A comprehensive analysis of the genetic diversity and environmental adaptability in worldwide Merino and Merino-derived sheep breeds

Abstract

Background: To enhance and extend the knowledge about the global historical and phylogenetic relationships between Merino and Merino-derived breeds, 19 populations were genotyped with the OvineSNP50 BeadChip specifically for this study, while an additional 23 populations from the publicly available genotypes were retrieved. Three complementary statistical tests, Rsb (extended haplotype homozygosity between-populations), XP-EHH (cross-population extended haplotype homozygosity), and runs of homozygosity (ROH) islands were applied to identify genomic variants with potential impact on the adaptability of Merino genetic type in two contrasting climate zones.

Results: The results indicate that a large part of the Merino's genetic relatedness and admixture patterns are explained by their genetic background and/or geographic origin, followed by local admixture. Multi-dimensional scaling, Neighbor-Net, Admixture, and TREEMIX analyses consistently provided evidence of the role of Australian, Rambouillet and German strains in the extensive gene introgression into the other Merino and Merino-derived breeds. The close relationship between Iberian Merinos and other South-western European breeds is consistent with the Iberian origin of the Merino genetic type, with traces from previous contributions of other Mediterranean stocks. Using Rsb and XP-EHH approaches, signatures of selection were detected spanning four genomic regions located on Ovis aries chromosomes (OAR) 1, 6 and 16, whereas two genomic regions on OAR6, that partially overlapped with the previous ones, were highlighted by ROH islands. Overall, the three approaches identified 106 candidate genes putatively under selection. Among them, genes related to immune response were identified via the gene interaction network. In addition, several candidate genes were found, such as LEKR1, LCORL, GHR, RBPJ, BMPR1B, PPARGC1A, and PRKAA1, related to morphological, growth and reproductive traits, adaptive thermogenesis, and hypoxia responses.

Conclusions: To the best of our knowledge, this is the first comprehensive dataset that includes most of the Merino and Merino-derived sheep breeds raised in different regions of the world. The results provide an in-depth picture of the genetic makeup of the current Merino and Merino-derived breeds, highlighting the possible selection pressures associated with the combined effect of anthropic and environmental factors. The study underlines the importance of Merino genetic types as invaluable resources of possible adaptive diversity in the context of the occurring climate changes.

Fig. 1

Multi-dimensional scaling plots of the Merino and Merino-derived sheep breeds. Dimension 1 vs 2 (a) and dimension 1 vs 3 (b). The different colours of the squares reflect the three clusters that include breeds with similar genetic background. For a full definition of breeds see Table 1.

Fig. 2

Neighbor-Net graph based on between-breed Reynolds’ distances for the whole dataset. For a full definition of breeds see Table 1

Fig. 3

Admixture software results in a circular fashion for K (number of clusters) = 2 to 5 (a), and geographic distribution of the genomic components corresponding to the K = 5 resolution (b). For a full definition of breeds see Table 1

Fig. 4

Maximum likelihood tree constructed with TreeMix when four migration events were allowed. Migration arrows are coloured according to their weight. For a full definition of breeds see Table 1

Fig. 5

Manhattan plots showing the results of Rsb and XP-EHH tests for the autosomes in the Merino and Merino-derived breeds. a Rsb test for Mediterranean vs Continental Merino and Merino-derived breeds. b XP-EHH for Mediterranean vs Continental Merino and Merino-derived breeds. Horizontal dashed lines mark the significance threshold applied to detect the outlier SNPs (−log10 (P value) = 4)