Regional population and seascape genomics of the smooth hammerhead shark Sphyrna zygaena reveals adaptive clinal variation despite high gene flow

Abstract

Globally, hammerhead sharks have experienced severe declines owing to continued overexploitation and anthropogenic change. The smooth hammerhead shark Sphyrna zygaena remains comparatively understudied compared to other members of the family Sphyrnidae, and despite its Vulnerable status, a comprehensive understanding of its genetic landscape remains lacking. The present study aimed to conduct a fine-scale genomic assessment of Sphyrna zygaena within the highly dynamic marine environment of South Africa’s coastline, using thousands of single nucleotide polymorphisms (SNPs) derived from restriction site-associated DNA sequencing (3RAD). A combination of differentiation-based outlier detection methods (OUTFlank and pcadapt) and Genotype-Environment Association (GEA) (Redundancy Analysis) analysis in Sphyrna zygaena were employed. Subsequent assessments of putatively adaptive loci revealed a distinctive south to east genetic cline. Amongst these, notable correlations between adaptive variation and sea-surface dissolved oxygen and salinity, in addition to spatial factors were evident. Conversely, analysis of 110, 965 neutral SNP markers revealed a lack of regional population differentiation, a finding that remained consistent across various analytical approaches, including an assessment of isolation-by-distance (IBD) and isolation-by-environment (IBE), genetic clustering analyses (LEA, fastSTRUCTURE, and find.clusters), and a discriminant analysis of principal components (DAPC). These results provide evidence for the presence of differential selection pressures within a limited spatial range, despite high gene flow implied by the selectively neutral dataset. This study offers notable insights regarding the potential impacts of genomic variation in response to fluctuating environmental conditions in the circumglobally distributed Sphyrna zygaena.