Like a rolling stone: Colonization and migration dynamics of the gray reef shark (Carcharhinus amblyrhynchos)

Abstract

Designing appropriate management plans requires knowledge of both the dispersal ability and what has shaped the current distribution of the species under consideration. Here, we investigated the evolutionary history of the endangered gray reef shark ( Carcharhinus amblyrhynchos ) across its range by sequencing thousands of RADseq loci in 173 individuals in the Indo‐Pacific (IP). We first bring evidence of the occurrence of a range expansion (RE) originating close to the Indo‐Australian Archipelago (IAA) where two stepping‐stone waves (east and westward) colonized almost the entire IP. Coalescent modeling additionally highlighted a homogenous connectivity ( Nm ~ 10 per generation) throughout the range, and isolation by distance model suggested the absence of barriers to dispersal despite the affinity of C. amblyrhynchos to coral reefs. This coincides with long‐distance swims previously recorded, suggesting that the strong genetic structure at the IP scale ( F ST ~ 0.56 between its ends) is the consequence of its broad current distribution and organization in a large number of demes. Our results strongly suggest that management plans for the gray reef shark should be designed on a range‐wide rather than a local scale due to its continuous genetic structure. We further contrasted these results with those obtained previously for the sympatric but strictly lagoon‐associated Carcharhinus melanopterus , known for its restricted dispersal ability. Carcharhinus melanopterus exhibits a similar RE dynamic but is characterized by a stronger genetic structure and a nonhomogeneous connectivity largely dependent on local coral reefs availability. This sheds new light on shark evolution, emphasizing the roles of IAA as source of biodiversity and of life‐history traits in shaping the extent of genetic structure and diversity.

Global genetic diversity and historical demography of the Bull Shark

“…Combosch & Vollmer, 2015;Harvey & Brumfield, 2015). However, few elasmobranchs have benefited yet (see Devloo-Delva et al, 2023;Feutry et al, 2020;Glaus et al, 2020;Lesturgie et al, 2023;Lesturgie, Lainé, et al, 2022;Lesturgie, Planes, & Mona, 2022;Maisano Delser et al, 2016, 2019 Main Conclusions: This study further confirms the role of marine biogeographic breaks in shaping the genetic history of large mobile marine predators. N e historical increases in N e are potentially linked to extended coastal habitat availability.…”

“…Sharks life history traits largely affect population structure (Lesturgie, Lainé, et al, 2022;Lesturgie, Planes, & Mona, 2022), but few species have been studied on a global scale with genomic datasets similar to the one presented here. Species exhibiting strict fidelity to coral reefs such as the Blacktip Reef and Grey Reef sharks present strong genetic structuring over the Indo-Pacific (Lesturgie et al, 2023;Maisano Delser et al, 2019). On the contrary, Tiger Shark, presenting a similar circumtropical distribution to C. leucas, is divided into two almost independent panmictic stocks (the Atlantic and the Indo-Pacific, Lesturgie, Planes, & Mona, 2022;Lesturgie, Lainé, et al, 2022).…”

High differentiation but low divergence: demographic history of grey reef sharks (Carcharhinus amblyrhynchos) across the Indian Ocean

“…> 100 km) migrations (Bonnin et al, 2019). Accordingly, C. amblyrhynchos populations show signi cant genetic differentiation between the western distribution range limit in the Indian Ocean and eastern ranges in central and west Paci c populations due to the large spatial separation and discontinued continental coastlines (Lesturgie et al, 2023;Ovenden et al, 2009;Walsh et al, 2022).…”

“…Given that both Chagos and Juan de Nova populations were included in previous grey reef shark studies showing strong allelic differentiation from Coral and Paci c Ocean populations (Lesturgie et al, 2023;Momigliano et al, 2017), we aimed to investigate: 1) whether they also show a high level of net divergence compared to within-population diversity characteristic of marine organisms; 2) how long ago they diverged from eastern Indian Ocean and Paci c populations, to understand whether there would be a justi cation for their designation as sub-species and/or as ESUs. Using reduced representation sequences from Indian Ocean and west Paci c grey reef shark populations, we investigated the degree of genetic connectivity, demographic history and projected divergence estimates in the future to understand 89 Carcharhinus amblyrhynchos DArTseq sequences were retrieved from previous studies Momigliano et al, 2017).…”

“…1A). Additionally, we retrieved 35 ddRAD-Seq sequences from Lesturgie et al (2023) from one west Indian Ocean population from Juan de Nova (Juan, n = 13), one Coral Sea population (Bampton, n = 10), and one population from the Central Paci c (Orona, n = 11). Sequences were aligned to the reference genome of the great hammerhead (Sphyrna mokorran, GenBank assembly accession: GCA_024679065.1) the only Carcharhinidae for which a genome assembly is currently available.…”