ABSTRACT
The ongoing decline of large marine vertebrates must be urgently mitigated, particularly under increasing levels of climate change and other anthropogenic pressures. However, characterizing the connectivity among populations remains one of the greatest challenges for the effective conservation of an increasing number of endangered species. Achieving conservation targets requires an understanding of which seascape features influence dispersal and subsequent genetic structure. This is particularly challenging for adult-disperser species, and when distribution-wide sampling is difficult. Here, we developed a two-step modelling framework to investigate how seascape features drive the genetic connectivity of marine species without larval dispersal, to better guide the design of marine protected area networks and corridors. We applied this framework to the endangered grey reef shark, Carcharhinus amblyrhynchos, a reef-associated shark distributed across the tropical Indo-Pacific. In the first step, we developed a seascape genomic approach based on isolation-by-resistance models involving circuit theory applied to 515 shark samples, genotyped for 4,491 nuclear single-nucleotide polymorphisms, to explore which parameters drive their population genetic differentiation. We show that deep oceanic areas act as strong barriers to dispersal, while proximity to habitat facilitates dispersal. In the second step, we predicted the resulting genetic differentiation across the entire distribution range of the species, providing both local and global-scale conservation units for future management guidance. We found that grey reef shark populations are more fragmented than expected for such a mobile species, raising concerns about the resilience of isolated populations under high anthropogenic pressures. We recommend the use of this framework to identify barriers to gene flow and to help in the delineation of conservation units at different scales, together with its integration across multiple species when considering marine spatial planning.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
Ethics Genetic samples in New Caledonia were collected under permits to Laurent Vigliola by the Government of New Caledonia (permit #2015-1351/GNC), the Northern Province of New Caledonia (permit #60912-1508-2015/JJC) and the Southern Province of New Caledonia (permits #479-2016/ARR/DENV and #2093-2016/ARR/DENV). Great Barrier Reef Marine Park permits include G01/356, G02/021 and G03/8048.1.
Conflict of interest The authors declare no conflict of interest.
Funding Sampling in New Caledonia was funded by research grants of Laurent Vigliola (Programme APEX, Government of New Caledonia, Pew Charitable Trust, Total Foundation, IRD core funding), and David Mouillot (Programme APEX, Total Foundation). Data collection in other countries was supported by the Great Barrier Reef Marine Park Authority, Cooperative Research Centre (CRC) Reef, Australian Coral Reef Society, and PADI Aware. This research was funded also by the Sea World Research and Rescue Foundation and the Academy of Finland (grant 316294 to PM).