On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data

Gabriele Senczuk,Hovirag Lancioni,Baldassare Portolano,Donata Marletta,Emiliano Lasagna,Christian Persichilli,Paolo Colangelo,Fabio Pilla,Zsolt Becskei,Elena Ciani,Francesca M Sarti,Taki Karsli,Paolo Ajmone-Marsan,Luca Ferretti,Salvatore Mastrangelo,Licia Colli

doi:10.1186/s12711-021-00639-w

Abstract

BackgroundDuring the Neolithic expansion, cattle accompanied humans and spread from their domestication centres to colonize the ancient world. In addition, European cattle occasionally intermingled with both indicine cattle and local aurochs resulting in an exclusive pattern of genetic diversity. Among the most ancient European cattle are breeds that belong to the so-called Podolian trunk, the history of which is still not well established. Here, we used genome-wide single nucleotide polymorphism (SNP) data on 806 individuals belonging to 36 breeds to reconstruct the origin and diversification of Podolian cattle and to provide a reliable scenario of the European colonization, through an approximate Bayesian computation random forest (ABC-RF) approach.ResultsOur results indicate that European Podolian cattle display higher values of genetic diversity indices than both African taurine and Asian indicine breeds. Clustering analyses show that Podolian breeds share close genomic relationships, which suggests a likely common genetic ancestry. Among the simulated and tested scenarios of the colonization of Europe from taurine cattle, the greatest support was obtained for the model assuming at least two waves of diffusion. Time estimates are in line with an early migration from the domestication centre of non-Podolian taurine breeds followed by a secondary migration of Podolian breeds. The best fitting model also suggests that the Italian Podolian breeds are the result of admixture between different genomic pools.ConclusionsThis comprehensive dataset that includes most of the autochthonous cattle breeds belonging to the so-called Podolian trunk allowed us not only to shed light onto the origin and diversification of this group of cattle, but also to gain new insights into the diffusion of European cattle. The most well-supported scenario of colonization points to two main waves of migrations: with one that occurred alongside with the Neolithic human expansion and gave rise to the non-Podolian taurine breeds, and a more recent one that favoured the diffusion of European Podolian. In this process, we highlight the importance of both the Mediterranean and Danube routes in promoting European cattle colonization. Moreover, we identified admixture as a driver of diversification in Italy, which could represent a melting pot for Podolian cattle.

Highlights

During the Neolithic expansion, cattle accompanied humans and spread from their domestication centres to colonize the ancient world
In this study, we used a comprehensive dataset including most of the autochthonous cattle breeds belonging to the so-called Podolian trunk to shed light into the origin and diversification of this group of European cattle
Several local breeds especially from the Italian Peninsula, show levels of genetic diversity that are similar to those observed in autochthonous breeds from the domestication centre, and intriguing explanations have been advanced to disclose this pattern

Summary

Introduction

During the Neolithic expansion, cattle accompanied humans and spread from their domestication centres to colonize the ancient world. The westward human-mediated expansion of cattle led to hybridization events between domesticated cattle and wild Bos primigenius present in both Europe and Africa [4] This general picture is well established, studies using either mitochondrial genome or nuclear single nucleotide polymorphism (SNP) data revealed greater complexity. The basal phylogenetic position occupied by these clades within the taurine radiation strongly supports Europe as an important centre of diversification of wild aurochs’ populations during the late Pleistocene, which later intermingled with domesticated cattle [8] This intriguing pattern led some authors to suggest that Italy might have been the site of an additional domestication or at least introgression event involving local aurochs [21]. Analysis of genomic data at the global scale has led to another picture, indicating three main clusters (B. t. indicus, European B. t. taurus and African B. t. taurus) with different levels of genetic admixture among them [4, 9, 22]

Results

Discussion

Conclusion