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Cited by 529Genetic and phenotypic traits in livestockGenetic diversity and population structureForensic and Genetic Research

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

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Decker, Jared E., McKay, Stephanie D., Rolf, Megan M., Kim, JaeWoo, Molina Alcalá, Antonio, Sonstegard, Tad S., Hanotte, Olivier, Götherström, Anders, Seabury, Christopher M., Praharani, Lisa, Babar, Masroor Ellahi, Correia de Almeida Regitano, Luciana, Yildiz, Mehmet Ali, Heaton, Michael P., Liu, Wan-Sheng, Lei, Chu-Zhao, Reecy, James M., Saif-Ur-Rehman, Muhammad, Schnabel, Robert D., Taylor, Jeremy F.·2014·PLoS Genetics
DOI 10.1371/journal.pgen.1004254PMC PMC3967955
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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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Figure 1 Principal component analysis of 1,543 animals genotyped with 43,043 SNPs. Points were colored according to geographic origin of breed; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe.
Figure 1 Principal component analysis of 1,543 animals genotyped with 43,043 SNPs. Points were colored according to geographic origin of breed; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe.CC0 · PubMed Central
Figure 2 Phylogram of the inferred relationships between 134 cattle breeds. Breeds were colored according to their geographic origin; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix (See [20]).
Figure 2 Phylogram of the inferred relationships between 134 cattle breeds. Breeds were colored according to their geographic origin; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix (See [20]).CC0 · PubMed Central
Figure 3 Phylogram of the inferred relationships between 74 cattle breeds. Breeds were colored according to their geographic origin; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix.
Figure 3 Phylogram of the inferred relationships between 74 cattle breeds. Breeds were colored according to their geographic origin; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix.CC0 · PubMed Central
Figure 4 Phylogenetic network of the inferred relationships between 74 cattle breeds. Breeds were colored according to their geographic origin; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix. Common ancestor of domesticated taurines is indicated by an asterisk. Migration edges were colored according to percent ancestry received from the donor population. Migration edge a is hypothesized to be from wild African auroch into domesticates from the Fertile Crescent. Migration edge b is hypothesized to be introgression from hybrid African cattle. Migration edge c is hypothesized to be introgression from Bali/indicine hybrids into other Indonesian cattle. Migration edge d signals introgression of African taurine into Iberia. Migration edges e and f represent introgression from Brahman into American Criollo.
Figure 4 Phylogenetic network of the inferred relationships between 74 cattle breeds. Breeds were colored according to their geographic origin; black: Africa, green: Asia, red: North and South America, orange: Australia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix. Common ancestor of domesticated taurines is indicated by an asterisk. Migration edges were colored according to percent ancestry received from the donor population. Migration edge a is hypothesized to be from wild African auroch into domesticates from the Fertile Crescent. Migration edge b is hypothesized to be introgression from hybrid African cattle. Migration edge c is hypothesized to be introgression from Bali/indicine hybrids into other Indonesian cattle. Migration edge d signals introgression of African taurine into Iberia. Migration edges e and f represent introgression from Brahman into American Criollo.CC0 · PubMed Central
Figure 5 Worldwide map with country averages of ancestry proportions with 3 ancestral populations (K = 3). Blue represents Eurasian Bos t. taurus ancestry, green represents Bos javanicus and Bos t. indicus ancestry, and dark grey represents African Bos. t. taurus ancestry. Please note, averages do not represent the entire populations of each country, as we do not have a geographically random sample.
Figure 5 Worldwide map with country averages of ancestry proportions with 3 ancestral populations (K = 3). Blue represents Eurasian Bos t. taurus ancestry, green represents Bos javanicus and Bos t. indicus ancestry, and dark grey represents African Bos. t. taurus ancestry. Please note, averages do not represent the entire populations of each country, as we do not have a geographically random sample.CC0 · PubMed Central
Figure 6 Ancestry models with 3 ancestral populations (K = 3). Blue represents Eurasian Bos t. taurus ancestry, green represents Bos javanicus and Bos t. indicus ancestry, and dark grey represents African Bos. t. taurus ancestry. See Supplementary Figures S5, S6, S7, S8, S9, S10 for other values of K.
Figure 6 Ancestry models with 3 ancestral populations (K = 3). Blue represents Eurasian Bos t. taurus ancestry, green represents Bos javanicus and Bos t. indicus ancestry, and dark grey represents African Bos. t. taurus ancestry. See Supplementary Figures S5, S6, S7, S8, S9, S10 for other values of K.CC0 · PubMed Central
Figure 7 Phylogenetic network of the inferred relationships between 14 cattle breeds. Breeds were colored according to their geographic origin; green: Asia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix. Migration edges were colored according to percent ancestry received from the donor population. Migration edges show indicine introgression into Mongolian cattle, African taurine and indicine ancestry in Marchigiana, and a northern European influence on Wagyu.
Figure 7 Phylogenetic network of the inferred relationships between 14 cattle breeds. Breeds were colored according to their geographic origin; green: Asia, and blue: Europe. Scale bar shows 10 times the average standard error of the estimated entries in the sample covariance matrix. Migration edges were colored according to percent ancestry received from the donor population. Migration edges show indicine introgression into Mongolian cattle, African taurine and indicine ancestry in Marchigiana, and a northern European influence on Wagyu.CC0 · PubMed Central

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Citations

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Research works printed but not linked: 2

  1. JL Stewart, 1951, The West African Shorthorn cattle. Their value to Africa as trypanosomiasis-resistant animals, Vet Rec, 63, 454
  2. D Reich, 2009, Reconstructing Indian population history, Nature, 461, 489, 10.1038/nature08365 · DOI · Paper page

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Metadata

Authors
Decker, J. E., McKay, S. D., Rolf, M. M., Kim, J., Molina Alcalá, A., Sonstegard, T. S., Hanotte, O., Götherström, A., Seabury, C. M., Praharani, L., Babar, M. E., Correia de Almeida Regitano, L., Yildiz, M. A., Heaton, M. P., Liu, W.-S., Lei, C.-Z., Reecy, J. M., Saif-Ur-Rehman, M., Schnabel, R. D., & Taylor, J. F.
Affiliations
  • University of Missouri (US)
  • University of Vermont (US)
  • Oklahoma State University (US)
  • Agricultural Research Service (US)
  • University of Nottingham (GB)
  • Uppsala University (SE)
  • Texas A&M University (US)
  • University of Veterinary and Animal Sciences (PK)
  • Roman L. Hruska U.S. Meat Animal Research Center (US)
  • Pennsylvania State University (US)
  • Iowa State University (US)
Corresponding author
  • Decker, Jared E.
  • Taylor, Jeremy F.
ORCID
Venue
PLoS Genetics
Publisher
Public Library of Science (PLoS)
Published
2014-03-27
Volume
10
Issue
3
Pages
e1004254
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1004254
PMC
PMC3967955
OpenAlex
W2177259980
Cited by
521
References
59
Citations by year
2026: 33 · 2025: 29 · 2024: 34 · 2023: 36 · 2022: 45 · 2021: 93 · 2020: 40 · 2019: 35 · 2018: 64 · 2017: 34 · 2016: 29 · 2015: 34 · 2014: 13
FWCI
24.02
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, public-domain)
  • Europe PMC (PubMed Central) (publishedVersion, public-domain)
  • PubMed Central (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
  • arXiv (Cornell University) (submittedVersion)
  • Iowa State University Digital Repository (Iowa State University) (submittedVersion)
  • KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Universidad de Córdoba Insitutional Repository (Universidad de Córdoba) (submittedVersion, cc-by-nc-nd)
  • OakTrust (Texas A&M University Libraries) (submittedVersion)
  • arXiv (Cornell University)
  • Greater South Information System
Funders
  • U.S. Department of Agriculture (#2011-68004-30367, 2013-68004-20364, 2013-68004, 2011-68004-30214)
  • National Institute of Food and Agriculture (2013-68004, 2011-68004-30214, 2011-68004-30367, 2013-68004-20364, 2009-65205-05635)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
Keywords
cattle breeds, population structure, admixture, hybridization, Bos indicus, taurine cattle, introgression, Shorthorn cattle, Criollo cattle, Iberian cattle, European cattle breeds, cattle, phylogenetic networks
MeSH terms
Alleles, Animals, Animals, Domestic, Breeding, Cattle, Gene Frequency, Genetics, Population, Humans, Phylogeny, Genetic Variation, Polymorphism, Single Nucleotide

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