We investigated the evolutionary history of the grey reef shark (Carcharhinus amblyrhynchos) in the Indo-Pacific (IP) by harnessing the power of thousands of RAD-seq loci sequenced in 175 individuals across its range. We bring strong evidences of the occurrence of a range expansion (RE) originating close to the Indo-Australian Archipelago (IAA) from which two stepping-stone waves (east and westward) started, colonizing almost the entire IP. Consequently, the demographic history of C. amblyrhynchos is best explained by a meta-population model, for which we estimated a homogenous connectivity throughout its range (Nm~10 per generation) by means of coalescent modeling coupled with an Approximate Bayesian Computation framework. An isolation by distance model further highlights the absence of either genetic barriers or preferential migration corridors, despite the dependency of C. amblyrhynchos from coral reefs occurrence. This is consistent with the long-distance swims observed, suggesting that the strong genetic structure at the IP scale (FST~0.56 between its ends) is rather the consequence of its large current distribution. We contrasted these results with those previously obtained for the sympatric but strictly lagoon-associated Carcharhinus melanopterus, a species well known for its restricted dispersal ability. While C. melanopterus exhibits a similar RE dynamic, it is characterized by stronger genetic structure and a non-homogeneous connectivity largely dependent on local coral reefs availability. The comparison between the two species sheds new light on shark evolution, emphasizing the role of IAA as source of biodiversity and of dispersal ability in shaping the extent of population structure and genetic diversity.

Dispersal abilities play a crucial role in shaping the extent of population genetic structure, with more mobile species being panmictic over large geographic ranges and less mobile ones organized in meta-populations exchanging migrants to different degrees. In turn, population structure directly influences the coalescent pattern of the sampled lineages, but the consequences on the estimated variation of the effective population size (Ne) over time obtained by means of unstructured demographic models remain poorly understood. However, this knowledge is crucial for biologically interpreting the observed Ne trajectory and further devising conservation strategies in endangered species. Here we investigated the demographic history of four shark species (Carharhinus melanopterus, Carharhinus limbatus, Carharhinus amblyrhynchos, Galeocerdo cuvier) with different degrees of endangered status and life history traits related to dispersal distributed in the Indo-Pacific and sampled off New Caledonia. We compared several evolutionary scenarios representing both structured (meta-population) and unstructured models and then inferred the Ne variation through time. By performing extensive coalescent simulations, we provided a general framework relating the underlying population structure and the observed Ne dynamics. On this basis, we concluded that the recent decline observed in three out of the four considered species when assuming unstructured demographic models can be explained by the presence of population structure. Furthermore, we also demonstrated the limits of the inferences based on the sole site frequency spectrum and warn that statistics based on linkage disequilibrium will be needed to exclude recent demographic events affecting meta-populations.

The reproductive systems of natural populations can greatly impact their genetic diversity by preventing or encouraging inbreeding. It is therefore crucial to have a comprehensive understanding of the mating system to evaluate a population's ability to maintain genetic diversity over time. In this study, we examine the mating system of an endangered population of green sea turtles in Tetiaroa, French Polynesia. We determine if different mating behaviours serve as strategies to avoid inbreeding. We genotyped 107 nesting females and 1483 hatchlings from 549 nests and used 23 microsatellite markers to reconstruct the genotypes of the fathers. We assessed the level of inbreeding and relatedness of the parent pairs and explored the correlation between relatedness and fitness parameters in the offspring. We determined the mating behaviours of both males and females and investigated if specific behaviours were linked to different levels of relatedness. Our results showed that 27 fathers and 31 mothers were responsible for the genotypes of 445 hatchlings from 105 nests. Global Fis was significant, and levels of relatedness were higher than expected through random mating, indicating inbreeding and non-random partner selection. However, we did not find any mating behaviours that were associated with lower relatedness levels than the general population, suggesting that they are not part of an inbreeding avoidance strategy. Ultimately, this study illuminates the reproductive system of green turtles and shows that this population is susceptible to inbreeding. Additionally, our research demonstrates the effectiveness of parentage analysis in understanding the reproductive behaviour of elusive species.

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 grey reef shark (Carcharhinus amblyrhynchos) across its range by sequencing thousands of RAD-seq 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 an 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 (FST ~ 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 grey 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. C. melanopterus exhibits similar RE dynamic, but is characterized by stronger genetic structure and a non-homogeneous 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.

Dispersal abilities play a crucial role in shaping the extent of population genetic structure, with more mobile species being panmictic over large geographic ranges and less mobile ones organized in meta-populations exchanging migrants to different degrees. In turn, population structure directly influences the coalescence pattern of the sampled lineages, but the consequences on the estimated variation of the effective population size (Ne) over time obtained by means of unstructured demographic models remain poorly understood. However, this knowledge is crucial for biologically interpreting the observed Ne trajectory and further devising conservation strategies in endangered species. Here we investigated the demographic history of four shark species (Carharhinus melanopterus, Carharhinus limbatus, Carharhinus amblyrhynchos, Galeocerdo cuvier) with different degrees of endangered status and life history traits related to dispersal distributed in the Indo-Pacific and sampled off New Caledonia. We compared several evolutionary scenarios representing both structured (meta-population) and unstructured models and then inferred the Ne variation through time. By performing extensive coalescent simulations, we provided a general framework relating the underlying population structure and the observed Ne dynamics. On this basis, we concluded that the recent decline observed in three out of the four considered species when assuming unstructured demographic models can be explained by the presence of population structure. Furthermore, we also demonstrated the limits of the inferences based on the sole site frequency spectrum and warn that statistics based on linkage disequilibrium will be needed to exclude recent demographic events affecting meta-populations.