Connections Across Open Water: A Bi-Organelle, Genomics-Scale Assessment of Atlantic-Wide Population Dynamics in a Pelagic, Endangered Apex Predator Shark (Isurus oxyrinchus)

Abstract

Large-bodied pelagic sharks are key regulators of oceanic ecosystem stability, but highly impacted by severe overfishing. One such species, the shortfin mako shark (Isurus oxyrinchus), a globally widespread, highly migratory predator, has undergone dramatic population reductions and is now Endangered (IUCN Red List), with Atlantic Ocean mako sharks in particular assessed by fishery managers as overfished and in need of urgent, improved management attention. Genomic-scale population assessments for this apex predator species have not been previously available to inform management planning; thus, we investigated the population genetics of mako sharks across the Atlantic using a bi-organelle genomics approach. Complete mitochondrial genome (mitogenome) sequences and genome-wide SNPs from sharks distributed across the Atlantic revealed contrasting patterns of population structure across marker types. Consistent with this species' long-distance migratory capabilities, SNPs showed high connectivity and Atlantic panmixia overall. In contrast, there was matrilineal population genetic structure across Northern and Southern Hemispheres, suggesting at least large regional-scale female philopatry. Linkage disequilibrium network analysis indicated that makos possess a chromosomal inversion that occurs Atlantic wide, a genome feature that may be informative for evolutionary investigations concerning adaptations and the global history of this iconic species. Mitogenome diversity in Atlantic makos was high compared to other elasmobranchs assessed at the mitogenome level, and nuclear diversity was high compared to the two other, highly migratory pelagic shark species assessed with SNPs. These results support management efforts for shortfin makos on at least Northern versus Southern Hemisphere scales to preserve their matrilineal genetic distinctiveness. The overall comparative genetic diversity findings provide a baseline for future comparative assessments and monitoring of genetic diversity, as called for by the United Nations Convention on Biological Diversity, and cautious optimism regarding the health and recovery potential of Atlantic shortfin makos if further population declines can be halted.