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Neutral Nuclear Variation in Baboons (Genus Papio) Provides Insights Into Their Evolutionary and Demographic Histories

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Neutral Nuclear Variation in Baboons (Genus Papio) Provides Insights Into Their Evolutionary and Demographic Histories AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 00:00–00 (2014) Neutral Nuclear Variation in Baboons (Genus Papio) Provides Insights into Their Evolutionary and Demographic Histories Stephane Boissinot,1,2* Lauren Alvarez,1 Juliana Giraldo-Ramirez,1 and Marc Tollis1,2,3 1Department of Biology, Queens College, the City University of New York, Queens, NY 2Ecology, Evolutionary Biology and Behavior, Graduate Center, the City University of New York, New York, NY 3School of Life Sciences, Arizona State University, Tempe, AZ KEY WORDS neutral variation; retrotransposon; species tree ABSTRACT Baboons (genus Papio) are distributed variation in baboons. We sequenced 13 noncoding, puta- over most of sub-Saharan Africa and in the southern por- tively neutral, nuclear regions, and scored the presence/ tion of the Arabian Peninsula. Six distinct morphotypes, absence of 18 polymorphic transposable elements in a with clearly defined geographic distributions, are recog- sample of 45 baboons belonging to five of the six recog- nized (the olive, chacma, yellow, Guinea, Kinda, and ham- nized baboon forms. We found that the chacma baboon is adryas baboons). The evolutionary relationships among the sister-taxon to all other baboons and the yellow baboon forms have long been a controversial issue. Phylo- baboon is the sister-taxon to an unresolved northern genetic analyses based on mitochondrial DNA sequences clade containing the olive, Guinea, and hamadryas revealed that the modern baboon morphotypes are mito- baboons. We estimated that the diversification of baboons chondrially paraphyletic or polyphyletic. The discordance occurred entirely in the Pleistocene, the earliest split dat- between mitochondrial lineages and morphology is indica- ing 1.5 million years ago, and that baboons have experi- tive of extensive introgressive hybridization between enced relatively large and constant effective population ancestral baboon populations. To gain insights into the sizes for most of their evolutionary history (30,000 to evolutionary relationships among morphotypes and their 95,000 individuals). Am J Phys Anthropol 000:000–000, demographic history, we performed an analysis of nuclear 2014. VC 2014 Wiley Periodicals, Inc. The genus Papio (the baboons) is one of the most of the genus Homo, it has been proposed that baboons widespread and ecologically successful primate genera. constitute a useful model to understand the evolution of Baboons are found across sub-Saharan Africa, only the human lineage over the last 2 million years (Jolly, avoiding the tropical humid forests of Central Africa, 2001). In addition, the past and current hybridization and in the southern portion of the Arabian Peninsula. between baboon morphotypes could help elucidate the Historically, six distinct forms of baboons have been rec- genetic exchanges that have occurred between ancestral ognized based on morphology (Jolly, 1993; Frost et al., human populations and Neandertals (Green et al., 2010; 2003): the chacma baboon (P. ursinus) found in the Sankararaman et al., 2012, 2014; Prufer et al., 2014) or Southern part of the African continent, the yellow Denisovans (Reich et al., 2010). Finally, the transition baboon (P. cynocephalus) from Eastern Africa, the olive from savanna-dwelling baboons to the multilevel social baboon (Papio anubis) which distribution extends from structure of the hamadryas baboon constitutes a useful western Kenya and south Ethiopia to Guinea and South- model to understand the evolution of hominin social ern Mali, the Guinea baboon (P. papio) which is limited behavior (Swedell and Plummer, 2012). to Senegal and western Guinea, the hamadryas baboon (Papio hamadryas) which inhabits semi-desert habitats in Ethiopia, Eritrea, and the Arabian peninsula, and the Kinda baboon (P. kindae) from Zambia. Depending on Lauren Alvarez and Juliana Giraldo-Ramirez contributed equally the authors, these forms have been considered either to this work. sub-species of P. hamadryas or separate species, but there is currently no consensus on the taxonomic status Grant sponsor: National Science Foundation Undergraduate of the different baboon morphotypes (Jolly, 1993; Frost Research Mentoring Program at Queens College; Grant number: et al., 2003). Although these six forms are morphologi- 0731613. cally and geographically distinct, they do hybridize in nature showing little reproductive isolation (Jolly, 1993; *Correspondence to: Stephane Boissinot, Department of Biology, Queens College, the City University of New York, Queens, NY Alberts and Altmann, 2001; Bergman et al., 2008; Tung 11367, USA. E-mail: [email protected] et al., 2008; Jolly et al., 2011). Mitochondrial analyses suggest that baboons diversified during the last 2 million Received 11 April 2014; revised 20 August 2014; accepted 8 years and that their differentiation could have been September 2014 driven by glacial and inter-glacial cycles during the late Pliocene and Pleistocene (Newman et al., 2004; Zinner DOI: 10.1002/ajpa.22618 et al., 2009). Because the geography and time scale of Published online 00 Month 2014 in Wiley Online Library the diversification of baboons mirrors the diversification (wileyonlinelibrary.com). Ó 2014 WILEY PERIODICALS, INC. 2 S. BOISSINOT ET AL. baboon that was the sister to all other forms (Williams- Blangero et al., 1990). More recently, a north/south model was proposed (Jolly, 1993) with the yellow and chacma baboons as sister taxa and a northern monophy- letic group composed of the olive, hamadryas, and Guinea baboons. In the past decade, several groups have attempted to resolve the evolutionary relationships among baboons using mitochondrial DNA sequences (Newman et al., 2004; Wildman et al., 2004; Sithaldeen et al., 2009; Zin- ner et al., 2009, 2013). All these studies support the existence of two clades (Fig. 1): a southern clade consist- ing of the chacma baboon, Kinda baboon, and yellow baboons from Zambia, Malawi, and southern Tanzania, and a northern clade consisting of the hamadryas baboon, Guinea baboon, olive baboon, and yellow baboons from Kenya and northern Tanzania. Depending on the study, the split between the northern and south- ern mitochondrial lineages occurred between 1.79 and 2.09 million years (my) ago. Within the northern clade, there is a clear break dated around 1.34–1.89 my between western baboons (Guinea baboon and olive baboons from Nigeria, Cameroon, and Ivory Coast) and eastern baboons (hamadryas, olive baboons from Kenya, Eritrea, and Ethiopia, and yellow baboons from Kenya and Tanzania). In the southern clade (which might be paraphyletic based on complete mitochondrial genome analyses; (Zinner et al., 2013)), there is a distinct south/ north split around 1.80 my between south chacma (South Africa and coastal Namibia) and a group com- posed of Kinda, northern chacma (Zimbabwe, south Zambia, Mozambique, and eastern Namibia), and south- ern yellow baboons. The different clades and sub-clades recovered by anal- ysis of the mitochondrial genome have clearly defined geographic distributions, possibly reflecting ancient frag- mentation and lineage divergence in the late Pliocene and Pleistocene (Zinner et al., 2009, 2011). However, the discordance between mitochondrial lineages and the dis- tribution of morphotypes suggests that introgressive hybridization has occurred frequently (Newman et al., 2004; Wildman et al., 2004; Zinner et al. 2009, 2011; Kel- ler et al., 2010). For instance, southern and northern Fig. 1. Phylogeny of mitochondrial sequences. We used a yellow baboons carry two highly divergent mitochondrial representative subset of the sequences used by Zinner et al. lineages while western and eastern olive baboons carry (2009) and we named the clades following the nomenclature mitochondrion that diverged approximately 1.4–1.9 my proposed by these authors. The samples used in this study are (Zinner et al. 2009, 2011). In contrast, northern yellow, indicated with letters. The tree was built using the maximum eastern olive, and hamadryas baboons share a 0.6 my likelihood method implemented in MEGA 5.0 (Tamura et al., 2011) using the HKY1G model of substitution. The tree was old mitochondrial lineage, although they have main- rooted using sequences from Theropithecus gelada. Numbers at tained their morphological distinctiveness (Zinner et al., the nodes indicate the robustness of each node assessed using 2009, 2011). This pattern is best explained by extensive 1,000 bootstrap replicates. Only bootstrap values >80% are and asymmetric gene flow. The proposed model, called shown. “nuclear swamping,” posits that hybridization followed by repeated asymmetric backcrossing between hybrid The evolutionary relationships between the different females and males of one of the parental morphotypes baboon forms have long been a subject of controversy. will result in individuals with the mitochondrion of one Based on morphological similarity, it has been proposed form and the nuclear genome of another form. For that the olive and chacma baboons are sister taxa (Eller- instance, when olive baboons expanded their distribution man et al., 1953; Kingdon, 1997). Other authors have into Ethiopian hamadryas territory (Wildman et al., suggested that Guinea and hamadryas baboons are 2004), hybrid females mated preferentially with olive sister-taxa due to their phenotypic and behavioral simi- males while the hybrid males had a lower reproductive larity and that the yellow baboon branches with the success (Phillips-Conroy and Jolly, 2004; Wildman et al., chacma and olive baboons
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