Domestication of cattle: Two or three events?

Daniel Pitt,Ezequiel L Nicolazzi,Michael W Bruford,Pablo Orozco‐Terwengel,Natalia Sevane,Stephen D E Park,Rodrigo Martinez,Licia Colli,David E Machugh

doi:10.1111/eva.12674

Abstract

Cattle have been invaluable for the transition of human society from nomadic hunter‐gatherers to sedentary farming communities throughout much of Europe, Asia and Africa since the earliest domestication of cattle more than 10,000 years ago. Although current understanding of relationships among ancestral populations remains limited, domestication of cattle is thought to have occurred on two or three occasions, giving rise to the taurine (Bos taurus) and indicine (Bos indicus) species that share the aurochs (Bos primigenius) as common ancestor ~250,000 years ago. Indicine and taurine cattle were domesticated in the Indus Valley and Fertile Crescent, respectively; however, an additional domestication event for taurine in the Western Desert of Egypt has also been proposed. We analysed medium density Illumina Bovine SNP array (~54,000 loci) data across 3,196 individuals, representing 180 taurine and indicine populations to investigate population structure within and between populations, and domestication and demographic dynamics using approximate Bayesian computation (ABC). Comparative analyses between scenarios modelling two and three domestication events consistently favour a model with only two episodes and suggest that the additional genetic variation component usually detected in African taurine cattle may be explained by hybridization with local aurochs in Africa after the domestication of taurine cattle in the Fertile Crescent. African indicine cattle exhibit high levels of shared genetic variation with Asian indicine cattle due to their recent divergence and with African taurine cattle through relatively recent gene flow. Scenarios with unidirectional or bidirectional migratory events between European taurine and Asian indicine cattle are also plausible, although further studies are needed to disentangle the complex human‐mediated dispersion patterns of domestic cattle. This study therefore helps to clarify the effect of past demographic history on the genetic variation of modern cattle, providing a basis for further analyses exploring alternative migratory routes for early domestic populations.

Highlights

Between the late Pleistocene and early Holocene, the most commonly occurring cattle species was the aurochs (Bos primigenius), ranging from northern Africa to both the Atlantic and Pacific coasts of Eurasia (Zeuner, 1963)
Similar to sheep and goats, archaeological and genomic evidence suggests that the ancestors of taurine cattle (Bos taurus) were domesticated from Bos primigenius primigenius in the Fertile Crescent during the Neolithic, more than 10,000 years ago (YA; Bruford, Bradley, & Luikart, 2003; Ajmone- Marsan, Garcia, & Lenstra, 2010; MacHugh, Larson, & Orlando, 2017)
MacHugh, Cunningham, and Loftus (1996), using maternal mitochondrial DNA, showed that African cattle feature a higher frequency of the T1 mitochondrial haplogroup than is common in other regions, estimated that the separation between African and European taurine ancestors occurred 22,000–26,000 YA, and found patterns of population expansions consistent with domestication that were more recent than the corresponding signature of African/European divergence

Summary

| INTRODUCTION

Between the late Pleistocene and early Holocene, the most commonly occurring cattle species was the aurochs (Bos primigenius), ranging from northern Africa to both the Atlantic and Pacific coasts of Eurasia (Zeuner, 1963). Bradley, MacHugh, Cunningham, and Loftus (1996), using maternal mitochondrial DNA (mtDNA), showed that African cattle feature a higher frequency of the T1 mitochondrial haplogroup than is common in other regions, estimated that the separation between African and European taurine ancestors occurred 22,000–26,000 YA (earlier than the Fertile Crescent domestication), and found patterns of population expansions consistent with domestication that were more recent than the corresponding signature of African/European divergence These results are supported by analyses of extant taurine cattle from Europe, the Middle East and Africa, as well as extinct British aurochs (Troy et al, 2001). To disentangle the long-standing debate around the existence of a third domestication event in north-east Africa, we used approximate Bayesian computation to model a variety of possible scenarios that could give rise to the extant patterns of cattle genetic diversity, including analyses to determine whether modern cattle derive from two or three domestication events and migratory patterns among breeds

| MATERIALS AND METHODS

Findings

| DISCUSSION