, M. J. Cohn, T. D. White, Proc. Natl. Acad. Sci. U.S.A. 96, 13247 (1999). 79. G. Suwa et al., Science 326, 68 (2009). 80. M. Nakatsukasa et al., J. Hum. Evol. 45, 179 (2003). 81. M. D. Sonntag, Proc. Zool. Soc. London 23, 323 (1923). 82. For funding, we thank the U.S. National Science Foundation and the Japan Society for the Promotion of Science. We thank the Ministry of Tourism and Culture, the Authority for Research and Conservation of the Cultural Heritage, and the National Museum of Ethiopia for permissions and facilitation. We thank the Afar Regional Government, the Afar people of the Middle Awash, and many other field workers for contributing directly to the data. We thank the following institutions and staff for access to comparative materials: National Museum of Ethiopia; National Museums of Kenya; Transvaal Museum South Africa; Cleveland Museum of Natural History; Royal Museum of Central Africa Tervuren; and the University of California at Berkeley Human Evolution Research Center. We thank K. Brudvik for illustration and editorial assistance. We thank the following individuals for cooperation with comparative data: M. Brunet and C. V. Ward. We thank R. Meindl for statistical advice and assistance and P. L. Reno, M. A. Serrat, M. A. McCollum, M. Selby, and B. A. Rosenman for aid in data collection and exceptionally helpful discussions.
Supporting Online Material www.sciencemag.org/cgi/content/full/326/5949/73/DC1 SOM Text S1 to S3 Figs. S1 to S15 Tables S1 to S3 References 4 May 2009; accepted 31 August 2009 10.1126/science.1175833
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Reexamining Human Origins in Light of Ardipithecus ramidus C. Owen Lovejoy Referential models based on extant African apes have dominated reconstructions of early human evolution since Darwin’s time. These models visualize fundamental human behaviors as intensifications of behaviors observed in living chimpanzees and/or gorillas (for instance, upright feeding, male dominance displays, tool use, culture, hunting, and warfare). Ardipithecus essentially falsifies such models, because extant apes are highly derived relative to our last common ancestors. Moreover, uniquely derived hominid characters, especially those of locomotion and canine reduction, appear to have emerged shortly after the hominid/chimpanzee divergence. Hence, Ardipithecus provides a new window through which to view our clade’s earliest evolution and its ecological context. Early hominids and extant apes are remarkably divergent in many cardinal characters. We can no longer rely on homologies with African apes for accounts of our origins and must turn instead to general evolutionary theory. A proposed adaptive suite for the emergence of Ardipithecus from the last common ancestor that we shared with chimpanzees accounts for these principal ape/human differences, as well as the marked demographic success and cognitive efflorescence of later Plio-Pleistocene hominids.
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n essential goal of human evolutionary studies is to account for human uniqueness, most notably our bipedality, marked demographic success, unusual reproductive physiology, and unparalleled cerebral and technological abilities. During the past several decades, it has been routinely argued that these hominid characters have evolved by simple modifications of homologs shared with our nearest living relatives, the chimpanzee and bonobo. This method is termed referential modeling (1). A central tenet has been the presumption (sometimes clearly stated but more often simply sub rosa) that Gorilla and Pan are so unusual and so similar to each other that they cannot have evolved in parallel; therefore, the earliest hominids must have also resembled these African apes (2, 3). Without a true early hominid fossil record, the de facto null hypothesis has been that Australopithecus was largely a bipedal manifestation of an African ape (especially the chimpanzee). Such proxy-based scenarios have been elevated to common wisdom by genomic comparisons, progressively establishing the phylogenetic relationships of Gorilla, Pan, and Homo (4). Early Australopithecus. Although Australopithecus was first encountered early in the last century (5), its biology was only slowly revealed. In the 1970s, abundant earlier Australopithecus fossils began to emerge in eastern Africa. These samples broadened our understanding of the genus and included partial skeletons (6) and even footprint trails [the latter extending our knowledge to 3.75 million years ago (Ma)] (7).
Department of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44242–0001, USA. E-mail:
[email protected]
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To many, these fossils were consistent with chimpanzee-based referential scenarios. Bipedality had long been argued to have occurred when early hominids ventured onto the expanding savannas and grasslands of the Pliocene (8, 9). More recently, bipedality is seen to have emerged from African ape behaviors, including feeding postures (10, 11), gorilla dominance displays (12), and even vertical climbing (13). Many mechanical/behavioral models have been proposed to explain the evolution of hominid bipedality, but most have presumed it to have evolved from a chimpanzee-like ancestor (4, 14, 15). A primary problem with these scenarios has been the remarkably advanced postcranium of early Australopithecus, which exhibits particularly advanced adaptations to upright walking (16–18). Ardipithecus ramidus. Ardipithecus ramidus now reveals that the early hominid evolutionary trajectory differed profoundly from those of our ape relatives from our clade’s very beginning. Ar. ramidus was already well-adapted to bipedality, even though it retained arboreal capabilities (19–25). Its postcranial anatomy reveals that locomotion in the chimpanzee/human last common ancestor (hereafter the CLCA) must have retained generalized above-branch quadrupedality, never relying sufficiently on suspension, vertical climbing, or knuckle walking to have elicited any musculoskeletal adaptations to these behaviors (26–28). Moreover, Ardipithecus was neither a ripefruit specialist like Pan, nor a folivorous browser like Gorilla, but rather a more generalized omnivore (19, 25). It had already abandoned entirely the otherwise universal sectorial canine complex (SCC), in which the larger, projecting upper canine is constantly honed by occlusion against the lower third molar of anthropoid primates (25),
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demonstrating that the large, projecting, interlocking, and honing male canines of apes had been eliminated before the dawn of the Pliocene and before the emergence of the dentognathic peculiarities of Australopithecus. What’s more, it appears to have been only slightly dimorphic in body size (25). Finally, the environmental context of Ardipithecus suggests that its primary habitat was not savanna or grassland, but instead woodlands (26–28). In retrospect, clues to this vast divide between the evolutionary trajectories of African apes and hominids have always been present. Apes are largely inept at walking upright. They exhibit reproductive behavior and anatomy profoundly unlike those of humans. African ape males have retained (or evolved, see below) a massive SCC and exhibit little or no direct investment in their offspring (their reproductive strategies rely primarily on varying forms of male-to-male agonism). Although they excel at some cognitive tasks, they perform at levels qualitatively similar to those of some extraordinary birds (29, 30) and mammals (31). The great apes are an isolated, uniquely specialized relict species surviving today only by their occupation of forest refugia (32). Even their gut structure differs substantially from that of humans (33). How and why did such profound differences between hominids and African apes evolve? Why did early hominids become the only primate to completely eliminate the SCC? Why did they become bipedal, a form of locomotion with virtually no measurable mechanical advantage (34)? Why did body-size dimorphism increase in their likely descendants? These are now among the ultimate questions of human evolution. We can, of course, only hypothesize their answers. Nevertheless, by illuminating the likely morphological structure and potential social behavior of the CLCA, Ar. ramidus now confirms that extant African ape– based models are no longer appropriate. Adaptive suites. An alternative to referential modeling is the adaptive suite, an extrapolation from optimization theory (35). Adaptive suites are semiformal, largely inductive algorithms that causally interrelate fundamental characters that may have contributed to an organism’s total adaptive pattern. One for the horned lizard (Phyrnosoma platyrhinos) of the southwesten U.S. serves as an excellent example (Fig. 1) (36, 37). For this species, the interrelation between a dietary concentration on ants and its impact on body form imply, at first counterintuitively, that elevation of clutch size and intensification of “r” strategy (maximize the number of offspring by minimizing paternal care) are the ultimate consequences of this specialization (35–37). Such character and behavioral interdependencies can have profound consequences on evolutionary trajectory, as demonstrated by the equally notable differences in clutch size in the common leopard frog (3500 to 6500 eggs) versus those of numerous species of so-called poison dart frogs
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Ardipithecus ramidus [typically less than 30 eggs; Table 1 (38)]. To enhance survival of their (as yet) nontoxic offspring, the latter engage in relatively intense male parental investment, a shift that has had a profound adaptive impact on their entire life-history strategy. The effective power of adaptive suites is demonstrable by their explanatory success. A virtually identical character constellation to that of the horned lizard has been discovered in an unrelated Australian ecological vicar, Moloch horridus (37), which is also an ant specialist. Even given such unexpected consilience, however, adaptive suites are obviously speculative, even for living organisms. In addition, for extant species, the processes by which current characters have emerged are also necessarily hidden in the past and, therefore, are no more accessible than for extinct taxa. Nevertheless, adaptive suites can serve as organizational procedures by which to examine evolutionary processes with increasing acumen. Of further benefit is the fact that they often pose novel testable hypotheses that might not have arisen without them. Many key human specializations are related to our reproductive physiology and anatomy; human reproduction is as extraordinary as our dentition, locomotion, and encephalization (39). Although it remains possible that such uniqueness emerged only during the Pleistocene, this is less likely in light of Ardipithecus, which shows very early evidence of a major social transformation (25). Moreover, it is the modern African apes that are most derived in many characters, whereas those which are specialized in human evolution (SCC elimination, bipedality) are now known to have been present near the origin of our clade. Our massive brains are obviously a Pleistocene development, but they are also probably sequelae to other major shifts now more fully recorded in the earlier fossil record. It is therefore possible, even likely, that many physiologies and soft tissue features that do not fossilize may have also evolved early in hominid evolution. If so, why were these characters exaptive to our advanced cognition and singular demographic success? Notwithstanding the revelations now provided by Ardipithecus, it should be noted that extensive studies of African apes and other primates have provided likely details of the sociobehavioral context from which hominids most likely first emerged (1, 11). These details were presumably present in the last common ancestor we shared with the African apes, and they almost certainly included aspects of great ape demography and social behavior, including male philopatry (males remain in their natal group), female exogamy (females transfer from natal group at sexual maturity), and prolonged inter-birth intervals, all cardinal characters of an intense “k” (maximized parental care of few offspring) reproductive strategy (32, 40). Moreover, investigations of the behavior of other living primates now provide a wealth of information that allows many contextual details of earliest human evolution to be reasonably hypothesized.
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Fig. 1. Adaptive suite of the horned lizard. An adaptive suite summarizes functional interrelations among physiological, locomotor, dietary, and reproductive characters. One is shown here for Phrynosoma platyrhinos. Horned lizards are ant specialists and thus consume copious amounts of indigestible chitin. This requires a large stomach–to–body mass ratio, which in turn generates the lizard’s unusual tanklike body form. The latter eliminates flight as an effective predator response, and selection has therefore replaced rapid flight (typical of sympatric lizards) with armor and crypsis (e.g., camouflage). These require motionlessness for long periods, which has generated a tolerance for high variance in body temperature, exceeding that of other sympatric lizards. Motionlessness also relaxes selection against large clutch size (which is very large in P. platyrhinos); self-weighting by large clutches in sympatric lizards does not occur because it reduces flight speed [(35), relevant background data available at http://uts.cc.utexas.edu/~varanus/pubs.html]. Table 1. Some differential effects of mating strategy on life-history variables in two amphibians. Character or behavior
Dart frogs*
Leopard frogs†
Clutch size (eggs) Longevity (years) Male egg attendance Male tadpole transport Female provisioning
4–30 13–15 yes yes yes
3500–6500 6–9 no no no
*Data from (37).
Sperm competition. Two key factors dominate anthropoid reproductive behavior and are therefore diagnostic of socio-sexual structure: (i) sperm competition and (ii) male-to-male competition for mates. Various anatomical correlates distinguish monogamous or single male primates from other species whose males engage in sperm competition. Among the most obvious is the much higher ratio of testes volume to body mass. Human ratios are generally similar to those of monogamous gibbons and solitary orangutans, but the ratios are three times higher in Pan (41, 42)
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†Data from (114).
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and other sperm-competing species such as Brachyteles (43). Moreover, human testes are most similar to those of gibbons with respect to their higher proportion of intertubular (nonseminiferous) tissue (42). Mammalian sperm competition is generally accompanied by elevated ejaculate quality (44), which is also notably poor in humans. In Homo sapiens, the absolute rate of sperm production is only about 20% that of much smaller rhesus macaques (45). Another measure, spermatogenesis efficiency (daily sperm production per gram of testes), “varies from about 2.65 ×
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Ardipithecus ramidus 107 in rabbits to <0.06 × 106 in humans” (46). The estimated corresponding value in chimpanzees is greater than that of humans by two orders of magnitude (42). The muscular coat of mammalian vasa deferentia can reasonably be regarded as a correlate of sperm transport rate during sexual stimulation. It is substantially thicker in chimpanzees than in humans or orangutans (47). The seminal vesicles of some monogamous primates are inconspicuous, whereas those of multimale (i.e., ovulating females usually mate with multiple males) macaques and chimpanzees are large; those in humans are only of moderate size (39). Whatever the social caveats may be, human ejaculatory rates (along with those of the monogamous genera Aotus and Symphalangus) are lower than those of 20 primate species (including Pan and Gorilla) by one order of magnitude (48, 49), and human sperm counts decrease at ejaculation frequencies of >4 per week (50). Human sperm midpiece volume, which reflects mitochondrial density and motility, falls in the lowest quartile of 21 primate species examined (51). Especially important is the coagulating reaction between some seminal proteins and prostate vesiculase (52). This coagulum, which blocks penetration of competing sperm by forming a vaginal plug, characterizes primates that robustly spermcompete (e.g., Ateles, Brachyteles, Macaca, Pan). This reaction is absent in humans and common marmosets, whose ejaculates are merely gelatinous (53). The structures of semenogelins I and II (SEMGI and SEMGII) (primary plug coagulates) illuminate the natural history of vaginal plugging. SEMGI suggests a selective sweep in chimpanzees and conversion to a pseudogene in gorillas; humans exhibit neither (52). Together, these data strongly suggest that the social structure in earlier hominids is unlikely to have been typically multimale. This conclusion is supported by recent analyses of primate immune systems, which compared basal white blood cell counts among primates with respect to the likely number of sexual partners as determined by social system (female mating promiscuity). Results showed that “humans align most closely with the [single male] gorilla ... and secondarily with … [the] monogamous gibbon” [(54), p. 1170]. Humans have the least complex penis morphology of any primate. Complexity is generally associated with multimale social structure (47), and humans lack keratinous penile surface mechanoreceptors that may promote rapid ejaculation that is common in many primates. Finally, humans are the only catarrhine without an os baculum (39). Competition for mates. If they did not spermcompete, did early hominid males instead compete for single or near-solitary control of female groups? The cardinal indicator of male-to-male agonism in hominoid primates is the SCC. It is regularly employed during both territory defense and dominance disputes. Hominids are often
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Research Articles characterized as having reduced canine dimorphism (55). Such reduction is only a secondary consequence of the primary hominid character, which is elimination of the SCC in its entirety. The SCC is not male-limited; that is, it is always expressed in both sexes of all anthropoids, even in species with reduced dimorphism (e.g., some New World atelines). Although females may express the SCC for advantage in conflicts with other females, they principally express its underlying structure themselves because amplification in their male offspring (presumably by androgens or reduced estrogens) enhances their fitness. Hylobatid canine monomorphism is sometimes erroneously confused with that of hominids, but gibbons evolved amplification of the female canine. Ar. ramidus shows that elimination of the SCC in hominids is unique among all higher primates and occurred long before Australopithecus. A frequent explanation of canine reduction (and bipedality) is that hand-held weapons replaced the SCC (56, 57). But if male-to-male agonism had been fundamental to early hominid fitness, what selective agency would have reduced its signature character? Additional human attributes belie the improbability of the weapons argument. An absence of sperm competition in gorillas and orangutans is accompanied by a dramatically reduced testes size and the elimination of a free scrotum (their testes are more judiciously sequestered in a post-penial bulge) (42, 58). In contrast, not only are human scrota more pendulous than even those of chimpanzees (58), but bipedality makes them extraordinarily vulnerable during upright combat (59). It seems illogical to attribute habitual uprightness to weapons that would demand even greater selection for testes sequestration than is present in other primates [which target them with their functional SCCs (60)]. Available evidence now suggests that the loss of the SCC was, as is theoretically most likely, a social adaptation. This evidence, derived from Ardipithecus, includes the following (25): (i) Change in the more socially important upper canine preceded that in the lower, (ii) progressive shape modification made the canine not only smaller but less weaponlike in form, (iii) male canines erupted relatively earlier than in largecanined species with high male-to-male agonism, making this event less likely to have represented a social signal of male maturity, and (iv) all of these changes took place within a dietary context that preceded any of the profound changes seen in later hominid dentitions. Humans are also unique among primates in lacking vocal sacs, which play a major role in the territoriality of all apes. Though there are no current means by which to judge the evolutionary history of the hominoid vocal apparatus (61), it does have potential developmental interactions with basicranial patterning, including an impact on location of the foramen magnum. The dramatic anterior translation of this foramen during
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the Plio-Pleistocene is almost certainly a corollary of cerebral reorganization and/or expansion (62). However, early hominid vocal apparatus reduction may have influenced initial differential trajectories of cranial form, currently only just detectable in P. paniscus and Ar. ramidus (29). Both cerebral reorganization and facial patterning are clearly central elements of that trajectory, and early reduction of vocal tract mass is thus a potential modulating factor, particularly because it is a possible social corollary of loss of the SCC. It has long been argued that Australopithecus was unusually dimorphic in body size, implying a largely single-male group structure, but this hypothesis has been biased by comparisons of temporally and geographically disparate samples (63). Of greater importance are (i) the absence of any useful correlation between body-size dimorphism and social structure in hominoids, because both chimpanzees and gorillas exhibit intense male-to-male agonism but exhibit opposite polarities in skeletal dimorphism (63); and (ii) the fact that male body size in many primates is not associated with competition for mates. Rather, it is equally likely to be an ecological specialization derived from reduced size of females (64) and/or male enlargement by selective agencies unrelated to mate acquisition. In any case, Ar. ramidus now transcends the debates over dimorphism in early Australopithecus because available samples indicate that it was minimally dimorphic, suggesting that this was the primitive hominid condition (19, 25) and that dimorphism increased in later hominids (see below). Reproductive biology of the CLCA. Apes radiated profusely during the Middle Miocene (~16 to 11.5 Ma) yet became largely extinct by its terminus (5.3 Ma), which coincided with the radiation of Old World monkeys (65). The nearly total replacement of great apes by cercopithecids is likely to have been closely associated with advanced K specialization in the former, shared by all surviving hominoids (66, 67). However, in dramatic contrast to all other ape descendants, hominids became remarkably ecologically and geographically cosmopolitan. What reproductive strategy permitted such success? Equally as important, what was the likely reproductive strategy of the species that was immediately ancestral to both the hominid and chimpanzee clades? Advanced K selection must have heavily affected the sociobiology of the earliest hominids. K-driven protraction of life history and increased social adhesion require behaviors that avert inbreeding: either isolation of adults as pairs or female transfer among larger social units (68). The latter proscribes male philopatry (males remain in their natal group) and kin selection (individual fitness is amplified by that of relatives) and greatly reduces female-to-female cooperation and its benefits (e.g., alloparenting), placing at a premium novel mechanisms that can enhance parenting.
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Fig. 2. Emergent adaptive suite in basal hominids. The last common ancestor (LCA) of humans and African apes probably exhibited multimale, multifemale (i.e., females mate with multiple males and vice versa) structure with moderate canine dimorphism and minimal male-to-male agonism, perhaps similar to New World atelines (e.g., Brachyteles), with moderate-to-substantial sperm competition, female transfer (i.e., females leave natal group at maturity), and male philopatry. Here, hominids are hypothesized to have evolved three entirely unique, primary characters (denoted by yellow triangles). Two of these characters, documented in the fossil record, are bipedality and SCC elimination. Modern humans exhibit the third: ovulatory crypsis. Interrelations are hypothesized as follows: (i) transport (object carrying but especially food) leads to habitual bipedality, (ii) female choice of males with limited agonism leads to eclipse of SCC, and (iii) protection against cuckoldry (both sexes) leads to ovulatory crypsis. Two natural sequences generated this adaptive milieu. (Left column) Simple feeding ecology from CLCA to early Ardipithecus and The primitive nature of the craniodental and postcranial anatomies of Ar. ramidus suggest that the CLCA, unlike extant African apes, was predominantly arboreal. However, all of its descendants have since developed relatively sophisticated adaptations to terrestrial locomotion (23). What
was the CLCA’s socio-reproductive structure before these events? Whereas African apes have, in the past, almost invariably been selected as CLCA vicars, Ar. ramidus now allows us to infer that they have undergone far too many pronounced and divergent specializations to occupy such a role.
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eventually Au. afarensis. (Right column) The demographic dilemma (32, 79) generated by intensified K selection. A solution for a hominoid confronting such selective forces is elaboration of sex-for-food exchanges observed in chimpanzees and bonobos. These and other elements shared with Pan acted as possible “social catalysts” [highlighted in red (e.g., copulatory feeding, extractive foraging, male-male patrols)]. Increased male body size and enhanced male-to-male cooperation in Au. afarensis reduced mortality during distanceforaging by multiple-male patrols (whose role was optimal foraging rather than territory defense). This culminated in savanna scavenging, primitive lithics for meat acquisition, marrow extraction, and cooperative hunting in Homo. This profound economic shift selected for advanced adaptations to bipedality, further enhanced social cohesion (reduced same-sex agonism in both sexes), increased energy available for parenting (and alloparenting), promoted survivorship and reduced birth spacing, and elevated the selective ceiling acting against metabolically expensive tissues (e.g., the brain).
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Possible alternative vicars are extant, K-selected atelines (New World forms such as spider and woolly monkeys), which exhibit many of the CLCA’s likely socio-reproductive characters, including male philopatry, minimal-to-moderate canine dimorphism, moderate–to–possibly intense
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Ardipithecus ramidus sperm competition, regular non-ovulatory based copulation (e.g., Brachyteles), and minimal-tomoderate body-size dimorphism. Minimal maleto-male agonism in some genera probably stems not only from male philopatry, but also from the logistic difficulty of defining and defending exclusively arboreal territories absent special spacing mechanisms and/or dietary adaptations present in related, but less K-adapted genera (e.g., howlers) (69, 70). Exploitation of ground-based resources and terrestrial travel to arboreal ones has encouraged substantial dietary reliance on low herbaceous vegetation in African apes. This has been accompanied by larger home ranges, more intense territoriality, or both. In Gorilla, home range appears to have been secondarily reduced, driven by the body size–dietary axis. These dietary specializations have led to a substantially reduced sex ratio (one to three males per group) and mate guarding in Gorilla, fission/fusion in P. paniscus, and aggressive multimale patrolling, as well as fission/fusion, in P. troglodytes. However, each of these mechanisms substantially discourages male parental investment. Hominids did not evolve any of the highly derived African ape characters associated with intense male-to-male agonism, reliance on nearground and terrestrial herbivory, or arboreal frugivory (25). Moreover, sperm competition appears to be vestigial in humans [e.g., retained pendulous scrotum, no pseudogenization of SEMGI (52)]. Elaborate periovulatory estrus signaling is therefore most likely a Pan specialization evolved to facilitate female transfer vis-àvis extreme group territoriality and a defense against potential infanticide (71, 72), as well as potentially a product of male mate choice in a context of intense sperm competition. Thus, the hominid and African ape clades evolved wholly divergent social, locomotor, and dietary strategies. Whereas some apes appear to have increased their reliance on terrestrial herbaceous vegetation as early as 10.5 Ma (73), the early hominid dentition remained more generalized (22, 25). What unique advantages, then, did bipedality afford only the hominid clade, and how might this unique locomotor pattern be evolutionarily related to elimination of the SCC? Bipedality and the SCC. Parsimony requires that most, if not all, specialized human attributes emerged within an integrated adaptive constellation, presumably in the same manner as trait complexes in other vertebrates. Figure 2 details one possible adaptive suite as it might have emerged at the base of the hominid clade. Facultative bipedality, a generalized dentition, and enamel isotopic data of Ar. ramidus demonstrate that early hominids continued to exploit both terrestrial and arboreal resources, but in a manner wholly different from those used by extant Pan and Gorilla (25). Terrestrial resources are more defensible than arboreal ones (74). Terrestriality has obviously elevated resource warding and extra-group male-
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Research Articles to-male agonism in Pan and in largely singlemale Gorilla. The elimination of the SCC in very early hominids, however, suggests that resource guarding was not feasible. Territories too large for successful defense have numerous correlates (e.g., patchy resources, elevated search time, enlarged core areas, and increased predator risk) (35). Each of these substantially compromises parenting efforts. A unique advantage of bipedality is that it permits food transport over long distances, a behavior not generally feasible for an arboreal or quadrupedal hominoid. Bipedality also facilitates the regular use of rudimentary tools, both as carrying devices and as implements for resource exploitation. In a partially ateline-like social structure (but lacking extreme anatomical adaptations to suspension) coupled with a likely early hominid ecological context, females might readily have employed the frequent Pan strategy of exchanging copulation for important food (11, 75, 76) (e.g., especially valuable meat or fruits high in fat and/or protein), particularly if such items required protracted search time. If obtained by male exploitation of day ranges logistically too large for territorial defense or for effective optimal foraging by females with dependent infants, such dietary items may have become pivotal (77). The role of tools has, of course, long been a tempting explanation for upright walking (78). However, it is now known that habitual bipedality evolved millions of years before any evidence of stone tools. Despite the potential facility of crude implements of any kind to improve extractive foraging, it remains unlikely that such simple implements would have, alone, been sufficiently critical to reproductive success to have required adaptations (bipedality) that would have simultaneously restricted access to the equally important arboreal resource base. Moreover, both capuchins and chimpanzees effectively transport tools without any reorganization of their postcrania. On the other hand, the common mammalian and avian strategy of provisioning provides myriad benefits directly associated with reproductive success (32, 79). Females and their offspring enjoy reduced predation risk, and males benefit from intensified mothering of their offspring. In such a context at the base of the hominid clade, temporary pair bonds based on sex-for-food exchanges would have further encouraged copulation with provisioning males, rather than males that relied on dominance or aggressive displacement of competitors abetted by large and projecting canines. Research has confirmed the selective advantages of such exchanges in Pan (11, 80). Even controlling for rank and age, chimpanzee males that practice meat-for-sex exchanges have elevated fitness levels, and provisioning on a long-term basis improves reproductive success, even after controlling for estrous state (81). Preference for a dominant male is an obvious female strategy, but it becomes increasingly less favorable when prolonged subadult dependency
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requires intensified parenting. Under such conditions, survivorship increasingly dominates fecundity. Basal hominid females may have become progressively more solicitous of smaller-canined (and thereby less agonistically equipped) males, particularly if they could encourage such males to habitually target them in preference to other females. Temporary or occasional coupling [including honeymoon pairs (80)] and male choice of particular females for such targeted provisioning would have increased their probabilities of both paternity and subsequent offspring survivorship, which is exceptionally valuable to the reproductive success of both participants. Any mammal species undergoing advanced K modifications must eventually approach a limit at which male parental investment becomes virtually mandatory. Typically, male mammals … do not form bonds with offspring or mates, and their social relationships are characterized by aggressive rather than affiliative behavior. However, in <5% of mammalian species … ecological demands, such as patchy resource distribution, a low population density of females, or increased predation risk, mean that a promiscuous strategy is not possible. In such species, males are monogamous and contribute to offspring care to safeguard their investment in reproduction…. Although it might seem that the evolution of monogamy in males would require a major reorganization of the brain, recent research has shown that the transition from promiscuity to monogamy might have required relatively trivial mechanistic changes (82), p. 562. Late Miocene hominoids probably faced a virtual perfect storm of disparate ecological demands. Increased omnivory elevated search time and exposure to predators. Prolonged lactation amenorrhea made ovulating females increasingly rare because birth spacing was progressively prolonged. What solutions to this dilemma could selection offer? Males might cooperate with kin to aggressively expand their territories and gain greater access to additional reproductive females (e.g., Pan), especially if they developed locomotor skills (vertical climbing) that allowed them to rely on high canopy resources and promoted access to ripe fruit. Alternatively, males might aggressively displace all or most others, even if kin-related, to optimize male-to-female ratios (e.g., Gorilla), especially if diet also permitted minimization of day path length so as to prevent female dispersal during feeding. A third possibility would have been proliferation of sex-for-food exchanges. These would have made provisioning an available solution for both sexes and would have heightened female preference for nonaggressive, provisioning males with which to have repeated copulations. Unlike the circumstances in the first two solutions (Gorilla
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Ardipithecus ramidus and Pan), in which the SCC would have been under positive selection pressure, the SCC would have been under moderate negative selection in such a clade, because canine retention would have discouraged provisioning in favor of retaining agonistic strategies of mate acquisition. Reproductive crypsis: the most unique human character. Elimination of the SCC and the ecological context of Ardipithecus at Aramis, Ethiopia, and earlier sites are consistent with the inference that male provisioning via resource transport (and concomitant terrestrial bipedality) antedated 4.4 Ma. Might such behaviors have first evolved nearer the base of the hominid clade? An obvious issue with the hypothesis outlined above is that Pan males prefer females with prominent signs of active ovulation (estrus). If minimal ovulatory signaling in the earliest hominids was primitive (as it is presumably in Gorilla), why did hominid females not prolong and intensify such signs so as to encourage sex-for-food exchanges? First, the extreme ovulatory-related displays in Pan appear to be derived, because they are associated with comparatively unique molecular signatures of accompanying adaptations (such as proteins necessary for vaginal plugging) absent in other hominoids, as well as appropriately specialized penile morphology. Second, it is unlikely that copulation offered by a female would be rejected by a male—this would be counterproductive given the substantial variability of the primate menstrual cycle and the rarity of hominoid females available for impregnation. Furthermore, habitual provisioning of a target female, even while still lactating for a dependent infant, would still make the repeatedly attendant male most likely to sire any successive offspring upon first reinstatement of ovulatory cycling. The latter point is critical. One of the most frequently cited objections to male provisioning in early hominids is the problem of cuckoldry during times that males would have been separated from a selected mate while in search of food (83, 84). But ovulation in hominoids is an exceptionally rare event, and it probably occurs only after extensive, 3- to 4-year-long periods during which female lactation amenorrhea prevents it. Male provisioning of rarely but obviously fertile females would enhance his fitness by several means: (i) Regular copulation would probabalistically establish an attendant male as the most likely to sire the target female’s succeeding offspring, provided that his mate did not “advertise” her ovulation and/or solicit multiple copulations. (ii) Repeated provisioning would accelerate reinstatement of ovulation by replenishing fat stores depleted by lactation. (iii) Accidental or pathological death of her dependent offspring (a not infrequent event) would also reinitialize ovulation, and selection would obviously favor habituation with nonaggressive males not predisposed to infanticide, which is already unlikely because of philopatry. To prevent cuckoldry, male provisioning within the context of a multimale group there-
RESEARCH ARTICLES fore requires selection of females with reproductive crypsis. That is, males could only succeed by provisioning mates with self-crypsis; they would otherwise be unprotected from female copulation with more dominant/aggressive males while ovulating. Broadly (but not entirely) nonovulatory copulation, as in Brachyteles (69, 70), would permit prolonged exclusivity in operational pair bonds, especially when provisioning males showed preference for females who were not observed to copulate with other males (85). In this context, it is therefore relevant that human females do not externally advertise ovulation [other hominoids exhibit some degree of ovulatory swelling, even if minimal (86)] and also fail to exhibit its substantial physiological self-perception, despite moderately elevated proceptivity during ovulation (39, 87). The neurophysiology of mate choice. Pair bonding is rare among mammals (~5%). A common criticism of an adaptive suite similar to that shown in Fig. 2 is that the transition to such a reproductive strategy would be behaviorally unlikely, even if it did confer the major reproductive benefits detailed above. But the recently discovered relation between brain neurophysiology and mating behavior in mammals may provide a rebuttal. In particular, the expression patterns of the receptors for the neuropeptides oxytocin (OT), arginine vasopressin (AVP), and prolactin (PRL) are now known to substantially influence mating and parenting behaviors (82, 88). Monogamous prairie voles exhibit distinct OT and AVP receptor distributions within the mesolimbic dopaminergic reward pathway [i.e., ventral tegmental area (VTA), ventral pallidum, and nucleus accumbens]. This is the central corridor that is activated in human cocaine addiction, and the transient actions of OT within this pathway are critical to establish mothering behavior in nonmonogamous females. Both OT and AVP are released centrally during sexual stimulation. Their receptors, abundantly expressed in critical brain areas of monogamous prairie voles (but only minimally so in polygynous montane voles), are activated in concert with dopamine release. This promotes associative relations with other neural signaling, especially stimuli emanating from the olfactory bulb, affecting the medial nucleus of the amygdala, and resulting in the formation of a pair bond. Because OT receptor up-regulation in the ventral forebrain occurs before parturition and mediates mother-to-infant bonding, this pathway has probably been co-opted as a means of encouraging monogamy, given the probable homology of mammalian neuroendocrine circuitry in both sexes (89, 90). AVP receptor distributions in monogamous marmosets (91, 92) and titi monkeys (93), as well as in polygnous rhesus macaques (94), parallel those observed in monogamous and promiscuous voles, respectively, confirming that this reward pathway functions similarly in primates. Although receptor distributions such as those now available for some monkey species are not yet available for
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humans, there are marked parallels in other related cerebral phenomena revealed by functional magnetic resonance imaging (see also below). Brain activity patterns in women who looked at photographs of men with whom they were in love “looked remarkably similar to those observed after cocaine or m-opiod infusions with heavy activation of the VTA and striatal dopamine regions” [(88), p. 1053]. As predicted, similar patterns were evoked by photographs of their children. PRL concentrations, also involved in the reward pathway, are strongly up-regulated in both rodents and callitrichid males exhibiting paternal care, but not in species lacking it; PRL is elevated in human males immediately before the birth of their first child (95). Equally notable is the impact of steroid hormones on paternal behavior in rodents and primates, including humans. Testosterone concentrations are suppressed in males by parturition in species with extensive paternal care, including numerous rodents, callitrichids, and humans. Such reductions may prevent aggression toward infants. Estradiol and progesterone, critical to normal maternal behavior, have not yet been surveyed in nonhuman primate males but are known to be elevated in human fathers (96). An early hominid adaptive suite. On the basis of their relatively advanced states in Ardipithecus, two of the three primary characters unique to hominids (bipedality, loss of SCC) probably extend well back into the Miocene, perhaps almost to the time of the CLCA. The emergence of these characters in combination is consistent with a strategy of increasingly targeted provisioning, as outlined in Fig. 2. Males would benefit from enhanced male-to-male cooperation by virtue of their philopatry, because it would improve not only their own provisioning capacity, but also that of their kin. Foraging could be achieved most productively by cooperative male patrols (homologous to but strategically entirely unlike those of Pan). Provisioning would reduce female-to-female competition by lowering reliance on individual “sub-territories” (as in chimpanzees) and/or resource warding (97) and would improve (or maintain) social cohesion. Fission/fusion of social groups would also be reduced, ameliorating likely novel predation risk and enhancing the stability of core areas. Further musculoskeletal adaptation to terrestrial bipedality would be imposed by the need to carry harvested foods, simple tools for extractive foraging, and eventually altricial offspring lacking pedal grasping capacity consequent to the adoption of permanent bipedality without a substantial arboreal component (as in Australopithecus). The third primary character shown in Fig. 2, female reproductive crypsis, cannot be directly traced in the fossil record. What can we surmise of its evolutionary history? As noted earlier, a central component of reproductive crypsis is the loss of visually prominent mammary gland cycling (i.e., concealed by permanent fat stores that simulate lactating glands) in humans. A common
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Ardipithecus ramidus explanation for permanently enlarged human mammae is that they serve as a male attractant because they may signal adequate fat stores for reproduction (98). But why would an attractant be required when female proceptivity is the only limiting factor acting on all other primate males (no matter what the underlying social system)? Again, as noted earlier, the elaborate periovulatory sexual swellings of Pan are an integral component of intense sperm competition, which hominids clearly lack. Moreover, whereas the loss of mammary cyclicity would be unlikely to evolve in Pan [copulation with lactating females is rare (99)], crypticism would not be a barrier in a context of copulatory vigilance within pair bonds (32, 79). Moreover, elimination of cyclicity would protect a provisioning (and thereby heavily invested) male from cuckoldry, because prominent mammaries would discourage interest by extra-pair males. The absence of cycling would simultaneously protect females from potential abandonment (79). An element of human reproductive crypsis not discussed earlier is the reduction of a male’s capacity to detect ovulation via olfactory signaling. It is again difficult to ascertain why selection would directly favor a precipitous loss in olfactory capacity. Yet the loss of olfactory receptors has occurred in the human lineage at a much faster rate than in other higher primates (100, 101) and is fully explicable as a product of female choice acting within the context of a provisioning strategy. If males could detect ovulation in this manner, provisioning would almost certainly have accompanied such detection, just as it does in Pan when ovulation is so acutely advertised. Ovulatory crypsis would therefore be a key element in maintaining targeted provisioning by a particular (pair-bonded) male. These kinds of unique, reproductively related characters are often broadly ascribed to an intensification of human social behavior during the Pleistocene (by largely undefined selective mechanisms) or have simply been ignored. But why should we simply presume that these various soft tissue structures and physiologies were not present in Australopithecus, or even in Ardipithecus, particularly when the latter shows that the CLCA was not morphologically or behaviorally chimpanzee-like? Relegating these derived characters to Homo almost certainly requires each to be assigned causation in near total isolation. One of the instructive aspects of adaptive suites is the demonstration of what must almost always be a complex network of character interaction, even in reptiles and amphibians. More often than not, such interconnectivity is likely to far exceed relatively simplistic arguments such as somatic budgeting. Viewing the sweep of hominid evolution in retrospect, it is increasingly unlikely that upright walking, elevation of skeletal dimorphism (in Australopithecus) despite simultaneous elimination of the SCC, loss of vocal sacs, precipitous reduction in olfactory receptors, development of
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Research Articles permanently enlarged mammary glands, loss of ovulatory-based female proceptivity, precipitous reduction in male fertility, unique maintenance of a pendulous scrotum despite substantial reduction in testes size, proliferation of epigamics (sexrelated traits used for male selection) in both sexes [implying mate choice in each (32, 79)], and unparalleled demographic success in a terrestrial primate have all been incidental and unrelated. These are far more likely to be multiple elements within a unique reproductive strategy that allowed early hominids to thrive relative to their ape relatives and could have ultimately accommodated rapid development of the unusually energythirsty brain of subadults in emergent Homo. Yet a large brain is not our most unique characteristic. Chimpanzees have relatively larger brains than cercopithecoids, which have relatively larger brains than lemurs. However, the combination of SCC elimination, habitual bipedality, and reproductive crypsis (each in itself an extreme rarity) is unique among all known mammals. Conversely, simple brain enlargement is readily explicable in myriad ways. If, for example, the acquisition and control of fire was somehow a causative factor, as has recently been suggested (102), what relations does this singular capacity have to the broad array of other entirely unique human characters that are known to have preceded it in the fossil record? Moreover, does the marked expansion of the human brain itself not signal a unique reproductive strategy rather than a simple physical character or capacity? Among the apes, hominids alone were successful before the major cultural advances of the Pleistocene, and Oldowan stone tools persisted unchanged for almost 1 million years. The molecular and cytological records suggest that hominid cerebral evolution extends deep into time, as extrapolated from the likely evolutionary progression in genes such as abnormal spindle-like microcephaly associated gene (ASPM) (103). The reconstructed history of its evolution suggests marked acceleration “along the entire lineage from the last ape ancestor to modern humans … [implying that] the human phenotype did not arise abruptly … but [is] instead the consequence of a lengthy and relatively continuous process” [(104), pp. 491–492]. Conclusion. As Au. afarensis was progressively revealed during the 1970s, its anatomy and antiquity still permitted a possible chimpanzeelike CLCA. Many models of human origins, largely referential, employed this perspective. Previous nonreferential attempts (32, 79) argued that only major changes in the social behavior of Au. afarensis and its ancestors could satisfactorily account for its unique combination of postcranial anatomy and unusual demographic success. The tempo and mode of such hypothetical earlier evolutionary events, however, have remained shrouded from our view. This has led to rejection of the hypothesis by many who preferred the comparative comfort and safety of more referential accounts.
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Even as its fossil record proliferated, however, Australopithecus continued to provide only an incomplete understanding of hominid origins. Paradoxically, in light of Ardipithecus, we can now see that Australopithecus was too derived— its locomotion too sophisticated, and its invasion of new habitats too advanced—not to almost entirely obscure earlier hominid evolutionary dynamics. Now, in light of Ar. ramidus, there are no longer any a priori reasons to suppose that acquisition of our unique reproductive anatomy and behavior are unconnected with other human specializations. The evidence is now conclusive: Elimination of the SCC occurred long before the eventual dentognathic hypertrophy of Australopithecus, and long before the likely horizon at which sufficient reliance on tool use would have encouraged abandonment of food and/or safety in the arboreal substrate. It is far more likely that our unique reproductive behavior and anatomy emerged in concert with habituation to bipedality and elimination of the SCC (Fig. 2). It is also now equally clear that Pan’s specialized reproductive constellation has been driven by an entirely different locomotor and dietary history. We currently know very little about the postcranium of hominids older than Ar. ramidus (e.g., Sahelanthropus, Orrorin) (105, 106). More fossils will further advance our understanding of the CLCA, and we anxiously await their discovery. Meanwhile, the opportunity of devising adaptive suites for both species of Pan and for Gorilla—grounded in hypotheses generated in light now thrown on the gorilla/chimpanzee/ human last common ancestor and CLCA by Ar. ramidus as to their locomotion, diet, and social behavior—is an intriguing prospect whose alternative outcomes will probably provide additional revelations. When viewed holistically, as any adaptive suite requires, the early hominid characters that were probably interwoven by selection to eventually generate cognition now seem every bit as biologically ordinary as those that have also affected the evolution of lizards, frogs, voles, monkeys, and chimpanzees. Comparing ourselves to our closest kin, it is somewhat sobering that the hominid path led to cognition, whereas that leading to Pan, our closest living relatives, did not, despite the near-synonymy of our genomes. As Darwin argued, the ultimate source of any explication of human acumen must be natural selection (78). The adaptive suite proposed here provides at least one evolutionary map by which cognition could have emerged without reliance on any special mammalian trait. The perspective offered by Ardipithecus suggests that our special cognitive abilities derive from a unique earlier interplay of otherwise commonplace elements of locomotion, reproductive biology, neurophysiology, and social behavior. In retrospect, we are as ordinary as corvids (107) and voles (108), although we are much more
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Ardipithecus ramidus fortunate, if self-cognition is deemed fortunate. We should never have doubted Darwin in his appreciation that the ultimate source of our matchlessness among mammals would prove commonplace when knowledge became sufficiently advanced. Ar. ramidus now enhances that knowledge. Even our species-defining cooperative mutualism can now be seen to extend well beyond the deepest Pliocene. References and Notes
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