Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics

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.

[1]  Junhyong Kim,et al.  Taxon sampling affects inferences of macroevolutionary processes from phylogenetic trees. , 2008, Systematic biology.

[2]  S. Carroll,et al.  More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. , 2005, Molecular biology and evolution.

[3]  L. Cavalli-Sforza,et al.  The mystery of Etruscan origins: novel clues from Bos taurus mitochondrial DNA , 2007, Proceedings of the Royal Society B: Biological Sciences.

[4]  E. Douzery,et al.  Molecular and morphological phylogenies of ruminantia and the alternative position of the moschidae. , 2003, Systematic biology.

[5]  B S Weir,et al.  Estimation of the coancestry coefficient: basis for a short-term genetic distance. , 1983, Genetics.

[6]  S. Kingsmore,et al.  Comprehensive human genome amplification using multiple displacement amplification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Wiens,et al.  Missing data, incomplete taxa, and phylogenetic accuracy. , 2003, Systematic biology.

[8]  Beth Shapiro,et al.  Rise and Fall of the Beringian Steppe Bison , 2004, Science.

[9]  D. Bradley,et al.  Mitochondrial diversity and the origins of African and European cattle. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Zachary A. Szpiech,et al.  Genotype, haplotype and copy-number variation in worldwide human populations , 2008, Nature.

[11]  J. Ohn,et al.  Does Adding Characters with Missing Data Increase or Decrease Phylogenetic Accuracy ? , 2003 .

[12]  R. DeSalle,et al.  Phylogeny of the Bovidae (Artiodactyla, Mammalia), based on mitochondrial ribosomal DNA sequences. , 1992, Molecular biology and evolution.

[13]  Robert D Schnabel,et al.  SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries , 2008, Nature Methods.

[14]  M. Shriver,et al.  Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). , 1997, Genetics.

[15]  M. Feldman,et al.  Worldwide Human Relationships Inferred from Genome-Wide Patterns of Variation , 2008 .

[16]  Pablo A. Goloboff,et al.  TNT, a free program for phylogenetic analysis , 2008 .

[17]  Timothy P. L. Smith,et al.  Selection and use of SNP markers for animal identification and paternity analysis in U.S. beef cattle , 2002, Mammalian Genome.

[18]  Robert D Schnabel,et al.  Genome-Wide Survey of SNP Variation Uncovers the Genetic Structure of Cattle Breeds , 2009, Science.

[19]  K. Iwamoto,et al.  Evaluation of whole genome amplification methods using postmortem brain samples , 2007, Journal of Neuroscience Methods.

[20]  P. Taberlet,et al.  The origin of European cattle: evidence from modern and ancient DNA. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Timothy P. L. Smith,et al.  Development and Characterization of a High Density SNP Genotyping Assay for Cattle , 2009, PloS one.

[22]  H. Ellegren,et al.  Cattle domestication in the Near East was followed by hybridization with aurochs bulls in Europe , 2005, Proceedings of the Royal Society B: Biological Sciences.

[23]  D. Bradley,et al.  Independent mitochondrial origin and historical genetic differentiation in North Eastern Asian cattle. , 2004, Molecular phylogenetics and evolution.

[24]  Paul Scheet,et al.  A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. , 2006, American journal of human genetics.

[25]  Weihua Chang,et al.  Whole-genome genotyping with the single-base extension assay , 2005, Nature Methods.

[26]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[27]  C. Moritz Uses of molecular phylogenies for conservation , 1995 .

[28]  P. Sharp,et al.  Evidence for two independent domestications of cattle. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.