Sex-linked differentiation in commercially exploited fishes : rethinking population structure in dynamic marine environments

Abstract

Understanding how genomic structure links with ecological and evolutionary processes is critical for forecasting species responses to dynamic marine environments, especially in commercially exploited marine species, where fishing pressure can impact genomic integrity. Here we investigate Merluccius paradoxus, a commercially exploited demersal fish that appears to be undergoing a range expansion along the southern African coastline. Using whole-genome sequence data of individuals from across the species' distribution (n = 37), we reveal that sex-linked divergence, rather than geography, is the principal driver of genomic variation, challenging conventional assumptions of regional geographic population structure. Divergence was concentrated on autosomal regions (primarily large regions on Chromosomes 1 and 2), rather than known sex-determining (SD) regions (Chromosome 9), and did not have structural variants or extended linkage disequilibrium (LD). Instead, patterns were consistent with sex-specific directional selection acting on genes enriched for neuronal function, metabolism and muscle development, traits that are likely linked to behaviour, physiology and environmental tolerance. Males had reduced nucleotide diversity (π), low observed heterozygosity (Ho) and longer runs of homozygosity (ROH) in these regions, suggesting recent selective sweeps or a reduced effective population size (Ne). Together with spatial differences in sex distribution and genomic diversity metrics, results suggest that males and females may differ in both range dynamics and adaptive potential. As M. paradoxus continues to shift its distribution across geo-political boundaries, sex-biased adaptation may have important consequences for reproductive output, resilience and sustainable fisheries management under a changing climate. This study highlights the need to incorporate sex-linked genomic variation into conservation planning, particularly in transboundary systems vulnerable to cumulative pressures of fishing and environmental change.