Genomic insights into the population history and adaptive traits of Latin American Criollo cattle

Abstract

Criollo cattle, the descendants of animals brought by Iberian colonists to the Americas, have been the subject of natural and human-mediated selection in novel tropical agroecological zones for centuries. Consequently, these breeds have evolved distinct characteristics such as resistance to diseases and exceptional heat tolerance. In addition to European taurine (Bos taurus) ancestry, it has been proposed that gene flow from African taurine and Asian indicine (Bos indicus) cattle has shaped the ancestry of Criollo cattle. In this study, we analysed Criollo breeds from Colombia and Venezuela using whole-genome sequencing (WGS) and single-nucleotide polymorphism (SNP) array data to examine population structure and admixture at high resolution. Analysis of genetic structure and ancestry components provided evidence for African taurine and Asian indicine admixture in Criollo cattle. In addition, using WGS data, we detected selection signatures associated with a myriad of adaptive traits, revealing genes linked to thermotolerance, reproduction, fertility, immunity and distinct coat and skin coloration traits. This study underscores the remarkable adaptability of Criollo cattle and highlights the genetic richness and potential of these breeds in the face of climate change, habitat flux and disease challenges. Further research is warranted to leverage these findings for more effective and sustainable cattle breeding programmes.

Keywords: Latin America; cattle; microevolution; population genomics; selection; thermotolerance.

Figure 1.

Approximate geographical origins of the animals from three Criollo breeds that were used to generate new whole-genome sequence (WGS) data. Map modified from the original using Mapswire (https://mapswire.com) (Creative Commons Attribution 4.0 International License CC-BY 4.0). Individual cattle art images modified from Felius [23] with permission of the author.

Figure 2.

Genetic diversity and admixture in Criollo and comparative cattle populations. (a) Results of the principal component analysis (principal component analysis (PCA) for 308 animals (47 from whole-genome sequence (WGS)go data and 261 from high-density SNP array data) with a shared set of 302 012 SNPs. The PCA plot shows the coordinates for each animal based on the first two principal components with the major breed groupings highlighted. Principal component 1 (PC1) differentiates the B. taurus and B. indicus lineages, whereas PC2 separates the African and European taurine groups. A histogram plot also shows the variance contributions for the first 20 PCs, with PC1 and PC2 accounting for 44.7% and 12.9% of this variance, respectively. (b) Unsupervised genetic structure plot for European and Iberian taurine, Criollo cattle, African taurine and American and Asian indicine populations. Results for ancestry clusters ranging from K = 3 to 6 are shown.

Figure 3.

Chromosome-wide Manhattan plots of the smooth composite selection signals (CSS) scores for Blanco Orejinegrio (a), Hartón del Valle (b) and Limonero (c). The dashed red lines indicate the genome-wide 0.1% thresholds of the empirical CSS scores. Green data points represent SNPs classified as significant and flanked by at least five additional SNPs among the top 1% of the CSS scores. Notable candidate genes are indicated and discussed further in the text. Individual cattle art images were modified from Felius [23] with the permission of the author.

Figure 4.

Gene ontology (GO) over-representation analysis results for the Blanco Orejinegrio (a), Hartón del Valle (b) and Limonero (c). The y-axis represents the negative log₁₀ FDR-p _adj. from the over-representation analysis. Individual cattle art images were modified from Felius [23] with the permission of the author.