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, 10 (3), e1004254
eCollection

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

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

Jared E Decker et al. PLoS Genet.

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
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 2
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 3
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 4
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 5
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 6
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 7
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.

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Grant support

This project was supported by National Research Initiative grants number 2008-35205-04687 and 2008-35205-18864 from the USDA Cooperative State Research, Education and Extension Service and National Research Initiative grants number 2009-65205-05635, 2011-68004-30214, 2011-68004-30367 and 2013-68004-20364 from the USDA National Institute of Food and Agriculture. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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