Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

PLoS Biol. 2020 Dec 3;18(12):e3000954. doi: 10.1371/journal.pbio.3000954. eCollection 2020 Dec.

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Biological Evolution
  • Cercopithecidae / genetics
  • Computational Biology / methods
  • Databases, Genetic
  • Fossils
  • Gene Flow / genetics
  • Genetic Introgression / genetics*
  • Genome / genetics
  • Models, Genetic
  • Phylogeny
  • Primates / genetics*
  • Sequence Analysis, DNA / methods

Associated data

  • Dryad/10.5061/dryad.rfj6q577d

Grants and funding

Funding for this study was provided by grants from the National Science Foundation, grant numbers: DBI-1564611 and DEB-1936187 awarded to M.W.H. Salary was provided to D.V. and M.W.H by grant number: DBI-1564611. Additional salary was provided to M.W.H by grant number: DEB-1936187. The authors received no specific funding for this work. Additional funding was provided by the Chan-Zuckerberg Initiative grant for Essential Open Source Software for Science (https://chanzuckerberg.com/eoss/) awarded to B.Q.M. and R.L. The authors received no specific funding for this work. Additional funding was provided by the Australian Research Council under grant number: DP-200103151 awarded to R.L., B.Q.M., and M.W.H. The authors received no specific funding for this work. Additional funding was provided by a Australian National University (https://www.anu.edu.au/) Futures grant awarded to R.L, which paid salary for B.Q.M. The sequencing and assembly of the colobus, pig-tailed macaque, and drill genomes was funded by National Institutes of Health grant number: U54-HG006484 awarded to R.G. Salaries from this award were received by R.G., J.R., K.W., S.M., D.H., and D.M. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.