Demography and rapid local adaptation shape Creole cattle genome diversity in the tropics

Abstract

The introduction of Iberian cattle in the Americas after Columbus’ arrival imposed high selection pressures on a limited number of animals over a brief period of time. Knowledge of the genomic regions selected during this process may help in enhancing climatic resilience and sustainable animal production. We first determined taurine and indicine contributions to the genomic structure of modern Creole cattle. Second, we inferred their demographic history using approximate Bayesian computation (ABC), linkage disequilibrium (LD) and Ne Slope (NeS) analysis. Third, we performed whole genome scans for selection signatures based on cross-population extended haplotype homozygosity (XP-EHH) and population differentiation (FST) to disentangle the genetic mechanisms involved in adaptation and phenotypic change by a rapid and major environmental transition. To tackle these questions, we combined SNP array data (~54,000 SNPs) in Creole breeds with their modern putative Iberian ancestors. Reconstruction of the population history of Creoles from the end of the 15th century indicated a major demographic expansion until the introduction of zebu and commercial breeds into the Americas ~180 years ago, coinciding with a drastic Ne contraction. NeS analysis provided insights into short-term complexity in population change and depicted a decrease/expansion episode at the end of the ABC-inferred expansion, as well as several additional fluctuations in Ne with the attainment of the current small Ne only towards the end of the 20th century. Selection signatures for tropical adaptation pinpointed the thermoregulatory slick hair coat region, identifying a new candidate gene (GDNF), as well as novel candidate regions involved in immune function, behavioural processes, iron metabolism and adaptation to new feeding conditions. The outcomes from this study will help in future-proofing farm animal genetic resources (FAnGR) by providing molecular tools that allow selection for improved cattle performance, resilience and welfare under climate change.