Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing

Abstract

Indicine cattle, also referred to as zebu (Bos taurus indicus), play a central role in pastoral communities across a wide range of agro-ecosystems, from extremely hot semiarid regions to hot humid tropical regions. However, their adaptive genetic changes following their dispersal into East Asia from the Indian subcontinent have remained poorly documented. Here, we characterize their global genetic diversity using high-quality whole-genome sequencing data from 354 indicine cattle of 57 breeds/populations, including major indicine phylogeographic groups worldwide. We reveal their probable migration into East Asia was along a coastal route rather than inland routes and we detected introgression from other bovine species. Genomic regions carrying morphology-, immune-, and heat-tolerance-related genes underwent divergent selection according to Asian agro-ecologies. We identify distinct sets of loci that contain promising candidate variants for adaptation to hot semi-arid and hot humid tropical ecosystems. Our results indicate that the rapid and successful adaptation of East Asian indicine cattle to hot humid environments was promoted by localized introgression from banteng and/or gaur. Our findings provide insights into the history and environmental adaptation of indicine cattle.

Fig. 1. Population genomic structuring and relationship among indicine cattle.

a Geographical locations of 74 taurine and indicine cattle breeds/populations included in this study. The map images were created by authors using https://impactlab.org/map. b Principal component analysis (PCA) showing PC1 versus PC2 of all cattle breeds/populations. c Neighbor-joining tree constructed using whole-genomic autosomal SNP data. d Admixture patterns for K = 2, dividing these cattle breeds/populations into indicine and taurine cattle, and K = 6, revealing each of the taurine and indicine phylogeographic groups.

Fig. 2. Selective sweeps within the South Asian indicine cattle.

a Manhattan plot of the F_ST values (y-axis) in windows of 50 kilobases (kb) using a 20 kb slide across all autosomes (X-axis). Names of genes within the highest peaks are shown. For a full list of the linked genes, see Supplementary Data 2. b and c Haplotype structures for selection regions on Bos taurus autosome (BTA) 6 and BTA13, respectively, in which rows represent individuals, columns represent polymorphic positions in the taurine cattle reference genome, and green and yellow indicate the alternative and reference alleles, respectively. Photos were taken by Quratulain Hanif. d and e Examples of genes with strong signals of selective sweeps in SAI cattle, in which θ_π estimates are plotted using a 10 kb sliding window  in the LEF1 and ASIP genomic regions on BTA6 and BTA13, respectively.

Fig. 3. Selective sweeps within East Asian indicine cattle.

a Manhattan plot of the population branch statistic (PBS) values (y-axis) in 50 kilobases (kb) windows with 20 kb steps across all autosomes (x-axis). Names of genes within the highest peaks are shown. A full list of the linked genes is included in Supplementary Table 6. b and c Examples of genes with strong selective sweep signals in EAI cattle, in which F_ST and θ_π estimates are plotted using a 10 kb sliding window in the TRPA1 and SEMA3F genomic regions on BTA14 and BTA22, respectively.

Fig. 4. Genome-wide introgression from banteng and gaur into East Asian indicine cattle.

a Map of the lengths and distributions of putatively adaptative introgressed segments in the EAI autosomes according to the results of the U20 statistic. The lengths of the colored columns are proportional to the physical lengths of the introgressed segments. b Introgressed segments from banteng into East Asian indicine (EAI) cattle show substantial enrichment for genes related to signal transduction and the digestive, endocrine, nervous, sensory, and circulatory systems. Word cloud color refers to the legend on the right of the terms. Font size is proportional to the gene number enriched in the pathway. c Plot of F_ST values for autosomal SNPs between EAI cattle and both African indicine (AFI) and South Asian indicine (SAI) cattle based on a 10 kb sliding window. d Phylogenetic analysis of SNPs in introgressed genes (HBM, HBA, HBA1, and HBQ1). e F_ST values of SNPs in a strong adaptive genomic region on Bos taurus autosome (BTA) 25 between EAI cattle and both SAI and AFI cattle as well as between EAI cattle and both banteng and gaur. f Different haplotypes of hemoglobin family members of banteng, gaur, gayal, kouprey, taurine, indicine, and other wild bovine species confirm the introgression from other bovine species into EAI cattle. g Geographical distribution of different haplotypes of hemoglobin family members in global cattle populations. h Amino acid sequence alignments of partial bovine HBA, HBA1, and HBQ1 along with their homologous sequences in other mammalian species. The map was drawn using the R package v4.1.0.

Fig. 5. The postulated global dispersal routes of indicine cattle.

The postulated dispersal routes of modern indicine cattle based on the distribution of Y haplogroups (a) and mitogenome haplogroups (b). The size of each circle is proportional to the number of samples per breed/population. c The synchronized routes and estimated times of the global dispersal of indicine cattle. The map was drawn using the ArcGIS v10.7.0.