On the origin of European sheep as revealed by the diversity of the Balkan breeds and by optimizing population-genetic analysis tools

Abstract

Background: In the Neolithic, domestic sheep migrated into Europe and subsequently spread in westerly and northwesterly directions. Reconstruction of these migrations and subsequent genetic events requires a more detailed characterization of the current phylogeographic differentiation. Results: We collected 50 K single nucleotide polymorphism (SNP) profiles of Balkan sheep that are currently found near the major Neolithic point of entry into Europe, and combined these data with published genotypes from southwest-Asian, Mediterranean, central-European and north-European sheep and from Asian and European mouflons. We detected clines, ancestral components and admixture by using variants of common analysis tools: geography-informative supervised principal component analysis (PCA), breed-specific admixture analysis, across-breed f 4 profiles and phylogenetic analysis of regional pools of breeds. The regional Balkan sheep populations exhibit considerable genetic overlap, but are clearly distinct from the breeds in surrounding regions. The Asian mouflon did not influence the differentiation of the European domestic sheep and is only distantly related to present-day sheep, including those from Iran where the mouflons were sampled. We demonstrate the occurrence, from southeast to northwest Europe, of a continuously increasing ancestral component of up to 20% contributed by the European mouflon, which is assumed to descend from the original Neolithic domesticates. The overall patterns indicate that the Balkan region and Italy served as post-domestication migration hubs, from which wool sheep reached Spain and north Italy with subsequent migrations northwards. The documented dispersal of Tarentine wool sheep during the Roman period may have been part of this process. Our results also reproduce the documented 18th century admixture of Spanish Merino sheep into several central-European breeds.

Clustering patterns mirror the geographical distribution and genetic history of Lemnos and Lesvos sheep populations

“…The linear negative correlation between observed heterozygosity and inbreeding levels (Fig 1) and the increased inbreeding coefficients estimated for Lemnos herds ( Table 1), suggests that heterozygote deficiency in the Lemnos sheep can be attributed to higher incidence of matings between relatives. In line with these findings, a linear inverse relationship between genetic diversity and inbreeding has also been established in other studies of Balkan and European sheep breeds [5].…”

“…Both sheep populations studied herein maintained sufficient genetic variation as inferred by H O with values in the range of 0.36 to 0.39. These estimates are comparable or higher to other southern and western European (0.22-0.38) [16] sheep breeds, are higher than the Oxford sheep breed (0.35) in the United States [17] and comparable (Lemnos) or higher (Lesvos) than other Greek breeds such as Chios, Kymi and Lesvos [5].…”

“…The latter breed has been reported to cluster with other mountainous breeds in Greece [ 1 ]. It is placed on the center of an east–west geographical cline and is an intermediate between fat-tailed Asian and European sheep [ 5 ]. Using microsatellite markers, Mastranestasis et al [ 4 ] estimated a heterozygote excess in the overall Lesvos sheep population as well as low genetic differentiation levels between herds attributable to high gene flow.…”

Local adaptations of Mediterranean sheep and goats through an integrative approach

“…For the study, we have targeted the Mediterranean arc in France, Italy and Spain. This region has the advantage of harboring closely related sheep and goat breeds, in spite of large environmental contrasts (Ciani et al, 2020; Colli et al, 2018; Kijas et al, 2009). We initially, considered 32 breeds of goats and 51 breeds of sheep (Supplementary Table 1).…”

“…This study aimed at identifying the genomic bases of adaptation, in local breeds of goats and sheep, distributed along the Mediterranean arc, in Italy, the south of France and Spain. The area under consideration harbours contrasting environments, such as high altitude areas (Alps, Pyrenees, Corsica), coastal areas, wetlands and arid areas, with closely related sheep and goat breeds (Ciani et al, 2020; Colli et al, 2018; Kijas et al, 2009). All these features provide an ideal situation for the identification of adaptation signatures.…”