Genome-wide coancestry reveals details of ancient and recent male-driven reticulation in baboons

INTRODUCTION: As a widespread but compar-atively young clade of six parapatric species, the baboons (Papio sp.) exemplify a frequently observed pattern of mammalian diversity. In particular, they provide analogs for the popula-tion structure of the multibranched prehuman lineage that occupied a similar geographic range before the hegemony of "modern" hu-mans, Homo sapiens. Despite phenotypic and genetic differences, interspecies hybridization has been described between baboons at sev-eral locations, and population relationships based on mitochondrial DNA (mtDNA) do not correspond with relationships based on pheno-type. These previous studies captured the broad outlines of baboon population genetic structure and evolutionary history but necessarily used data that were limited in genomic and geograph-ical coverage and therefore could not adequately document inter-and intrapopulation variation. In this study, we analyzed whole-genome se-quences of 225 baboons representing all six species and 19 geographic sites, with 18 local populations represented by multiple individuals.RATIONALE: Recent studies have identified sev-eral mammalian species groups in which ge-netically distinct lineages have hybridized to generate complex reticulate phylogenies. Baboons provide a valuable context for studying processes generating such population and phy-logenetic complexity because extant parapatric species form hybrid zones in several regions of Africa, allowing for direct observation of on-going introgression. Furthermore, prior studies of nuclear and mtDNA and phenotypic diversity have demonstrated gene flow among differ-entiated lineages but were unable to develop the detailed picture of process and history that is now possible using whole-genome sequences and modern computational methods. To ad-dress these questions, we designed a study that would provide a more fine-grained picture of recent and ancient genetic reticulation by comparing phenotypes and autosomal, X and Y chromosomal, and mtDNA sequences, along with polymorphic insertions of repetitive ele-ments across multiple baboon populations.RESULTS: Using deep whole-genome sequence data from 225 baboons representing multiple populations, we identified several previously unknown geographic sites of gene flow be-tween genetically distinct populations. We re-port that yellow baboons (P. cynocephalus) from western Tanzania are the first nonhuman primate found to have received genetic input from three distinct lineages. We compared the ancestry shared among individuals, estimated separately from the X chromosome and auto-somes, to distinguish shared ancestry due to ancestral population relationships from coancestry as a result of recent male-biased immigration and gene flow. This reveals di-rectionality and sex bias of recent gene flow in several locations. Analyses of population differences within species quantified dif-ferent degrees of interspecies introgression among populations with an essentially iden-tical phenotype.CONCLUSION: The population genetic structure and history of introgression among baboon lineages are even more complex than predicted from observed phenotypic diversity and prior studies of limited genetic data. Single popula-tions can carry genetic contributions from more than two ancestral sources. Populations that appear homogeneous on the basis of observ-able phenotype can display different levels of interspecies introgression. The evolutionary dy-namics and current structure of baboon popu-lation diversity indicate that other mammals displaying differentiated and geographically separate species may also have more-complex histories than anticipated. This may also be true for the morphologically defined hominin taxa from the past 4 million years.