New World cattle show ancestry from multiple independent domestication events

Abstract

Previous archeological and genetic research has shown that modern cattle breeds are descended from multiple independent domestication events of the wild aurochs (Bos primigenius) ∼10,000 y ago. Two primary areas of domestication in the Middle East/Europe and the Indian subcontinent resulted in taurine and indicine lines of cattle, respectively. American descendants of cattle brought by European explorers to the New World beginning in 1493 generally have been considered to belong to the taurine lineage. Our analyses of 47,506 single nucleotide polymorphisms show that these New World cattle breeds, as well as many related breeds of cattle in southern Europe, actually exhibit ancestry from both the taurine and indicine lineages. In this study, we show that, although European cattle are largely descended from the taurine lineage, gene flow from African cattle (partially of indicine origin) contributed substantial genomic components to both southern European cattle breeds and their New World descendants. New World cattle breeds, such as Texas Longhorns, provide an opportunity to study global population structure and domestication in cattle. Following their introduction into the Americas in the late 1400s, semiferal herds of cattle underwent between 80 and 200 generations of predominantly natural selection, as opposed to the human-mediated artificial selection of Old World breeding programs. Our analyses of global cattle breed population history show that the hybrid ancestry of New World breeds contributed genetic variation that likely facilitated the adaptation of these breeds to a novel environment.

Fig. 1.

Statistical summary of genetic variation in 1,461 cattle individuals genotyped at 1,814 SNP loci. Individuals are grouped by the region from which their breed originated, as described in Table 1. Principal component 1 (PC1) captures the split between indicine and taurine domestications. The position of individuals along this axis can be interpreted as the proportion of admixture between these two groups. PC2 captures the European–African split within taurine cattle.

Fig. 2.

Model-based population assignment for 1,461 individuals based on the 1,814 markers using STRUCTURE (61) and plotted using Distruct (64). Individuals are represented as thin vertical lines, with the proportion of different colors representing their estimated ancestry deriving from different populations. Individuals are grouped by breed as named when sampled; breeds are arranged by regions and are individually labeled by numbers at the bottom. Breed name associated with each number is listed in the “Figure legend” column in Table 1. The best-supported number of ancestral populations was two (K = 2). This split captures the known indicine–taurine split. Hybrid labels refer to Santa Gertrudis (group 45) and Beefmaster (group 46) cattle breeds developed from indicine–taurine crosses within the last 100 y. At K = 3, population groupings were not consistent across runs, but generally followed the division between indicine, European taurine, and African taurine cattle. At higher values of K, individual breed structure predominated, although some breeds (e.g., Jersey, group 35) consistently showed complex ancestry. K = 5 and K = 12 were selected to demonstrate these patterns.

Fig. 3.

Geographic structure of breed ancestry as estimated at K = 2 on the 1.8k dataset using STRUCTURE (61). Taurine ancestry is indicated in white and indicine ancestry in black in the pie diagrams. Breed name associated with each number is listed in the “Figure legend” column in Table 1. Note higher levels of indicine introgression in southern Europe, particularly for the Italian breeds Romagnola (group 36), Piedmontese (group 34), Chianina (group 37), and Marchigiana (group 38). The Brazilian breeds Nelore (group 54) and Guzerat (group 56) are recently developed breeds from indicine stock. Pie chart size is scaled to sample size. Breed location is based on the latitude/longitude coordinates from CIA World Factbook (65) of the breed’s country of origin. Silhouettes of cattle are reproduced from ref. . This figure was created using the software package GenGIS (66).