Seascape Genomics Uncovers Weak Signs of Local Adaptation Despite Bottleneck Events, High Inbreeding and Low Heterozygosity in the Vulnerable Smooth Hammerhead Shark ( Sphyrna zygaena )

Abstract

The smooth hammerhead shark ( Sphyrna zygaena ) is a highly migratory pelagic predator classified as Vulnerable due to overexploitation and rapid climate change. However, its genomic diversity, connectivity patterns and demographic history remain poorly understood. Using a reference‐based, genome‐wide ddRAD sequencing approach, we examined the population structure, genotype–environment relationships and demographic history across the Atlantic and Southwest Indian Oceans to assess evolutionary resilience and conservation‐related population dynamics. Genome‐wide SNP analyses revealed two main Management Units corresponding to the Atlantic and Southwest Indian Ocean, showing moderate yet significant differentiation and limited connectivity across ocean basins. Effective migration surface models highlighted the Gulf of Guinea, Madagascar and Réunion Island as key connectivity regions, suggesting their potential role as corridors maintaining genetic exchange. Genome scans identified a small number of loci linked to environmental gradients, including productivity, oceanographic circulation, temperature and bathymetry, indicating weak signals of local adaptation relative to neutral population structure. Estimates of genome‐wide heterozygosity were low in both regions, and runs of homozygosity indicated high levels of autozygosity, especially in the Atlantic lineage, consistent with high inbreeding. Demographic analysis suggested a historical population expansion during the Pleistocene, followed by a long decline and a recent severe bottleneck coinciding with the rise of industrial fisheries, resulting in critically low current effective population sizes. Overall, these results highlight genomic erosion in S. zygaena , underscoring the importance of preserving connectivity hotspots to support adaptive capacity and long‐term population survival.