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

Abstract

Baboons (genus Papio ) are a morphologically and behaviorally diverse clade of catarrhine monkeys that have experienced hybridization between phenotypically and genetically distinct phylogenetic species. We used high-coverage whole-genome sequences from 225 wild baboons representing 19 geographic localities to investigate population genomics and interspecies gene flow. Our analyses provide an expanded picture of evolutionary reticulation among species and reveal patterns of population structure within and among species, including differential admixture among conspecific populations. We describe the first example of a baboon population with a genetic composition that is derived from three distinct lineages. The results reveal processes, both ancient and recent, that produced the observed mismatch between phylogenetic relationships based on matrilineal, patrilineal, and biparental inheritance. We also identified several candidate genes that may contribute to species-specific phenotypes.

Abstract

INTRODUCTION

As a widespread but comparatively 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 population structure of the multibranched prehuman lineage that occupied a similar geographic range before the hegemony of “modern” humans, Homo sapiens . Despite phenotypic and genetic differences, interspecies hybridization has been described between baboons at several locations, and population relationships based on mitochondrial DNA (mtDNA) do not correspond with relationships based on phenotype. 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 geographical coverage and therefore could not adequately document inter- and intrapopulation variation. In this study, we analyzed whole-genome sequences of 225 baboons representing all six species and 19 geographic sites, with 18 local populations represented by multiple individuals.

RATIONALE

Recent studies have identified several mammalian species groups in which genetically distinct lineages have hybridized to generate complex reticulate phylogenies. Baboons provide a valuable context for studying processes generating such population and phylogenetic complexity because extant parapatric species form hybrid zones in several regions of Africa, allowing for direct observation of ongoing introgression. Furthermore, prior studies of nuclear and mtDNA and phenotypic diversity have demonstrated gene flow among differentiated 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 address 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 elements 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 between genetically distinct populations. We report 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 autosomes, to distinguish shared ancestry due to ancestral population relationships from coancestry as a result of recent male-biased immigration and gene flow. This reveals directionality and sex bias of recent gene flow in several locations. Analyses of population differences within species quantified different degrees of interspecies introgression among populations with an essentially identical 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 populations can carry genetic contributions from more than two ancestral sources. Populations that appear homogeneous on the basis of observable phenotype can display different levels of interspecies introgression. The evolutionary dynamics and current structure of baboon population 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.