Neutral nuclear variation in Baboons (genusPapio) provides insights into their evolutionary and demographic histories

The genus Papio (the baboons) is one of the most widespread and ecologically successful primate genera. Baboons are found across sub-Saharan Africa, only avoiding the tropical humid forests of Central Africa, and in the southern portion of the Arabian Peninsula. Historically, six distinct forms of baboons have been recognized based on morphology (Frost et al. 2003; Jolly 1993): the chacma baboon (P. ursinus) found in the Southern part of the African continent, the yellow baboon (P. cynocephalus) from Eastern Africa, the olive baboon (P. anubis) which distribution extends from western Kenya and south Ethiopia to Guinea and Southern Mali, the Guinea baboon (P. papio) which is limited to Senegal and western Guinea, the hamadryas baboon (P. hamadryas) which inhabits semi-desert habitats in Ethiopia, Eritrea and the Arabian peninsula and the Kinda baboon (P. kindae) from Zambia. Depending on the authors, these forms have been considered either sub-species of Papio hamadryas or separate species, but there is currently no consensus on the taxonomic status of the different baboon morphotypes (Frost et al. 2003; Jolly 1993). Although these six forms are morphologically and geographically distinct, they do hybridize in nature showing little reproductive isolation (Alberts and Altmann 2001; Bergman et al. 2008; Jolly 1993; Jolly et al. 2011; Tung et al. 2008). Mitochondrial analyses suggest that baboons diversified during the last 2 million years and that their differentiation could have been driven by glacial and inter-glacial cycles during the late Pliocene and Pleistocene (Newman et al. 2004; Zinner et al. 2009). Because the geography and time scale of the diversification of baboons mirrors the diversification of the genus Homo, it has been proposed that baboons constitute a useful model to understand the evolution of the human lineage over the last 2 million years (Jolly 2001). In addition, the past and current hybridization between baboon morphotypes could help elucidate the genetic exchanges that have occurred between ancestral human populations and Neandertals (Green et al. 2010; Prufer et al. 2014; Sankararaman et al. 2014; Sankararaman et al. 2012) or Denisovans (Reich et al. 2010). Finally, the transition from savanna-dwelling baboons to the multi-level social structure of the hamadryas baboon constitute a useful model to understand the evolution of hominin social behavior (Swedell and Plummer 2012). The evolutionary relationships between the different baboon forms have long been a subject of controversy. Based on morphological similarity it has been proposed that the olive and chacma baboons are sister taxa (Ellerman et al. 1953; Kingdon 1997). Other authors have suggested that Guinea and hamadryas baboons are sister-taxa due to their phenotypic and behavioral similarity and that the yellow baboon branches with the chacma and olive baboons (Hill 1967). Based on socio-ecological arguments, it was proposed that the hamadryas baboon is sister to all other baboons (Buettner-Janusch 1966; Thorington and Groves 1970) whereas biochemical analyses suggested that it was the Guinea 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 monophyletic 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; Sithaldeen et al. 2009; Wildman et al. 2004; Zinner et al. 2009; Zinner et al. 2013). All these studies support the existence of two clades (figure 1): a southern clade consisting 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 southern 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 composed of Kinda, northern chacma (Zimbabwe, south Zambia, Mozambique and eastern Namibia) and southern yellow baboons. Figure 1 Phylogeny of mitochondrial sequences. We used a representative subset of the sequences used by Zinner et al. (2009) and we named the clades following the nomenclature proposed by these authors. The samples used in the present study are indicated with ... The different clades and sub-clades recovered by analysis of the mitochondrial genome have clearly defined geographic distributions, possibly reflecting ancient fragmentation and speciation events in the late Pliocene and Pleistocene (Zinner et al. 2011; Zinner et al. 2009). However, the discordance between mitochondrial lineages and the distribution of morphotypes suggests that introgressive hybridization has occurred frequently (Keller et al. 2010; Newman et al. 2004; Wildman et al. 2004; Zinner et al. 2011; Zinner et al. 2009). For instance, southern and northern yellow baboons carry two highly divergent mitochondrial lineages while western and eastern olive baboons carry mitochondrion that diverged approximately 1.4 to 1.9 my (Zinner et al. 2011; Zinner et al. 2009). In contrast, northern yellow, eastern olive and hamadryas baboons share a 0.6 my old mitochondrial lineage, although they have maintained their morphological distinctiveness (Zinner et al. 2011; Zinner et al. 2009). This pattern is best explained by extensive and asymmetric gene flow. The proposed model, called “nuclear swamping”, posits that hybridization followed by repeated asymmetric backcrossing between hybrid females and males of one of the parental morphotypes will result in individuals with the mitochondrion of one form and the nuclear genome of another form. For instance, when olive baboons expanded their distribution into Ethiopian hamadryas territory (Wildman et al. 2004), hybrid females mated preferentially with olive males while the hybrid males had a lower reproductive success (Phillips-Conroy and Jolly 2004; Wildman et al. 2004). Subsequent and numerous generations of backcrossing resulted in baboons that are morphologically olive-like, but carry a hamadryas mitochondrion. The extensive discordance between mitochondrial lineages and morphology indicates that the evolution of baboons has been extremely complex and that mitochondrial analyses are of limited use to resolve the evolutionary relationships among baboons as well as the origin of the modern morphotypes. To decipher the evolutionary relationships among baboons we decided to perform an analysis using neutral nuclear polymorphisms. We analyzed 12 non-coding autosomal segments, one X-linked region and 18 polymorphic transposable element insertions in a sample of 45 baboons representing 5 of the 6 recognized morphotypes.