SPECIAL FEATURE: PERSPECTIVE PERSPECTIVE SPECIAL FEATURE: Neither chimpanzee nor human, Ardipithecus reveals the surprising ancestry of both Tim D. Whitea,1, C. Owen Lovejoyb, Berhane Asfawc, Joshua P. Carlsona, and Gen Suwad,1 aDepartment of Integrative Biology, Human Evolution Research Center, University of California, Berkeley, CA 94720; bDepartment of Anthropology, School of Biomedical Sciences, Kent State University, Kent, OH 44242–0001; cRift Valley Research Service, Addis Ababa, Ethiopia; and dThe University Museum, The University of Tokyo, Hongo, Bunkyo-ku Tokyo 113-0033, Japan Edited by Neil H. Shubin, University of Chicago, Chicago, IL, and approved September 10, 2014 (received for review April 25, 2014) Australopithecus fossils were regularly interpreted during the late 20th century in a framework that used living African apes, especially chimpanzees, as proxies for the immediate ancestors of the human clade. Such projection is now largely nullified by the discovery of Ardipithecus. In the context of accumulating evidence from genetics, developmental biology, anatomy, ecology, biogeography, and geology, Ardipithecus alters perspectives on how our earliest hominid ancestors—and our closest living relatives—evolved. human evolution | Australopithecus | hominid | Ethiopia “...the stock whence two or more species have chimpanzees, can serve as adequate repre- (5). Indeed, a widely used textbook still pro- sprung, need in no respect be intermediate sentations of the ancestral past. claims that, “Overall, Au. afarensis seems very between those species.” much like a missing link between the living Background T. H. Huxley, 1860 (1) Africanapesandlaterhomininsinitsdental, ’ Darwin s human evolution scenario attemp- cranial, and skeletal morphology” (6). Charles Darwin famously suggested that ted to explain hominid tool use, bipedality, Australopithecus can no longer be legiti- Africa was humanity’s most probable birth enlarged brains, and reduced canine teeth (2). mately viewed as a short-lived transition be- continent, but warned that without fossils, it It easily fit the fossil record of his day, when tween apes and humans. Rather, it represents was “...useless to speculate on this subject” Homo only a few Neanderthals were known. an adaptive plateau occupied for ∼3Maby (2). Nevertheless, Darwin and his less cau- erectus Austral- was found in the 1890s, and up to four species lineages of small-brained tious contemporaries and intellectual descen- opithecus in the 1920s. Both were rejected as African bipeds. Many assumed that when dants used humans and modern apes to hominids by eminent authorities, but two pre-afarensis fossils were eventually re- triangulate ancestral anatomy and behaviors, grades of human evolution were eventually covered they would increasingly resemble which promulgated the erroneous metaphor Australopithecus recognized. comprised chimpanzees. Today “conventional wisdom” of a hominid “missing link.” Even today, de- different species of small-brained but bi- continues to reflect the deeply held assump- spite thousands of available fossils, this deeply pedal Pliocene primates. Homo was its tion that Australopithecus is close to some embedded metaphor reinforces the mis- descendant. imagined chimpanzee-like Miocene ape spe- conceptions that extant apes—particularly In the 1960s molecular data challenged cies. Furthermore, because Australopithecus chimpanzees—can be viewed as “living notions that species lineages of modern apes is often found in open environments, hom- missing links,” or that that modern African and humans could be traced directly to early inid origins are frequently presented as the apes combined can be used to represent the and middle Miocene fossils. The data ulti- tale of a tropical forest ape forced to adapt to past “as time machines” (3). mately resolved the phylogenetic branching open savannas that expanded via global cli- The notion that modern great apes are order among extant great apes and humans. mate change. The new fossils disrupt such little changed from the last common ances- However, without our current appreciation frameworks. tors we shared with them promoted the of the power of regulatory mechanisms, faith assumption that hominid fossils anatomically in simple DNA similarity also helped reify Conventional Wisdom Challenged intermediate between living apes and our- the notion that chimpanzees were appropriate Ardipithecus is a primate that ruptures sev- selves would eventually be found. Now, primitive proxies for hominid ancestors (4). eral deeply held perceptions, particularly Australopithecus afarensis however, long sought and recently discovered During the 1970s those visualizing humans as “just a third African fossils provide escape from such discoveries pushed knowledge back to 3.7 persistent but inaccurate projection. These million years ago (Ma), but even the iconic paleontological discoveries do not yet include “Lucy” differed little from already known Author contributions: T.D.W., C.O.L., B.A., and G.S. designed research; the common ancestor we shared with chim- T.D.W., C.O.L., B.A., J.P.C., and G.S. performed research; T.D.W., C.O.L., South African fossils. The preoccupation B.A., J.P.C., and G.S. analyzed data; and T.D.W., C.O.L., B.A., J.P.C., and panzees (the CLCA). However, they sub- with chimpanzee comparisons led many to G.S. wrote the paper. stantially reveal the early evolution of the argue that Lucy and her conspecifics walked The authors declare no conflict of interest. “ ” hominid clade (the term hominid denoting like apes, without human-like hip and knee This article is a PNAS Direct Submission. all species on the human side of the human/ extension. Thus, despite a host of unique 1To whom correspondence may be addressed. Email: timwhite@ chimpanzee phylogenetic split). These fossils specializations to committed terrestrial bi- berkeley.edu or [email protected]. “ have begun to rectify the mistaken notion pedality, many declared this species ...very This article contains supporting information online at www.pnas.org/ that contemporary apes, in particular common close to what can be called a ‘missing link’” lookup/suppl/doi:10.1073/pnas.1403659111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1403659111 PNAS Early Edition | 1of8 Downloaded by guest on September 29, 2021 species of chimpanzee” (7). Broader aspects ramidus skeleton ARA-VP-6/500 (“Ardi”) However, the abundant colobine monkeys of Australopithecus paleobiology emerged preserves so many anatomical parts—in such andkudusfoundwithArdipithecus were not gradually during the 20th century. In contrast, clear ecological context—that it transforms adapted to open savannas (as evidenced by the Ardipithecus niche was comprehen- our understanding of early hominid evolution. their microwear, mesowear, isotopes, and sively revealed in ∼250 published pages Ardi preserves crucial elements from a postcranial ecomorphology). By analogous of a single issue of Science in 2009 (8). single adult female who died 4.4 Ma on a evidence, neither was Ardipithecus,which Perhaps because Ardipithecus was so sud- broad Ethiopian floodplain supporting grassy maintained a woodland-to-forest adaptation denly revealed in so many dimensions of woodlands. Her hands and feet are extraor- well into the Pliocene. Even the earliest context and anatomy—and is so different dinarily preserved. Less well preserved, but Australopithecus species appears to have re- from Australopithecus—aformof“cognitive nevertheless nearly complete elements of her tained elements of woodland adaptation (16). dissonance” settled over some practitioners of teeth, skull, arms, legs, and pelvis provide Accordingly, despite valiant efforts at its re- paleoanthropology. The condition’ssymp- further informative anatomy. This fossil and surrection (17), the hypothesis that opening toms range from post hoc cautionary advice associated evidence allow assessment of lo- grasslands led to hominid emergence and (9) to speculation (10) or inexplicable omis- comotion, diet, habitat preference, and even bipedality now stands effectively falsified. sion (11). However, Ardipithecus was one social behavior. of the few surviving lineages of the Miocene The remains of well over 100 additional Locomotion ape adaptive radiation: it preserved funda- individuals from Ardi’s species confirm that Living primates display a wide range of lo- mental arboreal adaptations and it exclu- her critical morphologies are not idiosyn- comotor abilities. Primatologists have for de- “ ” sively shares several independent character cratic but characteristic of the species. Fur- cades attempted to parse these into modes, “ ” complexes with all later hominids. This pri- thermore, these additional individuals reveal such as vertical clinging and leaping, “ ” “ ” mate therefore illuminates human and normal variation for several body parts, such quadrupedalism, and brachiation. In char- chimpanzee origins in ways that Austral- as the dentition (SI Text, Note 1; Tables S1– acterizations of postural/locomotor adapta- opithecus never could. S4), allowing, for example, assessment of tions of both living and fossil primates, such The Ardipithecus fossils fortuitously ar- sexual dimorphism. These fossils belong labels are combined with standard postural “ ” rived at an auspicious time in the history of to a stratigraphically associated, geologically designations, such as orthograde (upright “ ” biology, just as revelations of developmental contemporaneous, >7,000-specimen assem- trunk