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

Abstract

Background During 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. Results Our 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. Conclusions This 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.

Large‐scale mitogenome sequencing reveals consecutive expansions of domestic taurine cattle and supports sporadic aurochs introgression

“…The variation found in South‐east European cattle can be attributed to Neolithic migrations, as haplogroups T 3 , T 2 and Q were already present in Serbia and Greece ~7.0 kyBP (Verdugo et al, 2019 ). Boskarin and Slavonian Syrmian Podolian cattle, two representatives of the two Podolian clusters (Senczuk et al, 2021 ), were predominantly assigned to the T 3 haplogroup, with the exception of three T 5 haplotypes in the latter breed. This result is consistent with the conclusions of Di Lorenzo et al ( 2018 ), who found no mitogenome differences between Podolian cattle from Central Europe and the Balkans and Podolian cattle from Italy.…”

“…and Slavonian Syrmian Podolian cattle, two representatives of the two Podolian clusters(Senczuk et al, 2021), were predominantly assigned to the T 3 haplogroup, with the exception of three T 5 haplotypes in the latter breed. This result is consistent with the conclusions of DiLorenzo et al (2018), who found no mitogenome differences between Podolian cattle from Central Europe and the Balkans and Podolian cattle from Italy.…”

How Geography and Climate Shaped the Genomic Diversity of Italian Local Cattle and Sheep Breeds

“…Interestingly, the first axis clearly discriminated all breeds that belonged to the so-called Podolian trunk. These breeds have a complex evolutionary history, recently dissected using genomewide SNPs, and probably belong to a secondary wave of migration through both the Danubian and Mediterranean routes after the arrival of indicine cattle in the Middle East [ 38 ]. On the other hand, the second axis mainly distinguishes some breeds from Central Italy, and in particular two breeds from Tuscany, the Pontremolese, and Garfagnina.…”

“…The genomic architecture of these two species is complex due to a combination of several factors, including the heterogeneous predomestication genomic pool, the European diffusion via different spatiotemporal migration routes, and the subsequent admixture with both wild counterparts ( Bos primigeneus for cattle, mouflon for sheep) and local populations [ 38 , 44 , 45 , 46 ].…”

Seven Shades of Grey: A Follow-Up Study on the Molecular Basis of Coat Colour in Indicine Grey Cattle Using Genome-Wide SNP Data

“…These results are of a certain relevance, not only because they corroborate, and thus validate, the previously published differential selection signals (likely related with the genetic architecture of premature hair greying) detected in taurine cattle [ 17 ] in an independent set of indicine cattle breeds, but also because they may point to a common origin of the genetic mechanisms underlying this adaptation-related phenotype in both cattle subspecies. A number of recent papers [ 24 , 52 , 54 , 55 ] reported variable proportions of indicine ancestry into central and southern Italian taurine cattle breeds belonging to the Podolian trunk (Chianina, Calvana, Romagnola, Marchigiana, Maremmana, Italian Podolica), assuming this indicine heritage in taurine cattle as remnant of remote post-domestication introgression events likely occurred in Asia and/or at the Asia/Europe border, coupled with subsequent westward cattle migration events. Under such assumption, we can hence consider that the premature hair greying observed today in cattle breeds from both subspecies was an ancestral condition in the early genetic stock of Asiatic indicine origin, where it may have played a positive role on environmental robustness (i.e., higher thermo-tolerance and lower UV-induced damage due to higher solar reflectance), while having been a posterior acquisition in taurine cattle breeds.…”