Genomic adaptation to extreme climate conditions in beef cattle as a consequence of cross-breeding program

Abstract

Background: Understanding the evolutionary forces related to climate changes that have been shaped genetic variation within species has long been a fundamental pursuit in biology. In this study, we generated whole-genome sequence (WGS) data from 65 cross-bred and 45 Mongolian cattle. Together with 62 whole-genome sequences from world-wide cattle populations, we estimated the genetic diversity and population genetic structure of cattle populations. In addition, we performed comparative population genomics analyses to explore the genetic basis underlying variation in the adaptation to cold climate and immune response in cross-bred cattle located in the cold region of China. To elucidate genomic signatures that underlie adaptation to cold climate, we performed three statistical measurements, fixation index (FST), log₂ nucleotide diversity (θπ ratio) and cross population composite likelihood ratio (XP-CLR), and further investigated the results to identify genomic regions under selection for cold adaptation and immune response-related traits.

Results: By generating WGS data, we investigated the population genetic structure and phylogenetic relationship of studied cattle populations. The results revealed clustering of cattle groups in agreement with their geographic distribution. We detected noticeable genetic diversity between indigenous cattle ecotypes and commercial populations. Analysis of population structure demonstrated evidence of shared genetic ancestry between studied cross-bred population and both Red-Angus and Mongolian breeds. Among all studied cattle populations, the highest and lowest levels of linkage disequilibrium (LD) per Kb were detected in Holstein and Rashoki populations (ranged from ~ 0.54 to 0.73, respectively). Our search for potential genomic regions under selection in cross-bred cattle revealed several candidate genes related with immune response and cold shock protein on multiple chromosomes. We identified some adaptive introgression genes with greater than expected contributions from Mongolian ancestry into Molgolian x Red Angus composites such as TRPM8, NMUR1, PRKAA2, SMTNL2 and OXR1 that are involved in energy metabolism and metabolic homeostasis. In addition, we detected some candidate genes probably associated with immune response-related traits.

Conclusion: The study identified candidate genes involved in responses to cold adaptation and immune response in cross-bred cattle, including new genes or gene pathways putatively involved in these adaptations. The identification of these genes may clarify the molecular basis underlying adaptation to extreme environmental climate and as such they might be used in cattle breeding programs to select more efficient breeds for cold climate regions.

Keywords: Cattle; Cold adaptation; TRPM8; Whole-genome sequence.

Fig. 1

(A) Locations of cattle breeds for each geographic groups. Populations are colored to mirror their geographic origin. (B) PCA of cattle populations. (C) ADMIXTURE results for k = 2 to k = 5. (D) The decay of LD estimated as the squared correlation coefficient by pairwise physical distance in cattle populations and (E) Boxplots of nucleotide diversity, calculated in 50 kb sliding window with 20 kb increments across the genome

Fig. 2

Correlation of nucleotide diversity (θπ) (50-kb non-overlapping window) between cross-bred group (green) and different cattle groups; (A) Mongolian cattle, (B) Red-Angus breed and (C) other populations (orange)

Fig. 3

Genome-wild introgressions (black lines) from Mongolian cattle into cross-bred population

Fig. 4

Genomic regions with selection signals in cross-bred cattle group. (A) Distribution of the pairwise fixation index (FST) (y axis) and θπ ln ratio (x axis) between Red-Angus cattle and cross-bred group. (B) Selection signals around TRPM8. FST based on SNPs is shown as a line using a nonoverlapping 10-kb sliding window