Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

Author:

Vanderpool DanORCID,Minh Bui Quang,Lanfear RobertORCID,Hughes Daniel,Murali Shwetha,Harris R. AlanORCID,Raveendran MuthuswamyORCID,Muzny Donna M.,Hibbins Mark S.ORCID,Williamson Robert J.ORCID,Gibbs Richard A.,Worley Kim C.ORCID,Rogers JeffreyORCID,Hahn Matthew W.ORCID

Abstract

Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.

Funder

National Science Foundation

Chan-Zuckerberg Initiative grant for Essential Open Source Software for Science

Australian Research Council

Australian National University Futures Grant

Publisher

Public Library of Science (PLoS)

Subject

General Agricultural and Biological Sciences,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Neuroscience

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