Loss of genetic diversity and isolation by distance and by environment in populations of a keystone ungulate species

Abstract

Adaptive genetic and neutral variations are essential for maintaining population viability in changing environmental conditions. Habitat loss and fragmentation can be reflected in the patterns of genetic variation in the populations. White-lipped peccaries (WLPs, Tayassu pecari) are wide-ranging Neotropical ungulates with important ecological roles in the ecosystem suffering local extinctions worldwide. Here, we used a RAD-seq protocol to genotype 192 individuals. After filtering, we identified sets of SNP markers (ranging from 147 to 151,792 SNPs) to assess the genetic diversity and population structure of WLPs from Pantanal, Cerrado, and Atlantic Forest in Brazil. We found signals of loss (θw < θπ) and lower genetic diversity (allelic richness, nucleotide diversity, and observed and expected heterozygosities) in the Central Cerrado and Atlantic Forest populations. Principal Component Analysis (PCA) and admixture analyses (NGSAdmix) using genome-wide and neutral SNP data sets showed three major genetic clusters according to the biomes. Multiple matrix regression with randomization (MMRR) analysis found an isolation-by-distance pattern explaining the neutral genetic differentiation. We used Latent Factor Mixed Models (LFMM) and Redundancy Analysis (RDA) to identify candidate SNPs involved in different biological processes, such as metabolism and immune and neuronal responses, mainly associated with temperature and precipitation variables. We found an adaptive population genetic structure, suggesting three adaptive units with significant patterns of isolation-by-distance and isolation-by-environment. Our results highlighted the importance of conservation strategies for maintaining the genetic diversity of WLP populations. Furthermore, conservation plans and translocation programs should preserve and consider the adaptive variation.