A Molecular Phylogeny of Living Primates
Polina Perelman1¤, Warren E. Johnson1, Christian Roos2, Hector N. Seuánez3, Julie E. Horvath4, Miguel A. M. Moreira3, Bailey Kessing5, Joan Pontius5, Melody Roelke5, Yves Rumpler6, Maria Paula C. Schneider7, Artur Silva7, Stephen J. O'Brien1, Jill Pecon-Slattery1*
1 Laboratory of Genomic Diversity, National Cancer Institute–Frederick, Frederick, Maryland, United States of America, 2 Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Göttingen, Germany, 3 Division of Genetics, Instituto Nacional de Câncer and Department of Genetics, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, 4 Department of Evolutionary Anthropology and Institute for Genome Sciences and Policy, Duke University, Durham, North Carolina, United States of America, 5 SAIC–Frederick, Laboratory of Genomic Diversity, National Cancer Institute–Frederick, Frederick, Maryland, United States of America, 6 Physiopathologie et Médecine Translationnelle, Faculté de Médecine, Université Louis Pasteur, Strasbourg, France, 7 Universidade Federal do Pará, Belém, Brazil
Comparative genomic analyses of primates offer considerable potential to define and understand the processes that mold, shape, and transform the human genome. However, primate taxonomy is both complex and controversial, with marginal unifying consensus of the evolutionary hierarchy of extant primate species. Here we provide new genomic sequence (~8 Mb) from 186 primates representing 61 (~90%) of the described genera, and we include outgroup species from Dermoptera, Scandentia, and Lagomorpha. The resultant phylogeny is exceptionally robust and illuminates events in primate evolution from ancient to recent, clarifying numerous taxonomic controversies and providing new data on human evolution. Ongoing speciation, reticulate evolution, ancient relic lineages, unequal rates of evolution, and disparate distributions of insertions/deletions among the reconstructed primate lineages are uncovered. Our resolution of the primate phylogeny provides an essential evolutionary framework with far-reaching applications including: human selection and adaptation, global emergence of zoonotic diseases, mammalian comparative genomics, primate taxonomy, and conservation of endangered species.
Advances in human biomedicine, including those focused on changes in genes triggered or disrupted in development, resistance/susceptibility to infectious disease, cancers, mechanisms of recombination, and genome plasticity, cannot be adequately interpreted in the absence of a precise evolutionary context or hierarchy. However, little is known about the genomes of other primate species, a situation exacerbated by a paucity of nuclear molecular sequence data necessary to resolve the complexities of primate divergence over time. We overcome this deficiency by sequencing 54 nuclear gene regions from DNA samples representing ~90% of the diversity present in living primates. We conduct a phylogenetic analysis to determine the origin, evolution, patterns of speciation, and unique features in genome divergence among primate lineages. The resultant phylogenetic tree is remarkably robust and unambiguously resolves many long-standing issues in primate taxonomy. Our data provide a strong foundation for illuminating those genomic differences that are uniquely human and provide new insights on the breadth and richness of gene evolution across all primate lineages.
Citation: Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, et al. (2011) A Molecular Phylogeny of Living Primates. PLoS Genet 7(3): e1001342. doi:10.1371/journal.pgen.1001342
Editor: Jürgen Brosius, University of Münster, Germany
Received: September 15, 2010; Accepted: February 16, 2011; Published: March 17, 2011
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: This project has supported with federal funds from the National Cancer Institute, National Institutes of Health, under contract N01-CO-12400. This research has been supported (in part) by the Intramural Research Program of the NIH, NCI, Center for Cancer Research, the Duke Primate Genomics Initiative, and Institute for Genome Sciences and Policy at Duke University. In Brazil, support included CNPq grant 303583/2007-0 (HNS) and CNPq grant 304403/2008-3 (MAMM). The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does its mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: slatterJ@mail.nih.gov
¤ Current address: Laboratory of Cytogenetics of Animals, Institute of Chemical Biology and Fundamental Medicine, Novosibirsk, Russia