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 N e 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 N e 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 N e with the attainment of the current small N e 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.

Domestication of cattle: Two or three events?

“…The genetic composition of Asian hybrids (QIN, LUX) was more balanced between Asian indicine and taurine origins. As expected, Creole cattle were placed closer to the European taurine cluster (Decker et al., ; Martínez et al., ; Pitt et al., ), and American indicine cattle clustered with Asian indicine breeds (Orozco‐terWengel et al., ).…”

“…Illumina's BovineSNP50 v.1, v.2 and Bovine High Density BeadChip 770k SNP array data were merged from several previously published studies ( Supporting Information Table S1; Bovine Hapmap et al 2009;Decker et al, 2009;Gautier, Laloë, & Moazami-Goudarzi, 2010;McTavish, Decker, Schnabel, Taylor, & Hillis, 2013;Decker et al, 2014;Mbole-Kariuki et al, 2014;Orozco-terWengel et al, 2015;Park et al, 2015;Iso-Touru et al, 2016;Upadhyay et al, 2017;Pitt et al, 2018). After removing duplicated copies of individuals, the final data set comprised ~54,000 SNPs in most samples and corresponded to 3,196 individuals representing 180 breeds/populations of both taurine (n = 2,041) and indicine (n = 408) cattle, including hybrids of the two subspecies (Supporting Information Table S1).…”

“…Despite Crescent (Decker et al, 2014;Karimi et al, 2016;Loftus et al, 1999). cluster (Decker et al, 2014;Martínez et al, 2012;Pitt et al, 2018),…”

The genomics of domestication special issue editorial

“…The fourth section explores demographic processes in domestication (Pitt, Bruford et al., ; Pitt, Sevane et al., ;). Pitt, Sevane et al.…”

“…In another contribution, Pitt, Bruford et al. () explore how creole cattle underwent serial demographic fluctuations in Colombia, based on changing human trait preference and changes in local breed preferences, again highlighting how large changes in effective population size can occur over short time frames. Further, they identified genes that have led to adaptation to tropical humid environments (linking to the last topic in this special issue), different from their ancestors’ Iberian conditions.…”