Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics
Jared E. Deckera, J. Chris Piresb, Gavin C. Conanta, Stephanie D. McKaya, Michael P. Heatonc, Kefei Chend, Alan Cooperd, Johanna Vilkkie, Christopher M. Seaburyf, Alexandre R. Caetanog, Gary S. Johnsonh, Rick A. Brennemani, Olivier Hanottej,k, Lori S. Eggertb, Pamela Wienerl, Jong-Joo Kimm, Kwan Suk Kimn, Tad S. Sonstegardo, Curt P. Van Tassello, Holly L. Neibergsp, John C. McEwanq, Rudiger Brauningq, Luiz L. Coutinhor, Masroor E. Babars, Gregory A. Wilsont, Matthew C. McClurea, Megan M. Rolfa, JaeWoo Kima, Robert D. Schnabela and Jeremy F. Taylora,1
+ Author Affiliations
Divisions of
aAnimal Sciences,
bBiological Sciences, and
hDepartment of Veterinary Pathobiology, University of Missouri, Columbia MO 65211;
cUnited States Department of Agriculture, Agricultural Research Service, Meat Animal Research Center, Clay Center NE 68933;
dAustralian Centre for Ancient DNA, School of Earth and Environmental Sciences, University of Adelaide, Adelaide SA 5005, Australia;
eAgrifood Research Finland MTT, FIN-31600, Jokioinen, Finland;
fVeterinary Pathobiology, Texas A&M University, College Station TX 77843;
gEmbrapa Recursos Geneticos e Biotecnologia, Brasilia-DF, C.P. 02372, 70770-900, Brasil;
iHenry Doorly Zoo, Omaha NE 68107;
jInternational Livestock Research Institute, P.O. Box 30709, Nairobi 00100, Kenya;
kSchool of Biology, University of Nottingham, Nottingham NG7 2RD, United Kingdom;
lThe Roslin Institute, and R(D)SVS, University of Edinburgh, Roslin, Midlothian EH25 9PS, United Kingdom;
mSchool of Biotechnology, Yeungnam University, Gyeongsan, Republic of Korea;
nDepartment of Animal Science, Chungbuk National University, Cheongju, Republic of Korea;
oUnited States Department of Agriculture, Agricultural Research Service, Bovine Functional Genomics Laboratory, Beltsville MD 20705;
pDepartment of Animal Sciences, Washington State University, Pullman WA 99164;
qAnimal Genomics, AgResearch, Invermay, PB 50034, Mosgiel, New Zealand;
rDepartamento de Zootecnia, ESALQ-USP, Av. Padua Dias, 11, Piracicaba, SP 13418-900, Brasil;
sDepartment of Livestock Production, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan; and
tCanadian Wildlife Service, 200 4999 98th Avenue Northwest, Edmonton AB, Canada T6B 2X3
Edited by James E. Womack, Texas A&M University, College Station, TX, and approved September 14, 2009 (received for review April 29, 2009)
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 11 of the 15 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 up to 29 million years ago and that the produced genotypes can be used to resolve the phylogeny for this rapidly radiated infraorder. We used 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 method to amplify and screen genomic information from extinct species, and place Bison priscus within the Bovidae. The quality of genotype calls and the placement of samples within a well-supported phylogeny may provide an important test for 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.
ancient DNA Pecorans domestication
Footnotes
1To whom correspondence should be addressed. E-mail: taylorjerr@missouri.edu
Author contributions: J.E.D. designed research; J.E.D., S.D.M., K.C., A.C., M.C.M., M.M.R., J.W.K., R.D.S., and J.F.T. performed research; M.P.H., K.C., A.C., J.V., C.M.S., A.R.C., G.S.J., R.A.B., O.H., L.S.E., P.W., J.-J.K., K.S.K., T.S.S., C.P.V.T., H.L.N., L.L.C., M.E.B., and G.A.W. contributed new reagents/analytic tools; J.E.D., J.C.P., G.C.C., J.C.M., R.B., R.D.S., and J.F.T. analyzed data; and J.E.D. and J.F.T. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
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