Mitochondrial phylogeography of baboons (Papio spp.): indication for introgressive hybridization?

Abstract

Background: Baboons of the genus Papio are distributed over wide ranges of Africa and even colonized parts of the Arabian Peninsula. Traditionally, five phenotypically distinct species are recognized, but recent molecular studies were not able to resolve their phylogenetic relationships. Moreover, these studies revealed para- and polyphyletic (hereafter paraphyletic) mitochondrial clades for baboons from eastern Africa, and it was hypothesized that introgressive hybridization might have contributed substantially to their evolutionary history. To further elucidate the phylogenetic relationships among baboons, we extended earlier studies by analysing the complete mitochondrial cytochrome b gene and the 'Brown region' from 67 specimens collected at 53 sites, which represent all species and which cover most of the baboons' range.

Results: Based on phylogenetic tree reconstructions seven well supported major haplogroups were detected, which reflect geographic populations and discordance between mitochondrial phylogeny and baboon morphology. Our divergence age estimates indicate an initial separation into southern and northern baboon clades 2.09 (1.54-2.71) million years ago (mya). We found deep divergences between haplogroups within several species (~2 mya, northern and southern yellow baboons, western and eastern olive baboons and northern and southern chacma baboons), but also recent divergence ages among species (< 0.7 mya, yellow, olive and hamadryas baboons in eastern Africa).

Conclusion: Our study confirms earlier findings for eastern Africa, but shows that baboon species from other parts of the continent are also mitochondrially paraphyletic. The phylogenetic patterns suggest a complex evolutionary history with multiple phases of isolation and reconnection of populations. Most likely all these biogeographic events were triggered by multiple cycles of expansion and retreat of savannah biomes during Pleistocene glacial and inter-glacial periods. During contact phases of populations reticulate events (i.e. introgressive hybridization) were highly likely, similar to ongoing hybridization, which is observed between East African baboon populations. Defining the extent of the introgressive hybridization will require further molecular studies that incorporate additional sampling sites and nuclear loci.

Figure 1

Geographical distribution of baboons. Distribution based on the map in Kingdon [11], revised in accordance with Sarmiento [12] and Galat-Luong et al. [13]. Sampling sites are indicated by coloured points and labelled with a three-letter code according to Additional file 1.

Figure 2

MtDNA phylogeny of baboons. Bayesian phylogram based on combined 'Brown region' and cytb haplotype sequences from 67 Papio individuals. Tip labels contain the unique identifier (number), the sampling site in form of a three-letter code as depicted in Figure 1 and country of origin of sequences within a haplotype. Colours indicate the traditionally recognized baboon species: brown = chacma, red = Guinea, grey = hamadryas, green = olive and yellow = yellow. Bayesian posterior probabilities and maximum-likelihood bootstrap values are depicted above the branches. A – G indicate the seven major clades, grey bars on the right indicate ten terminal haplogroups and the paraphyletic clade of southern yellow baboons.

Figure 3

Geographical distribution of mtDNA-haplogroups. Approximate geographical distribution of terminal haplogroups. Points represent sample locations, shaded areas approximate ranges of haplogroups. Numbers indicate important future sampling areas (1 = contact zone between olive and Guinea baboons in Mauretania, 2 = isolated olive baboon populations from the Sahara desert, 3 = olive baboons from the Central African Republic, Congo and north eastern DRC, 4 = contact zone between olive-hamadryas, olive-yellow and central olive baboon clades, 5 = contact zones between coastal, northern and southern yellow baboons, 6 = contact zones between Kinda, northern chacma and southern yellow baboons, 7 = baboon populations in eastern Zambia and Angola, 8 = contact zones of southern and northern chacma baboons).

Figure 4

Divergence age estimates. Ultrametric tree with divergence age estimates resulting from the combined posterior distribution of 45,002 samples from four replicates of the BEAST analysis based on combined 'Brown region' and cytb sequence data from 18 Papio individuals. The mean age estimate for each node is given in mya, with the respective 95% credibility intervals indicated by the grey bars. Nodes of interest are arbitrarily numbered (N1-N19). C3 refers to one of the three nodes used for calibration (C1 and C2 not shown). A geological time scale is given on the left. Full details of age estimates are presented in Table 1.