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The Radiation of Macaques out of Africa: Evidence from Mitogenome Divergence Times and the Fossil Record

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The Radiation of Macaques out of Africa: Evidence from Mitogenome Divergence Times and the Fossil Record Journal of Human Evolution 133 (2019) 114e132 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol The radiation of macaques out of Africa: Evidence from mitogenome divergence times and the fossil record * Christian Roos a, b, , Maximilian Kothe a, David M. Alba c, Eric Delson d, e, f, g, c, * Dietmar Zinner h, a Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077, Gottingen,€ Germany b Gene Bank of Primates, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077, Gottingen,€ Germany c Institut Catala de Paleontologia Miquel Crusafont, Universitat Autonoma de Barcelona, Edifici ICTA-ICP, c/ Columnes s/n, Campus de la UAB, Cerdanyola del Valles, 08193, Barcelona, Spain d Department of Anthropology, Lehman College of the City University of New York, 250 Bedford Park Boulevard West, Bronx, NY, 10468, USA e Department of Vertebrate Paleontology, American Museum of Natural History, 200 Central Park West, New York, NY, 10024, USA f The Graduate Center of the City University of New York, 365 Fifth Avenue, New York, NY, 10016, USA g New York Consortium in Evolutionary Primatology, New York, NY, USA h Cognitive Ethology Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077, Gottingen,€ Germany article info abstract Article history: Fossil evidence indicates that numerous catarrhine clades of African origin expanded or shifted their Received 15 July 2018 ranges into Eurasia, among them macaques Macaca Lacep ede, 1799. Macaques represent the sister taxon Accepted 31 May 2019 of African papionins and can thus be used as a model comparing an ‘out-of-Africa’ with an intra-African, e.g., baboonsdPapio Erxleben, 1777 evolutionary history. The first step for such a comparison is to establish a well-resolved phylogeny of macaques with reliably estimated divergence times and to Keywords: compare it with that of baboons and the fossil record. Therefore, we used mitochondrial (mtDNA) Cercopithecoidea genome data deposited in GenBank of 16 out of 23 extant macaque species and of all six baboon taxa. We Papionini Papio reconstructed phylogenetic trees using maximum-likelihood and Bayesian inferences and dated differ- Macaca entiation events using three fossil-based calibration sets. The obtained tree topology is in agreement Dispersal events with findings from earlier mtDNA studies, but yielded stronger nodal supports. We observed some para- Fossils and polyphylies in macaques and baboons, suggesting that ancient gene flow among divergent lineages has been common in both genera. Our divergence time estimates are in broad agreement with earlier findings and with the fossil record. Macaques started to diversify 7.0e6.7 Ma, followed by a stepwise radiation into several species groups in Asia, whereas baboons commenced diversification around 2.2 Ma. Accordingly, divergence of species groups and species in macaques clearly predates divergences in baboons. Based on our phylogenetic results with estimated divergence times and the recorded chronostratigraphic ranges of extinct macaque and baboon taxa, we compare the evolutionary radiations of both genera from paleobiogeographic and adaptive viewpoints. © 2019 Elsevier Ltd. All rights reserved. 1. Introduction Stringer and Galway-Witham, 2018). Members of the genus Homo, however, are not the only catarrhine primates of African There is general consensus that the genus Homo originated in origin that expanded or shifted their ranges into Eurasia. Indeed, Africa and that it dispersed several times into Eurasia (Beyin, 2006; fossil evidence indicates that multiple catarrhine groups dispersed Shea, 2008; Hublin, 2009; Green et al., 2010; Armitage et al., 2011; into that continent (and some of them subsequently radiated there) Anton et al., 2014; Groucutt et al., 2018; Hershkovitz et al., 2018; throughout the Neogene and Quaternary, at least: (1) the unknown stem catarrhine that must have given rise to the Eurasian putative clade known as the Pliopithecoidea (e.g., Begun, 2002, 2017; Harrison, 2013), first recorded ~18e17 Ma; (2) the ancestor of the small-bodied putative stem hominoid Pliobates, recorded in Europe * Corresponding authors. E-mail addresses: [email protected] (C. Roos), [email protected] (D. Zinner). 11.6 Ma (Alba et al., 2015a), unless it is interpreted as a member of https://doi.org/10.1016/j.jhevol.2019.05.017 0047-2484/© 2019 Elsevier Ltd. All rights reserved. C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 115 the pliopithecoid radiation (Nengo et al., 2017, but see Pugh et al., accompanied by numerous cases of secondary gene flow. Most of 2018 for the record of another non-pliopithecoid stem hominoid the studies using mtDNA investigated only fragments of the mtDNA in Asia); (3) the as yet unidentified ancestor of the Hylobatidae, genome and were not able to solve the branching pattern among which are apparently not recorded until 7e6 Ma in China (Harrison macaques with significance, while complete mtDNA genome data et al., 2008; Harrison, 2017); (4) large-bodied hominoids, first allowed a much better resolution of the matrilineal phylogeny (e.g., recorded by Griphopithecus and Kenyapithecus between 16.5 and Liedigk et al., 2014, 2015; Jiang et al., 2016; Roos, 2018). 14 Ma in Europe and Turkey (Heizmann and Begun, 2001; Andrews In this study, we rely on currently available mtDNA genome data and Kelley, 2007; Casanovas-Vilar et al., 2011; Harrison, 2017), and to establish a robust and well-resolved phylogeny of macaques that subsequently by dryopithecines and pongines from ~13 Ma onward also enables a reliable estimation of divergence times based on the (Kelley, 2005; Alba, 2012; Begun, 2015; Gilbert et al., 2017); (5) calibration using the fossil record. With this aim in mind, we pro- colobines, as represented by Mesopithecus, first recorded at least vide several calibration sets based on updated paleontological data 8.5 Ma (Delson, 1974, 1975a; Alba et al., 2015b) and possibly a on fossil catarrhines. On the basis of our phylogenetic results and separate clade including the ancestor of the extant Asian colobines; estimated divergence times, as well as in the recorded chro- (6) cercopithecine monkeys, as recorded by a guenon from Abu nostratigraphic ranges of extinct macaque and baboon taxa, we also Dhabi dated to ~8.0e6.5 Ma (Gilbert et al., 2014); (7) early papio- compare the evolutionary radiation of macaques (genus Macaca) nins assigned to cf. Macaca sp., first recorded 5.9e5.3 Ma (Kohler€ with that of baboons (genus Papio) from paleobiogeographic and et al., 2000; Alba et al., 2014a); (8) geladas (Theropithecus), first adaptive viewpointsdwith emphasis on various hypotheses that recorded in Eurasia 1.6e1.2Ma(Alba et al., 2014b, and references might explain the greater species diversity attained by macaques as therein); and (9) baboons Papio Erxleben, 1777, which dispersed compared to that of baboons. We focused on the maternally- into Arabia 0.13e0.012 Ma according to molecular data (Winney inherited mtDNA as macaques and most baboon species are et al., 2004; Kopp et al., 2014). strongly female philopatric (Grueter and Zinner, 2004; Grueter Representing one of the most successful primate radiations, et al., 2012) and thus information about the primary radiation extant macaques exhibit the second largest geographic range (before times of secondary gene-flow) of both genera can be ob- among primates, after humans. Macaques constitute the sister tained. However, when only a maternally-inherited marker is subtribe (Macacina) of the predominantly African Papionina (Papio, analyzed the evolutionary history of a taxon remains incomplete. Theropithecus, Rungwecebus, Lophocebus, Mandrillus and Cercoce- Consequently, we also discuss differences between mtDNA and bus). Paleontological and molecular studies suggest an African published nucDNA phylogenies and respective divergence times. origin of macaques (Delson, 1980; Tosi et al., 2000; Jablonski and Frost, 2010; Liedigk et al., 2014, 2015). The most basal extant 2. Methods member of the genus Macaca Lacep ede, 1799, the Barbary macaque (Macaca sylvanus; e.g., Perelman et al., 2011), still occurs in North 2.1. Molecular data Africa. It is the only extant member of the genus occurring outside Asia, with a natural disjunct distribution in Morocco and Algeria To perform the phylogenetic analyses, we downloaded mtDNA (Fooden, 2007), as well as a colony of human-mediated origin in genome data from macaques, baboons and various outgroups from Gibraltar (Modolo et al., 2005; Fooden, 2007). GenBank.2 We did not include representatives of the genera Man- After reaching Asia, macaques seem to have experienced a rapid drillus, Cercocebus, Lophocebus and Rungwecebus as available data fi diversi cation into several species groups and species. Currently, are limited and, moreover, not the focus of our study. We screened macaques comprise seven species groups with 23 species (Zinner mtDNA genomes and selected those that (1) were complete, (2) et al., 2013a; Roos et al., 2014; species counting updated after the contained no indications for the presence of nuclear copies of recent description of Macaca leucogenys by Li et al., 2015), although mtDNA fragments (numts) by checking correct and full-length some of the species may better be recognized as subspecies. The translation of the 13 protein-coding genes, (3) could be reliably number and composition of the macaque species
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