A comprehensive genome-wide scan detects genomic regions related to local adaptation and climate resilience in Mediterranean domestic sheep

Abstract

Background: The management of farm animal genetic resources and the adaptation of animals to climate change will probably have major effects on the long-term sustainability of the livestock sector. Genomic data harbour useful relevant information that needs to be harnessed for effectively managing genetic resources. In this paper, we report the genome characterization of the highly productive Mediterranean Chios dairy sheep and focus on genetic diversity measures related with local adaptation and selection and the genetic architecture of animal resilience to weather fluctuations as a novel adaptative trait linked to climate change.

Results: We detected runs of homozygosity (ROH) and heterozygosity (ROHet) that revealed multiple highly homozygous and heterozygous hotspots across the Chios sheep genome. A particularly highly homozygous region was identified on chromosome 13 as a candidate of directional genetic selection associated with milk traits, which includes annotated genes that were previously shown to be linked to local adaptation to harsh environmental conditions. Favourable heterozygosity related with a potentially protective role against livestock diseases and enhanced overall fitness was revealed in heterozygous-rich regions on sheep chromosomes 3, 10, 13 and 19. Furthermore, genomic analyses were conducted on sheep resilience phenotypes that display changes in milk production in response to weather variation. Sheep resilience to heat stress was a significantly heritable trait (h² = 0.26) and genetically antagonistic to milk production. Genome-wide association and regional heritability mapping analyses revealed novel genomic markers and regions on chromosome 5 that were significantly associated with sheep resilience to climate change. Subsequently, an annotation analysis detected a set of genes on chromosome 5 that were associated with olfactory receptor complexes that could participate in heat stress mitigation through changes in respiration rate and respiratory evaporation. Other genes were grouped in previously reported biological processes relevant to livestock heat dissipation, including stress and immune response.

Conclusions: Our results may contribute to the optimal management of sheep genetic resources and inform modern selective breeding programmes that aim at mitigating future environmental challenges towards sustainable farming, while better balancing animal adaptation and productivity. Our results are directly relevant to the studied breed and the respective environmental conditions; however, the methodology may be extended to other livestock species of interest.

Fig. 1

Individual run of homozygosity (ROH)-based inbreeding levels (F_ROH) in Chios sheep. A, B, C correspond to the farm of origin of the animals

Fig. 2

Manhattan plots showing the frequency of a SNP within homozygous and heterozygous segments in Chios sheep. a Runs of homozygosity (ROH), and b runs of heterozygosity (ROHet). Grey lines indicate the 99.9 quantile thresholds, defining the respective ROH/ROHet islands

Fig. 3

Principal component analysis (PCA) of Chios sheep. a Proportion of variation (%) corresponding to each principal component of the decomposed genomic relationship matrix; and b First and second principal components showing the population stratification attributed to the farm origin of individual sheep

Fig. 4

Chios sheep milk performance resilience to air temperature variation. The curve represents the average change in daily milk yield (DMY) in response to temperature variation (Tavg, °C)

Fig. 5

Comparison of estimated genomic breeding values (GEBV) of Chios sheep resilience to cold (Tavg10) and hot (Tavg25) weather conditions, lifetime milk production (tmilk), and length of productive life (tdim). a Resilience to cold and b hot weather compared to lifetime milk production respectively, c comparison between resilience to cold and hot weather conditions, d comparison of resilience to cold, e hot weather with length of productive life respectively, and f comparison between lifetime milk production and length of productive life

Fig. 6

Genome-wide association results for Chios sheep resilience to temperature change and performance-related traits. a Resilience to hot weather conditions, b resilience to cold weather conditions, c lifetime milk yield, and d length of productive life. Red and blue lines indicate the genome-wide and suggestive (one false positive per genome scan) significance thresholds, respectively

Fig. 7

Regional heritability mapping results for Chios sheep resilience to temperature change and performance-related traits. a Resilience to hot weather conditions, b resilience to cold weather conditions, c lifetime milk yield, and d length of productive life. Red and blue lines indicate the genome-wide and suggestive (one false positive per genome scan) significance thresholds, respectively