RESEARCH ◥ the European “dryopith” apes and the Asian REVIEW SUMMARY pongines before 12.5 Ma. Some authors inter- pret dryopiths as stem hominines and support PRIMATE EVOLUTION their back-to-Africa dispersal in the latest Miocene, subsequently evolving into modern Fossil apes and human evolution African apes and hominins. Others interpret dryopiths as broadly ancestral to hominids or Sergio Almécija*, Ashley S. Hammond, Nathan E. Thompson, Kelsey D. Pugh, an evolutionary dead end. Salvador Moyà-Solà, David M. Alba Increased habitat fragmentation during the late Miocene in Africa might explain the evolution of African ape knuckle walking BACKGROUND: Ever since the writings of Darwin views remains at the core of the human ori- and hominin bipedalism from an orthograde and Huxley, humans’ place in nature relative to gins problem. arboreal ancestor. Bipedalism might have al- apes (nonhuman hominoids) and the geo- lowed humans to escape the great ape “special- graphic origins of the human lineage (hom- ADVANCES: There is no consensus on the ization trap”—an adaptive feedback loop inins) have been heavily debated. Humans phylogenetic positions of the diverse and widely between diet, specialized arboreal locomotion, diverged from apes [specifically, the chim- distributed Miocene apes. Besides their frag- cognition, and life history. However, under- panzee lineage (Pan)] at some point between mentary record, disagreements are due to the standing the different selection pressures that ~9.3 million and ~6.5 million years ago (Ma), complexity of interpreting fossil morphologies underlie knuckle walking and bipedalism is and habitual bipedalism evolved early in hom- that present mosaics of primitive and derived hindered by locomotor uncertainties about inins (accompanied by enhanced manipulation features, likely because of parallel evolution the Pan-Homo LCA and its Miocene forebears. Downloaded from and, later on, cognition). To understand the se- (i.e., homoplasy). This has led some authors to In turn, the functional interpretation of Mio- lective pressures surrounding hominin origins, exclude known Miocene apes from the mod- cene ape mosaic morphologies is challenging it is necessary to reconstruct the morphology, ern hominoid radiation. However, most re- because it depends on the relevance of prim- behavior, and environment of the Pan-Homo searchers identify some fossil apes as either itive features. Furthermore, adaptive complexes last common ancestor (LCA). “Top-down” ap- stem or crown members of the hominid clade can be co-opted to perform new functions proaches have relied on living apes (especially [i.e., preceding the divergence between orang- during evolution. For instance, features that http://science.sciencemag.org/ chimpanzees) to reconstruct hominin origins. utans (pongines) and African great apes and are functionally related to quadrupedalism or However, “bottom-up” perspectives from the humans (hominines), or as a part of the modern orthogrady can be misinterpreted as bipedal fossil record suggest that modern hominoids great ape radiation]. European Miocene apes adaptations. Miocene apes show that the represent a decimated and biased sample of a have prominently figured in discussions about orthograde body plan, which predates below- larger ancient radiation and present alternative the geographic origin of hominines. “Kenyapith” branch suspension, is likely an adaptation for possibilities for the morphology and geography apes dispersed from Africa into Eurasia ~16 to vertical climbing that was subsequently co-opted of the Pan-Homo LCA. Reconciling these two 14 Ma, and some of them likely gave rise to for other orthograde behaviors, including habit- ual bipedalism. Catarrhines: Cercopithecoids and hominoids Hominoids: Apes and humans OUTLOOK: Future research efforts on hominin Hominids: Great apes and humans origins should focus on (i) fieldwork in un- on May 6, 2021 Hominins: The human lineage explored areas where Miocene apes have yet to be found, (ii) methodological advances in morphology-based phylogenetics and pale- oproteomics to retrieve molecular data beyond ancient DNA limits, and (iii) modeling driven by experimental data that integrates morphological Old World monkeys Hylobatids Pongo Gorilla Pan Homo and biomechanical information, to test locomo- Pleistocene 0 tor inferences for extinct taxa. It is also impe- ?? ?? Plio- rative to stop assigning a starring role to each 5 new fossil discovery to fit evolutionary scenar- Ardipithecus ios that are not based on testable hypotheses. Early hominins likely originated in Africa ? 10 “Dryopith” apes from a Miocene LCA that does not match any Nakalipithecus Miocene Sivapithecus living ape (e.g., it might not have been adapted 15 specifically for suspension or knuckle walk- ing). Despite phylogenetic uncertainties, fossil Chimpanzee-human “ Nacholapithecus 20 apes remain essential to reconstruct the start- last common ancestor ing point” from which humans and chimpan- zees evolved.▪ Ekembo 25 Million years ago The list of author affiliations is available in the full article online. The evolutionary history of apes and humans is largely incomplete. Whereas the phylogenetic relationships *Corresponding author. Email: [email protected] (S.A.) Cite this article as S. Almécija et al., Science 372,eabb4363 among living species can be retrieved using genetic data, the position of most extinct species remains (2021). DOI: 10.1126/science.abb4363 contentious. Surprisingly, complete-enough fossils that can be attributed to the gorilla and chimpanzee lineages remain to be discovered. Assuming different positions of available fossil apes (or ignoring them owing to READ THE FULL ARTICLE AT uncertainty) markedly affects reconstructions of key ancestral nodes, such as that of the chimpanzee-human LCA. https://doi.org/10.1126/science.abb4363 Almécija et al., Science 372, 587 (2021) 7 May 2021 1of1 RESEARCH ◥ a narrative: Australopithecus remains from REVIEW Chad indicate that early hominins were living ~2500kmwestoftheEastAfricanRift~3.5Ma PRIMATE EVOLUTION (20). Furthermore, if Sahelanthropus is a hom- inin, it would push back the human lineage Fossil apes and human evolution presence in north-central Africa to ~7 Ma (21). Moreover, continued fieldwork efforts in less Sergio Almécija1,2,3*, Ashley S. Hammond1,2, Nathan E. Thompson4, Kelsey D. Pugh1,2, explored areas have shown that hominoids Salvador Moyà-Solà3,5,6, David M. Alba3 lived across Afro-Arabia during the Miocene (22–25). In addition, remains of putative hom- Humans diverged from apes (chimpanzees, specifically) toward the end of the Miocene ~9.3 million to inines have been found in East Africa (26, 27), 6.5 million years ago. Understanding the origins of the human lineage (hominins) requires reconstructing perhaps even in Europe (28, 29). Finally, paleo- the morphology, behavior, and environment of the chimpanzee-human last common ancestor. Modern environmental reconstructions for late Miocene hominoids (that is, humans and apes) share multiple features (for example, an orthograde body plan facilitating apes and hominins suggest that the Pan-Homo upright positional behaviors). However, the fossil record indicates that living hominoids constitute narrow LCA inhabited woodlands, not tropical rain- representatives of an ancient radiation of more widely distributed, diverse species, none of which exhibit the forests (30–33). entire suite of locomotor adaptations present in the extant relatives. Hence, some modern ape similarities Current debates about the transition from might have evolved in parallel in response to similar selection pressures. Current evidence suggests that an ape into a bipedal hominin are centered hominins originated in Africa from Miocene ape ancestors unlike any living species. on the morphological and locomotor recon- struction of the Pan-Homo LCA, as well as its paleobiogeography. Discrepancies are caused Downloaded from n1871,Darwin(1)speculatedthathumans pronograde”) behaviors, with the torso posi- by conflicting evolutionary signals among originated in Africa based on the anatom- tioned vertically (6, 7). Extant ape features also living and fossil hominoids, indicating rampant ical similarities with African apes (gorillas include enhanced joint mobility, long forelimbs “homoplasy” (independent evolution causing I and chimpanzees) identified by Huxley relative to hindlimbs, and (except gorillas) long “false homology”), and are further complicated (2). However, Darwin urged caution until hands with high-to-very-high finger curvature by the highly incomplete and fragmentary — – more fossils became available the European (8 10). The orthograde body plan is generally nature of the hominoid fossil record. This http://science.sciencemag.org/ Dryopithecus was the only recognized fossil interpreted as a suspensory adaptation (11, 12), review argues that, despite the limitations, ape at the time (3). After 150 years of con- or as an adaptation for vertical climbing sub- the information provided by fossil apes is tinuous discoveries, essential information about sequently co-opted for suspension (13). essential to inform evolutionary scenarios of human origins remains elusive owing to debates Based on similarities between chimpanzees human origins. surrounding the interpretation of fossil apes and gorillas, a prevalent evolutionary model (Figs. 1 and 2). argues that African apes represent “living Evidence as to humans’ place in nature Genomic data indicate that humans and fossils” and that knuckle-walking