Resolving the Evolution of Extant and Extinct Ruminants With High-Throughput Phylogenomics

Authors: DECKER, JARED - University Of Missouri; PIRES, J - University Of Missouri; CONANT, GAVIN - University Of Missouri; MCKAY, STEPHANIE - University Of Missouri; Heaton, Michael - Mike; CHEN, KEFEI - University Of Adelaide; COOPER, ALAN - University Of Adelaide; VILKKI, JOHANNA - Mtt Agrifood Research Finland; SEABURY, CHRISTOPHER - Texas A&M University Health Science Center; CAETANO, ALEXANDRE - Embrapa Genetic Resources; JOHNSON, GARY - University Of Missouri; BRENNEMAN, RICK - Omaha Henry Doorly Zoo; HANOTTE, OLIVIER - University Of Nottingham; EGGERT, LORI - University Of Missouri; WIENER, PAMELA - Roslin Institute; KIM, JONG-JOO - Yeungnam University; KIM, KWAN - Chungbuk National University; Sonstegard, Tad; Van Tassell, Curtis - Curt; NEIBERGS, HOLLY - Washington State University; MCEWAN, JOHN - Agresearch; BRAUNING, RUDIGER - Agresearch; COUTINHO, LUIZ - Universidad De Sao Paulo; BABAR, MASROOR - University Of Veterinary And Animal Sciences; WILSON, GREGORY - Canadian Wildlife Service; MCCLURE, MATTHEW - University Of Missouri; ROLF, MEGAN - University Of Missouri; KIM, JAEWOO - University Of Missouri; SCHNABEL, ROBERT - University Of Missouri; TAYLOR, JEREMY - University Of Missouri

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/16/2009
Publication Date: 11/3/2009
Citation: Decker, J.E., Pires, J.C., Conant, G.C., McKay, S.D., Heaton, M.P., Chen, K., Cooper, A., Vilkki, J., Seabury, C.M., Caetano, A.R., Johnson, G.S., Brenneman, R.A., Hanotte, O., Eggert, L.S., Wiener, P., Kim, J.J., Kim, K.S., Sonstegard, T.S., Van Tassell, C.P., Neibergs, H.L., McEwan, J.C., Brauning, R., Coutinho, L.L., Babar, M.E., Wilson, G.A., McClure, M.C., Rolf, M.M., Kim, J., Schnabel, R.D., Taylor, J.F. 2009. Resolving the Evolution of Extant and Extinct Ruminants With High-Throughput Phylogenomics. Proceedings of the National Academy of Sciences. 106(44):18644-18649.

Interpretive Summary: This is the first report demonstrating that high-throughput DNA technology designed for one species can be used to genotype ancient DNA from a related extinct species that diverged up to 29 million years ago. The results from a 20,000 year-old DNA sample placed an extinct Bison species close to modern bison within the family of antelopes, cattle, gazelles, goats, and sheep. The DNA technology was also used to resolve the evolutionary relationships for many of the horned ruminant species that currently exist around the world. The report provides insights into the history of domestication and breed formation in cattle and is of broad scientific interest to the research community. These findings also introduce the era of high-throughput phylogenomics in which highly-resolved evolutionary relationships are rapidly and inexpensively constructed for species that are in existence or have become extinct.

Technical Abstract: The Pecorans (higher ruminants) are believed to have rapidly speciated in the Mid-Eocene, resulting in five distinct extant families; Antilocapridae, Giraffidae, Moschidae, Cervidae, and Bovidae. Due to the rapid radiation, the Pecoran phylogeny has proven difficult to resolve and eleven of the fifteen possible rooted phylogenies describing ancestral relationships among the Antilocapridae, Giraffidae, Cervidae, and Bovidae have each been argued as representations of the true phylogeny. Here we demonstrate that a genome-wide single nucleotide polymorphism (SNP) genotyping platform designed for one species can be used to genotype ancient DNA from an extinct species and DNA from species diverged by up to 29 million years and that the produced genotypes can be used to resolve the phylogeny for this rapidly radiated infraorder. We utilized a high-throughput assay with 54,693 SNP loci developed for Bos taurus taurus to rapidly genotype 678 individuals representing 61 Pecoran species. We produced a highly resolved phylogeny for this diverse group based upon 40,843 genome-wide SNP, which is five times as many informative characters as have previously been analyzed. We also establish a new method to amplify and screen genomic information from extinct species, and place Bison priscus within the Bovidae. Examining the produced genotypes and placement of samples within a well-supported phylogeny should be an important step in validating the fidelity and integrity of ancient samples. Finally, we constructed a phylogenomic network to accurately describe the relationships between 48 cattle breeds and facilitate inferences concerning the history of domestication and breed formation.