Worldwide Patterns of Ancestry, Divergence, and Admixture in Domesticated Cattle

Abstract

The domestication and development of cattle has considerably impacted human societies, but the histories of cattle breeds and populations have been poorly understood especially for African, Asian, and American breeds. Using genotypes from 43,043 autosomal single nucleotide polymorphism markers scored in 1,543 animals, we evaluate the population structure of 134 domesticated bovid breeds. Regardless of the analytical method or sample subset, the three major groups of Asian indicine, Eurasian taurine, and African taurine were consistently observed. Patterns of geographic dispersal resulting from co-migration with humans and exportation are recognizable in phylogenetic networks. All analytical methods reveal patterns of hybridization which occurred after divergence. Using 19 breeds, we map the cline of indicine introgression into Africa. We infer that African taurine possess a large portion of wild African auroch ancestry, causing their divergence from Eurasian taurine. We detect exportation patterns in Asia and identify a cline of Eurasian taurine/indicine hybridization in Asia. We also identify the influence of species other than Bos taurus taurus and B. t. indicus in the formation of Asian breeds. We detect the pronounced influence of Shorthorn cattle in the formation of European breeds. Iberian and Italian cattle possess introgression from African taurine. American Criollo cattle originate from Iberia, and not directly from Africa with African ancestry inherited via Iberian ancestors. Indicine introgression into American cattle occurred in the Americas, and not Europe. We argue that cattle migration, movement and trading followed by admixture have been important forces in shaping modern bovine genomic variation.

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References 61

1. 1.

   Novembre J, Ramachandran S (2011 ) Perspectives on human population structure at the cusp of the sequencing era. Annu Rev Genomics Hum Genet 12: 245–274 Available: http://www.ncbi.nlm.nih.gov/pubmed/21801023.

   Not in our library10.1146/annurev-genom-090810-183123

2. 2.

   Gibbs RA, Taylor JF, Van Tassell CP, Barendse W, Eversole KA, et al (2009 ) Genome-wide survey of SNP variation uncovers the genetic structure of cattlebreeds. Science (80-) 324: 528–532 Available: http://www.ncbi.nlm.nih.gov/pubmed/19390050.

   Not in our library10.1126/science.1167936

3. 3.

   Decker JE, Pires JC, Conant GC, McKay SD, Heaton MP, et al (2009 ) Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc Natl Acad Sci U S A 106: 18644–18649 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2765454&tool=pmcentrez&rendertype=abstract. Accessed 13 August 2013.

   Not in our library10.1073/pnas.0904691106

4. 4.
   Insights into the Genetic History of French Cattle from Dense SNP Data on 47 Worldwide Breeds · 2010

   Corrected
5. 5.
   A Genome Wide Survey of SNP Variation Reveals the Genetic Structure of Sheep Breeds · 2009

   No notice
6. 6.

   Vonholdt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, et al (2010 ) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464: 898–902 Available: http://www.ncbi.nlm.nih.gov/pubmed/20237475. Accessed 2 March 2012.

   Not in our library10.1038/nature08837

7. 7.
   A High Density SNP Array for the Domestic Horse and Extant Perissodactyla: Utility for Association Mapping, Genetic Diversity, and Phylogeny Studies · 2012

   No notice
8. 8.

   Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L (2009 ) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458: 342–345 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2782482&tool=pmcentrez&rendertype=abstract. Accessed 31 July 2013.

   Not in our library10.1038/nature07670

9. 9.

   Yang H, Wang JR, Didion JP, Buus RJ, Bell TA, et al (2011 ) Subspecific origin and haplotype diversity in the laboratory mouse. Nat Genet 43: 648–655 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3125408&tool=pmcentrez&rendertype=abstract.

   Not in our library10.1038/ng.847

10. 10.
    Genome Patterns of Selection and Introgression of Haplotypes in Natural Populations of the House Mouse (Mus musculus) · 2012

    No notice
11. 11.

    McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, et al (2009 ) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci U S A 106: 12273–12278 Available: http://www.pnas.org/cgi/content/long/106/30/12273. Accessed 31 July 2013.

    Not in our library10.1073/pnas.0900992106

12. 12.
    Genomic Diversity and Introgression in O. sativa Reveal the Impact of Domestication and Breeding on the Rice Genome · 2010

    No notice
13. 13.
    Genetic Characterization and Linkage Disequilibrium Estimation of a Global Maize Collection Using SNP Markers · 2009

    No notice
14. 14.

    Van Heerwaarden J, Doebley J, Briggs WH, Glaubitz JC, Goodman MM, et al (2011 ) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proc Natl Acad Sci U S A 108: 1088–1092 Available: http://www.pnas.org/cgi/content/long/1013011108v1. Accessed 4 December 2012.

    Not in our library10.1073/pnas.1013011108

15. 15.

    Van Heerwaarden J, Hufford MB, Ross-Ibarra J (2012 ) Historical genomics of North American maize. Proc Natl Acad Sci U S A 109: 12420–12425 Available: http://www.pnas.org/cgi/content/long/109/31/12420. Accessed 31 July 2013.

    Not in our library10.1073/pnas.1209275109

16. 16.
    The Genomic Signature of Crop-Wild Introgression in Maize · 2013

    Corrected
17. 17.

    Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, et al (2011 ) Genetic structure and domestication history of the grape. Proc Natl Acad Sci U S A 108: 3530–3535 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3048109&tool=pmcentrez&rendertype=abstract. Accessed 14 March 2012.

    Not in our library10.1073/pnas.1009363108

18. 18.

    Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, et al (2013 ) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci U S A 110: 8057–8062 Available: http://www.pnas.org/cgi/content/long/110/20/8057. Accessed 31 July 2013.

    Not in our library10.1073/pnas.1217133110

19. 19.
    Population Structure and Eigenanalysis · 2006

    No notice
20. 20.
    Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data · 2012

    No notice
21. 21.

    Alexander DH, Novembre J, Lange K (2009 ) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19: 1655–1664 Available: http://www.ncbi.nlm.nih.gov/pubmed/19648217.

    Not in our library10.1101/gr.094052.109

22. 22.

    Loftus RT, MacHugh DE, Bradley DG, Sharp PM, Cunningham P (1994 ) Evidence for two independent domestications of cattle. Proc Natl Acad Sci U S A 91: 2757–2761 Available: http://www.ncbi.nlm.nih.gov/pubmed/8146187.

    Not in our library10.1073/pnas.91.7.2757

23. 23.
    A Genealogical Interpretation of Principal Components Analysis · 2009

    No notice
24. 24.

    Diamond J (2002 ) Evolution, consequences and future of plant and animal domestication. Nature 418: 700–707 Available: http://www.ncbi.nlm.nih.gov/pubmed/12167878.

    Not in our library10.1038/nature01019

25. 25.

    Felius M (1995) Cattle breeds - an encyclopedia. Doetinchem, Netherlands: Misset.

    Not in our library

26. 26.

    Evanno G, Regnaut S, Goudet J (2005 ) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620 Available: http://www.ncbi.nlm.nih.gov/pubmed/15969739. Accessed 3 October 2012.

    Not in our library10.1111/j.1365-294x.2005.02553.x

27. 27.

    Reich D, Thangaraj K, Patterson NJ, Price AL, Singh L (2009 ) Reconstructing Indian population history. Nature 461: 489–494 Available: http://www.ncbi.nlm.nih.gov/pubmed/19779445.

    Not in our library10.1038/nature08365

28. 28.

    Loftus RT, Ertugrul O, Harba AH, El-Barody MA, MacHugh DE, et al (1999 ) A microsatellite survey of cattle from a centre of origin: the Near East. Mol Ecol 8: 2015–2022 Available: http://www.ncbi.nlm.nih.gov/pubmed/10632853. Accessed 5 September 2013.

    Not in our library10.1046/j.1365-294x.1999.00805.x

29. 29.

    Christian D (2000 ) Silk roads or steppe roads? The silk roads in world history. J World Hist 11: 1–26 Available: http://muse.jhu.edu/journals/jwh/summary/v011/11.1christian.html. Accessed 6 January 2014.

    Not in our library

30. 30.

    Stock F, Gifford-Gonzalez D (2013 ) Genetics and African Cattle Domestication. African Archaeol Rev 30: 51–72 Available: http://link.springer.com/10.1007/s10437-013-9131-6.

    Not in our library

31. 31.

    Linseele V (2004 ) Size and size change of the African aurochs during the Pleistocene and Holocene. J African Archaeol 2: 165–185 Available: http://www.african-archaeology.de/index.php?page_id=154&journal_id=6&pdf_id=96. Accessed 10 December 2013.

    Not in our library

32. 32.

    Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, et al (2001 ) Genetic evidence for Near-Eastern origins of European cattle. Nature 410: 1088–1091 Available: http://www.ncbi.nlm.nih.gov/pubmed/11323670.

    Not in our library10.1038/35074088

33. 33.

    Bradley DG, MacHugh DE, Cunningham P, Loftus RT (1996 ) Mitochondrial diversity and the origins of African and European cattle. Proc Natl Acad Sci U S A 93: 5131–5135 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=39419&tool=pmcentrez&rendertype=abstract.

    Not in our library10.1073/pnas.93.10.5131

34. 34.

    Hanotte O, Bradley DG, Ochieng JW, Verjee Y, Hill EW, et al (2002 ) African pastoralism: genetic imprints of origins and migrations. Science (80-) 296: 336–339 Available: http://www.ncbi.nlm.nih.gov/pubmed/11951043.

    Not in our library10.1126/science.1069878

35. 35.

    Marshall F, Weissbrod L (2011 ) Domestication Processes and Morphological Change. Curr Anthropol 52: S397–S413 Available: http://www.jstor.org/stable/info/10.1086/658389. Accessed 24 August 2013.

    Not in our library

36. 36.

    Pérez-Pardal L, Royo LJ, Beja-Pereira a, Chen S, Cantet RJC, et al (2010 ) Multiple paternal origins of domestic cattle revealed by Y-specific interspersed multilocus microsatellites. Heredity (Edinb) 105: 511–519 Available: http://www.ncbi.nlm.nih.gov/pubmed/20332805. Accessed 11 September 2013.

    Not in our library10.1038/hdy.2010.30

37. 37.

    Falush D, Stephens M, Pritchard JK (2003 ) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1462648&tool=pmcentrez&rendertype=abstract.

    Not in our library10.1093/genetics/164.4.1567

38. 38.

    Larson G, Burger J (2013 ) A population genetics view of animal domestication. Trends Genet 29: 197–205 Available: http://www.ncbi.nlm.nih.gov/pubmed/23415592. Accessed 22 May 2013.

    Not in our library10.1016/j.tig.2013.01.003

39. 39.
    Origin and spread of Bos taurus: new clues from mitochondrial genomes belonging to haplogroup T1. · 2012

    Not checked
40. 40.

    Larson G, Albarella U, Dobney K, Rowley-Conwy P, Schibler J, et al (2007 ) Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc Natl Acad Sci U S A 104: 15276–15281 Available: http://www.pnas.org/content/104/39/15276.short. Accessed 28 August 2013.

    Not in our library10.1073/pnas.0703411104

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