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Molecular Systematics of the Old World Monkey Tribe Papionini

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Molecular Systematics of the Old World Monkey Tribe Papionini Eugene E. Harris* Molecular systematics of the Old World Department of Anthropology, monkey tribe Papionini: analysis of the 25 Waverly Place, New York total available genetic sequences University, New York, NY 10003, U.S.A. The phylogenetic relationships among the genera of the tribe Received 23 March 1998 Papionini are inferred using a taxonomic congruence approach in Revision received which gene trees derived for eight unlinked genetic sequence datasets 20 January 1999 and are compared. Population genetics theory predicts that species accepted 10 April 1999 relationships will be revealed with greater probability when the topology of gene trees from many unlinked loci are found to be Keywords: Old World congruent. The theory underlying this approach is described. monkeys, Papionini, Monophyly of the mangabeys is not supported by any of the gene molecular phylogeny, trees; instead, they are polyphyletic with Cercocebus found to be the systematics, mangabeys, sister taxon to Mandrillus in five gene trees (with no conflicting Papio, Theropithecus, trees), and Lophocebus found to be closely related to Papio and/or Mandrillus, Lophocebus, Theropithecus in all trees. Theropithecus and Papio are not strongly Cercocebus, Macaca. supported as sister taxa (present in one or two trees only); Lophocebus and Papio are supported as sister taxa in the majority of trees. A close relationship between Mandrillus and Papio is not supported in any of the trees. The relationships among Papio, Lophocebus, and Theropithecus cannot be resolved by congruence, probably due to the short time interval estimated between their divergences. The mtDNA COII sequences are used to estimate divergence dates within the papionins. The internode between the divergences of these species is estimated to be between 290 ka and 370 ka. Lastly, the evolution of morpho- logical features such as long faces, suborbital facial fossae, and terrestrial skeletal adaptations is discussed. 2000 Academic Press Journal of Human Evolution (2000) 38, 235–256 doi: 10.1006/jhev.1999.0318 Available online at http://www.idealibrary.com on Introduction Lophocebus), as opposed to the largely Asian distributed macaque genus (Macaca) The Papionini comprise a group of six (Strasser & Delson, 1987; Disotell, 1992; genera of Old World monkeys which are 1994; Disotell et al., 1992; Morales & geographically widespread and ecologically Melnick, 1998). As a group, papionins are diverse. They can be subdivided into two characterized by facial lengthening, usually groups, the exclusively African papionins, some development of facial fossae, increased including geladas (Theropithecus), baboons 1 use of terrestrial substrates, and a diploid (Papio), mandrills and drills (Mandrillus), karyotype of 42. All known systematic and the mangabeys (Cercocebus and studies of the Old World monkeys, based *Present address and address for correspondence: on either genetic or morphological data, Eugene E. Harris, Department of Genetics, Nelson Biological Labs, 604 Allison Road, Busch Campus, have found the papionin tribe to be a Rutgers University, Piscataway, NJ 08855-1059, monophyletic group. U.S.A.. Tel: (732)-445-2681; Fax: (732)-445-5870; The phylogenetic relationships among E-mail: [email protected] 1A population of Papio hamadryas is known to inhabit genera have been studied using essentially coastal regions of Yemen and Saudi Arabia. two classes of evidence, morphological and 0047–2484/00/020235+22$35.00/0 2000 Academic Press 236 . Macaca Theropithecus Cercocebus Lophocebus Mandrillus Papio Macaca Cercocebus Lophocebus Theropithecus Mandrillus Papio a b Figure 1. Two morphologically-based trees of papionin phylogeny. Tree (a) was advocated by Kuhn (1967), Szalay and Delson (1979),andStrasser and Delson (1987); tree (b) is after Delson and Dean (1993). molecular. The various hypotheses for their molecular trees based on immunology and relationships based on morphology, how- mtDNA encoded COII sequences (Sarich, ever, strongly disagree with most molecu- 1970; Cronin & Meikle, 1979, 1982; lar phylogenies. This discordance among Disotell, 1992, 1994; Disotell et al., 1992)? hypotheses, while strongly apparent between There now exist nine datasets of DNA molecular and morphological hypotheses, and amino acid sequences for papionin is not peculiar to this dichotomy and is genera, which can be analyzed together to also found, although to a lesser extent, examine these three questions. These among molecular hypotheses (as this study sequences derive from genomic regions describes). belonging to different chromosomes or dif- There are two central systematic ferent genomes (i.e., nuclear and mito- questions. First, are mangabeys mono- chondrial) and therefore can be subdivided phyletic as posited by most morphological into separate linkage groups. A linkage trees (see Figure 1; Jolly, 1967; Kuhn, 1967; group represents a unit of the genome which Hill, 1974; Szalay & Delson, 1979; Strasser segregates independently and recombines & Delson, 1987) or polyphyletic as pro- freely with respect to other such groups. posed in molecular and chromosomal The tree estimated based on each gene studies (Cronin & Sarich, 1976; Hewett- region is properly conceived of as a gene tree Emmett et al., 1976; Hewett-Emmett & in contrast to a species trees (see Hey, Cook, 1978; Dutrillaux et al., 1979; 1994). The terminal branches of gene trees Disotell, 1992, 1994; Disotell et al., 1992; bear homologous gene sequences and not Harris & Disotell, 1998) and some morpho- organisms or ‘‘species’’. Likewise, the nodes logical studies (Groves, 1978; Fleagle & of gene trees represent ancestral DNA McGraw, 1989)? Furthermore, if they are sequences and not ancestral organisms or polyphyletic how is each mangabey genus ‘‘species’’. Proceeding back in time from the related within the papionin group? Second, terminal DNA sequences to the ancestral do the genera Papio and Mandrillus share a DNA sequence represents a process known close relationship within the papionins as as coalescence. proposed by all morphologically based It is often assumed that gene trees hypotheses (see Figure 1), or is Theropithecus accurately estimate the species tree. How- most closely related to Papio as proposed by ever, there are several reasons why this 237 assumption may be incorrect. First, gene when species divergences have occurred trees may be incorrectly estimated because relatively close in time (Nei, 1987; Pamilo & of sampling bias when trees are estimated Nei, 1988). from relatively short sequences. Tradition- A solution to the problem of gene tree/ ally, the length of homologous DNA species tree mismatch lies in the search for sequences compared across species is on the congruence among the branching patterns order of several hundred base pairs. Saitou of gene trees that are derived from separate and Nei (1986) show that this problem can linkage groups (Saitou & Nei, 1986; Pamilo be diminished if amply long DNA sequences & Nei, 1988; Wu, 1991). This is because are compared. Second, natural selection population level processes like speciation are could have constrained variation among expected to produce similar effects across lineages resulting in a tree that conflicts with many loci. In contrast, processes that can actual phylogenetic relationships. Third, obfuscate species relationships like random assuming that gene trees have been correctly lineage sorting and natural selection are estimated, incongruence between gene trees expected to have locus specificeffects (Hey, and the species tree can be due to random 1994). Following this reasoning, when a lineage sorting. The theoretical basis of majority of gene regions are concordant in random lineage sorting has been discussed supporting trees showing the same branch- extensively in the population genetics litera- ing pattern, the most likely explanation is ture (see Hudson, 1983; Nei, 1987; Pamilo & that this pattern was shaped by the actual Nei, 1988; Rogers, 1993; Hey, 1994; Moore, species divergences. Congruence among 1995, 1997; Avise & Wollenberg, 1997; gene trees derived from unlinked loci is Hoelzer, 1997; Doyle, 1997; Maddison, therefore a powerful tool for inferring 1997) and is briefly described here. species trees. This general approach has The coalescence time of homologous gene been described as taxonomic congruence sequences sampled from two sister species (Mickevich, 1978)—the agreement among will predate the divergence time of the the supported topologies of different data species. When the coalescence of homolo- sets (Miyamoto & Fitch, 1995). gous gene sequences occurs in the most In this paper, a robust phylogenetic tree recent common ancestral population of two for all papionin genera is developed using a species, the topology of the gene tree will be taxonomic congruence approach in which the same as the species tree. But if the two the total available genetic sequences for homologous DNA sequences fail to coalesce papionin genera are analyzed. The central in the ancestral population of these two phylogenetic questions presented above are species, instead coalescing in the common the focus of the study. The pattern of dis- ancestral population that these species share cordance among gene trees is interpreted in with a third species, then the gene tree may terms of population genetics theory and its not reflect the actual order of divergences significance for understanding the evolu- among the species. This is because the DNA tionary history of papionins is discussed. lineages found
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