Identification of Selection Signals on the X-Chromosome in East Adriatic Sheep: A New Complementary Approach

Abstract

Sheep are one of the most important livestock species in Croatia, found mainly in the Mediterranean coastal and mountainous regions along the East Adriatic coast, well adapted to the environment and mostly kept extensively. Our main objective was therefore to map the positive selection of the X-chromosome (18,983 SNPs that passed quality control), since nothing is known about the adaptation genes on this chromosome for any of the breeds from the Balkan cluster. Analyses were performed on a sample of eight native Croatian breeds (101 females and 100 males) representing the East Adriatic metapopulation and on 10 mouflons (five females and males), all sampled in Croatia. Three classical within-population approaches (extreme Runs of Homozygosity islands, integrated Haplotype Score, and number of Segregating Sites by Length) were applied along with our new approach called Haplotype Richness Drop (HRiD), which uses only the information contained in male haplotypes. We have also shown that phylogenetic analyses, such as the Median-joining network, can provide additional information when performed with the selection signals identified by HRiD. Our new approach identifies positive selection signals by searching for genomic regions that exhibit a sudden decline in haplotype richness. In total, we identified 14 positive selection signals, 11 using the classical approach and three using the HRiD approach, all together containing 34 annotated genes. The most reliable selection signal was mapped by all four approaches in the same region, overlapping between 13.17 and 13.60 Mb, and assigned to the CA5B, ZRSR2, AP1S2, and GRPR genes. High repeatability (86%) of results was observed, as 12 identified selection signals were also confirmed in other studies with sheep. HRiD offers an interesting possibility to be used complementary to other approaches or when only males are genotyped, which is often the case in genomic breeding value estimations. These results highlight the importance of the X-chromosome in the adaptive architecture of domestic ruminants, while our novel HRiD approach opens new possibilities for research.

Selection, recombination and population history effects on runs of homozygosity (ROH) in wild red deer (Cervus elaphus)

“…A number of studies have identified ROH hotspots to be sites of positive selection (Grilz-Seger et al 2019 ; Peripolli et al 2018 ; Purfield et al 2017 ; Sabeti et al 2002 ; Shihabi et al 2022 ). When accounting for the influence of recombination rate, the red deer population on Rum showed five genomic regions with a ROH in more than 15% of the population (Fig.…”

“…3 ). It can be assumed that positive selection leads to a sudden decrease in haplotype diversity (Shihabi et al 2022 ), as certain haplotypes are being favoured. This assumption is also supported by our simulations.…”

Selection, recombination and population history effects on runs of homozygosity (ROH) in wild red deer (Cervus elaphus)

“…A number of studies have identified ROH hotspots to be sites of positive selection (Grilz-Seger et al , 2019; Peripolli et al , 2018; Purfield et al , 2017; Sabeti et al , 2002; Shihabi et al , 2022). When accounting for the influence of recombination rate, the red deer population on Rum showed five genomic regions with a ROH in more than 15% of the population (Figure 2).…”

“…First, there is a sharp decrease in haplotype diversity at the onset of these two ROH hotspots (Figure 3). It can be assumed that positive selection leads to a sudden decrease in haplotype diversity (Shihabi et al , 2022), as certain haplotypes are being favoured. This assumption is also supported by our simulations.…”

High-Density Genomic Characterization of Native Croatian Sheep Breeds

“…The authors suggested that Balkan breeds are evolutionary connected with the domestication process and are one of the hub regions from which the migration of sheep spread to the rest of Europe. Recently, Shihabi et al (2022) identified specific adaptive selection signals on the X chromosome of the individuals used in this analysis.…”