Journal of Human Evolution - NYCEPpages.nycep.org/ed/download/pdf/Delson_2019c.pdf · 2019. 10. 16. · concept, while D.M.A. and E.D. prefer to recognize them as a single (super)species

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Journal of Human Evolution 133 (2019) 114e132

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Journal of Human Evolution

journal homepage: www.elsevier .com/locate/ jhevol

The radiation of macaques out of Africa: Evidence from mitogenomedivergence 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, G€ottingen, Germanyb Gene Bank of Primates, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077, G€ottingen, Germanyc Institut Catal�a de Paleontologia Miquel Crusafont, Universitat Aut�onoma de Barcelona, Edifici ICTA-ICP, c/ Columnes s/n, Campus de la UAB, Cerdanyola delVall�es, 08193, Barcelona, Spaind Department of Anthropology, Lehman College of the City University of New York, 250 Bedford Park Boulevard West, Bronx, NY, 10468, USAe Department of Vertebrate Paleontology, American Museum of Natural History, 200 Central Park West, New York, NY, 10024, USAf The Graduate Center of the City University of New York, 365 Fifth Avenue, New York, NY, 10016, USAg New York Consortium in Evolutionary Primatology, New York, NY, USAh Cognitive Ethology Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077, G€ottingen, Germany

a r t i c l e i n f o

Article history:Received 15 July 2018Accepted 31 May 2019

Keywords:CercopithecoideaPapioniniPapioMacacaDispersal eventsFossils

* Corresponding authors.E-mail addresses: [email protected] (C. Roos), dzinner

https://doi.org/10.1016/j.jhevol.2019.05.0170047-2484/© 2019 Elsevier Ltd. All rights reserved.

a b s t r a c t

Fossil evidence indicates that numerous catarrhine clades of African origin expanded or shifted theirranges into Eurasia, among them macaques Macaca Lac�ep�ede, 1799. Macaques represent the sister taxonof 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 toestablish a well-resolved phylogeny of macaques with reliably estimated divergence times and tocompare it with that of baboons and the fossil record. Therefore, we used mitochondrial (mtDNA)genome data deposited in GenBank of 16 out of 23 extant macaque species and of all six baboon taxa. Wereconstructed phylogenetic trees using maximum-likelihood and Bayesian inferences and dated differ-entiation events using three fossil-based calibration sets. The obtained tree topology is in agreementwith findings from earlier mtDNA studies, but yielded stronger nodal supports. We observed some para-and polyphylies in macaques and baboons, suggesting that ancient gene flow among divergent lineageshas been common in both genera. Our divergence time estimates are in broad agreement with earlierfindings and with the fossil record. Macaques started to diversify 7.0e6.7 Ma, followed by a stepwiseradiation into several species groups in Asia, whereas baboons commenced diversification around2.2 Ma. Accordingly, divergence of species groups and species in macaques clearly predates divergencesin baboons. Based on our phylogenetic results with estimated divergence times and the recordedchronostratigraphic ranges of extinct macaque and baboon taxa, we compare the evolutionary radiationsof both genera from paleobiogeographic and adaptive viewpoints.

© 2019 Elsevier Ltd. All rights reserved.

1. Introduction

There is general consensus that the genus Homo originated inAfrica and that it dispersed several times into Eurasia (Beyin, 2006;Shea, 2008; Hublin, 2009; Green et al., 2010; Armitage et al., 2011;Ant�on et al., 2014; Groucutt et al., 2018; Hershkovitz et al., 2018;

@gwdg.de (D. Zinner).

Stringer and Galway-Witham, 2018). Members of the genusHomo, however, are not the only catarrhine primates of Africanorigin that expanded or shifted their ranges into Eurasia. Indeed,fossil evidence indicates that multiple catarrhine groups dispersedinto that continent (and some of them subsequently radiated there)throughout the Neogene and Quaternary, at least: (1) the unknownstem catarrhine that must have given rise to the Eurasian putativeclade known as the Pliopithecoidea (e.g., Begun, 2002, 2017;Harrison, 2013), first recorded ~18e17 Ma; (2) the ancestor of thesmall-bodied putative stem hominoid Pliobates, recorded in Europe11.6 Ma (Alba et al., 2015a), unless it is interpreted as a member of

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1 Taxonomy is a dynamic science, and species delimitations have to be regardedas taxonomic hypotheses. Due to the application of molecular methods and thephylogenetic species concept (Cracraft, 1983), the taxonomy of primates, as of othertaxa, has changed considerably. However, some of the changes in primate taxon-omy are debated, which is reflected in the divergent opinions among the authors ofthis contribution. Here M.K., D.Z. and C.R. recognize the six commonly acceptedextant baboon taxa as distinct species according to the phylogenetic speciesconcept, while D.M.A. and E.D. prefer to recognize them as a single (super)species(Papio hamadryas) with six subspecies (see Gilbert et al., 2018 for further details onthe pros and cons of the latter view). As a result, we refer to (sub)species whenwriting generally, or to Papio [hamadryas] ursinus, etc., when discussing a specifictaxon, in order to avoid a controversial disagreement. This is not a formalnomenclatural statement under the Code (ICZN, 1999). Note that Jolly (e.g., Jolly,1993) has implied that more than six equally distinct taxa may be recognizablewithin extant Papio. For macaques all authors agreed on seven species groups,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-ment might be useful.

2 Ethical note: We used only mtDNA genome sequences deposited in GenBank.No animals were sacrificed for the purpose of this study.

C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132 115

the pliopithecoid radiation (Nengo et al., 2017, but see Pugh et al.,2018 for the record of another non-pliopithecoid stem hominoidin Asia); (3) the as yet unidentified ancestor of the Hylobatidae,which are apparently not recorded until 7e6 Ma in China (Harrisonet al., 2008; Harrison, 2017); (4) large-bodied hominoids, firstrecorded by Griphopithecus and Kenyapithecus between 16.5 and14 Ma in Europe and Turkey (Heizmann and Begun, 2001; Andrewsand Kelley, 2007; Casanovas-Vilar et al., 2011; Harrison, 2017), andsubsequently by dryopithecines and pongines from ~13 Ma onward(Kelley, 2005; Alba, 2012; Begun, 2015; Gilbert et al., 2017); (5)colobines, as represented by Mesopithecus, first recorded at least8.5 Ma (Delson, 1974, 1975a; Alba et al., 2015b) and possibly aseparate clade including the ancestor of the extant Asian colobines;(6) cercopithecine monkeys, as recorded by a guenon from AbuDhabi dated to ~8.0e6.5 Ma (Gilbert et al., 2014); (7) early papio-nins assigned to cf. Macaca sp., first recorded 5.9e5.3 Ma (K€ohleret al., 2000; Alba et al., 2014a); (8) geladas (Theropithecus), firstrecorded in Eurasia 1.6e1.2 Ma (Alba et al., 2014b, and referencestherein); and (9) baboons Papio Erxleben, 1777, which dispersedinto Arabia 0.13e0.012 Ma according to molecular data (Winneyet al., 2004; Kopp et al., 2014).

Representing one of the most successful primate radiations,extant macaques exhibit the second largest geographic rangeamong primates, after humans. Macaques constitute the sistersubtribe (Macacina) of the predominantly African Papionina (Papio,Theropithecus, Rungwecebus, Lophocebus, Mandrillus and Cercoce-bus). Paleontological and molecular studies suggest an Africanorigin of macaques (Delson, 1980; Tosi et al., 2000; Jablonski andFrost, 2010; Liedigk et al., 2014, 2015). The most basal extantmember of the genusMacaca Lac�ep�ede, 1799, the Barbary macaque(Macaca sylvanus; e.g., Perelman et al., 2011), still occurs in NorthAfrica. It is the only extant member of the genus occurring outsideAsia, with a natural disjunct distribution in Morocco and Algeria(Fooden, 2007), as well as a colony of human-mediated origin inGibraltar (Modolo et al., 2005; Fooden, 2007).

After reaching Asia, macaques seem to have experienced a rapiddiversification into several species groups and species. Currently,macaques comprise seven species groups with 23 species (Zinneret al., 2013a; Roos et al., 2014; species counting updated after therecent description ofMacaca leucogenys by Li et al., 2015), althoughsome of the species may better be recognized as subspecies. Thenumber and composition of the macaque species groups have beendebated for decades. Originally, Fooden (1976) listed four speciesgroups based on male penile morphology, which Delson (1980)modified slightly to separate M. sylvanus from the Macaca silenus-M. sylvanus group (and link Macaca arctoides to the Macaca sinicagroup), while Groves (2001) recognized six species groups based onmolecular data. More recently, Zinner et al. (2013a) and Roos et al.(2014) proposed seven species groups and separated M. arctoidesfrom the Macaca fascicularis group, due to the putative hybridorigin of the former (Tosi et al., 2000, 2003; Jiang et al., 2016; Fanet al., 2018). Three of these groups are monotypic (at least, whenonly extant species are considered): those of M. sylvanus,M. arctoides, andM. fascicularis. The remaining groups are polytypicand contain 3e6 species each: Macaca mulatta group (3 species),M. silenus group (5 species), M. sinica group (6 species), and theMacaca nigra or Sulawesi macaque group (6 species).1

Various molecular phylogenies of macaques, using mainlymitochondrial DNA (mtDNA), but also nuclear DNA (nucDNA)markers, have been published in recent decades (Tosi et al., 2000,2003; Deinard and Smith, 2001; Evans et al., 2003, 2017; Ziegleret al., 2007; Li et al., 2009; Perelman et al., 2011; Liedigk et al.,2014, 2015; Fan et al., 2014, 2018; Roos and Zinner, 2015; Jianget al., 2016; Matsudaira et al., 2017; Yao et al., 2017; Roos, 2018),suggesting that macaques experienced rapid radiations

accompanied by numerous cases of secondary gene flow. Most ofthe studies usingmtDNA investigated only fragments of themtDNAgenome and were not able to solve the branching pattern amongmacaques with significance, while complete mtDNA genome dataallowed a much better resolution of the matrilineal phylogeny (e.g.,Liedigk et al., 2014, 2015; Jiang et al., 2016; Roos, 2018).

In this study, we rely on currently available mtDNA genome datato establish a robust and well-resolved phylogeny of macaques thatalso enables a reliable estimation of divergence times based on thecalibration using the fossil record. With this aim in mind, we pro-vide several calibration sets based on updated paleontological dataon fossil catarrhines. On the basis of our phylogenetic results andestimated divergence times, as well as in the recorded chro-nostratigraphic ranges of extinct macaque and baboon taxa, we alsocompare the evolutionary radiation of macaques (genus Macaca)with that of baboons (genus Papio) from paleobiogeographic andadaptive viewpointsdwith emphasis on various hypotheses thatmight explain the greater species diversity attained bymacaques ascompared to that of baboons. We focused on the maternally-inherited mtDNA as macaques and most baboon species arestrongly female philopatric (Grueter and Zinner, 2004; Grueteret al., 2012) and thus information about the primary radiation(before times of secondary gene-flow) of both genera can be ob-tained. However, when only a maternally-inherited marker isanalyzed the evolutionary history of a taxon remains incomplete.Consequently, we also discuss differences between mtDNA andpublished nucDNA phylogenies and respective divergence times.

2. Methods

2.1. Molecular data

To perform the phylogenetic analyses, we downloaded mtDNAgenome data from macaques, baboons and various outgroups fromGenBank.2 We did not include representatives of the genera Man-drillus, Cercocebus, Lophocebus and Rungwecebus as available dataare limited and, moreover, not the focus of our study. We screenedmtDNA genomes and selected those that (1) were complete, (2)contained no indications for the presence of nuclear copies ofmtDNA fragments (numts) by checking correct and full-lengthtranslation of the 13 protein-coding genes, (3) could be reliablyassigned to (sub)species by comparing them with partial sequencedata in GenBank, and (4) for macaques and baboons, cover as many(sub)species and populations as possible. Thirty-seven mtDNA ge-nomes matched these criteria and were chosen for further analyses

3 African and Asian colobines are either classified as tribes Colobini and Pres-bytini or as subtribes Colobina and Presbytina.

C. Roos et al. / Journal of Human Evolution 133 (2019) 114e132116

(for GenBank accession numbers, see Supplementary OnlineMaterial [SOM] Table S1). For instance, the mtDNA genomes fromputative Macaca nemestrina (KP765688.1) and M. nigra(KP072068.1) individuals were discarded as both cluster incorrectlywith the M. mulatta group. The 18 selected macaque sequencesrepresent all seven species groups and 16 out of 23 species, whilethe ten baboon sequences represent all six (sub)species and theseven major mtDNA clades (Zinner et al., 2009, 2013b).

2.2. Molecular analyses

Sequences were aligned with Muscle 3.8.31 (Edgar, 2010) inAliView 1.18 (Larsson, 2014) and corrected by eye. The final align-ment had a length of 16,927 bp and was reduced to 15,774 bp afterindels and poorly aligned positions were removed with Gblocks0.91b (Castresana, 2000). Phylogenetic trees were reconstructedwith maximum-likelihood (ML) and Bayesian algorithms using IQ-TREE 1.5.2 (Nguyen et al., 2015) and MrBayes 3.2.6 (Ronquist et al.,2012), respectively. The optimal model of sequence evolution(TIM2þIþG) was determined with ModelFinder (Chernomor et al.,2016; Kalyaanamoorthy et al., 2017) under the Bayesian Informa-tion Criterion (BIC) as implemented in IQ-TREE. The ML analysiswas performed with 10,000 ultrafast bootstrap (BS) replications(Minh et al., 2013). Bayesian trees were reconstructed via four in-dependent Markov Chain Monte Carlo (MCMC) runs. All repetitionswere run for 10 million generations with tree and parametersampling setting in every 100 generations. To check convergence ofall parameters and the adequacy of a 25% burn-in, we assessed theuncorrected potential scale reduction factor (PSRF; Gelman andRubin, 1992) as calculated by MrBayes. Posterior probabilities (PP)and a phylogram with mean branch lengths were calculated fromthe posterior density of trees in MrBayes.

In addition to producing a well-resolved phylogeny, estimatingreliable divergence times is a parallel goal of our research. Molec-ular dating can either be done by applying a known mutation rateor by setting node constraints using information from the fossilrecord, as we do below. Before estimating divergence times we firstchecked for the most appropriate clock model using the steppingstone method as implemented in MrBayes. For this analysis, weapplied the best-fit model of sequence evolution and investigatedthe mean marginal likelihoods (ln) for trees under strict, non-clockand relaxed clock hypotheses. Based on these results (see below),we estimated divergence times applying a relaxed clock model.Divergence time calculations were performed with the BEAST 2.4.8package (Bouckaert et al., 2014) using a relaxed lognormal clockmodel of lineage variation (Drummond et al., 2006) and applying aYule tree prior and the best-fit model of sequence evolution asobtained by ModelFinder. All BEAST analyses were run for 100million generations with tree and parameter sampling setting inevery 5000 generations. To assess the adequacy of a 10% burn-inand convergence of all parameters, we inspected the trace of theparameters across generations using Tracer 1.6 (Rambaut et al.,2014). We combined sampling distributions of multiple indepen-dent replicates with LogCombiner 2.4.8 and summarized trees (10%burn-in) using TreeAnnotator 2.4.8 (both programs are part of theBEAST package). All resulting trees were visualized in FigTree 1.4.2(Rambaut, 2014).

2.3. Paleontological calibration

To calibrate the molecular clock, we set constraints on ten nodesusing information from the fossil record (Table 1): (1) Hominoideae Cercopithecoidea; (2) Hominidae e Hylobatidae; (3) Ponginae e

Homininae; (4) Gorilla e (Pan þ Homo); (5) Homo e Pan; (6)Colobinae e Cercopithecinae; (7) Colobina e Presbytina3; (8)

Papionini e Cercopithecini; (9) Macacina e Papionina; (10) Papio e

Theropithecus. For all ten nodes, we applied a gamma-distributedprior with the minimum age of nodes (Table 1) as offset, an alphavalue of 2.0 and variable values for beta to reach the soft maximumbound (Table 1; for BEAST settings see SOM Table S2). Especiallysetting correct maximum constraints is challenging because thefossil record can only provide minimum divergence dates. How-ever, molecular clock analysis generally requires both minimumand maximum age constraints (see review in Benton andDonoghue, 2007): minimum divergence calibration dates are‘hard' bounds, in the sense that they are absolute (unless they arebased on an incorrect phylogenetic assumption), whereasmaximum dates are ‘soft’ bounds, because actual divergence datescould theoretically fall beyond them. Following Benton andDonoghue (2007), based on a combination of phylogenetic brack-eting (maximum ages of sister groups) and stratigraphic bounding(absence of fossils of the respective clade in an underlying suitablefossiliferous formation), hard minimum age constraints may bedetermined on the basis of the youngest possible age of the sedi-ments where the oldest integral member of a clade has been found;in turn, soft maximum age constraints may be determined based onthe oldest possible age of the sediments where the oldest membersof the sister-taxon or the stem lineage of the clade under consid-eration, but no members of the crown clade itself, have been found.

Besides dating uncertainties and the incompleteness of thefossil record, the most serious source of error that may be intro-duced by any calibration set arguably relates to the validity of theunderlying phylogenetic hypotheses. For this reason, we derivedtwo different sets: set-1 is less conservative, in the sense that itconsiders some older taxa whose phylogenetic status is debatable,thereby yielding older bounds; in contrast, set-2 is more conser-vative, in the sense that it relies on taxa for which there is ampleconsensus about their phylogenetic status, thereby resulting inyounger bounds. Some criterion is also required when selecting thetaxa to be considered for setting a maximum bound. If the sister-taxon of a given clade (e.g., crown catarrhines) is defined as theextant clade more closely related to it (platyrrhines), the maximumbound will be defined by the oldest member of the stem lineage ofthe focal clade (here stem catarrhines, i.e., propliopithecids) or ofthe sister-taxon (platyrrhines), irrespective of which members ofthe stem lineage are more closely related to the clade underconsideration. This approach has been used to derive set-1. How-ever, it might be argued that more reasonable maximum boundscould be established by focusing on the oldest member of the mostclosely related sister-taxon of the clade under consideration, irre-spective of whether that clade is extant or extinct (i.e., based on themost derived member of its stem lineage, here Saadanius, which isarguably the most derived known stem catarrhine). The latterapproach, which will generally provide younger maximum bounds,has been used to derive set-2. Only when the oldest recordedmember of the clade under consideration predates the mostderived member of the stem lineage would it be necessary toinspect successively more basal members of the stem lineage toestablish the maximum bound (this does not apply in the example,since Saadanius is older than the earliest putative crowncatarrhines).

We briefly explain below the rationale that underpins our se-lection of extinct taxa to derive the two aforementioned calibrationsets. Both sets have been combined into another one (set-3) by

Table 1Calibration sets based on extinct taxa, used in this work to estimate divergence times onmolecular grounds. Set-2 takes a more conservative view than set-1 with regard to theselection 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 (hardbound, in Ma)

Maximum (softbound, in Ma)

Hominoidea e

CercopithecoideaNsungwepithecus gunnelli and/orRukwapithecus fleaglei

Perupithecus ucayaliensis 25.2 36.0

Hominidae e

HylobatidaeKenyapithecus wickeri and Kenyapithecuskizili

Nsungwepithecus gunnelli and/or Rukwapithecusfleaglei

13.7 25.2

Ponginae e Homininae Sivapithecus indicus Kenyapithecus kizili 13.0 14.9Gorilla e (Pan þ Homo) Chororapithecus abyssinicus Sivapithecus indicus 8.0 13.0Homo e Pan Sahelanthropus tchadensis Chororapithecus abyssinicus 6.8 8.0Colobinae e

CercopithecinaeColobinae indet. (Kabasero) Nsungwepithecus gunnelli 12.5 25.2

Colobina e Presbytina Mesopithecus pentelicus Colobinae indet. (Kabasero) 8.5 12.5Papionini e

Cercopithecinicf. Papionini indet. (Chorora) Colobinae indet. (Kabasero) 8.0 12.5

Macacina e Papionina ?Macaca sp. (Menacer) and Macaca libyca Cercopithecini indet. (Baynunah) and cf. Papioniniindet. (Chorora)

5.8 8.0

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 (hardbound, in Ma)


Hominoidea e

CercopithecoideaProconsul meswae Saadanius hijazensis 20.0 29.0

Hominidae e


Proconsul meswae 13.7 20.0

Ponginae e Homininae Sivapithecus indicus Kenyapithecus kizili 13.0 14.9Gorilla e (Pan þ Homo) Sahelanthropus tchadensis Sivapithecus indicus 6.8 13.0Homo e Pan Ardipithecus kadabba Sahelanthropus tchadensis 5.5 7.2Colobinae e

CercopithecinaeColobinae indet. (Kabasero) Victoriapithecidae 12.5 20.0

Colobina e Presbytina Cercopithecoides sp. (Laetoli) Colobinae indet. (Kabasero) 3.5 12.5Papionini e

CercopitheciniCercopithecini indet. (Baynunah) Colobinae indet. (Kabasero) 6.5 12.5

Macacina e Papionina Macaca libyca and “Parapapio”lothagamensis

Cercopithecini indet. (Baynunah) and cf. Papioniniindet. (Chorora)

5.0 8.0


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


Hominoidea e

CercopithecoideaProconsul meswae Perupithecus ucayaliensis 20.0 36.0

Hominidae e


Nsungwepithecus gunnelli and/or Rukwapithecusfleaglei

13.7 25.2

Ponginae e Homininae Sivapithecus indicus Kenyapithecus kizili 13.0 14.9Gorilla e (Pan þ Homo) Sahelanthropus tchadensis Sivapithecus indicus 6.8 13.0Homo e Pan Ardipithecus kadabba Chororapithecus abyssinicus 5.5 8.0Colobinae e

CercopithecinaeColobinae indet. (Kabasero) Nsungwepithecus gunnelli 12.5 25.2

Colobina e Presbytina Cercopithecoides sp. (Laetoli) Colobinae indet. (Kabasero) 3.5 12.5Papionini e

Cercopithecinicf. Papionini indet. (Chorora) Colobinae indet. (Kabasero) 6.5 12.5

Macacina e Papionina Macaca libyca and “Parapapio”lothagamensis

Cercopithecini indet. (Baynunah) and cf. Papioniniindet. (Chorora)

5.0 8.0


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 maximumbound of both sets.Crown Catarrhini (Hominoidea–Cercopithecoidea) With an age of25.2 Ma, the oldest putative representatives of the crown catar-rhine clade are Nsungwepithecus gunnelli and Rukwapithecus flea-glei, respectively interpreted as a stem cercopithecoid and a stemhominoid (Stevens et al., 2013). Note that, since the material fromboth species comes from the same locality, it is irrelevantwhether one of these taxa is interpreted as a stem catarrhinepreceding the cercopithecoid-hominoid divergence, since theother taxon would still set the minimum bound at 25.2 Ma (set-1). It would require considering that both taxa are stemcatarrhines to discount such an age. In that case, even thoughseveral stem cercopithecoid (victoriapithecid) genera are known

from the Early Miocene (Miller et al., 2009; Jablonski and Frost,2010), they appear slightly younger than Proconsul meswae(>20.0 Ma; Harrison and Andrews, 2009). Even if some authorsstill consider Proconsul as a stem catarrhine preceding thecercopithecoid-hominoid divergence (Harrison, 2010), mostconsider this genus as a stem hominoid (e.g., Stevens et al., 2013;Begun, 2013, 2015; Alba et al., 2015a), which would consequentlyestablish a minimum bound of 20.0 Ma in set-2. The olderKamoyapithecus hamiltoni (~27e23 Ma) has been proposed as theearliest hominoid (Leakey et al., 1995), but preserved evidence isinconclusive and suggests instead it is best interpreted as a stemcatarrhine (Harrison, 2010, 2013; Seiffert, 2012; Begun, 2015). Asfor the maximum bound, in the most conservative approach (set-1) it would be established by the earliest putative stem


catarrhines or members of the closest extant sister taxon ofcatarrhines (i.e., platyrrhines). There are reasons to think thatoligopithecids are stem anthropoids preceding the platyrrhine-catarrhine divergence (Harrison, 2013). However, if they areconsidered stem catarrhines (e.g., Seiffert et al., 2010; Seiffert,2012), the maximum bound could be established by Catopithecusbrowni at ~34.0 Madif it was not for the fact that the oldestremains from South America tentatively assigned to stemplatyrrhines (Perupithecus ucayaliensis and some other unnamedgenera; Bond et al., 2015) may be somewhat older (~36 Ma). Thephylogenetic affinities of older but poorly-known taxa fromAfricadsuch as Talahpithecus parvus from Libya (39e38 Ma),previously considered an oligopithecoid (Jaeger et al., 2010) oreven a stem platyrrhine (Bond et al., 2015)dare uncertain(Seiffert, 2012), so that these taxa can be discounted. In contrast,the platyrrhine status of Perupithecus is reasonable onpaleobiogeographic grounds, thereby setting the maximumbound at 36 Ma in set-1, even if this dating is very tentative.Alternatively, the maximum bound could be established on thebasis of undoubted stem catarrhines, first represented by thepropliopithecid Propliopithecus ankeli at ~31.5 Ma (Seiffert et al.,2010). However, the advanced stem catarrhine Saadaniushijazensis (29e28 Ma) has been further proposed to set themaximum bound for the cercopithecoid-hominoid divergence(Zalmout et al., 2010), because it appears more closely related tocrown catarrhines than are propliopithecids (Seiffert, 2012;Harrison, 2013). This argument was criticized based on the claimthat stem taxa cannot inform about maximum bounds (Pozziet al., 2011), but this is not entirely correct as long as it isrecognized that maximum constraints are soft instead of hardbounds (Benton and Donoghue, 2007). If Saadanius is taken as theclosest sister-taxon of the crown catarrhine clade, then 29 Ma canbe arguably used as the maximum bound (set-2).Crown Hominoidea (Hylobatidae–Hominidae) TheMiocene recordof hylobatids is virtually non-existent, although the possibilitycannot be discounted that some small-bodied catarrhines fromEurasia known by very fragmentary remains might be stemhylobatids instead of stem catarrhines (i.e., pliopithecids). Albaet al. (2015a) noted some hylobatid-like features in Pliobates, butgiven the mosaic of stem catarrhine-like and modern hominoid-like features displayed by this taxon, these might be consideredas primitive features for crown hominoids as a whole. Indeed,Alba et al.'s (2015a) cladistic analysis failed to support a closerrelationship with hylobatids and instead supported a stemhominoid status for Pliobates, whereas independent analyses haveplaced it close to pliopithecids (Nengo et al., 2017). The nextMiocene hylobatid candidate is Yuanmoupithecus from China(7e6 Ma; Harrison et al., 2008; Harrison, 2016, 2017), whichclearly postdates the divergence between hylobatids andhominids considerably. As such, the minimum bound for thisnode must be established on the basis of the oldest record ofhominids (i.e., great apes). There is some controversy regardingwhat extinct taxa preceding dryopithecines must be consideredstem hominids instead of afropithecids (the latter generallyconsidered stem hominoids). Alba (2012) tentatively consideredthat kenyapithecines (including Equatorius, Nacholapithecus,Kenyapithecus and Griphopithecus) are hominids, but here wefollow a more conservative approach (e.g., Harrison, 2010) byconsidering that this is only relatively well substantiated forKenyapithecus wickeri (13.7 Ma), which shares withdryopithecines and crown hominids the possession of a highzygomatic root (Harrison, 1992, 2010; Alba, 2012). This genus isfurther recorded at Pasalar (Turkey) by a second species,Kenyapithecus kizili (see Kelley et al., 2008), which would beroughly dated to 14.9e13.7 Ma (Casanovas-Vilar et al., 2011). On

the basis of both species, the minimum bound is set to 13.7 Ma inboth sets. In turn, the maximum bound would be established bythe earliest stem hominoids or cercopithecoids (see above), i.e., at25.2 Ma by Nsungwepithecus and/or Rukwapithecus (set-1), or at20.0 by Proconsul (set-2).Crown Hominidae (Ponginae–Homininae) The divergence be-tween the orangutan and the African ape and human lineages(respectively, Ponginae and Homininae) is somewhat controversial,given the insistence of some researchers that the European Dry-opithecinae are stem hominines (e.g., Begun et al., 2012; Begun,2013, 2015) instead of stem hominids (e.g., Alba, 2012). Even ifwe discount dryopithecin and hispanopithecin dryopithecines(sensu Alba, 2012) as stem hominines, a reasonable case mightstill be made in the case of Ouranopithecus macedoniensis (firstrecorded at ~9.6 Ma; de Bonis and Koufos, 2004) andGraecopithecus freybergi (7.2 Ma; Koufos and de Bonis, 2005; Fusset al., 2017) from Greece. However, such debate is irrelevant here,since neither these nor putative hominines from Africa predatethe record of Sivapithecus in Asia, which is generally consideredas a member of the orangutan clade (Kelley, 2005; Alba, 2012;Begun, 2013, 2015). The oldest remains of this genus, with an ageof ~12.7 Ma, are generally assigned to Sivapithecus indicus (e.g.,Kelley, 2005). Even if they are not completely diagnostic of thegenus, at least they display derived features of the Ponginae(Begun, 2015) and therefore permit us to set the minimumbound. Other Sivapithecus-bearing sediments might be somewhatolder (Gilbert et al., 2017), suggesting that 13.0 Ma is a reasonableestimate of the minimum bound. The maximum bound, in turn,should be determined based on the hominid stem lineage (sincethe age of the oldest putative hylobatid known postdates theminimum bound; see above). Based on the oldest possible age ofKenyapithecus (see above), we set the maximum bound at 14.9 Ma.Crown Homininae (gorillas–chimpanzeesþhominins) The diver-gence date of the gorilla lineage from the rest of the African-ape-and-human clade is also controversial, given the virtual lack ofunquestionable Mio-Pliocene representatives of the African greatape lineages. Chororapithecus abyssinicus was proposed as a basalmember of the gorilla clade by Suwa et al. (2007), initially withan age of 10.5e10 Ma, which was subsequently revised to~8.0 Ma (Katoh et al., 2016). This taxon has been tentativelylinked to Nakalipithecus nakayamai (9.9e9.8 Ma; Kunimatsu et al.,2007; Katoh et al., 2016), also from Africa, which would slightlypredate the oldest record of the Eurasian Ouranopithecus. Thestatus of these taxa as crown hominines is very uncertain, withthe possible exception of Chororapithecus (Suwa et al., 2007;Katoh et al., 2016), which would enable us to set the minimumdivergence age at 8.0 Ma (set-1). If Chororapithecus is consideredinstead a stem hominine of uncertain affinities that might havepreceded the divergence of gorillas (Harrison, 2010), andNakalipithecus, Ouranopithecus and Graecopithecus are discountedon the same grounds, then the minimum bound would bedetermined at 6.8 Ma (set-2) by Sahelanthropus tchadensis(7.2e6.8 Ma: Brunet et al., 2002; Lebatard et al., 2008),irrespective of whether it is considered a hominin or a hominineof indeterminate affinities (see below). In turn, the maximumbound would be set by the oldest pongine (Sivapithecus) at 13.0Ma (see above), since it predates other extinct taxa proposed bysome authors as stem hominines (including dryopithecines, seeabove).Pan–Homo The known fossil record of putative extinct hominins ismuch older than that of chimpanzees, and goes back to the LateMiocene, including S. tchadensis (7.2e6.8 Ma: Brunet et al., 2002;Lebatard et al., 2008), Orrorin tugenensis (6.0e5.7 Ma: Senut et al.,2001; Sawada et al., 2002) and Ardipithecus kadabba (oldestremains: 5.78e5.5 Ma; Haile-Selassie, 2001; WoldeGabriel et al.,


2001; Haile-Selassie et al., 2004). Although the hominin status ofthe oldest of these putative hominins (Sahelanthropus) has beendisputed by some researchers (Wolpoff et al., 2006), in generalthe three above-mentioned genera are considered early homininsby most authors (e.g., MacLatchy et al., 2010; Simpson, 2013;White et al., 2015; Harrison, 2017). As such, Sahelanthropusenables us to set the minimum bound for the Pan-Homodivergence in set-1 at 6.8 Ma. Alternatively, if the evidenceprovided by Sahelanthropus and Orrorin is consideredinconclusive (set-2), that bound should be set at 5.5 Ma based onArdipithecusdeven if this genus is only well known on the basisof the early Pliocene species Ardipithecus ramidus (White et al.,2009, 2015). As for the maximum bound, Chororapithecus, ifconsidered a stem member of the gorilla lineage (see above),would set the maximum divergence age between the chimp andhuman lineages at 8.0 Ma (set-1). Alternatively, if the LateMiocene taxa from Africa are considered at most stem homininespreceding the divergence of gorillas (set-2), then the maximumbound for the Homo-Pan divergence would be determined by theoldest possible age of Sahelanthropus, which must be at leastinterpreted as a hominine preceding that divergence (Wolpoffet al., 2006).Cercopithecidae (Colobinae–Cercopithecinae) The minimumbound would be set at 12.5 Ma by the earliest known colobine,isolated teeth from Kabasero (Kenya; Rossie et al., 2013), whereasthe maximum bound would be determined at 25.2 Ma byN. gunnelli (set-1; assuming it is a cercopithecoid, see above), oralternatively (set-2) by the oldest victoriapithecids from the earlyMiocene, such as Prohylobates tandyi, first recorded at ~20.0 Ma(Miller et al., 2009).Colobinae (Colobina–Presbytina) The minimum bound might beset by Mesopithecus pentelicus, first recorded from the Greek lo-cality of Nikiti-2, correlated to the earliest Turolian (MN11; e.g.,Koufos, 2006), ~8.5 Ma, if it is assumed (set-1) that this genus isthe earliest recorded member of the Asian colobine clade(Presbytina). This was classically supported on biogeographicgrounds (Szalay and Delson, 1979) and more recently based oncladistic analyses (Jablonski, 1998, 2002). However, this is veryuncertain, and currently available evidence is consistent withMesopithecus being a stem colobine (Frost et al., 2015; Alba et al.,2015b). The oldest definitive member of either modern subtribeis Cercopithecoides williamsi from Koobi Fora (Kenya) dated to1.9 Ma (Frost et al., 2015), which preserves the reduced thumbdiagnostic of the African Colobina; specimens of this species areknown as old as 3.4 Ma (Harrison, 2011). Earlier (unnamed)members of this genus date back to 3.8e3.5 Ma at Laetoli(Tanzania; Harrison, 2011) and perhaps to "Cercopithecoides"kerioensis from an indeterminate level at Lothagam, Kenya,probably dating to ~5e4 Ma (Leakey et al., 2003). Libypithecusmarkgrafi from Wadi Natrun, Egypt (roughly dated to 6.2e5.0 Maaccording to Werdelin, 2010) shares a maxillary sinus withseveral Cercopithecoides species, which might indicate a phyleticlink, but this feature is not present in any extant colobine(summarized in Frost et al., 2015). Several fossils from Asia havebeen referred to extant genera of Presbytina, but most are muchyounger than the above. Semnopithecus gwebinensis includesisolated teeth from Myanmar dated to 4e3 Ma and assigned tothe extant genus after careful comparative study (Takai et al.,2016). Other Asian colobines include younger fossils allocated tothe extant genera Semnopithecus, Trachypithecus andRhinopithecus, as well as older large taxa which are notdefinitively presbytinan as opposed to stem colobines (see, e.g.,Takai et al., 2015). All in all, the most conservative minimumbound (set-2) would be 3.5 Ma, based on the youngest possibleage of Cercopithecoides from Laetoli. The maximum bound would

be set at 12.5 Ma by the Kabasero stem colobine (see above),which is older than the earliest known cercopithecine (see below).Cercopithecinae (Cercopithecini–Papionini) The oldest known(and well-dated) cercopithecines come from the ChororaFormation, with an age of ~8.0 Ma (Suwa et al., 2015). Some ofthese remains have been tentatively assigned to papionins andcoincide with the maximum possible age of an indeterminateguenon (Cercopithecini) from the Baynunah Formation, AbuDhabi (~8.0e6.5 Ma; Gilbert et al., 2014). It is difficult todistinguish stem cercopithecines from stem papionins, becausethe papionin dentition is plesiomorphic except for a lack oflingual enamel on lower incisors (Delson, 1973, 1980; Szalay andDelson, 1979), and these teeth are not preserved at Chorora. If thepapionin status of the latter is accepted (set-1), the minimumbound for the cercopithecin-papionin divergence can be set at8.0 Ma. Otherwise (set-2), the minimum bound would be set bythe cercopithecin from Abu Dhabi, whose minimum possible age(6.5 Ma) is older than those of other Miocene papionins fromAfrica (see below). As for the maximum bound, given the lack ofolder stem cercopithecines, it would be set by the oldest colobinefrom Kabasero at 12.5 Ma (see above).Papionini (Macacina–Papionina) The oldest unambiguous papio-nins include ?Macaca sp. (using the modern nomen as a paleon-tological ‘form genus’) from Menacer (formerly Marceau), Algeria(Delson, 1975a, 1980; Szalay and Delson, 1979), ~7.0e5.8 Ma(following Werdelin, 2010), Macaca libyca from Wadi Natrun,Egypt and possibly As Sahabi, Libya (Delson, 1975a, 1980; Szalayand Delson, 1979; Benefit et al., 2008), respectively 6.2e5.0 Maand 6.3e5.3 Ma (Werdelin, 2010), and "Parapapio" lothagamensisfrom Lothagam (~7.4e5.0 Ma; Leakey et al., 2003; Jablonski andFrost, 2010). In spite of taxonomic uncertainties, both theMenacer and the Lothagam samples must belong to the Papioninibased on the lack of lingual enamel on lower incisors. Therefore,a minimum bound of 5.8 Ma appears justified for the (stem)MacacinaePapionina divergence in set-1 based on ?Macaca fromMenacer. Alternatively, since it is debatable whether the Menacerfossils correspond to a macacinan or to a stem papionin (giventhe lack of diagnostic features unambiguously linking it withextant taxa; Benefit, 2008), M. libyca and “P.” lothagamensis moresecurely establish the above-mentioned minimum bound in set-2at 5.0 Ma. With regard to the maximum bound, it would be set at8.0 Ma by the age of the putative papionins from Chorora as wellas the maximum possible age of the cercopithecin from AbuDhabi mentioned above.Papionina (Papio–Theropithecus) The oldest published remains ofTheropithecus correspond to cf. Theropithecus sp. from Kanapoi(Kenya, ~4.2 Ma; Harris et al., 2003; Jablonski and Frost, 2010),whereas the earliest species of Papio would be the younger Papiorobinsoni (see Gilbert et al., 2018). Therefore, the minimum boundshould be set at 4.2 Ma based on the former. The maximumbound would be in turn determined by the oldest possible age of“P.” lothagamensis (7.4 Ma), which probably predates that of?Macaca from Menacer (~7.0 Ma), irrespective of whether thesetaxa are considered crown or stem papionins (see above).

3. Results

Phylogenetic reconstructions using ML and Bayesian algorithmsrevealed identical tree topologies and most nodes were stronglysupported (BS >95%, PP ¼ 1.0; Fig. 1). Only the branching patternsamong the three Sulawesi macaque species (BS ¼ 73%, PP ¼ 0.99)and the two western Papio [hamadryas] anubis and Papio [hama-dryas] papio (BS ¼ 74%, PP ¼ 0.97) as well as the basal position ofsouthern Papio [hamadryas] ursinus among baboons (BS ¼ 82%,PP ¼ 1.0) gained lower statistical support.

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 BSand 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-ages that correspond to the classification of the genus into sevenspecies groups (Zinner et al., 2013a; Roos et al., 2014). Among them,the African M. sylvanus group diverged first, followed by an initialseparation of extant Asian macaques into a clade consisting of theM. silenus group and M. nigra group, and all remaining speciesgroups. Among the latter, the M. sinica group diverged first, fol-lowed by theM. fascicularis group, while theM. arctoides group andM. mulatta group separated last. Within the M. mulatta group,M. mulatta is paraphyletic, with Indian M. mulatta representing asister lineage to a clade consisting of Chinese M. mulatta, Macacafuscata andMacaca cyclopis. Note that these mtDNA-based patternsdiffer slightly from phyletic geometry based on nucDNA (see sec-tion 4.1 below).

Also in baboons, various strongly supported clades were found,but clade composition and phylogenetic relationships among themreflect more a geographic pattern and disagree with baboonmorphology and taxonomic classification. According to our phy-logeny, southern P. [hamadryas] ursinus separated first. The

remaining baboons then segregated into a southern cladecombining northern P. [hamadryas] ursinus, southern Papio [ham-adryas] cynocephalus and Papio [hamadryas] kindae, and a northernclade that further diverged into a western (western P. [hamadryas]anubis, P. [hamadryas] papio) and an eastern (eastern P. [hamadryas]anubis, P. [hamadryas] hamadryas, northern P. [hamadryas] cyn-ocephalus) subclade.

A relaxed clock hypothesis was clearly favored over strict clockand non-clock hypotheses by the stepping stone analysis (non-clock: mean ln ¼ �133677.80; strict clock: mean ln ¼ �133653.89;relaxed clock: mean ln ¼ �133622.35). Accordingly, all divergencetime calculations were performed under a relaxed clock model.Estimated divergence times obtained from calculations usingdifferent calibration sets are highly similar, although estimates forcercopithecoids from set-1 and set-2 are slightly more recent thanthose from set-3 (Fig. 1; Table 2; SOM Table S3; SOM Figs. 1e3). Thedivergence between Macaca and Papio/Theropithecus has beendated to 10.30e11.10 (95% highest posterior density[HPD] ¼ 8.80e12.82) Ma. Interestingly this node was used as

Table 2Divergence 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) ~1.4LCA 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 of8.0 Ma. Accordingly, the obtained estimates for this node are mucholder than suggested from the fossil record. We also used thedivergence between Papio and Theropithecus for calibration pur-poses, but the obtained estimates of 5.04e5.26 (4.33e6.05) Ma arewithin the applied calibration range of 4.2e7.4 Ma. For the lastcommon ancestor (LCA) of Papio we obtained an age of 2.18e2.29(1.83e2.62) Ma and the radiation into the four major geographiclineages/clades (P. [h.] ursinus South, Papio southern clade, Papionortheastern clade, Papio northwestern clade) has been completedby 1.47e1.54 (1.23e1.79) Ma. In contrast, estimates for divergenceevents within macaques are much older. The LCA of Macaca hasbeen dated at 6.67e7.02 (5.68e8.00) Ma and Asian macaquesstarted to diversify 5.97e6.28 (5.08e7.17) Ma. The seven macaquespecies groups have been established latest by 3.26e3.43(2.70e3.95) Ma.

4. Discussion

The aim of our study was to establish a robust and time-datedmtDNA phylogeny of macaques and to compare it with that ofbaboons and with the macaque fossil record. Therefore, we usedcomplete mtDNA genome data from 16 out of 23 extant macaquespecies and all six baboon (sub)species. For divergence time esti-mations, we applied three well-grounded fossil-based calibrationsets. Overall, we show that the obtained tree topology and molec-ular divergence estimates are in general agreement with earlierstudies and the fossil record. We also discuss differences inbranching pattern and dating results between phylogenies derivedfrom mtDNA and nucDNA data.

4.1. Phylogeny, hybridization and divergence times

Our phylogenetic reconstructions using ML and Bayesian in-ferences revealed identical tree topologies with significant BS andPP values for most nodes. The obtained tree topology is in agree-ment with findings from earlier mtDNA studies (Tosi et al., 2002;Evans et al., 2003; Ziegler et al., 2007; Zinner et al., 2013b;Liedigk et al., 2014, 2015; Jiang et al., 2016), but yielded strongernodal support. Only the branching pattern among the Sulawesimacaque species, the basal position of southern P. [hamadryas]ursinus among baboons, and the branching pattern in the north-western Papio clade gained lower supports. According to our phy-logeny, macaques segregate into seven well-supported clades orlineages that refer to the taxonomic classification of the genus intoseven species groups. In baboons, the mtDNA phylogeny disagreeswith taxonomic classification and instead reflects more ageographic, demic pattern. In particular, southern P. [hamadryas]ursinus is suggested as the sister lineage to all other baboon line-ages, while the remaining taxa diverged into southern, north-western and northeastern clades.

Although studies using nucDNA markers revealed generallysimilar phylogenies, for some baboon and macaque taxa and

lineages discordant phylogenetic relationships compared to themtDNA phylogeny were obtained. Besides incomplete lineagesorting (ILS), introgression and hybridization are discussed as mainreasons for such discordances (Salzburger et al., 2002; Seehausen,2004; Arnold and Meyer, 2006; Zinner et al., 2009, 2011; Rooset al., 2011). For instance, in macaques, nucDNA markers linkM. arctoides with the M. sinica group and not with the M. mulattagroup as indicated by mtDNA (Tosi et al., 2000, 2003; Deinard andSmith, 2001; Li et al., 2009; Jiang et al., 2016; Fan et al., 2018),suggesting that M. arctoides is of hybrid origin. Similarly, geneticdata provide evidence for ancient hybridization betweenM. mulatta and Macaca thibetana in China (Fan et al., 2014) andbetween M. mulatta and M. fascicularis on the Southeast Asianmainland, north of the Isthmus of Kra (Tosi et al., 2002; Tosi andCoke, 2007; Kanthaswamy et al., 2008; Yan et al., 2011; Higashinoet al., 2012; Haus et al., 2014). Hybridization between the lattertwo species is an ongoing process with awide active hybrid zone onthe Southeast Asian mainland (Hamada et al., 2006; Satkoski Trasket al., 2012). Another case of hybridization involves the Myanmarlong-tailed macaque M. fascicularis aureus, which carries mtDNArelated to members of the M. sinica group, while Y chromosomalmarkers link the taxon, as expected, with M. fascicularis(Matsudaira et al., 2017). Further, several authors (Melnick andHoelzer, 1992; Morales and Melnick, 1998; Tosi et al., 2002, 2003;Tosi and Coke, 2007) have recognized mtDNA paraphyly ofM. mulatta, with IndianM. mulatta representing a sister lineage to aclade consisting of Chinese M. mulatta, M. fuscata and M. cyclopis,while nucDNA data suggest monophyly of M. mulatta (Melnick andHoelzer, 1992; Tosi et al., 2000, 2003). A discordant phylogeneticposition between mtDNA and nucDNA is also found for BorneanM. nemestrina. While nucDNA data group individuals of this pop-ulation with those from Sumatra and the Malay Peninsula, mtDNAsuggests a close relationship with the Sulawesi macaques (Evanset al., 1999; Tosi et al., 2000, 2003). Also among Sulawesi ma-caques, hybridization occurred in the past (Evans et al., 2001, 2017)and is still ongoing wherever the ranges of two species meet (Cianiet al., 1989; Watanabe and Matsumura, 1991; Watanabe et al.,1991a,b; Supriatna et al., 1992; Bynum et al., 1997; Evans et al.,2001, 2003).

Likewise, also for baboons mtDNA revealed various para- andpolyphyletic relationships suggesting that hybridization amongtaxa and populations has been common (Newman et al., 2004;Zinner et al., 2009, 2013b; Keller et al., 2010; Liedigk et al., 2014).In contrast and as expected, nucDNA data support a six taxa clas-sification with a southern clade (P. [hamadryas] ursinus, P. [hama-dryas] cynocephalus and P. [hamadryas] kindae) and a northernclade (P. [hamadryas] anubis, P. [hamadryas] hamadryas and P.[hamadryas] papio) (Boissinot et al., 2014; Walker et al., 2017;Rogers et al., 2019), and support the hybridization and introgres-sion hypothesis (Walker et al., 2017; Rogers et al., 2019). Hybridi-zation between baboon taxa can be observed also nowadays incontact zones of various taxon pairs (Phillips-Conroy et al., 1991;Alberts and Altmann, 2001; Bergman et al., 2008; Burrell, 2008;


Stevison and Kohn, 2009; Jolly et al., 2011; Charpentier et al., 2012;Bergey, 2015).

Our divergence times, estimated using different calibration sets,are generally similar and in agreement with previous estimates(Perelman et al., 2011; Springer et al., 2012; Finstermeier et al.,2013; Zinner et al., 2013b; Pozzi et al., 2014; Liedigk et al., 2014,2015; Jiang et al., 2016; Yao et al., 2017). However, we obtainedslightly older dates which can be largely attributed to the fact thatwe set different node constraints compared to other studies,particularly for nodes within Papionini. For instance, earlier studiesconstrained the divergence between Papio and Theropithecus withan age of 4.0 (4.5e3.5) Ma (Perelman et al., 2011; Finstermeier et al.,2013; Zinner et al., 2013b; Jiang et al., 2016) or 5.0 (6.5e3.5) Ma(Pozzi et al., 2014; Liedigk et al., 2014, 2015; Yao et al., 2017), whilewe allowed a window of 7.4e4.2 Ma. Further, some earlier studiesused an age of 5.5 Ma with ranges of ±0.4, 0.5 or 1.0 Ma for thedivergence between African and Asian macaques (Zinner et al.,2013b; Liedigk et al., 2014, 2015; Jiang et al., 2016; Yao et al.,2017) and thus giving a maximum bound of 6.5e5.9 Ma, whilewe did not constrain this node at all. Instead, we constrained thedivergence between Macacina and Papionina with hard minimumbounds of 5.8 or 5.0 Ma and a soft maximum bound of 8.0 Ma. Thisnode was rarely used in earlier studies. Only Perelman et al. (2011)and Finstermeier et al. (2013) used this node and set an age of 7.0(8.0e6.0) Ma. Interestingly, Perelman et al.'s (2011) study, basedsolely on nucDNA markers, estimated the split between both sub-tribes at 8.13 (9.68e6.69) Ma, while mtDNA reveals generally olderestimates, ~11e9 Ma (this study; see also Finstermeier et al., 2013;Pozzi et al., 2014; Jiang et al., 2016). The reason for the discrepancybetween mtDNA and nucDNA divergence time estimates for thisnode remains unknown and needs further investigations. However,divergence time estimates derived from mtDNA and nucDNAmarkers for nodes within macaques and baboons are generallysimilar when the same calibration sets have been applied. Forinstance, Jiang et al. (2016) investigated various nucDNA loci andmtDNA from several macaques and revealed similar estimates fromboth markers, although the 95% HPDs for nucDNA were extremelylarge. For baboons, nucDNA information is still limited. Rogers et al.(2019) used mutation rate to calculate the LCA of Papio based onwhole genome data and revealed an age of ~1.4 Ma, which isslightly more recent than mtDNA-based estimates of ~2.2 Ma (thisstudy; Newman et al., 2004; Zinner et al., 2009, 2013b; Liedigket al., 2014). Although differences in divergence time estimatesbetween mtDNA and nucDNA exist, several of these discordancescan be explained by the use of different calibration sets, whileothers might be in fact real due to for example secondary gene flowthat occurred after the initial divergence of two taxa. Overall,despite some disparities between different studies there is generalconsensus that extant macaques diversified around 7.0e5.5 Ma,and extant baboons about 2.5e2.0 Ma. The divergence times esti-mated formacaque species groups and species clearly predate (sub)species divergences in baboons and even partially the divergencebetween Papio and Theropithecus.

4.2. Comparing mitochondrial divergence times with the fossilrecord

The currently known fossil record indicates that the divergencebetween the two papionin subtribes (macacinans and papioninans)occurred before 5 Ma and allows us to establish a soft maximumbound for the divergence date at 8 Ma (Table 1). Based on thesefigures, our results provide a molecular dating for the divergencebetween 11 and 10 Ma. It is generally agreed that the expansion ofthe Sahara desert belt may have been partly responsible for thedivergence of the two subtribes, but the date of such expansion is

unclear. Delson (1973, 1975b) suggested that reports of sand in theearlier Late Miocene of the Beglia Formation (Bled Douarah) mightindicate that the Sahara was already becoming desertic and that itcould have formed a zoogeographic barrier to cercopitheciddispersal and gene flow. Thomas (1979) and Thomas et al. (1982)further discussed some of these ideas. More recently, additionalresearchers have focused on the age of the Sahara as an arid belt.Pickford (2000) discussed crocodiles from the Beglia Formation,which indicated the presence of large perennial rivers, presumablyflowing across the Sahara toward the Mediterranean. He supportedan aridification of the region by 7 Ma from faunal evidence as wellas the deep-sea core studies of Tiedemann et al. (1989). Douadyet al. (2003) reported a molecular phylogenetic study of elephantshrews which suggested that the Sahara served as a vicariant bar-rier by 11Ma. Schuster et al. (2006a) argued for the presence of LateMiocene (7e6 Ma?) eolian deposits in Chad (but see critical re-sponses by Kroepelin, 2006 and Swezey, 2006, as well as a counter-reply by Schuster et al., 2006b). In a longer review, Swezey (2009)argued that the Sahara was arid only during the Pleistocene (after2.5 Ma). Zhang et al. (2014), however, suggested aridity during theLate Miocene (11e7 Ma), and B€ohme et al. (2017) reported Sahara-derived dust in Greek deposits yielding mammalian fossils by7.4Ma. In sum, it appears that mammals, including cercopithecines,might have been blocked at least at intervals between 11 and 5 Mafrom crossing the Sahara, thus keeping macaques separate frompapioninans in the Late Miocene.

In turn, our molecular results indicate the appearance of theLCA of macaques 7.0e6.7 Ma, in line with the Late Miocene Africanrecord of the genus (Delson, 1973, 1975a, 1980; Szalay and Delson,1979; Thomas and Petter, 1986; Benefit et al., 2008; Gilbert et al.,2014), which comprises isolated teeth from Menacer, Algeria(Fig. 2; SOM Table S4), and perhaps Ongoliba, Congo, tentativelyassigned to the genus as ?Macaca sp. (~7.0e5.8 Ma), as well as theremains of M. libyca (6.2e5.0 Ma) from Wadi Natrun (Egypt) andSahabi (Libya). It is uncertain whether this species belongs to thesame lineage as M. sylvanus, but our molecular results suggest thatsoon thereafter macaques separated into an African and Eurasianlineage. Outside Africa, the oldest macaque fossils are recordedfrom Spain (5.9e5.3 Ma; K€ohler et al., 2000; Marig�o et al., 2014)and Italy (5.5e5.3 Ma; Alba et al., 2014a). Their absence in olderlocalities suggests that their dispersal from Africa coincided withthe sea level drop associated with the Messinian Salinity Crisis(Alba et al., 2014a, 2015b). During this time interval (5.9e5.3 Ma),the Mediterranean Sea became isolated from the Atlantic Ocean bythe closing of the Mediterranean-Atlantic Straits (i.e., Betic and RifCorridors) and subsequently desiccated, thus favoring terrestrialdispersal routes out of Africa (Adams et al., 1977; Krijgsman et al.,1999). However, intercontinental faunal exchanges began in facteven before the onset of the crisis (Agustí et al., 2006; Gibert et al.,2013). Indeed, as previously noted by Alba et al. (2015b), it isuncertain whether macaques dispersed from Africa into Europethrough the Gibraltar area (e.g., Gibert et al., 2013), or followingthe longer route through the Middle East. The latter must havebeen available from pre-Messinian times, as evidenced not only bythe earlier records of Mesopithecus (Alba et al., 2015b, and refer-ences therein), but also by the record of a cercopithecin in Arabia~8.0e6.5 Ma (Gilbert et al., 2014). Reaching Asia, macaques seemto have experienced a rapid and stepwise radiation into severalspecies groups between 6.3 and 3.3 Ma. Delson (1996) reportedthe presence of cf. Macaca sp. in China ~5.5 Ma, but this has beensubsequently revised to indicate that the material most likelycomes from Pliocene deposits (Alba et al., 2014a), so that thepresence of macaques in Asia before the early Pliocene remains tobe demonstrated (see below for further discussion).

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 providemuch clarification of these dates or branching events, but somedata are relevant. The earliest macaque-like fossils, as discussedabove, occur across northern Africa in the Late Miocene (probablybetween 8.0 and 5.3 Ma). None of those specimens is completeenough to definitively identify them as Macaca as opposed to sub-Saharan Parapapio or another as yet unknown genus, but referringthem tomacaques is most parsimonious. Cercopithecine teeth fromSpain and Italy dated between 5.9 and 5.3 Ma are similarly‘generalized’, but they are usually regarded as potential early rep-resentatives of M. sylvanus, which agrees with the moleculardivergence date for this species. Additional specimens range in age

from early Pliocene to late Pleistocene across Europe from Portugalto Ukraine (see Fig. 2), but few preserve more than teeth, jaws andfragmentary limb bones. One specimen from Gajtan (Albania),probably of later middle Pleistocene age, consists of partial leftfacial elements, which may permit assessment of morphologicalsimilarities (if not relationships) within Macaca. A preliminarystudy indicated links toM. sylvanus (Shearer and Delson, 2012), anda new reconstruction of the fossil is under study. All the fossilmacaques from the Plio-Pleistocene of Europe are generally clas-sified as time-successive subspecies of M. sylvanus, except for theinsular endemic Macaca majori of Sardinia, which is currentlyconsidered a distinct species but nevertheless thought to belong to


the same clade (Delson, 1974, 1980; Szalay and Delson, 1979; Rookand O'Higgins, 2005; Alba et al., 2008, 2011, 2016). While the spe-cies allocation of these subspecies has been widely accepted, theirdistinction from each other has been questioned due to the currentlack of clear-cut distinguishing criteria (e.g., Alba et al., 2008, 2011).

The fossil record of macaques (i.e., smaller cercopithecines) inAsia is less clear and in many ways less complete, despite thepresence of several quite good specimens and samples. One of themajor problems is the lack of a solid chronostratigraphic frame-work and the limited provenance data for many specimens. Theearliest fossils are probably two collections from the Yushe Basin ofcentral eastern China (Fig. 3; SOM Table S4)dsee Tedford et al.

Figure 3. Fossil sites in South, East and South-East Asia (numbers refer to fossil sites as in

(2013) for geological background and history. Both sets of teethwere purchased, and their exact provenance is unclear. They camefrom the Yuncu Subbasin, which preserves a long sequence from~6.7e2.2 Ma (with gaps). In 1988, E.D. was informed that the olderset of three isolated teeth (a colobine M3 and two papionin uppermolars purchased by Z.-x. Qiu) had been recovered from the LateMiocene Mahui Fm., and he mentioned this in a brief abstract(Delson, 1996). Later, he was told that in fact the specimens prob-ably derived from deposits correlated to the Gaozhuangian landmammal age of early Pliocene age (~4.9e3.6 Ma) or possibly theearly Mazegouan age (3.6e3.0 Ma). A second collection of 17 iso-lated papionin upper cheek teeth can be sorted into two

SOM Table 4; numbers of sites mentioned in text are underlined).


reconstructed partial toothrows (based on shape, size and contactfacets) with two isolated molars presumably of different in-dividuals. They were purchased by L. Ginsburg and probably derivefrom Mazegouan deposits (3.6e2.6 Ma). Preliminary analysis in-dicates that all papionin specimens are comparable in size to largermacaques, but as yet no further taxonomic allocation is possible.

Two partial mandibular specimens of roughly comparable sizewere first reported by Lydekker (1884) from ‘Upper Siwalik’ de-posits in India. They were originally thought to be colobine, andsome authors (e.g., Jablonski, 2002) subsequently identified themas such, but Delson (1980), Szalay and Delson (1979) and Delsonet al. (2000) considered them definitively papionin. Their age isagain uncertain, but perhaps between 3.2 and 1.7 Ma (see Barry,1987). They have not yet been associated with any extant ma-caque clade.

Potentially more interesting specimens are known from thePleistocene record of China. A nearly complete male face was re-ported by Schlosser (1924), who named it Macaca anderssoni. Thespecimen was recovered from Mianchi, in Henan province, north-ern China, which is dated faunally between 2.5 and 1.0 Ma byvarious authors (Delson, 1977, 1980; Szalay and Delson, 1979; Tsenget al., 2013). Qiu et al. (2004) referred a mandible from Longdan(Gansu Province, ~2 Ma) to this species, but direct comparison isnot possible, and few authors have assessed this specimen. Young(1934) named Macaca robusta on the basis of several jaws fromZhoukoudian locality 1 (now dated to roughly 800e400 ka; seeShen et al., 2009), and Pei (1936) mentioned the find of a nearlycomplete ‘skull’ similar to M. anderssoni, which was neverdescribed. Delson (1977, 1980; Szalay and Delson, 1979) locatedcasts of a male cranium and subadult female mandible in theAmerican Museum of Natural History, where they had been sentbefore the originals disappeared in 1941; these presumablyrepresent the specimen(s) noted by Pei (1936). Tong (2014)described additional Zhoukoudian specimens, including a partialdamaged subadult cranium. Jouffroy (1959) described a nearlycomplete male cranium from the Late Pleistocene of Tung-lang,northern Vietnam, naming it Macaca speciosa subfossilis (at thetime, M. speciosa was the name often used for M. arctoides).

Delson (1980; see also Szalay and Delson, 1979) suggested thatall three putative (sub)species might be conspecific and related towhat he considered as the common ancestor of extantM. assamensis, M. thibetana and M. arctoides. Fooden (1990) re-evaluated the fossil crania and compared morphological details ofthe zygoma and nasals. He suggested that M. s. subfossilis wasindeed likely to be related to M. arctoides, probably a member ofthat species (sharing a derived zygomatic orientation). Ito et al.(2009) also found shared derived features of the cranium in M. s.subfossilis and M. arctoides. Fooden (1990) further found that bothM. anderssoni and M. robusta from Zhoukoudian had relativelysmall male canines (likeM. arctoides) and a conservative zygomatic(like M. thibetana), but differed in nasal elevation (greater inM. robusta) and thus might not be conspecific. The lower nasalelevation inM. anderssoni is comparable to that ofM. thibetana, butFooden (1990) did not indicate whether this was likely a derived orancestral condition.

Ito et al. (2014) reported a novel derived feature in modernM. arctoides, M. thibetana and M. assamensis (the latter twogenerally considered closely related). Their internal nasal cavity islaterally expanded anteriorly, while the posterior part of the cavityis wide in M. arctoides but constricted in the latter two species.M. anderssoni follows the M. thibetana and M. assamensis pattern,although the anterior expansion is slightly less than in the moderntaxa. Ito et al. (2014) concluded that M. anderssoni was most likelyrelated to some of these species or their possible commonancestor.

Alternatively, Jablonski and Pan (1988) suggested thatM. anderssoni (including M. robusta) might be more closely relatedto the extantM. fuscata andM. cyclopis (and perhapsM. fascicularis)on the basis of geography as well as limited morphology. Tong(2014) suggested that M. robusta might be closer to M. mulattabecause of similarity in size and some morphological features.These suggested relationships to the M. mulatta and M. fascicularisgroups do not seem as likely as the links to M. thibetana andM. arctoides. The latter interpretation, similar to that of Delson(1980) and in part to that of Fooden (1990), indicates potentiallygreat age in northern China for the currently more southerlyM. thibetana and M. assamensis (and perhaps M. arctoides). If cor-rect, the ancestry of M. thibetana could be traced back to at least1 Ma, while specimens similar to M. arctoides might occur as farback as 2 Ma.

The genetic divergence dates of Figure 1 and SOM Table S3 canbe compared to these inferences. The split between M. sinica andthe common ancestor ofM. assamensis andM. thibetanawas around3 Ma, while the latter two species might have diverged around0.75 Ma. M. robustawould be well placed to represent the putativecommon ancestor. Based on mtDNA evidence, M. arctoides wouldhave separated from the LCA of the M. mulatta group ~3.4 Ma. Thelatter divergence fits well with fossil data suggesting M. anderssonimight have been present in northern China at this time.

Pan et al. (1992) described a partial mandible they namedMacaca jiangchuanensis from the ‘early Pleistocene’ of Jiangchuan,southwestern China; however, associated fossils included taxasimilar to those of Zhoukoudian, so an early middle Pleistocene agemay be possible. Jablonski (1993) indicated that this fossil wasmorphologically similar to M. arctoides. Fang et al. (2002) namedMacaca peii based on mandibular remains from Tuozi Cave, Tang-shan (near Nanjing, Jiangsu Province), estimated to be ~2 Ma (seealso Fang and Gu, 2007); an additional maxilla was reported byDong et al. (2013). Other than robusticity, no clear features distin-guish this taxon.

Other early macaque fossils belong to the M. fascicularis/M. mulatta group(s). As reviewed by Ito et al. (2014), there areM. fascicularis fossils in Java dating to about 0.9 Ma, while innortheast Asia, M. cyclopis is known in Taiwan in the late early tomiddle Pleistocene (~1.0e0.4 Ma), and M. fuscata is found in Japanin the middle Pleistocene (probably 0.5e0.125 Ma). This supportsthe idea that Taiwan and Japan were populated in the early middlePleistocene by descendants of a southern M. mulatta-like ancestor,which may have replaced populations related toM. thibetana in thenorth. Ito et al. (2018) discussed a maxillofacial fragment fromKorea which had previously been referred to M. robusta, but theyfound that it was morphologically most similar to JapaneseM. fuscata; this suggests a wider geographic range for the latter butdoes not increase its known age range. Our genetic divergencedating suggests that the M. mulatta group had separated fromM. arctoides around 3.4 Ma, and M. fuscata was distinct by about1.5 Ma; these dates fit well with the paleontological evidence.Fossils of M. mulatta are not definitively known in the middlePleistocene or before, but it would be interesting to locate these inorder to better understand their dispersal. The late Pleistocene ofChina has produced numerous fragmentary remains which areoften not identified to species, but the undated cave sites of Xiashanand Shanbeiyan (Luoding county, Guangdong Province) were saidto yield fossils of M. assamensis, M. thibetana, M. mulatta and anunidentified species (Gu et al., 1996).

Even more interesting is the report by Takai et al. (2014) sum-marizing primate fossils recovered from a series of 14 site units inthe Chongzuo region (Guangxi Province [ZAR], south-central China)estimated to date between 2.2 Ma and 5 ka. They recovered at leastthree size classes of macaque teeth: large M. cf. anderssoni from


levels dating between 2.2 and 0.8 Ma, small specimens referred toM. fascicularis which continued into the youngest levels but do notoccur in China today, and intermediate-sized teeth possibly iden-tified as M. cf. arctoides, M. cf. nemestrina and/or M. cf. mulattathroughout the sequence. Further analysis may provide more de-tails of the pattern of occurrence of different macaque species insouthern China.

4.3. Evolutionary history of macaques and baboons

The lineage basal to all extant Asian macaques dispersed intoEurasia and then diversified into several species groups and speciesin waves of radiation. Despite some disparities in the date of ma-caque origin, there is general consensus that macaques started todiversify around 7.0e5.5 Ma in Africa. Leaving Africa, early ma-caques expanded their range into Europe and Asia. In Europe,M. sylvanus expanded its range northward only in interglacial ep-isodes and was restricted to Mediterranean areas during glacials(Fooden, 2007; Elton and O'Regan, 2014), which coupled with theirsparse (even if geographically wide) record suggests that subopti-mal climate conditions posed some kind of barrier for macaquedispersal (Elton and O'Regan, 2014; Alba et al., 2016). However,which route the ancestor of Asian macaques might have taken(northward into Eurasia during the Messinian, or via the MiddleEast) is a matter of speculation, and even a dispersal event fromAfrica independent from that of the European macaques' ancestorcannot be discounted.

It is remarkable that despite a long evolutionary history of morethan fivemillion years in Europe, theM. sylvanus lineage apparentlyonly gave rise to one other species (M. majori from Sardinia), con-trasting with the much greater diversification documented in Asia,where the impact of vicariance due to geographic barriers andfounder events might have played a great role in macaque specia-tion (see below). It is also possible that the Europeanmacaque cladegave rise to the large, terrestrial Pliocene Paradolichopithecus.

Earlier studies suggested that Miocene and Pliocene Himalayanuplift, especially in the north and east, may have triggered plantand animal diversification (Zhao et al., 2016). Climate inducedenvironmental changes that can promote dispersal of taxa throughrestricted corridors (e.g., evergreen forests during wet climate ep-isodes) can also lead to the separation of continuous landscapes,promoting divergence of taxa (Abegg and Thierry, 2002; Ziegleret al., 2007). As a very dynamic geographic area in Asia, the Sun-daland region has been impacted by climatic fluctuations severaltimes. In the Early Pliocene (5.3e4.5 Ma) sea levels were high,disrupting land bridges between the Sundaland islands and split-ting the Malay peninsula at the Isthmus of Kra (Bird et al., 2005;Woodruff, 2003, 2010). This phase coincides with the ~4.5 Madivergence of the M. silenus and M. nigra groups (which hadseparated from the remaining macaques ~6.3 Ma). During this time,range expansion throughout Sundaland was triggered by evergreenforest due to wetter climate conditions (Morley, 2000). Later, theancestor of the Sulawesi macaques reached Sulawesi, most likely bynatural rafting from east Borneo (Meijaard, 2003), and diversifiedinto numerous taxa in a short period of time. The ancestor ofM. silenus moved to Southwest India and was isolated there,probably due to shrinkage of suitable habitats (Ziegler et al., 2007).

Looking more broadly, in contrast to the morphologically lessdiverse Macacina, the Papionina exhibit greater disparity taxo-nomically and probably on a molecular scale. Papionina, in contrastto macaques, went through several episodes of refugia and re-expansion of suitable habitat that might have driven speciationand adaptation to different habitats (Hamilton and Taylor, 1991;Maley, 1996) while macaques may only have adapted to localhabitats without restriction to refugia, leading to a less diverse

phenotype. The differentiation of macaques into species groups andof the Papionina into genera took place over a similar time span.The fact that macaques show relatively low morphological-taxonomic disparity while being diverse molecularly suggeststhat speciation in macaques could have been triggered bygeographical barriers, vicariance, and adaptation to local environ-ments. For instance, an early M. sinica member perhaps movednorthward from India into China and became larger and shorter-tailed, a common morphological adaptation to cooler climates(‘Bergmann's Rule’; Bergmann, 1847; Smith et al., 1995; Ashtonet al., 2000; Buck et al., 2018).

4.4. Adaptations of macaques versus baboons

Macaques and baboons are both successful and widespreadgenera which receive a lot of attention in evolutionary, social andmedical science. Both groups are interesting because they differ inmany aspects, although they belong to the same tribe of primates.In terms of species number, macaques with 23 species clearlysurmount baboons with only six (sub)species (Zinner et al., 2009,2013a,b; Roos et al., 2014). The great discrepancy in speciesnumbers might simply be due to the longer evolutionary history ofmacaques. While baboons started to diversify around 2 Ma ma-caques had started around 7 Ma, giving macaques more time todiversify and adapt to local conditions. On the other hand, papio-ninans diversified into many extant and extinct genera over thesame time span. Macaques occur from tropical lowland, montanerainforests and high-elevation areas to dry forests and woodlandareas (Zinner et al., 2013a). Even within species the widespreadM. mulatta or M. fascicularis are variable in habitat use, dependingon local conditions (Sha and Hanya, 2013). Their adaptability andecological plasticity as generalists also allow macaques to live inrural and urban areas and temples (Richard et al., 1989), as do ba-boons. Also widespread, baboons can be found in several differenthabitat types such as semi-deserts, deciduous and dry forests,woodlands, and arid bushland and shrubland, and they are equallyadaptable to different environments as macaques (Zinner et al.,2013a), although they are never fully arboreal. The great adapt-ability of macaques and baboons to various habitats is also reflectedby their diets. Although predominantly frugivorous, both baboonsand macaques are eclectic generalists and feed on literally almosteverything that is available, from fruits, leaves and other plant partsto invertebrates and small vertebrates (Thierry, 2011; Swedell,2011).

Interestingly, macaques presumably competed with Asiancolobines, whose radiation probably began earlier and whichdiversified into many genera and species. However, since Asiancolobines were most likely predominantly folivorous, the ‘frugiv-orous primate niche’was probably not occupied everywhere in Asiaonce most Miocene hominoids had become extinct and beforemacaques started to diversify. If this was the case, Asian macaqueshad less interspecific food competition than baboons in Africa.Papio (or their ancestors) competed not only with its sister taxonLophocebus (and to some extent Theropithecus), but also withMandrillus/Cercocebus (and their fossil relatives) and with theCercopithecinidbut probably not much with African colobinesother than the extinct Cercopithecoides, which was quite terres-trialdremaining basically fully to moderately terrestrial animals.Substrate preference also varies greatly among macaques and to alarger extent than in baboons. The only semiterrestrial cercopi-thecid competitor of macaques is Semnopithecus. The lack of largespans of fully open country resulted in few highly terrestrial ma-caques, although the extinct Procynocephalus flourished in some ofthose environments.


Overall, macaques are smaller in body size compared to baboons(3e13 kg for females and 5e18 kg for males in macaques versus10e12 kg for females and 16e35 kg for males in baboons; Delsonet al., 2000; Swedell, 2011; Thierry, 2011). The social organiza-tions of baboons and macaques differ in their complexity. Whilemacaques are organized in multi-male/multi-female units withfemale philopatry and male dispersal, baboons show multi-levelsystems and more complex organization (Grueter and Zinner,2004; Grueter et al., 2012). For instance, P. [hamadryas] hama-dryas and P. [hamadryas] papio are organized inmulti-layered socialsystems consisting of one-male units (OMUs), clans (parties), bands(gangs) and troops (community) (Kummer, 1968; Abegglen, 1984;Schreier and Swedell, 2009; Fischer et al., 2017). Also, both, maledispersal and female dispersal are present, andmale philopatry andfemale dispersal is common in P. [hamadryas] papio and P. [hama-dryas] hamadryas (Kopp et al., 2015).

5. Summary and conclusions

We established a time-dated mtDNA phylogeny of macaquesand compared it with that of baboons and the macaque fossil re-cord. To obtain divergence time estimates, we reviewed the fossilrecord of catarrhine primates and determined likely branchingdates for ten major nodes, which were then converted into threecalibration sets. The overall phylogeny is strongly supported andestimated divergence times are highly similar and in agreementwith earlier studies. Accordingly, the divergence between Macacaand Papio/Theropithecuswas dated to 11.1e10.3 Ma. The divergenceof Papio and Theropithecus was estimated at ~5 Ma (based on theoldest published Theropithecus fossil at 4.2 Ma) and the LCAs ofPapio and Macaca were dated at ~2.3 Ma and 7.0e6.7 Ma, respec-tively. Hence, differentiation events in macaques clearly predatethose in baboons. Moreover, in both genera we found paraphyleticrelationships suggesting that introgression and hybridization islikewise common in macaques and baboons.

A review of the fossil record of cercopithecines in North Africaindicated that putative macaque populations occurred between~7e5 Ma, close to the inferred date for the LCA of Macaca. Theearliest European fossils allocated tentatively to the M. sylvanusspecies group range in age from 5.9 to 5.3 Ma, again close to theestimated divergence between European and Asian macaques. Theoldest Asian specimens putatively identified as Macaca probablydate to 4.9e3.6 Ma in China, but they cannot be allocated to aspecies group, nor can slightly younger fossils from the UpperSiwaliks (probably ~3.2e1.7 Ma). Several more complete crania andmandibles are known from China and Vietnam. A probably lateEarly or early Middle Pleistocene mandible and a late Late Pleis-tocene or Holocene cranium appear to be on theM. arctoides clade,while a late Early Pleistocene face (M. anderssoni) seems to besimilar to M. thibetana, suggesting that at least the latter speciesmight date back to around 1 Ma. Middle Pleistocene M. robustafrom Zhoukoudian and other northern sites cannot yet be assignedto a species group. Specimens allocated toM. fascicularis are knownon Java at c~0.9 Ma, whileM. cyclopis is known in Taiwan in the lateEarly to Middle Pleistocene and M. fuscata is found in Japan andKorea in the Middle Pleistocene.

The fact that macaques show relatively low morphologicaldisparity while being diverse on a molecular scale indicates thatspeciation in macaques could have been triggered by geographicalbarriers, vicariance, and adaptation to local environments. On theother hand, baboons went through several episodes of refugia andre-expansion of suitable habitat that might have driven speciationand adaptation to different habitats. Although predominantlyfrugivorous, both baboons and macaques are dietarily eclecticgeneralists, and they also inhabit a great range of habitats; Papio is

more typically found in open environments. Baboons are neverfully arboreal and show a greater diversity of social systems (uni-level multi-male/multi-female with predominantly female phil-opatry to complex multi-level systems with predominantly femaledispersal), while macaques do not range into semi-desert biomesand are organized in uni-level multi-male/multi-female groupswith female philopatry and male dispersal. Baboons presumablycompeted for food and habitat with a variety of other papioninans(including extinct genera), cercopithecins, and even with theextinct terrestrial colobine Cercopithecoides, which may havelimited the number of Papio (sub)species. In contrast, macaques inAsia had few frugivorous competitors (as their diversificationpostdated the extinction of most hominoids, and themajority of thediverse colobine radiation is folivorous) and were not limited intheir substrate preference other than by the rarity of large spans offully open country (as few colobines are or were even semi-terrestrial; e.g., Semnopithecus).

Acknowledgements

We thank the organizers of the symposium Frontiers in BaboonResearch for inviting us to contribute to this special issue. D.M.A.and E.D. have been supported by the Generalitat de Catalunya(CERCA Program), and the Spanish Agencia Estatal de Inves-tigaci�on/European Regional Development Fund of the EuropeanUnion (CGL2016-76431-P and CGL2017-82654-P, AEI/FEDER, EU).E.D.'s work on macaque and baboon evolution was partially fun-ded by grants (numbers 669381, 662495, 664333, 665407, 65295-43 and 66189-44) from the PSC-CUNY faculty research awardprogram and by NSF 0966166 (NYCEP IGERT). We thank the editorSarah Elton and two anonymous reviewers for comments thathelped to improve a previous version of this paper. An earlierversion of this paper was presented at the symposium Frontiers inBaboon Research supported by the German Science Foundation (FI707/21-1).

Supplementary Online Material

Supplementary online material to this article can be found on-line at https://doi.org/10.1016/j.jhevol.2019.05.017.

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Journal of Human Evolution - NYCEPpages.nycep.org/ed/download/pdf/Delson_2019c.pdf · 2019. 10. 16. · concept, while D.M.A. and E.D. prefer to recognize them as a single (super)species