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Primate evolution – in and out of Africa

1998; Elsevier BV; Volume: 8; Issue: 21 Linguagem: Inglês

10.1016/s0960-9822(07)00476-9

1879-0445

Michael M. Miyamoto, Timothy S. Young, Carol V. Ward, Adrienne L. Zihlman, Jerold M. Lowenstein, Colin P. Groves, Herbert H. Covert, Caro‐Beth Stewart, Todd R. Disotell,

Genetic diversity and population structure

Stewart and Disotell [[1]Stewart C-B Disotell TR Primate evolution – in and out of Africa.Curr Biol. 1998; 8: R582-R588Abstract Full Text Full Text PDF PubMed Google Scholar] have controversially proposed that the hominoid lineage dispersed from Africa to Eurasia about 20 million years ago, and that the common ancestor of human, chimpanzee and gorilla returned to Africa within the past 10 million years. Their model relied on the phylogeny shown in Figure 1a to estimate the minimum number of migrations under two different scenarios: dispersals only from Africa to Eurasia (scenario A); or dispersals in both directions (scenario B). Scenario B is strongly supported by the phylogeny because it requires only two dispersals to explain the distributions of extant and fossil hominoids. Scenario A invokes a minimum of six dispersals to explain hominoid distributions. This phylogeny was derived by synthesis of molecular data for living hominoids and morphological data for both extant and fossil groups. The hominoid phylogeny of Begun et al. [[2]Begun DR Ward CV Rose MD Events in hominoid evolution.in: Begun DR Ward CV Rose MD Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations. Plenum Press, New York1997: 389-415Crossref Google Scholar] was emphasized, as it incorporated 240 cranial and post-cranial characters for the same extant and fossil genera as considered by Stewart and Disotell. Relationships among extant hominoids are well established and not in dispute [[3]Goodman M Porter CA Czelusniak J Page SL Schneider H Shoshani J et al.Toward a phylogenetic classification of primates based on DNA evidence complemented by fossil evidence.Mol Phylogenet Evol. 1998; 9: 585-598Crossref PubMed Scopus (519) Google Scholar], but many questions persist about the positions of the extinct genera, because of the fragmentary nature of their morphological data (Figure 1). To what extent is the controversial model of Stewart and Disotell based on an unreliable estimate of hominoid phylogeny [[4]Gibbons A New study points to Eurasian ape as great ape ancestor.Science. 1998; 281: 622-623Crossref Google Scholar]? To address this question, we have re-analyzed the 240 morphological characters of Begun et al. [[2]Begun DR Ward CV Rose MD Events in hominoid evolution.in: Begun DR Ward CV Rose MD Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations. Plenum Press, New York1997: 389-415Crossref Google Scholar] and have identified all of the shortest trees with four, three, two or one dispersal(s) under scenario A (Figure 1): parsimony analyses show that these are 448, 452, 463, and 492 steps long, respectively (2, 6, 17 and 46 steps longer than the most-parsimonious phylogeny, respectively). The two phylogenies of 452 steps, each requiring three dispersals out of Africa, are not significantly worse than the most-parsimonious tree, according to their Templeton tests of character support (p = 0.126 and 0.227 for the two comparisons, α = 0.05, two-tailed testing [[5]Swofford DL Olsen GJ Waddell PJ Hillis DM Phylogenetic inference.in: Hillis DM Moritz C Mable BK Molecular Systematics,2. Sinauer, Sunderland, MA1996: 407-514Google Scholar]). The same conclusion applies to the four phylogenies of 448 steps, with four dispersals. The eight trees of 463 changes, with two dispersals, are significantly worse than the most-parsimonious phylogeny (p = 0.002–0.012), as is the one tree of 492 steps with one dispersal. Although these results re-emphasize that the Stewart and Disotell model is most-parsimonious and requires the fewest dispersals, the evidence for this model cannot be regarded as conclusive, as there are trees of insignificantly longer length which invoke only one or two extra migrations under scenario A (e.g. see Figure 1b). Retaining these trees forces one to consider whether a single inferred migration is enough to convincingly reject scenario A in favor of scenario B. The failure of the morphological data to distinguish between the most-parsimonious phylogeny and these alternatives can be most easily attributed to the large numbers of missing data for most extinct genera [3Goodman M Porter CA Czelusniak J Page SL Schneider H Shoshani J et al.Toward a phylogenetic classification of primates based on DNA evidence complemented by fossil evidence.Mol Phylogenet Evol. 1998; 9: 585-598Crossref PubMed Scopus (519) Google Scholar, 4Gibbons A New study points to Eurasian ape as great ape ancestor.Science. 1998; 281: 622-623Crossref Google Scholar]. There remains a critical need for more complete specimens of known fossil genera. With more complete material, gaps in the morphological matrix can be filled, allowing the assignment of these fossil genera to the hominoid phylogeny with greater certainty and permitting more precise estimates of the number and timing of hominoid dispersals ‘out of and into Africa’. We thank Michele R. Tennant for her suggestions about our study and David L. Swofford for permission to use his latest version of PAUP∗ The model of catarrhine evolution presented by Stewart and Disotell [[1]Stewart C-B Disotell TR Primate evolution – in and out of Africa.Curr Biol. 1998; 8: R582-R588Abstract Full Text Full Text PDF PubMed Google Scholar] highlights the roles of parallelism and competitive exclusion in shaping adaptations in various lineages. It is interesting to note that for most of the time that monkeys were predominantly terrestrial, apes were abundant and arboreal. In Africa, about the time colobines became increasingly arboreal, the gorilla, chimp and human lineages appeared, and hominids became terrestrial bipeds. In Asia, arboreal monkeys appeared about the time fossil apes disappeared. Arboreality in its various forms appears to have evolved at different times and rates in different lineages. Old World monkeys were largely terrestrial for most of their evolutionary history, with many returning to the trees only recently. Re-invasion of an arboreal niche seems to have happened after the divergence of Asian and African colobine lineages. Shared arboreal traits among colobines, then, must represent independent evolutionary acquisitions, suggesting that mechanical requirements of an arboreal lifestyle select for predictable morphological changes given a similar ancestral form. Hominoids have always been predominantly arboreal, even in the earliest parts of the lineage. The only fossil hominoid that has been interpreted as displaying any apparent adaptations to part-time terrestriality is Kenyapithecus[[6]McCrossin ML Benefit BR On the relationships and adaptations of Kenyapithecus, a large-bodied hominoid from the Middle Miocene of eastern Africa.in: Begun DR Ward CV Rose MD Function, Phylogeny and Fossils: Miocene Hominoid Evolution and Adaptations. Plenum Press, New York1997: 241-268Crossref Google Scholar]. It would also be surprising if Proconsul major and Gigantopithecus sp. were not at least partly terrestrial, due to their gorilla-like body sizes. The rest were generalized, above-branch arboreal creatures. Below-branch arboreal specializations probably originated with the modern ape clade. Fossil evidence suggests, however, that the extreme adaptations seen in extant apes were only ‘completed’ independently in the gibbon/siamang ancestor, in orangutans, at least once in the African ape and human clade, and perhaps again in the early Miocene ape Morotopithecus. Like the apparent parallelisms seen in colobines, this supports the hypothesis that evolution produces similar morphologies under similar selective regimes in closely related primates. What is missing from the synthesis reported by Stewart and Disotell [[1]Stewart C-B Disotell TR Primate evolution – in and out of Africa.Curr Biol. 1998; 8: R582-R588Abstract Full Text Full Text PDF PubMed Google Scholar] is a study of the comparative anatomy and locomotor behavior of living apes, evidence that may further strengthen their hypothesis. The paradox in interpreting ape evolution is that the Asian apes, belonging to the older hominoid lineage, are dependent upon continuous forest canopy. Their younger African cousins, chimpanzees and gorillas, are equally at home in the trees and on the ground. Knuckle-walking accommodates weight-bearing on their long forelimbs and their massive hindlimbs approach those of quadrupedal, terrestrial Old World monkeys [[7]McFarland RK Zihlman AL Body composition in male chimpanzees, P. paniscus and P. troglodytes: a preliminary report.Amer J Phys. Anthrop suppl. 1996; 22: 177Google Scholar]. As global cooling occurred in the Miocene, the Asian forests contracted, the Himalayas rose, and the Tethys Sea shrank. These environmental changes probably contributed to the extinction of Miocene ape genera, such as Sivapithecus in Asia and Europe [[8]Laporte L Zihlman AL Plates, climates, and hominoid evolution.So Af J Sci. 1983; 79: 96-110Google Scholar]. One of the survivors may well have been the ancestor of the gorilla and the chimp, anatomically equipped to travel quadrupedally between discontinuous forests and to radiate into new habitats. Presumably the ancestor, like the living gorilla and chimp, was able to survive outside of primary rain forest; gorillas in fact seem to prefer secondary forests, and chimpanzees survive in deciduous forests. The more specialized anatomy of gibbons and orangutans, the small size of the former and the extreme joint flexibility of the latter, has evidently evolved during the millions of years since they diverged from their common ancestor with each other and with their earlier and later African relatives. Further discussion is needed on the timing, as a gibbon branch at 13–14 million years ago, rather than 18 million years ago, would seem to better accommodate the anatomical data. The weakest link in Stewart and Disotell's scenario is the fossil record. Although Miocene fossil apes exist in Eurasia and Africa, limited evidence of their locomotor anatomy shows little affinity with living apes. For the time of the supposed remigration into Africa during the past 8–10 million years, the fossil cupboard is virtually bare. We nevertheless congratulate Stewart and Disotell for presenting a well-defined and testable model. The new model proposed by Stewart and Disotell [[1]Stewart C-B Disotell TR Primate evolution – in and out of Africa.Curr Biol. 1998; 8: R582-R588Abstract Full Text Full Text PDF PubMed Google Scholar] is controversial, but it is an ideal scientific hypothesis: it is testable, and it is supported by the discovery of new specimens of a long-known East African fossil, now named Morotopithecus, and its redating at more than 20 million years ago. The new material shows clear affinities with modern hominoids, in a way which Proconsul and Afropithecus do not, confirming that these two genera form separate lineages [[9]Gebo D MacLatchy L Kityo R Deino A Kingston J Pilbeam D A Hominoid genus from the Early Miocene of Uganda.Science. 1997; 276: 401-404Crossref PubMed Scopus (123) Google Scholar]. The more diverse the early African hominoid group turns out to be, the more support there is for the Stewart and Disotell model. On the other hand David Pilbeam has queried the once seemingly unassailable orangutan affinities of Sivapithecus[[10]Pilbeam D Genetic and morphological records of the Hominoidea and hominid origins: a synthesis.Mol Phylogenet Evol. 1996; 5: 155-168Crossref PubMed Scopus (154) Google Scholar], and such a proposal would argue against the model. Among the new research that may be stimulated by the hypothesis, I would like to see work to determine the real affinities of Asian fossils including Sivapithecus, Indopithecus and Gigantopithecus, and new investigations of the late Miocene fossils of southern Europe, Graecopithecus and Ankarapithecus, which could probably fit into either scenario. There are some potential problems with Stewart and Disotell's [[1]Stewart C-B Disotell TR Primate evolution – in and out of Africa.Curr Biol. 1998; 8: R582-R588Abstract Full Text Full Text PDF PubMed Google Scholar] analysis that need to considered before the results are considered to be compelling. The most vexing is the overly simplistic biogeographic approach. In their Figure 2, such Eurasian forms as Oreopithecus, Dryopithecus, Lufengpithecus, Ouranopithecus and Sivapithecus are included. While each is known from Eurasian localities, it would be more accurate to note that some are from Western Europe, others central Europe, one from the Indian subcontinent, and one from eastern Asia. In fact, only Lufengpithecus is known from geographic localities within 1,500 km of the range of modern Asian apes. To make this analysis more meaningful, the authors should divide Eurasia and Africa into three or four regions and repeat the analysis. For example, Eurasia might simply be divided into Europe, Western Asia and Eastern Asia, and Africa divided into Saharan Africa, East Africa, West Africa and southern Africa. The authors would then be treating biogeographic data at a level of detail approaching that with which they treat the morphological and molecular data. We thank the authors of the above letters for their thoughtful comments, and wish to make a few comments in response. Foremost, we encourage the authors to perform the various analyses that they suggest here. Given that all of the data matrices used in our analyses have been explicitly presented in the literature, anyone can test various evolutionary hypotheses by reanalyzing these data, recoding them or adding new characters as they see fit. For example, Miyamoto and Young present an elegant illustration of how Swofford's computer program, PAUP∗[[11]Swofford D PAUP∗ (Phylogenetic Methods Using Parsimony and Other Methods). Sinauer, Sunderland, MA1998Google Scholar], can be used to statistically test various evolutionary hypotheses about hominoid evolutionary relationships and dispersal patterns. They present a reanalysis of the dataset of Begun et al. [[2]Begun DR Ward CV Rose MD Events in hominoid evolution.in: Begun DR Ward CV Rose MD Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations. Plenum Press, New York1997: 389-415Crossref Google Scholar], the main one we used for our placement of the hominoid fossils in the primate evolutionary tree. We applaud Miyamoto and Young for taking our study one step further, and showing how rigorous phylogenetic analysis can be performed to rule out alternative evolutionary hypotheses. They have set a new standard in the field of paleoanthropology. Covert rightly suggests that more sophisticated biogeographical analyses could be performed to better understand the details of primate dispersal patterns. We chose to focus on the simple, traditional dichotomy between Africa and Eurasia for several reasons. Importantly, the water and desert that have separated Africa and Eurasia during most of evolutionary history have presented major barriers to primate dispersal between these land masses. Thus, the major dispersal events between Africa and Eurasia are the first that need to be studied before more sophisticated analyses are performed. Whether multiple dispersals out of Africa should be considered more or less likely than one dispersal out of and another back into Africa depends, in part, on the locomotor behavior of the migrant species, as discussed originally by Sarich and Cronin [[12]Sarich VM Cronin JE Molecular systematics of the primates.in: Goodman M Tashian RE Tashian JH Molecular Anthropology. Plenum Press, New York1976: 141-170Crossref Google Scholar] and here by Ward, Zihlman and Lowenstein We note that the common ancestor of the modern African apes was most likely a semi-terrestrial quadruped, as are gorillas and chimpanzees (and young humans). Similarly, the fossil colobine Mesopithecus is believed to have been semi-terrestrial. So both of the ancestral primate groups that we propose dispersed about 10 million years ago were probably capable of quadrupedal, terrestrial locomotion through suboptimal, thinly-forested environments. The longer trees that Miyamoto and Young present have implications for the divergence date of the orangutan and African ape lineages, one of the most important and hotly-contested dates in primate evolution. It is often claimed that calibration of this key divergence date relies solely on the placement of Sivapithecus on the orangutan lineage, but this is not true. Any hominoid fossils that cluster with either the African ape or orangutan clade are relevant to this divergence date, as we previously explained. In Figure 1b above, for example, Dryopithecus and Ouranopithecus are found to cluster with the orangutan clade, rather than with the African apes, as they do in the most parsimonious tree (Figure 1a above); either of these placements suggests that the African ape and orangutan lineages diverged before the earliest appearance of these fossil hominoids. Indeed, the placement of any of these Eurasian hominoid fossils on either the orangutan or African ape lineages precludes this key divergence date from being as recent as 8.6 million years ago, as proposed by Kumar and Hedges [[13]Kumar S Hedges SB A molecular timescale for vertebrate evolution.Nature. 1998; 392: 917-920Crossref PubMed Scopus (1567) Google Scholar] based on analysis of a few unidentified proteins. Thus, this key divergence date does not rely solely on the phylogenetic position of Sivapithecus. Groves points out the controversy surrounding Sivapithecus, which derives from relatively recent discoveries of a few postcranial bones that are thought to belong to this genus. Few paleoanthropologists contest the detailed likeness of the Sivapithecus face and palate to that of the orangutan, but the arm bones display a curious mix of ape and monkey-like features that suggest a quadrupedal locomotor pattern unlike that seen in the arboreally-committed orangutans. Some authors, notably Pilbeam [[10]Pilbeam D Genetic and morphological records of the Hominoidea and hominid origins: a synthesis.Mol Phylogenet Evol. 1996; 5: 155-168Crossref PubMed Scopus (154) Google Scholar], have taken these postcranial features to imply that Sivapithecus may not be uniquely related to the orangutan lineage. Importantly, however, parsimony analysis of the Begun et al. [[2]Begun DR Ward CV Rose MD Events in hominoid evolution.in: Begun DR Ward CV Rose MD Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations. Plenum Press, New York1997: 389-415Crossref Google Scholar] data matrix indicates that Sivapithecus does branch with orangutans, and with a respectively high bootstrap support of 80% (Figure 1a, above). This placement suggests that the Sivapithecus-like ancestor was more terrestrial than are orangutans, a locomotor behavior that would have more easily allowed their dispersal into southeast Asia. We also agree with these authors that more — and more complete — fossil primates need to be included in computer-aided parsimony analyses. Sadly, more complete fossils do exist for some of the genera shown in these trees, but they have not yet been made available for such analyses. Due in part to logistical difficulties, some paleontologists do not allow access to ‘their’ fossils by many other researchers in the field; nor do all present explicit data matrices that can be reanalyzed, challenged or augmented. These situations are unacceptable in modern science. We call for a change in the culture of paleoanthropology, such that all relevant specimens can be examined by other researchers and all data used to infer evolutionary hypotheses must be explicitly presented. Modern imaging and computer technologies will allow the acquisition and storage of three-dimensional images of fossils, making the primary data widely available. MM Miyamoto, Department of Zoology, University of Florida, Gainesville, Florida 32611, USA, e-mail: [email protected] . TS Young, Department of Zoology, University of Florida, Gainesville, Florida 32611, USA, e-mail: [email protected] . C Ward, Department of Anthropology and Department of Pathology and Anatomical Sciences, 107 Swallow Hall, University of Missouri, Columbia, MO 65211, USA, e-mail: [email protected] . AL Zihlman, Social Sciences 1, University of California Santa Cruz, Santa Cruz, CA 95064, USA, e-mail: [email protected] . JM Lowenstein, Department of Nuclear Medicine, California Pacific Medical Center, San Francisco, CA 94115, USA, e-mail: [email protected] . C Groves, Department of Archaeology and Anthropology, The Australian National University, Canberra 0200, Australia. H Covert, Department of Anthropology, C.B. 233, University of Colorado, Boulder, Colorado 80309-0233, USA. CB Stewart, Department of Biological Sciences, University at Albany, State University of New York, 1400 Washington Avenue, Albany, New York 12222, USA, e-mail: [email protected] . TR Disotell, Department of Anthropology, New York University, 25 Waverly Place, New York, New York 10003, USA, e-mail: [email protected] .