Genetic paleohistory of domestic cows shows major differentiation in Africa

A new study reveals that African Bos taurus breeds are quite deeply diverged from the Eurasian branch, showing an early differentiation of both continental populations, admixture with African wild auroch and livestock export from Europe to Asia. 

Jared E. Decker et al., Worldwide Patterns of Ancestry, Divergence, and Admixture in Domesticated Cattle. PLoS ONE 2014. Open access → LINK [doi:10.1371/journal.pgen.1004254]

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.

The triple (indicine or zebuine, Eurasian taurine, African taurine) division is apparent even in the limited scope of Principal Component Analysis, with African taurine breeds standing out in the intra-taurine distinctiveness in PC2 while PC1 shows the pre-Neolithic taurine-indicine distinction:

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.

An admixture-enabled phylogeny shows more clearly the deep divergence of the African branch of taurine cows:

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.

Admixture K=3 is also consistent with this triple pattern:

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.

The authors find that modern Anatolian breeds are not representative of early Neolithic cows:

Anatolian breeds (AB, EAR, TG, ASY, and SAR) are admixed between blue Fertile Crescent, grey African-like, and green indicine-like cattle (Figures 5 and 6), and we infer that they do not represent the taurine populations originally domesticated in this region due to a history of admixture. Zavot (ZVT), a crossbred breed [25], has a different history with a large portion of ancestry similar to Holsteins (Figures 2 and S8, S9, S10). The placement of Anatolian breeds along principal components 1 and 2 in Figure 1 [23], the ancestry estimates in Figure 6, their extremely short branch lengths in Figures 2–4, and significant f₃ statistics confirm that modern Anatolian breeds are admixed (see Methods for explanation of f-statistics).

As mentioned above, they also find that African taurines are much deeper diverged from Eurasian taurines than would be expected if they all diverged in a simple model from early Neolithic cows. This is partly caused, according to the study, because of a later history of back-migration (or export) of European cows to Asia, including the Far East:

We conclude that there were two waves of European introgression into Far East Asian cattle, first with Mediterranean cattle (which carried African taurine and indicine alleles) brought along the Silk Road [29] and later from 1868 to 1918 when Japanese cattle were crossed with British and Northwest European cattle [25].

However there is more: African breeds also appear to have important levels of admixture (~26%) with native African wild auroch:

The second factor that we believe underlies the divergence of African taurine is a high level of wild African auroch [30], [31] introgression. Principal component (Figure 1), phylogenetic trees (Figures 2 and 3), and admixture (Figure 6) analyses all reveal the African taurines as being the most diverged of the taurine populations. Because of this divergence, it has been hypothesized that there was a third domestication of cattle in Africa [32]–[36]. If there was a third domestication, African taurine would be sister to the European and Asian clade. When no migration events were fit in the TreeMix analyses, African cattle were the most diverged of the taurine populations (Figures 2 and 3), but when admixture was modeled to include 17 migrations, all African cattle, except for East African Shorthorn Zebu and Zebu from Madagascar which have high indicine ancestry, were sister to European cattle and were less diverged than Asian or Anatolian cattle (Figure 4), thus ruling out a separate domestication. Our phylogenetic network (Figure 4) shows that there was not a third domestication process, rather there was a single origin of domesticated taurine (Asian, African, and European all share a recent common ancestor denoted by an asterisk in Figure 4, with Asian cattle sister to the rest of the taurine lineage), followed by admixture with an ancestral population in Africa (migration edge a in Figure 4, which is consistent across 6 separate TreeMix runs, Figure S4). This ancestral population (origin of migration edge a in Figure 4) was approximately halfway between the common ancestor of indicine and the common ancestor of taurine. We conclude that African taurines received as much as 26% (estimated as 0.263 in the network, p-value<2.2e-308) of their ancestry from admixture with wild African auroch, with the rest being Fertile Crescent domesticate in origin.

As it is well known, African breeds also show variable frequencies of indicine (zebu) ancestry, which is c. 0-20% in West Africa and as much as 74% in some East African breeds, owing to greater exchanges with Asia in historical times. 

... we revealed two clusters of indicine ancestry possibly resulting from the previously suggested two waves of indicine importation into Africa, the first occurring in the second millennium BC and the second during and after the Islamic conquests [25], [34], [48].

However the study notices that, after controlling for the African wild auroch's admixture effect, the appearance of indicine admixture in some breeds collapses to zero (and is reduced in other cases):

Thus, we conclude that contrary to the assumptions and conclusions of [55] cattle with pure taurine ancestry do exist in Africa.

Other results are a confirmation of SE origin of European cows, a specific founder effect in Europe for shorthorn breeds and significant (8-23%) African admixture in Iberian breeds. Some American breeds are indeed a colonial mix of taurine and indicine. 

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.