Journal of Human Evolution 133 (2019) 114e132

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Journal of Human Evolution

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The radiation of 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 Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077, Gottingen,€ Germany b Gene Bank of , 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 and the fossil record. Therefore, we used mitochondrial (mtDNA) Cercopithecoidea genome data deposited in GenBank of 16 out of 23 extant species and of all six taxa. We 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 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 (), 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, 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 groups have been assigned to (sub)species by comparing them with partial sequence debated for decades. Originally, Fooden (1976) listed four species data in GenBank, and (4) for macaques and baboons, cover as many groups based on male penile morphology, which Delson (1980) (sub)species and populations as possible. Thirty-seven mtDNA ge- fi modi ed slightly to separate M. sylvanus from the Macaca silenus- nomes matched these criteria and were chosen for further analyses M. sylvanus group (and link Macaca arctoides to the Macaca sinica group), while Groves (2001) recognized six species groups based on molecular data. More recently, Zinner et al. (2013a) and Roos et al. (2014) proposed seven species groups and separated M. arctoides 1 is a dynamic science, and species delimitations have to be regarded from the Macaca fascicularis group, due to the putative hybrid as taxonomic hypotheses. Due to the application of molecular methods and the origin of the former (Tosi et al., 2000, 2003; Jiang et al., 2016; Fan phylogenetic species concept (Cracraft, 1983), the taxonomy of primates, as of other et al., 2018). Three of these groups are monotypic (at least, when taxa, has changed considerably. However, some of the changes in primate taxon- fl only extant species are considered): those of M. sylvanus, omy are debated, which is re ected in the divergent opinions among the authors of this contribution. Here M.K., D.Z. and C.R. recognize the six commonly accepted M. arctoides, and M. fascicularis. The remaining groups are polytypic extant baboon taxa as distinct species according to the phylogenetic species and contain 3e6 species each: Macaca mulatta group (3 species), concept, while D.M.A. and E.D. prefer to recognize them as a single (super)species M. silenus group (5 species), M. sinica group (6 species), and the (Papio hamadryas) with six subspecies (see Gilbert et al., 2018 for further details on Macaca nigra or Sulawesi macaque group (6 species).1 the pros and cons of the latter view). As a result, we refer to (sub)species when fi Various molecular phylogenies of macaques, using mainly writing generally, or to Papio [hamadryas] ursinus, etc., when discussing a speci c taxon, in order to avoid a controversial disagreement. This is not a formal mitochondrial DNA (mtDNA), but also nuclear DNA (nucDNA) nomenclatural statement under the Code (ICZN, 1999). Note that Jolly (e.g., Jolly, markers, have been published in recent decades (Tosi et al., 2000, 1993) has implied that more than six equally distinct taxa may be recognizable 2003; Deinard and Smith, 2001; Evans et al., 2003, 2017; Ziegler within extant Papio. For macaques all authors agreed on seven species groups, et al., 2007; Li et al., 2009; Perelman et al., 2011; Liedigk et al., although E.D. notes that there is a hierarchical structure to the macaque cladogram (see Fig. 1 below) and suggests that a reassessment of the species-group arrange- 2014, 2015; Fan et al., 2014, 2018; Roos and Zinner, 2015; Jiang ment might be useful. et al., 2016; Matsudaira et al., 2017; Yao et al., 2017; Roos, 2018), 2 Ethical note: We used only mtDNA genome sequences deposited in GenBank. suggesting that macaques experienced rapid radiations No were sacrificed for the purpose of this study. 116 C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132

(for GenBank accession numbers, see Supplementary Online Papionini e ; (9) Macacina e Papionina; (10) Papio e Material [SOM] Table S1). For instance, the mtDNA genomes from Theropithecus. For all ten nodes, we applied a gamma-distributed putative Macaca nemestrina (KP765688.1) and M. nigra prior with the minimum age of nodes (Table 1) as offset, an alpha (KP072068.1) individuals were discarded as both cluster incorrectly value of 2.0 and variable values for beta to reach the soft maximum with the M. mulatta group. The 18 selected macaque sequences bound (Table 1; for BEAST settings see SOM Table S2). Especially represent all seven species groups and 16 out of 23 species, while setting correct maximum constraints is challenging because the the ten baboon sequences represent all six (sub)species and the fossil record can only provide minimum divergence dates. How- seven major mtDNA clades (Zinner et al., 2009, 2013b). ever, molecular clock analysis generally requires both minimum and maximum age constraints (see review in Benton and 2.2. Molecular analyses Donoghue, 2007): minimum divergence calibration dates are ‘hard' bounds, in the sense that they are absolute (unless they are Sequences were aligned with Muscle 3.8.31 (Edgar, 2010)in based on an incorrect phylogenetic assumption), whereas AliView 1.18 (Larsson, 2014) and corrected by eye. The final align- maximum dates are ‘soft’ bounds, because actual divergence dates ment had a length of 16,927 bp and was reduced to 15,774 bp after could theoretically fall beyond them. Following Benton and indels and poorly aligned positions were removed with Gblocks Donoghue (2007), based on a combination of phylogenetic brack- 0.91b (Castresana, 2000). Phylogenetic trees were reconstructed eting (maximum ages of sister groups) and stratigraphic bounding with maximum-likelihood (ML) and Bayesian algorithms using IQ- (absence of fossils of the respective clade in an underlying suitable TREE 1.5.2 (Nguyen et al., 2015) and MrBayes 3.2.6 (Ronquist et al., fossiliferous formation), hard minimum age constraints may be 2012), respectively. The optimal model of sequence evolution determined on the basis of the youngest possible age of the sedi- (TIM2þIþG) was determined with ModelFinder (Chernomor et al., ments where the oldest integral member of a clade has been found; 2016; Kalyaanamoorthy et al., 2017) under the Bayesian Informa- in turn, soft maximum age constraints may be determined based on tion Criterion (BIC) as implemented in IQ-TREE. The ML analysis the oldest possible age of the sediments where the oldest members was performed with 10,000 ultrafast bootstrap (BS) replications of the sister-taxon or the stem lineage of the clade under consid- (Minh et al., 2013). Bayesian trees were reconstructed via four in- eration, but no members of the crown clade itself, have been found. dependent Markov Chain Monte Carlo (MCMC) runs. All repetitions Besides dating uncertainties and the incompleteness of the were run for 10 million generations with tree and parameter fossil record, the most serious source of error that may be intro- sampling setting in every 100 generations. To check convergence of duced by any calibration set arguably relates to the validity of the all parameters and the adequacy of a 25% burn-in, we assessed the underlying phylogenetic hypotheses. For this reason, we derived uncorrected potential scale reduction factor (PSRF; Gelman and two different sets: set-1 is less conservative, in the sense that it Rubin, 1992) as calculated by MrBayes. Posterior probabilities (PP) considers some older taxa whose phylogenetic status is debatable, and a phylogram with mean branch lengths were calculated from thereby yielding older bounds; in contrast, set-2 is more conser- the posterior density of trees in MrBayes. vative, in the sense that it relies on taxa for which there is ample In addition to producing a well-resolved phylogeny, estimating consensus about their phylogenetic status, thereby resulting in reliable divergence times is a parallel goal of our research. Molec- younger bounds. Some criterion is also required when selecting the ular dating can either be done by applying a known mutation rate taxa to be considered for setting a maximum bound. If the sister- or by setting node constraints using information from the fossil taxon of a given clade (e.g., crown catarrhines) is defined as the record, as we do below. Before estimating divergence times we first extant clade more closely related to it (platyrrhines), the maximum checked for the most appropriate clock model using the stepping bound will be defined by the oldest member of the stem lineage of stone method as implemented in MrBayes. For this analysis, we the focal clade (here stem catarrhines, i.e., propliopithecids) or of applied the best-fit model of sequence evolution and investigated the sister-taxon (platyrrhines), irrespective of which members of the mean marginal likelihoods (ln) for trees under strict, non-clock the stem lineage are more closely related to the clade under and relaxed clock hypotheses. Based on these results (see below), consideration. This approach has been used to derive set-1. How- we estimated divergence times applying a relaxed clock model. ever, it might be argued that more reasonable maximum bounds Divergence time calculations were performed with the BEAST 2.4.8 could be established by focusing on the oldest member of the most package (Bouckaert et al., 2014) using a relaxed lognormal clock closely related sister-taxon of the clade under consideration, irre- model of lineage variation (Drummond et al., 2006) and applying a spective of whether that clade is extant or extinct (i.e., based on the Yule tree prior and the best-fit model of sequence evolution as most derived member of its stem lineage, here Saadanius, which is obtained by ModelFinder. All BEAST analyses were run for 100 arguably the most derived known stem catarrhine). The latter million generations with tree and parameter sampling setting in approach, which will generally provide younger maximum bounds, every 5000 generations. To assess the adequacy of a 10% burn-in has been used to derive set-2. Only when the oldest recorded and convergence of all parameters, we inspected the trace of the member of the clade under consideration predates the most parameters across generations using Tracer 1.6 (Rambaut et al., derived member of the stem lineage would it be necessary to 2014). We combined sampling distributions of multiple indepen- inspect successively more basal members of the stem lineage to dent replicates with LogCombiner 2.4.8 and summarized trees (10% establish the maximum bound (this does not apply in the example, burn-in) using TreeAnnotator 2.4.8 (both programs are part of the since Saadanius is older than the earliest putative crown BEAST package). All resulting trees were visualized in FigTree 1.4.2 catarrhines). (Rambaut, 2014). We briefly explain below the rationale that underpins our se- lection of extinct taxa to derive the two aforementioned calibration 2.3. Paleontological calibration sets. Both sets have been combined into another one (set-3) by

To calibrate the molecular clock, we set constraints on ten nodes using information from the fossil record (Table 1): (1) Hominoidea e Cercopithecoidea; (2) Hominidae e Hylobatidae; (3) Ponginae e e þ e Homininae; (4) Gorilla (Pan Homo); (5) Homo Pan; (6) 3 African and Asian colobines are either classified as tribes Colobini and Pres- 3 Colobinae e ; (7) Colobina e Presbytina ; (8) bytini or as subtribes Colobina and Presbytina. C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 117

Table 1 Calibration sets based on extinct taxa, used in this work to estimate divergence times on molecular grounds. Set-2 takes a more conservative view than set-1 with regard to the selection of taxa on phylogenetic grounds. See the main text for further details. Bold type denotes the bounds that are different among the various sets.

Divergence e Set-1 Oldest clade members (subclade) Oldest sister-taxon/stem member record Minimum (hard Maximum (soft bound, in Ma) bound, in Ma)

Hominoidea e Nsungwepithecus gunnelli and/or Perupithecus ucayaliensis 25.2 36.0 Cercopithecoidea Rukwapithecus fleaglei Hominidae e Kenyapithecus wickeri and Kenyapithecus Nsungwepithecus gunnelli and/or Rukwapithecus 13.7 25.2 Hylobatidae kizili fleaglei Ponginae e Homininae Sivapithecus indicus Kenyapithecus kizili 13.0 14.9 Gorilla e (Pan þ Homo) Chororapithecus abyssinicus Sivapithecus indicus 8.0 13.0 Homo e Pan Sahelanthropus tchadensis Chororapithecus abyssinicus 6.8 8.0 Colobinae e Colobinae indet. (Kabasero) Nsungwepithecus gunnelli 12.5 25.2 Cercopithecinae Colobina e Presbytina Mesopithecus pentelicus Colobinae indet. (Kabasero) 8.5 12.5 Papionini e cf. Papionini indet. (Chorora) Colobinae indet. (Kabasero) 8.0 12.5 Cercopithecini Macacina e Papionina ?Macaca sp. (Menacer) and Macaca libyca Cercopithecini indet. (Baynunah) and cf. Papionini 5.8 8.0 indet. (Chorora) Papio e Theropithecus cf. Theropithecus sp. (Kanapoi) “Parapapio” lothagamensis 4.2 7.4

Divergence e Set-2 Oldest clade members (subclade) Oldest sister-taxon/stem member record Minimum (hard Maximum (soft bound, in Ma) bound, in Ma)

Hominoidea e Proconsul meswae Saadanius hijazensis 20.0 29.0 Cercopithecoidea Hominidae e Kenyapithecus wickeri and Kenyapithecus Proconsul meswae 13.7 20.0 Hylobatidae kizili Ponginae e Homininae Sivapithecus indicus Kenyapithecus kizili 13.0 14.9 Gorilla e (Pan þ Homo) Sahelanthropus tchadensis Sivapithecus indicus 6.8 13.0 Homo e Pan Ardipithecus kadabba Sahelanthropus tchadensis 5.5 7.2 Colobinae e Colobinae indet. (Kabasero) Victoriapithecidae 12.5 20.0 Cercopithecinae Colobina e Presbytina Cercopithecoides sp. (Laetoli) Colobinae indet. (Kabasero) 3.5 12.5 Papionini e Cercopithecini indet. (Baynunah) Colobinae indet. (Kabasero) 6.5 12.5 Cercopithecini Macacina e Papionina Macaca libyca and “Parapapio” Cercopithecini indet. (Baynunah) and cf. Papionini 5.0 8.0 lothagamensis indet. (Chorora) Papio e Theropithecus cf. Theropithecus sp. (Kanapoi) “Parapapio” lothagamensis 4.2 7.4

Divergence e Set-3a Oldest clade members (subclade) Oldest sister-taxon/stem member record Minimum (hard Maximum (soft bound, in Ma) bound, in Ma)

Hominoidea e Proconsul meswae Perupithecus ucayaliensis 20.0 36.0 Cercopithecoidea Hominidae e Kenyapithecus wickeri and Kenyapithecus Nsungwepithecus gunnelli and/or Rukwapithecus 13.7 25.2 Hylobatidae kizili fleaglei Ponginae e Homininae Sivapithecus indicus Kenyapithecus kizili 13.0 14.9 Gorilla e (Pan þ Homo) Sahelanthropus tchadensis Sivapithecus indicus 6.8 13.0 Homo e Pan Ardipithecus kadabba Chororapithecus abyssinicus 5.5 8.0 Colobinae e Colobinae indet. (Kabasero) Nsungwepithecus gunnelli 12.5 25.2 Cercopithecinae Colobina e Presbytina Cercopithecoides sp. (Laetoli) Colobinae indet. (Kabasero) 3.5 12.5 Papionini e cf. Papionini indet. (Chorora) Colobinae indet. (Kabasero) 6.5 12.5 Cercopithecini Macacina e Papionina Macaca libyca and “Parapapio” Cercopithecini indet. (Baynunah) and cf. Papionini 5.0 8.0 lothagamensis indet. (Chorora) Papio e Theropithecus cf. Theropithecus sp. (Kanapoi) “Parapapio” lothagamensis 4.2 7.4

a Minimum and maximum bounds for set-3 determined based on set-2 and set-1, respectively.

taking the youngest minimum bound and the oldest maximum from the Early (Miller et al., 2009; Jablonski and Frost, bound of both sets. 2010), they appear slightly younger than Proconsul meswae Crown (Hominoidea–Cercopithecoidea) With an age of (>20.0 Ma; Harrison and Andrews, 2009). Even if some authors 25.2 Ma, the oldest putative representatives of the crown catar- still consider Proconsul as a stem catarrhine preceding the rhine clade are Nsungwepithecus gunnelli and Rukwapithecus flea- cercopithecoid-hominoid divergence (Harrison, 2010), most glei, respectively interpreted as a stem cercopithecoid and a stem consider this genus as a stem hominoid (e.g., Stevens et al., 2013; hominoid (Stevens et al., 2013). Note that, since the material from Begun, 2013, 2015; Alba et al., 2015a), which would consequently both species comes from the same locality, it is irrelevant establish a minimum bound of 20.0 Ma in set-2. The older whether one of these taxa is interpreted as a stem catarrhine Kamoyapithecus hamiltoni (~27e23 Ma) has been proposed as the preceding the cercopithecoid-hominoid divergence, since the earliest hominoid (Leakey et al., 1995), but preserved evidence is other taxon would still set the minimum bound at 25.2 Ma (set- inconclusive and suggests instead it is best interpreted as a stem 1). It would require considering that both taxa are stem catarrhine (Harrison, 2010, 2013; Seiffert, 2012; Begun, 2015). As catarrhines to discount such an age. In that case, even though for the maximum bound, in the most conservative approach (set- several stem cercopithecoid (victoriapithecid) genera are known 1) it would be established by the earliest putative stem 118 C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 catarrhines or members of the closest extant sister taxon of the basis of both species, the minimum bound is set to 13.7 Ma in catarrhines (i.e., platyrrhines). There are reasons to think that both sets. In turn, the maximum bound would be established by oligopithecids are stem anthropoids preceding the platyrrhine- the earliest stem hominoids or cercopithecoids (see above), i.e., at catarrhine divergence (Harrison, 2013). However, if they are 25.2 Ma by Nsungwepithecus and/or Rukwapithecus (set-1), or at considered stem catarrhines (e.g., Seiffert et al., 2010; Seiffert, 20.0 by Proconsul (set-2). 2012), the maximum bound could be established by Catopithecus Crown Hominidae (Ponginae–Homininae) The divergence be- browni at ~34.0 Madif it was not for the fact that the oldest tween the orangutan and the African and human lineages remains from South America tentatively assigned to stem (respectively, Ponginae and Homininae) is somewhat controversial, platyrrhines (Perupithecus ucayaliensis and some other unnamed given the insistence of some researchers that the European Dry- genera; Bond et al., 2015) may be somewhat older (~36 Ma). The opithecinae are stem hominines (e.g., Begun et al., 2012; Begun, phylogenetic affinities of older but poorly-known taxa from 2013, 2015) instead of stem hominids (e.g., Alba, 2012). Even if Africadsuch as Talahpithecus parvus from Libya (39e38 Ma), we discount dryopithecin and hispanopithecin dryopithecines previously considered an oligopithecoid (Jaeger et al., 2010)or (sensu Alba, 2012) as stem hominines, a reasonable case might even a stem platyrrhine (Bond et al., 2015)dare uncertain still be made in the case of Ouranopithecus macedoniensis (first (Seiffert, 2012), so that these taxa can be discounted. In contrast, recorded at ~9.6 Ma; de Bonis and Koufos, 2004) and the platyrrhine status of Perupithecus is reasonable on Graecopithecus freybergi (7.2 Ma; Koufos and de Bonis, 2005; Fuss paleobiogeographic grounds, thereby setting the maximum et al., 2017) from Greece. However, such debate is irrelevant here, bound at 36 Ma in set-1, even if this dating is very tentative. since neither these nor putative hominines from Africa predate Alternatively, the maximum bound could be established on the the record of Sivapithecus in Asia, which is generally considered basis of undoubted stem catarrhines, first represented by the as a member of the orangutan clade (Kelley, 2005; Alba, 2012; propliopithecid Propliopithecus ankeli at ~31.5 Ma (Seiffert et al., Begun, 2013, 2015). The oldest remains of this genus, with an age 2010). However, the advanced stem catarrhine Saadanius of ~12.7 Ma, are generally assigned to Sivapithecus indicus (e.g., hijazensis (29e28 Ma) has been further proposed to set the Kelley, 2005). Even if they are not completely diagnostic of the maximum bound for the cercopithecoid-hominoid divergence genus, at least they display derived features of the Ponginae (Zalmout et al., 2010), because it appears more closely related to (Begun, 2015) and therefore permit us to set the minimum crown catarrhines than are propliopithecids (Seiffert, 2012; bound. Other Sivapithecus-bearing sediments might be somewhat Harrison, 2013). This argument was criticized based on the claim older (Gilbert et al., 2017), suggesting that 13.0 Ma is a reasonable that stem taxa cannot inform about maximum bounds (Pozzi estimate of the minimum bound. The maximum bound, in turn, et al., 2011), but this is not entirely correct as long as it is should be determined based on the hominid stem lineage (since recognized that maximum constraints are soft instead of hard the age of the oldest putative hylobatid known postdates the bounds (Benton and Donoghue, 2007). If Saadanius is taken as the minimum bound; see above). Based on the oldest possible age of closest sister-taxon of the crown catarrhine clade, then 29 Ma can Kenyapithecus (see above), we set the maximum bound at 14.9 Ma. be arguably used as the maximum bound (set-2). Crown Homininae (gorillas–chimpanzeesþhominins) The diver- Crown Hominoidea (Hylobatidae–Hominidae) The Miocene record gence date of the gorilla lineage from the rest of the African-ape- of hylobatids is virtually non-existent, although the possibility and-human clade is also controversial, given the virtual lack of cannot be discounted that some small-bodied catarrhines from unquestionable Mio-Pliocene representatives of the African great Eurasia known by very fragmentary remains might be stem ape lineages. Chororapithecus abyssinicus was proposed as a basal hylobatids instead of stem catarrhines (i.e., pliopithecids). Alba member of the gorilla clade by Suwa et al. (2007), initially with et al. (2015a) noted some hylobatid-like features in Pliobates, but an age of 10.5e10 Ma, which was subsequently revised to given the mosaic of stem catarrhine-like and modern hominoid- ~8.0 Ma (Katoh et al., 2016). This taxon has been tentatively like features displayed by this taxon, these might be considered linked to Nakalipithecus nakayamai (9.9e9.8 Ma; Kunimatsu et al., as primitive features for crown hominoids as a whole. Indeed, 2007; Katoh et al., 2016), also from Africa, which would slightly Alba et al.'s (2015a) cladistic analysis failed to support a closer predate the oldest record of the Eurasian Ouranopithecus. The relationship with hylobatids and instead supported a stem status of these taxa as crown hominines is very uncertain, with hominoid status for Pliobates, whereas independent analyses have the possible exception of Chororapithecus (Suwa et al., 2007; placed it close to pliopithecids (Nengo et al., 2017). The next Katoh et al., 2016), which would enable us to set the minimum Miocene hylobatid candidate is Yuanmoupithecus from China divergence age at 8.0 Ma (set-1). If Chororapithecus is considered (7e6 Ma; Harrison et al., 2008; Harrison, 2016, 2017), which instead a stem hominine of uncertain affinities that might have clearly postdates the divergence between hylobatids and preceded the divergence of gorillas (Harrison, 2010), and hominids considerably. As such, the minimum bound for this Nakalipithecus, Ouranopithecus and Graecopithecus are discounted node must be established on the basis of the oldest record of on the same grounds, then the minimum bound would be hominids (i.e., great ). There is some controversy regarding determined at 6.8 Ma (set-2) by Sahelanthropus tchadensis what extinct taxa preceding dryopithecines must be considered (7.2e6.8 Ma: Brunet et al., 2002; Lebatard et al., 2008), stem hominids instead of afropithecids (the latter generally irrespective of whether it is considered a hominin or a hominine considered stem hominoids). Alba (2012) tentatively considered of indeterminate affinities (see below). In turn, the maximum that kenyapithecines (including Equatorius, Nacholapithecus, bound would be set by the oldest pongine (Sivapithecus) at 13.0 Kenyapithecus and Griphopithecus) are hominids, but here we Ma (see above), since it predates other extinct taxa proposed by follow a more conservative approach (e.g., Harrison, 2010)by some authors as stem hominines (including dryopithecines, see considering that this is only relatively well substantiated for above). Kenyapithecus wickeri (13.7 Ma), which shares with Pan–Homo The known fossil record of putative extinct hominins is dryopithecines and crown hominids the possession of a high much older than that of chimpanzees, and goes back to the Late zygomatic root (Harrison, 1992, 2010; Alba, 2012). This genus is Miocene, including S. tchadensis (7.2e6.8 Ma: Brunet et al., 2002; further recorded at Pas¸ alar (Turkey) by a second species, Lebatard et al., 2008), Orrorin tugenensis (6.0e5.7 Ma: Senut et al., Kenyapithecus kizili (see Kelley et al., 2008), which would be 2001; Sawada et al., 2002) and Ardipithecus kadabba (oldest roughly dated to 14.9e13.7 Ma (Casanovas-Vilar et al., 2011). On remains: 5.78e5.5 Ma; Haile-Selassie, 2001; WoldeGabriel et al., C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 119

2001; Haile-Selassie et al., 2004). Although the hominin status of be set at 12.5 Ma by the Kabasero stem colobine (see above), the oldest of these putative hominins (Sahelanthropus) has been which is older than the earliest known cercopithecine (see below). disputed by some researchers (Wolpoff et al., 2006), in general Cercopithecinae (Cercopithecini–Papionini) The oldest known the three above-mentioned genera are considered early hominins (and well-dated) cercopithecines come from the Chorora by most authors (e.g., MacLatchy et al., 2010; Simpson, 2013; Formation, with an age of ~8.0 Ma (Suwa et al., 2015). Some of White et al., 2015; Harrison, 2017). As such, Sahelanthropus these remains have been tentatively assigned to papionins and enables us to set the minimum bound for the Pan-Homo coincide with the maximum possible age of an indeterminate divergence in set-1 at 6.8 Ma. Alternatively, if the evidence guenon (Cercopithecini) from the Baynunah Formation, Abu provided by Sahelanthropus and Orrorin is considered Dhabi (~8.0e6.5 Ma; Gilbert et al., 2014). It is difficult to inconclusive (set-2), that bound should be set at 5.5 Ma based on distinguish stem cercopithecines from stem papionins, because Ardipithecusdeven if this genus is only well known on the basis the papionin dentition is plesiomorphic except for a lack of of the early Pliocene species Ardipithecus ramidus (White et al., lingual enamel on lower incisors (Delson, 1973, 1980; Szalay and 2009, 2015). As for the maximum bound, Chororapithecus,if Delson, 1979), and these teeth are not preserved at Chorora. If the considered a stem member of the gorilla lineage (see above), papionin status of the latter is accepted (set-1), the minimum would set the maximum divergence age between the chimp and bound for the cercopithecin-papionin divergence can be set at human lineages at 8.0 Ma (set-1). Alternatively, if the Late 8.0 Ma. Otherwise (set-2), the minimum bound would be set by Miocene taxa from Africa are considered at most stem hominines the cercopithecin from Abu Dhabi, whose minimum possible age preceding the divergence of gorillas (set-2), then the maximum (6.5 Ma) is older than those of other Miocene papionins from bound for the Homo-Pan divergence would be determined by the Africa (see below). As for the maximum bound, given the lack of oldest possible age of Sahelanthropus, which must be at least older stem cercopithecines, it would be set by the oldest colobine interpreted as a hominine preceding that divergence (Wolpoff from Kabasero at 12.5 Ma (see above). et al., 2006). Papionini (Macacina–Papionina) The oldest unambiguous papio- Cercopithecidae (Colobinae–Cercopithecinae) The minimum nins include ?Macaca sp. (using the modern nomen as a paleon- bound would be set at 12.5 Ma by the earliest known colobine, tological ‘form genus’) from Menacer (formerly Marceau), Algeria isolated teeth from Kabasero (Kenya; Rossie et al., 2013), whereas (Delson, 1975a, 1980; Szalay and Delson, 1979), ~7.0e5.8 Ma the maximum bound would be determined at 25.2 Ma by (following Werdelin, 2010), Macaca libyca from Wadi Natrun, N. gunnelli (set-1; assuming it is a cercopithecoid, see above), or Egypt and possibly As Sahabi, Libya (Delson, 1975a, 1980; Szalay alternatively (set-2) by the oldest victoriapithecids from the early and Delson, 1979; Benefit et al., 2008), respectively 6.2e5.0 Ma Miocene, such as Prohylobates tandyi, first recorded at ~20.0 Ma and 6.3e5.3 Ma (Werdelin, 2010), and "Parapapio" lothagamensis (Miller et al., 2009). from Lothagam (~7.4e5.0 Ma; Leakey et al., 2003; Jablonski and Colobinae (Colobina–Presbytina) The minimum bound might be Frost, 2010). In spite of taxonomic uncertainties, both the set by Mesopithecus pentelicus, first recorded from the Greek lo- Menacer and the Lothagam samples must belong to the Papionini cality of Nikiti-2, correlated to the earliest Turolian (MN11; e.g., based on the lack of lingual enamel on lower incisors. Therefore, Koufos, 2006), ~8.5 Ma, if it is assumed (set-1) that this genus is a minimum bound of 5.8 Ma appears justified for the (stem) the earliest recorded member of the Asian colobine clade MacacinaePapionina divergence in set-1 based on ?Macaca from (Presbytina). This was classically supported on biogeographic Menacer. Alternatively, since it is debatable whether the Menacer grounds (Szalay and Delson, 1979) and more recently based on fossils correspond to a macacinan or to a stem papionin (given cladistic analyses (Jablonski, 1998, 2002). However, this is very the lack of diagnostic features unambiguously linking it with uncertain, and currently available evidence is consistent with extant taxa; Benefit, 2008), M. libyca and “P.” lothagamensis more Mesopithecus being a stem colobine (Frost et al., 2015; Alba et al., securely establish the above-mentioned minimum bound in set-2 2015b). The oldest definitive member of either modern subtribe at 5.0 Ma. With regard to the maximum bound, it would be set at is Cercopithecoides williamsi from Koobi Fora (Kenya) dated to 8.0 Ma by the age of the putative papionins from Chorora as well 1.9 Ma (Frost et al., 2015), which preserves the reduced thumb as the maximum possible age of the cercopithecin from Abu diagnostic of the African Colobina; specimens of this species are Dhabi mentioned above. known as old as 3.4 Ma (Harrison, 2011). Earlier (unnamed) Papionina (Papio–Theropithecus) The oldest published remains of members of this genus date back to 3.8e3.5 Ma at Laetoli Theropithecus correspond to cf. Theropithecus sp. from Kanapoi (Tanzania; Harrison, 2011) and perhaps to "Cercopithecoides" (Kenya, ~4.2 Ma; Harris et al., 2003; Jablonski and Frost, 2010), kerioensis from an indeterminate level at Lothagam, Kenya, whereas the earliest species of Papio would be the younger Papio probably dating to ~5e4Ma(Leakey et al., 2003). Libypithecus robinsoni (see Gilbert et al., 2018). Therefore, the minimum bound markgrafi from Wadi Natrun, Egypt (roughly dated to 6.2e5.0 Ma should be set at 4.2 Ma based on the former. The maximum according to Werdelin, 2010) shares a maxillary sinus with bound would be in turn determined by the oldest possible age of several Cercopithecoides species, which might indicate a phyletic “P.” lothagamensis (7.4 Ma), which probably predates that of link, but this feature is not present in any extant colobine ?Macaca from Menacer (~7.0 Ma), irrespective of whether these (summarized in Frost et al., 2015). Several fossils from Asia have taxa are considered crown or stem papionins (see above). been referred to extant genera of Presbytina, but most are much younger than the above. Semnopithecus gwebinensis includes 3. Results isolated teeth from Myanmar dated to 4e3 Ma and assigned to the extant genus after careful comparative study (Takai et al., Phylogenetic reconstructions using ML and Bayesian algorithms 2016). Other Asian colobines include younger fossils allocated to revealed identical tree topologies and most nodes were strongly the extant genera Semnopithecus, Trachypithecus and supported (BS >95%, PP ¼ 1.0; Fig. 1). Only the branching patterns Rhinopithecus, as well as older large taxa which are not among the three Sulawesi macaque species (BS ¼ 73%, PP ¼ 0.99) definitively presbytinan as opposed to stem colobines (see, e.g., and the two western Papio [hamadryas] anubis and Papio [hama- Takai et al., 2015). All in all, the most conservative minimum dryas] papio (BS ¼ 74%, PP ¼ 0.97) as well as the basal position of bound (set-2) would be 3.5 Ma, based on the youngest possible southern Papio [hamadryas] ursinus among baboons (BS ¼ 82%, age of Cercopithecoides from Laetoli. The maximum bound would PP ¼ 1.0) gained lower statistical support. 120 C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132

Figure 1. Ultrametric tree showing phylogenetic relationships and divergence times among investigated Cercopithecinae taxa as inferred from BEAST analysis and calibration set-3 (the complete tree is shown in SOM Fig. S3). Node support <100% ML BS and <1.0 Bayesian PP is given at respective nodes (in italic), all other nodes are supported with 100% ML BS and 1.0 Bayesian PP. Red numbers indicate estimated mean divergence times of splits and node bars indicate 95% HPDs. The time scale below indicates million years before present. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Macaques segregated into seven well-supported clades or line- remaining baboons then segregated into a southern clade ages that correspond to the classification of the genus into seven combining northern P. [hamadryas] ursinus, southern Papio [ham- species groups (Zinner et al., 2013a; Roos et al., 2014). Among them, adryas] cynocephalus and Papio [hamadryas] kindae, and a northern the African M. sylvanus group diverged first, followed by an initial clade that further diverged into a western (western P. [hamadryas] separation of extant Asian macaques into a clade consisting of the anubis, P. [hamadryas] papio) and an eastern (eastern P. [hamadryas] M. silenus group and M. nigra group, and all remaining species anubis, P. [hamadryas] hamadryas, northern P. [hamadryas] cyn- groups. Among the latter, the M. sinica group diverged first, fol- ocephalus) subclade. lowed by the M. fascicularis group, while the M. arctoides group and A relaxed clock hypothesis was clearly favored over strict clock M. mulatta group separated last. Within the M. mulatta group, and non-clock hypotheses by the stepping stone analysis (non- M. mulatta is paraphyletic, with Indian M. mulatta representing a clock: mean ln ¼133677.80; strict clock: mean ln ¼133653.89; sister lineage to a clade consisting of Chinese M. mulatta, Macaca relaxed clock: mean ln ¼133622.35). Accordingly, all divergence fuscata and Macaca cyclopis. Note that these mtDNA-based patterns time calculations were performed under a relaxed clock model. differ slightly from phyletic geometry based on nucDNA (see sec- Estimated divergence times obtained from calculations using tion 4.1 below). different calibration sets are highly similar, although estimates for Also in baboons, various strongly supported clades were found, cercopithecoids from set-1 and set-2 are slightly more recent than but clade composition and phylogenetic relationships among them those from set-3 (Fig. 1; Table 2; SOM Table S3; SOM Figs. 1e3). The reflect more a geographic pattern and disagree with baboon divergence between Macaca and Papio/Theropithecus has been morphology and taxonomic classification. According to our phy- dated to 10.30e11.10 (95% highest posterior density logeny, southern P. [hamadryas] ursinus separated first. The [HPD] ¼ 8.80e12.82) Ma. Interestingly this node was used as C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 121

Table 2 Divergence time estimates for major splits. Given are the divergence estimates in Ma and their 95% HPDs in parentheses (for a full list of estimates see SOM Table S3).

Divergence Set 1 Set 2 Set 3 Nuclear DNAa

Macaca e Papio/Theropithecus 10.30 (8.90e11.81) 10.48 (8.80e12.16) 11.10 (9.39e12.82) 8.13 (6.69e9.68) Papio e Theropithecus 5.09 (4.36e5.87) 5.04 (4.33e5.79) 5.26 (4.47e6.05) 4.06 (3.36e4.70) LCAb Papio 2.26 (1.91e2.62) 2.18 (1.83e2.51) 2.29 (1.94e2.62) ~1.4 LCA Macaca 6.81 (5.90e7.74) 6.67 (5.68e7.64) 7.02 (6.05e8.00) 5.12 (4.27e5.93) LCA Asian macaques 6.09 (5.26e6.90) 5.97 (5.08e6.82) 6.28 (5.42e7.17) 4.13 (3.26e5.01)

a LCA Papio based on Rogers et al. (2019), all others based on Perelman et al. (2011). b LCA refers to the last common ancestor of the crown group (i.e., excluding members of the stem lineage).

calibration point and constrained with a soft maximum bound of lineages discordant phylogenetic relationships compared to the 8.0 Ma. Accordingly, the obtained estimates for this node are much mtDNA phylogeny were obtained. Besides incomplete lineage older than suggested from the fossil record. We also used the sorting (ILS), introgression and hybridization are discussed as main divergence between Papio and Theropithecus for calibration pur- reasons for such discordances (Salzburger et al., 2002; Seehausen, poses, but the obtained estimates of 5.04e5.26 (4.33e6.05) Ma are 2004; Arnold and Meyer, 2006; Zinner et al., 2009, 2011; Roos within the applied calibration range of 4.2e7.4 Ma. For the last et al., 2011). For instance, in macaques, nucDNA markers link common ancestor (LCA) of Papio we obtained an age of 2.18e2.29 M. arctoides with the M. sinica group and not with the M. mulatta (1.83e2.62) Ma and the radiation into the four major geographic group as indicated by mtDNA (Tosi et al., 2000, 2003; Deinard and lineages/clades (P. [h.] ursinus South, Papio southern clade, Papio Smith, 2001; Li et al., 2009; Jiang et al., 2016; Fan et al., 2018), northeastern clade, Papio northwestern clade) has been completed suggesting that M. arctoides is of hybrid origin. Similarly, genetic by 1.47e1.54 (1.23e1.79) Ma. In contrast, estimates for divergence data provide evidence for ancient hybridization between events within macaques are much older. The LCA of Macaca has M. mulatta and Macaca thibetana in China (Fan et al., 2014) and been dated at 6.67e7.02 (5.68e8.00) Ma and Asian macaques between M. mulatta and M. fascicularis on the Southeast Asian started to diversify 5.97e6.28 (5.08e7.17) Ma. The seven macaque mainland, north of the Isthmus of Kra (Tosi et al., 2002; Tosi and species groups have been established latest by 3.26e3.43 Coke, 2007; Kanthaswamy et al., 2008; Yan et al., 2011; Higashino (2.70e3.95) Ma. et al., 2012; Haus et al., 2014). Hybridization between the latter two species is an ongoing process with a wide active hybrid zone on 4. Discussion the Southeast Asian mainland (Hamada et al., 2006; Satkoski Trask et al., 2012). Another case of hybridization involves the Myanmar The aim of our study was to establish a robust and time-dated long-tailed macaque M. fascicularis aureus, which carries mtDNA mtDNA phylogeny of macaques and to compare it with that of related to members of the M. sinica group, while Y chromosomal baboons and with the macaque fossil record. Therefore, we used markers link the taxon, as expected, with M. fascicularis complete mtDNA genome data from 16 out of 23 extant macaque (Matsudaira et al., 2017). Further, several authors (Melnick and species and all six baboon (sub)species. For divergence time esti- Hoelzer, 1992; Morales and Melnick, 1998; Tosi et al., 2002, 2003; mations, we applied three well-grounded fossil-based calibration Tosi and Coke, 2007) have recognized mtDNA paraphyly of sets. Overall, we show that the obtained tree topology and molec- M. mulatta, with Indian M. mulatta representing a sister lineage to a ular divergence estimates are in general agreement with earlier clade consisting of Chinese M. mulatta, M. fuscata and M. cyclopis, studies and the fossil record. We also discuss differences in while nucDNA data suggest monophyly of M. mulatta (Melnick and branching pattern and dating results between phylogenies derived Hoelzer, 1992; Tosi et al., 2000, 2003). A discordant phylogenetic from mtDNA and nucDNA data. position between mtDNA and nucDNA is also found for Bornean M. nemestrina. While nucDNA data group individuals of this pop- 4.1. Phylogeny, hybridization and divergence times ulation with those from Sumatra and the Malay Peninsula, mtDNA suggests a close relationship with the Sulawesi macaques (Evans Our phylogenetic reconstructions using ML and Bayesian in- et al., 1999; Tosi et al., 2000, 2003). Also among Sulawesi ma- ferences revealed identical tree topologies with significant BS and caques, hybridization occurred in the past (Evans et al., 2001, 2017) PP values for most nodes. The obtained tree topology is in agree- and is still ongoing wherever the ranges of two species meet (Ciani ment with findings from earlier mtDNA studies (Tosi et al., 2002; et al., 1989; Watanabe and Matsumura, 1991; Watanabe et al., Evans et al., 2003; Ziegler et al., 2007; Zinner et al., 2013b; 1991a,b; Supriatna et al., 1992; Bynum et al., 1997; Evans et al., Liedigk et al., 2014, 2015; Jiang et al., 2016), but yielded stronger 2001, 2003). nodal support. Only the branching pattern among the Sulawesi Likewise, also for baboons mtDNA revealed various para- and macaque species, the basal position of southern P. [hamadryas] polyphyletic relationships suggesting that hybridization among ursinus among baboons, and the branching pattern in the north- taxa and populations has been common (Newman et al., 2004; western Papio clade gained lower supports. According to our phy- Zinner et al., 2009, 2013b; Keller et al., 2010; Liedigk et al., 2014). logeny, macaques segregate into seven well-supported clades or In contrast and as expected, nucDNA data support a six taxa clas- lineages that refer to the taxonomic classification of the genus into sification with a southern clade (P. [hamadryas] ursinus, P. [hama- seven species groups. In baboons, the mtDNA phylogeny disagrees dryas] cynocephalus and P. [hamadryas] kindae) and a northern with taxonomic classification and instead reflects more a clade (P.[hamadryas] anubis, P. [hamadryas] hamadryas and P. geographic, demic pattern. In particular, southern P. [hamadryas] [hamadryas] papio)(Boissinot et al., 2014; Walker et al., 2017; ursinus is suggested as the sister lineage to all other baboon line- Rogers et al., 2019), and support the hybridization and introgres- ages, while the remaining taxa diverged into southern, north- sion hypothesis (Walker et al., 2017; Rogers et al., 2019). Hybridi- western and northeastern clades. zation between baboon taxa can be observed also nowadays in Although studies using nucDNA markers revealed generally contact zones of various taxon pairs (Phillips-Conroy et al., 1991; similar phylogenies, for some baboon and macaque taxa and Alberts and Altmann, 2001; Bergman et al., 2008; Burrell, 2008; 122 C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132

Stevison and Kohn, 2009; Jolly et al., 2011; Charpentier et al., 2012; unclear. Delson (1973, 1975b) suggested that reports of sand in the Bergey, 2015). earlier Late Miocene of the Beglia Formation (Bled Douarah) might Our divergence times, estimated using different calibration sets, indicate that the Sahara was already becoming desertic and that it are generally similar and in agreement with previous estimates could have formed a zoogeographic barrier to cercopithecid (Perelman et al., 2011; Springer et al., 2012; Finstermeier et al., dispersal and gene flow. Thomas (1979) and Thomas et al. (1982) 2013; Zinner et al., 2013b; Pozzi et al., 2014; Liedigk et al., 2014, further discussed some of these ideas. More recently, additional 2015; Jiang et al., 2016; Yao et al., 2017). However, we obtained researchers have focused on the age of the Sahara as an arid belt. slightly older dates which can be largely attributed to the fact that Pickford (2000) discussed crocodiles from the Beglia Formation, we set different node constraints compared to other studies, which indicated the presence of large perennial rivers, presumably particularly for nodes within Papionini. For instance, earlier studies flowing across the Sahara toward the Mediterranean. He supported constrained the divergence between Papio and Theropithecus with an aridification of the region by 7 Ma from faunal evidence as well an age of 4.0 (4.5e3.5) Ma (Perelman et al., 2011; Finstermeier et al., as the deep-sea core studies of Tiedemann et al. (1989). Douady 2013; Zinner et al., 2013b; Jiang et al., 2016) or 5.0 (6.5e3.5) Ma et al. (2003) reported a molecular phylogenetic study of elephant (Pozzi et al., 2014; Liedigk et al., 2014, 2015; Yao et al., 2017), while shrews which suggested that the Sahara served as a vicariant bar- we allowed a window of 7.4e4.2 Ma. Further, some earlier studies rier by 11 Ma. Schuster et al. (2006a) argued for the presence of Late used an age of 5.5 Ma with ranges of ±0.4, 0.5 or 1.0 Ma for the Miocene (7e6 Ma?) eolian deposits in Chad (but see critical re- divergence between African and Asian macaques (Zinner et al., sponses by Kroepelin, 2006 and Swezey, 2006, as well as a counter- 2013b; Liedigk et al., 2014, 2015; Jiang et al., 2016; Yao et al., reply by Schuster et al., 2006b). In a longer review, Swezey (2009) 2017) and thus giving a maximum bound of 6.5e5.9 Ma, while argued that the Sahara was arid only during the Pleistocene (after we did not constrain this node at all. Instead, we constrained the 2.5 Ma). Zhang et al. (2014), however, suggested aridity during the divergence between Macacina and Papionina with hard minimum Late Miocene (11e7 Ma), and Bohme€ et al. (2017) reported Sahara- bounds of 5.8 or 5.0 Ma and a soft maximum bound of 8.0 Ma. This derived dust in Greek deposits yielding mammalian fossils by node was rarely used in earlier studies. Only Perelman et al. (2011) 7.4 Ma. In sum, it appears that , including cercopithecines, and Finstermeier et al. (2013) used this node and set an age of 7.0 might have been blocked at least at intervals between 11 and 5 Ma (8.0e6.0) Ma. Interestingly, Perelman et al.'s (2011) study, based from crossing the Sahara, thus keeping macaques separate from solely on nucDNA markers, estimated the split between both sub- papioninans in the Late Miocene. tribes at 8.13 (9.68e6.69) Ma, while mtDNA reveals generally older In turn, our molecular results indicate the appearance of the estimates, ~11e9 Ma (this study; see also Finstermeier et al., 2013; LCA of macaques 7.0e6.7 Ma, in line with the Late Miocene African Pozzi et al., 2014; Jiang et al., 2016). The reason for the discrepancy record of the genus (Delson, 1973, 1975a, 1980; Szalay and Delson, between mtDNA and nucDNA divergence time estimates for this 1979; Thomas and Petter, 1986; Benefit et al., 2008; Gilbert et al., node remains unknown and needs further investigations. However, 2014), which comprises isolated teeth from Menacer, Algeria divergence time estimates derived from mtDNA and nucDNA (Fig. 2; SOM Table S4), and perhaps Ongoliba, Congo, tentatively markers for nodes within macaques and baboons are generally assigned to the genus as ?Macaca sp. (~7.0e5.8 Ma), as well as the similar when the same calibration sets have been applied. For remains of M. libyca (6.2e5.0 Ma) from Wadi Natrun (Egypt) and instance, Jiang et al. (2016) investigated various nucDNA loci and Sahabi (Libya). It is uncertain whether this species belongs to the mtDNA from several macaques and revealed similar estimates from same lineage as M. sylvanus, but our molecular results suggest that both markers, although the 95% HPDs for nucDNA were extremely soon thereafter macaques separated into an African and Eurasian large. For baboons, nucDNA information is still limited. Rogers et al. lineage. Outside Africa, the oldest macaque fossils are recorded (2019) used mutation rate to calculate the LCA of Papio based on from Spain (5.9e5.3 Ma; Kohler€ et al., 2000; Marigo et al., 2014) whole genome data and revealed an age of ~1.4 Ma, which is and Italy (5.5e5.3 Ma; Alba et al., 2014a). Their absence in older slightly more recent than mtDNA-based estimates of ~2.2 Ma (this localities suggests that their dispersal from Africa coincided with study; Newman et al., 2004; Zinner et al., 2009, 2013b; Liedigk the sea level drop associated with the Messinian Salinity Crisis et al., 2014). Although differences in divergence time estimates (Alba et al., 2014a, 2015b). During this time interval (5.9e5.3 Ma), between mtDNA and nucDNA exist, several of these discordances the Mediterranean Sea became isolated from the Atlantic Ocean by can be explained by the use of different calibration sets, while the closing of the Mediterranean-Atlantic Straits (i.e., Betic and Rif others might be in fact real due to for example secondary gene flow Corridors) and subsequently desiccated, thus favoring terrestrial that occurred after the initial divergence of two taxa. Overall, dispersal routes out of Africa (Adams et al., 1977; Krijgsman et al., despite some disparities between different studies there is general 1999). However, intercontinental faunal exchanges began in fact consensus that extant macaques diversified around 7.0e5.5 Ma, even before the onset of the crisis (Agustí et al., 2006; Gibert et al., and extant baboons about 2.5e2.0 Ma. The divergence times esti- 2013). Indeed, as previously noted by Alba et al. (2015b),itis mated for macaque species groups and species clearly predate (sub) uncertain whether macaques dispersed from Africa into Europe species divergences in baboons and even partially the divergence through the Gibraltar area (e.g., Gibert et al., 2013), or following between Papio and Theropithecus. the longer route through the Middle East. The latter must have been available from pre-Messinian times, as evidenced not only by 4.2. Comparing mitochondrial divergence times with the fossil the earlier records of Mesopithecus (Alba et al., 2015b, and refer- record ences therein), but also by the record of a cercopithecin in Arabia ~8.0e6.5 Ma (Gilbert et al., 2014). Reaching Asia, macaques seem The currently known fossil record indicates that the divergence to have experienced a rapid and stepwise radiation into several between the two papionin subtribes (macacinans and papioninans) species groups between 6.3 and 3.3 Ma. Delson (1996) reported occurred before 5 Ma and allows us to establish a soft maximum the presence of cf. Macaca sp. in China ~5.5 Ma, but this has been bound for the divergence date at 8 Ma (Table 1). Based on these subsequently revised to indicate that the material most likely figures, our results provide a molecular dating for the divergence comes from Pliocene deposits (Alba et al., 2014a), so that the between 11 and 10 Ma. It is generally agreed that the expansion of presence of macaques in Asia before the early Pliocene remains to the Sahara desert belt may have been partly responsible for the be demonstrated (see below for further discussion). divergence of the two subtribes, but the date of such expansion is C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 123

Figure 2. Fossil sites in Africa and western Eurasia (numbers refer to fossil sites as in SOM Table 4; numbers of sites mentioned in text are underlined).

Unfortunately, the fossil record of macaques does not provide from early Pliocene to late Pleistocene across Europe from Portugal much clarification of these dates or branching events, but some to Ukraine (see Fig. 2), but few preserve more than teeth, jaws and data are relevant. The earliest macaque-like fossils, as discussed fragmentary limb bones. One specimen from Gajtan (Albania), above, occur across northern Africa in the Late Miocene (probably probably of later middle Pleistocene age, consists of partial left between 8.0 and 5.3 Ma). None of those specimens is complete facial elements, which may permit assessment of morphological enough to definitively identify them as Macaca as opposed to sub- similarities (if not relationships) within Macaca. A preliminary Saharan Parapapio or another as yet unknown genus, but referring study indicated links to M. sylvanus (Shearer and Delson, 2012), and them to macaques is most parsimonious. Cercopithecine teeth from a new reconstruction of the fossil is under study. All the fossil Spain and Italy dated between 5.9 and 5.3 Ma are similarly macaques from the Plio-Pleistocene of Europe are generally clas- ‘generalized’, but they are usually regarded as potential early rep- sified as time-successive subspecies of M. sylvanus, except for the resentatives of M. sylvanus, which agrees with the molecular insular endemic Macaca majori of Sardinia, which is currently divergence date for this species. Additional specimens range in age considered a distinct species but nevertheless thought to belong to 124 C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 the same clade (Delson, 1974, 1980; Szalay and Delson, 1979; Rook (2013) for geological background and history. Both sets of teeth and O'Higgins, 2005; Alba et al., 2008, 2011, 2016). While the spe- were purchased, and their exact provenance is unclear. They came cies allocation of these subspecies has been widely accepted, their from the Yuncu Subbasin, which preserves a long sequence from distinction from each other has been questioned due to the current ~6.7e2.2 Ma (with gaps). In 1988, E.D. was informed that the older lack of clear-cut distinguishing criteria (e.g., Alba et al., 2008, 2011). set of three isolated teeth (a colobine M3 and two papionin upper The fossil record of macaques (i.e., smaller cercopithecines) in molars purchased by Z.-x. Qiu) had been recovered from the Late Asia is less clear and in many ways less complete, despite the Miocene Mahui Fm., and he mentioned this in a brief abstract presence of several quite good specimens and samples. One of the (Delson, 1996). Later, he was told that in fact the specimens prob- major problems is the lack of a solid chronostratigraphic frame- ably derived from deposits correlated to the Gaozhuangian land work and the limited provenance data for many specimens. The age of early Pliocene age (~4.9e3.6 Ma) or possibly the earliest fossils are probably two collections from the Yushe Basin of early Mazegouan age (3.6e3.0 Ma). A second collection of 17 iso- central eastern China (Fig. 3; SOM Table S4)dsee Tedford et al. lated papionin upper cheek teeth can be sorted into two

Figure 3. Fossil sites in South, East and South-East Asia (numbers refer to fossil sites as in SOM Table 4; numbers of sites mentioned in text are underlined). C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 125 reconstructed partial toothrows (based on shape, size and contact Alternatively, Jablonski and Pan (1988) suggested that facets) with two isolated molars presumably of different in- M. anderssoni (including M. robusta) might be more closely related dividuals. They were purchased by L. Ginsburg and probably derive to the extant M. fuscata and M. cyclopis (and perhaps M. fascicularis) from Mazegouan deposits (3.6e2.6 Ma). Preliminary analysis in- on the basis of geography as well as limited morphology. Tong dicates that all papionin specimens are comparable in size to larger (2014) suggested that M. robusta might be closer to M. mulatta macaques, but as yet no further taxonomic allocation is possible. because of similarity in size and some morphological features. Two partial mandibular specimens of roughly comparable size These suggested relationships to the M. mulatta and M. fascicularis were first reported by Lydekker (1884) from ‘Upper Siwalik’ de- groups do not seem as likely as the links to M. thibetana and posits in India. They were originally thought to be colobine, and M. arctoides. The latter interpretation, similar to that of Delson some authors (e.g., Jablonski, 2002) subsequently identified them (1980) and in part to that of Fooden (1990), indicates potentially as such, but Delson (1980), Szalay and Delson (1979) and Delson great age in northern China for the currently more southerly et al. (2000) considered them definitively papionin. Their age is M. thibetana and M. assamensis (and perhaps M. arctoides). If cor- again uncertain, but perhaps between 3.2 and 1.7 Ma (see Barry, rect, the ancestry of M. thibetana could be traced back to at least 1987). They have not yet been associated with any extant ma- 1 Ma, while specimens similar to M. arctoides might occur as far caque clade. back as 2 Ma. Potentially more interesting specimens are known from the The genetic divergence dates of Figure 1 and SOM Table S3 can Pleistocene record of China. A nearly complete male face was re- be compared to these inferences. The split between M. sinica and ported by Schlosser (1924), who named it Macaca anderssoni. The the common ancestor of M. assamensis and M. thibetana was around specimen was recovered from Mianchi, in Henan province, north- 3 Ma, while the latter two species might have diverged around ern China, which is dated faunally between 2.5 and 1.0 Ma by 0.75 Ma. M. robusta would be well placed to represent the putative various authors (Delson, 1977,1980; Szalay and Delson, 1979; Tseng common ancestor. Based on mtDNA evidence, M. arctoides would et al., 2013). Qiu et al. (2004) referred a mandible from Longdan have separated from the LCA of the M. mulatta group ~3.4 Ma. The (Gansu Province, ~2 Ma) to this species, but direct comparison is latter divergence fits well with fossil data suggesting M. anderssoni not possible, and few authors have assessed this specimen. Young might have been present in northern China at this time. (1934) named Macaca robusta on the basis of several jaws from Pan et al. (1992) described a partial mandible they named Zhoukoudian locality 1 (now dated to roughly 800e400 ka; see Macaca jiangchuanensis from the ‘early Pleistocene’ of Jiangchuan, Shen et al., 2009), and Pei (1936) mentioned the find of a nearly southwestern China; however, associated fossils included taxa complete ‘skull’ similar to M. anderssoni, which was never similar to those of Zhoukoudian, so an early middle Pleistocene age described. Delson (1977, 1980; Szalay and Delson, 1979) located may be possible. Jablonski (1993) indicated that this fossil was casts of a male cranium and subadult female mandible in the morphologically similar to M. arctoides. Fang et al. (2002) named American Museum of Natural History, where they had been sent Macaca peii based on mandibular remains from Tuozi Cave, Tang- before the originals disappeared in 1941; these presumably shan (near Nanjing, Jiangsu Province), estimated to be ~2 Ma (see represent the specimen(s) noted by Pei (1936). Tong (2014) also Fang and Gu, 2007); an additional maxilla was reported by described additional Zhoukoudian specimens, including a partial Dong et al. (2013). Other than robusticity, no clear features distin- damaged subadult cranium. Jouffroy (1959) described a nearly guish this taxon. complete male cranium from the Late Pleistocene of Tung-lang, Other early macaque fossils belong to the M. fascicularis/ northern Vietnam, naming it Macaca speciosa subfossilis (at the M. mulatta group(s). As reviewed by Ito et al. (2014), there are time, M. speciosa was the name often used for M. arctoides). M. fascicularis fossils in Java dating to about 0.9 Ma, while in Delson (1980; see also Szalay and Delson, 1979) suggested that northeast Asia, M. cyclopis is known in Taiwan in the late early to all three putative (sub)species might be conspecific and related to middle Pleistocene (~1.0e0.4 Ma), and M. fuscata is found in Japan what he considered as the common ancestor of extant in the middle Pleistocene (probably 0.5e0.125 Ma). This supports M. assamensis, M. thibetana and M. arctoides. Fooden (1990) re- the idea that Taiwan and Japan were populated in the early middle evaluated the fossil crania and compared morphological details of Pleistocene by descendants of a southern M. mulatta-like ancestor, the zygoma and nasals. He suggested that M. s. subfossilis was which may have replaced populations related to M. thibetana in the indeed likely to be related to M. arctoides, probably a member of north. Ito et al. (2018) discussed a maxillofacial fragment from that species (sharing a derived zygomatic orientation). Ito et al. Korea which had previously been referred to M. robusta, but they (2009) also found shared derived features of the cranium in M. s. found that it was morphologically most similar to Japanese subfossilis and M. arctoides. Fooden (1990) further found that both M. fuscata; this suggests a wider geographic range for the latter but M. anderssoni and M. robusta from Zhoukoudian had relatively does not increase its known age range. Our genetic divergence small male canines (like M. arctoides) and a conservative zygomatic dating suggests that the M. mulatta group had separated from (like M. thibetana), but differed in nasal elevation (greater in M. arctoides around 3.4 Ma, and M. fuscata was distinct by about M. robusta) and thus might not be conspecific. The lower nasal 1.5 Ma; these dates fit well with the paleontological evidence. elevation in M. anderssoni is comparable to that of M. thibetana, but Fossils of M. mulatta are not definitively known in the middle Fooden (1990) did not indicate whether this was likely a derived or Pleistocene or before, but it would be interesting to locate these in ancestral condition. order to better understand their dispersal. The late Pleistocene of Ito et al. (2014) reported a novel derived feature in modern China has produced numerous fragmentary remains which are M. arctoides, M. thibetana and M. assamensis (the latter two often not identified to species, but the undated cave sites of Xiashan generally considered closely related). Their internal nasal cavity is and Shanbeiyan (Luoding county, Guangdong Province) were said laterally expanded anteriorly, while the posterior part of the cavity to yield fossils of M. assamensis, M. thibetana, M. mulatta and an is wide in M. arctoides but constricted in the latter two species. unidentified species (Gu et al., 1996). M. anderssoni follows the M. thibetana and M. assamensis pattern, Even more interesting is the report by Takai et al. (2014) sum- although the anterior expansion is slightly less than in the modern marizing primate fossils recovered from a series of 14 site units in taxa. Ito et al. (2014) concluded that M. anderssoni was most likely the Chongzuo region (Guangxi Province [ZAR], south-central China) related to some of these species or their possible common estimated to date between 2.2 Ma and 5 ka. They recovered at least ancestor. three size classes of macaque teeth: large M. cf. anderssoni from 126 C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 levels dating between 2.2 and 0.8 Ma, small specimens referred to phenotype. The differentiation of macaques into species groups and M. fascicularis which continued into the youngest levels but do not of the Papionina into genera took place over a similar time span. occur in China today, and intermediate-sized teeth possibly iden- The fact that macaques show relatively low morphological- tified as M. cf. arctoides, M. cf. nemestrina and/or M. cf. mulatta taxonomic disparity while being diverse molecularly suggests throughout the sequence. Further analysis may provide more de- that speciation in macaques could have been triggered by tails of the pattern of occurrence of different macaque species in geographical barriers, vicariance, and adaptation to local environ- southern China. ments. For instance, an early M. sinica member perhaps moved northward from India into China and became larger and shorter- 4.3. Evolutionary history of macaques and baboons tailed, a common morphological adaptation to cooler climates (‘Bergmann's Rule’; Bergmann, 1847; Smith et al., 1995; Ashton The lineage basal to all extant Asian macaques dispersed into et al., 2000; Buck et al., 2018). Eurasia and then diversified into several species groups and species in waves of radiation. Despite some disparities in the date of ma- caque origin, there is general consensus that macaques started to 4.4. Adaptations of macaques versus baboons diversify around 7.0e5.5 Ma in Africa. Leaving Africa, early ma- caques expanded their range into Europe and Asia. In Europe, Macaques and baboons are both successful and widespread M. sylvanus expanded its range northward only in interglacial ep- genera which receive a lot of attention in evolutionary, social and isodes and was restricted to Mediterranean areas during glacials medical science. Both groups are interesting because they differ in (Fooden, 2007; Elton and O'Regan, 2014), which coupled with their many aspects, although they belong to the same tribe of primates. sparse (even if geographically wide) record suggests that subopti- In terms of species number, macaques with 23 species clearly mal climate conditions posed some kind of barrier for macaque surmount baboons with only six (sub)species (Zinner et al., 2009, dispersal (Elton and O'Regan, 2014; Alba et al., 2016). However, 2013a,b; Roos et al., 2014). The great discrepancy in species which route the ancestor of Asian macaques might have taken numbers might simply be due to the longer evolutionary history of (northward into Eurasia during the Messinian, or via the Middle macaques. While baboons started to diversify around 2 Ma ma- East) is a matter of speculation, and even a dispersal event from caques had started around 7 Ma, giving macaques more time to Africa independent from that of the European macaques' ancestor diversify and adapt to local conditions. On the other hand, papio- cannot be discounted. ninans diversified into many extant and extinct genera over the It is remarkable that despite a long evolutionary history of more same time span. Macaques occur from tropical lowland, montane than five million years in Europe, the M. sylvanus lineage apparently rainforests and high-elevation areas to dry forests and woodland only gave rise to one other species (M. majori from Sardinia), con- areas (Zinner et al., 2013a). Even within species the widespread trasting with the much greater diversification documented in Asia, M. mulatta or M. fascicularis are variable in habitat use, depending where the impact of vicariance due to geographic barriers and on local conditions (Sha and Hanya, 2013). Their adaptability and founder events might have played a great role in macaque specia- ecological plasticity as generalists also allow macaques to live in tion (see below). It is also possible that the European macaque clade rural and urban areas and temples (Richard et al., 1989), as do ba- gave rise to the large, terrestrial Pliocene Paradolichopithecus. boons. Also widespread, baboons can be found in several different Earlier studies suggested that Miocene and Pliocene Himalayan habitat types such as semi-deserts, deciduous and dry forests, uplift, especially in the north and east, may have triggered plant woodlands, and arid bushland and shrubland, and they are equally and diversification (Zhao et al., 2016). Climate induced adaptable to different environments as macaques (Zinner et al., environmental changes that can promote dispersal of taxa through 2013a), although they are never fully arboreal. The great adapt- restricted corridors (e.g., evergreen forests during wet climate ep- ability of macaques and baboons to various habitats is also reflected isodes) can also lead to the separation of continuous landscapes, by their diets. Although predominantly frugivorous, both baboons promoting divergence of taxa (Abegg and Thierry, 2002; Ziegler and macaques are eclectic generalists and feed on literally almost et al., 2007). As a very dynamic geographic area in Asia, the Sun- everything that is available, from fruits, leaves and other plant parts daland region has been impacted by climatic fluctuations several to invertebrates and small vertebrates (Thierry, 2011; Swedell, times. In the Early Pliocene (5.3e4.5 Ma) sea levels were high, 2011). disrupting land bridges between the Sundaland islands and split- Interestingly, macaques presumably competed with Asian ting the Malay peninsula at the Isthmus of Kra (Bird et al., 2005; colobines, whose radiation probably began earlier and which Woodruff, 2003, 2010). This phase coincides with the ~4.5 Ma diversified into many genera and species. However, since Asian divergence of the M. silenus and M. nigra groups (which had colobines were most likely predominantly folivorous, the ‘frugiv- separated from the remaining macaques ~6.3 Ma). During this time, orous primate niche’ was probably not occupied everywhere in Asia range expansion throughout Sundaland was triggered by evergreen once most Miocene hominoids had become extinct and before forest due to wetter climate conditions (Morley, 2000). Later, the macaques started to diversify. If this was the case, Asian macaques ancestor of the Sulawesi macaques reached Sulawesi, most likely by had less interspecific food competition than baboons in Africa. natural rafting from east Borneo (Meijaard, 2003), and diversified Papio (or their ancestors) competed not only with its sister taxon into numerous taxa in a short period of time. The ancestor of Lophocebus (and to some extent Theropithecus), but also with M. silenus moved to Southwest India and was isolated there, Mandrillus/Cercocebus (and their fossil relatives) and with the probably due to shrinkage of suitable habitats (Ziegler et al., 2007). Cercopithecinidbut probably not much with African colobines Looking more broadly, in contrast to the morphologically less other than the extinct Cercopithecoides, which was quite terres- diverse Macacina, the Papionina exhibit greater disparity taxo- trialdremaining basically fully to moderately terrestrial animals. nomically and probably on a molecular scale. Papionina, in contrast Substrate preference also varies greatly among macaques and to a to macaques, went through several episodes of refugia and re- larger extent than in baboons. The only semiterrestrial cercopi- expansion of suitable habitat that might have driven speciation thecid competitor of macaques is Semnopithecus. The lack of large and adaptation to different habitats (Hamilton and Taylor, 1991; spans of fully open country resulted in few highly terrestrial ma- Maley, 1996) while macaques may only have adapted to local caques, although the extinct Procynocephalus flourished in some of habitats without restriction to refugia, leading to a less diverse those environments. C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 127

Overall, macaques are smaller in body size compared to baboons more typically found in open environments. Baboons are never (3e13 kg for females and 5e18 kg for males in macaques versus fully arboreal and show a greater diversity of social systems (uni- 10e12 kg for females and 16e35 kg for males in baboons; Delson level multi-male/multi-female with predominantly female phil- et al., 2000; Swedell, 2011; Thierry, 2011). The social organiza- opatry to complex multi-level systems with predominantly female tions of baboons and macaques differ in their complexity. While dispersal), while macaques do not range into semi-desert biomes macaques are organized in multi-male/multi-female units with and are organized in uni-level multi-male/multi-female groups female philopatry and male dispersal, baboons show multi-level with female philopatry and male dispersal. Baboons presumably systems and more complex organization (Grueter and Zinner, competed for food and habitat with a variety of other papioninans 2004; Grueter et al., 2012). For instance, P. [hamadryas] hama- (including extinct genera), cercopithecins, and even with the dryas and P. [hamadryas] papio are organized in multi-layered social extinct terrestrial colobine Cercopithecoides, which may have systems consisting of one-male units (OMUs), clans (parties), bands limited the number of Papio (sub)species. In contrast, macaques in (gangs) and troops (community) (Kummer, 1968; Abegglen, 1984; Asia had few frugivorous competitors (as their diversification Schreier and Swedell, 2009; Fischer et al., 2017). Also, both, male postdated the extinction of most hominoids, and the majority of the dispersal and female dispersal are present, and male philopatry and diverse colobine radiation is folivorous) and were not limited in female dispersal is common in P. [hamadryas] papio and P. [hama- their substrate preference other than by the rarity of large spans of dryas] hamadryas (Kopp et al., 2015). fully open country (as few colobines are or were even semi- terrestrial; e.g., Semnopithecus). 5. Summary and conclusions Acknowledgements We established a time-dated mtDNA phylogeny of macaques and compared it with that of baboons and the macaque fossil re- We thank the organizers of the symposium Frontiers in Baboon cord. To obtain divergence time estimates, we reviewed the fossil Research for inviting us to contribute to this special issue. D.M.A. record of catarrhine primates and determined likely branching and E.D. have been supported by the Generalitat de Catalunya dates for ten major nodes, which were then converted into three (CERCA Program), and the Spanish Agencia Estatal de Inves- calibration sets. The overall phylogeny is strongly supported and tigacion/European Regional Development Fund of the European estimated divergence times are highly similar and in agreement Union (CGL2016-76431-P and CGL2017-82654-P, AEI/FEDER, EU). with earlier studies. Accordingly, the divergence between Macaca E.D.'s work on macaque and baboon evolution was partially fun- e and Papio/Theropithecus was dated to 11.1 10.3 Ma. The divergence ded by grants (numbers 669381, 662495, 664333, 665407, 65295- of Papio and Theropithecus was estimated at ~5 Ma (based on the 43 and 66189-44) from the PSC-CUNY faculty research award oldest published Theropithecus fossil at 4.2 Ma) and the LCAs of program and by NSF 0966166 (NYCEP IGERT). We thank the editor e Papio and Macaca were dated at ~2.3 Ma and 7.0 6.7 Ma, respec- Sarah Elton and two anonymous reviewers for comments that tively. Hence, differentiation events in macaques clearly predate helped to improve a previous version of this paper. An earlier those in baboons. Moreover, in both genera we found paraphyletic version of this paper was presented at the symposium Frontiers in relationships suggesting that introgression and hybridization is Baboon Research supported by the German Science Foundation (FI likewise common in macaques and baboons. 707/21-1). A review of the fossil record of cercopithecines in North Africa indicated that putative macaque populations occurred between Supplementary Online Material ~7e5 Ma, close to the inferred date for the LCA of Macaca. The earliest European fossils allocated tentatively to the M. sylvanus Supplementary online material to this article can be found on- species group range in age from 5.9 to 5.3 Ma, again close to the line at https://doi.org/10.1016/j.jhevol.2019.05.017. estimated divergence between European and Asian macaques. The oldest Asian specimens putatively identified as Macaca probably date to 4.9e3.6 Ma in China, but they cannot be allocated to a References species group, nor can slightly younger fossils from the Upper e Abegg, C., Thierry, B., 2002. Macaque evolution and dispersal in insular south-east Siwaliks (probably ~3.2 1.7 Ma). Several more complete crania and Asia. Biological Journal of the Linnean Society 75, 555e576. mandibles are known from China and Vietnam. A probably late Abegglen, J.J., 1984. On Socialization in Hamadryas Baboons: A Field Study. Bucknell Early or early Middle Pleistocene mandible and a late Late Pleis- University Press, Lewisburg. Adams, C.G., Benson, R.H., Kidd, R.B., Ryan, W.B.F., Wright, R.C., 1977. 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Journal of Human Evolution 55, 1160e1163. on Java at c~0.9 Ma, while M. cyclopis is known in Taiwan in the late Alba, D.M., Carlos Calero, J.A., Mancheno,~ M.A., Montoya, P., Morales, J., Rook, L., Early to Middle Pleistocene and M. fuscata is found in Japan and 2011. Fossil remains of Macaca sylvanus florentina (Cocchi, 1872) (Primates, Korea in the Middle Pleistocene. Cercopithecidae) from the Early Pleistocene of Quibas (Murcia, Spain). Journal e The fact that macaques show relatively low morphological of Human Evolution 61, 703 718. Alba, D.M., 2012. Fossil apes from the Valles-Pened es Basin. Evolutionary Anthro- disparity while being diverse on a molecular scale indicates that pology 21, 254e269. speciation in macaques could have been triggered by geographical Alba, D.M., Delson, E., Carnevale, G., Colombero, S., Delfino, M., Giuntelli, P., barriers, vicariance, and adaptation to local environments. On the Pavia, M., Pavia, G., 2014a. First joint record of Mesopithecus and cf. 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