Local adaptation with gene flow in a highly dispersive shark

Abstract

Adaptive divergence in response to environmental clines are expected to be common in species occupying heterogeneous environments. Despite numerous advances in techniques appropriate for non-model species, gene-environment association studies in elasmobranchs are still scarce. The bronze whaler or copper shark (Carcharhinus brachyurus) is a large coastal shark with a wide distribution and one of the most exploited elasmobranchs in southern Africa. Here, we assessed the distribution of neutral and adaptive genomic diversity in C. brachyurus across a highly heterogeneous environment in southern Africa based on genome-wide SNPs obtained through a restriction site-associated DNA method (3RAD). A combination of differentiation-based genome-scan (outflank) and genotype-environment analyses (redundancy analysis, latent factor mixed models) identified a total of 234 differentiation-based outlier and candidate SNPs associated with bioclimatic variables. Analysis of 26,299 putatively neutral SNPs revealed moderate and evenly distributed levels of genomic diversity across sites from the east coast of South Africa to Angola. Multivariate and clustering analyses demonstrated a high degree of gene flow with no significant population structuring among or within ocean basins. In contrast, the putatively adaptive SNPs demonstrated the presence of two clusters and deep divergence between Angola and all other individuals from Namibia and South Africa. These results provide evidence for adaptive divergence in response to a heterogeneous seascape in a large, mobile shark despite high levels of gene flow. These results are expected to inform management strategies and policy at the national and regional level for conservation of C. brachyurus populations.

Keywords: adaptive divergence; elasmobranchs; genotype–environment association; population genomics; seascape genomics.