Genome-wide scan of fat-tail sheep identifies signals of selection for fat deposition and adaptation

Abstract

Fat tail in sheep represents a valuable energy reserve for facing future climate changes. The identification of genes with a role in the fat-tail phenotype may contribute to understanding the physiology of fat deposition and the mechanisms of adaptation. Genotypic data obtained with the OvineSNP50K array in 13 thin-tail sheep breeds from Italy were used to identify selection signatures of fat tail through pairwise thin- versus fat-tail sheep breed comparisons, with the following fat-tail breeds of the Mediterranean area: two unique Italian fat-tail breeds (Barbaresca and Laticauda), a Barbary sheep breed from Libya, Ossimi breed from Egypt, Cyprus Fat-Tail and Chios from the Greek islands Cyprus and Chios, respectively. Fst and χ2 values obtained for >40000 polymorphic markers allowed confirmation of 12 fat-tail associations that were previously reported in Chinese and Iranian breeds. Two of these signals – on OAR 7 and OAR 13 – are in the proximity of two genes – VRTN and BMP2 – with a role in the variation of vertebral number and in fat-tail formation respectively. Two identified signals on OAR 6 and OAR 15 encompass two genes, PDGFRA and PDGFD, involved in the differentiation of preadipocytes. Further signals detected herein were reported in Chinese sheep as signatures of adaptation to desert areas. For several of the detected associations, the known role in either fat deposition or adaptation, thus contributing to revealing the molecular basis underlying mechanisms of energy storage and climate adaptation.

Novel and known signals of selection for fat deposition in domestic sheep breeds from Africa and Eurasia

“…Out of the ten genes found in this region, only ANAPC1 has been associated with obesity-related traits by Comuzzie et al [23] in a Genome-Wide Association Study (GWAS) on Hispanic children. The signature on OAR3:154.0-155.6 Mb (S2 Fig and Table 4), detected in the Laticauda and the Libyan Barbary breeds, had already been reported for the Barbaresca, Laticauda and Chios breeds [9]. Yuan et al [11], in a GWAS on seven indigenous Chinese sheep, by contrasting fat-tail versus thin-tail phenotypes, detected a signature in this region encompassing the MSRB3 , that has been identified as a candidate gene associated with adaptation [24].…”

“…Moreover, this selection signature overlapped with the ROH island identified in the Ethiopian fat-tail breeds, which include 17 and 29 homozygous markers respectively for the two groups of breeds (the eleven Ethiopian fat-tail, and the six Ethiopian long fat-tail). The signal on OAR6:38.1-39.6 Mb (S4 Fig and Table 4) was detected in Barbaresca and Laticauda and was previously reported as selection signature for fat-tail in these two breeds, also when compared with 13 Italian thin-tail breeds [9]. It includes the SLIT2 gene, a potential candidate for internal organ weights in Simmental beef cattle [32] and therefore possibly connected with fat deposition.…”

“…A large region on OAR5:47.0-49.0 Mb (S3 Fig and Table 4) turned out here to encode putative fat deposition genes in the two groups of Ethiopian sheep: the one composed only by the long fat-tail, and the one including all the eleven Ethiopian fat-tail breeds. Although Fariello et al [29] reported that this region encoded a signature differentiating prolific and non-prolific Asian sheep, the involvement of a signature in this region in the fat-tail phenotype had been previously reported [9,12]. This involvement is corroborated by genetic studies of body mass index in humans, describing a role played in obesity by the CXXC5 gene in Americans [30] and the PSD2 gene in the Japanese population [31].…”

“…All authors used, for their comparisons, sheep of the same geographic regions to prevent referring to the fat-tail differentiation signals arising from different origins or isolation by distance. These studies included indigenous Chinese [4,8,10,11], Mediterranean-North African [9,12], Iranian [3] and Ethiopian breeds [13]. Similarly, in this study, the genomes of fat-tail sheep from different regions of Africa and Eurasia were contrasted with the genomes of thin-tail sheep of the same geographical area.…”

Identifying loci under positive selection in complex population histories

“…The derived allele at this SNP is at more than 50% frequency in all 1000 Genomes East Asian panels but at less than 2% frequency in all the other worldwide panels, except for South Asians where it reaches frequencies of around 10%. Interestingly, the TARBP1 gene has been identified as a target for positive selection in milkproducing cattle [62] and in sheep breeds [63,64]. It has also been associated with resistance to gastrointestinal nematodes in sheep [65].…”