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.

Keywords: Carcharhinus amblyrhynchos; Carcharhinus melanopterus; Radseq; demographic history; meta‐population; range expansion.

FIGURE 1

Map of the sampling sites. From west to east, Indian Ocean (IND): Juan (n = 13) and Zelee (n = 6); Chesterfield islands (CHE): Bampton (n = 10) and Avond (n = 5), New Caledonia (NCA): Belep (n = 7) and Poindimie (n = 5); Phoenix islands (PHO): Niku (n = 21), Mckean (n = 7), Orona (n = 11), Kanton (n = 10), Birnie (n = 2), and Enderbury (n = 13); Palmyra (PAL, n = 38); French Polynesia (POL): Moorea (n = 5), Fakarava (n = 17), Faaite (n = 1), Raraka (n = 1), and Nengo (n = 1). Colors represent the region of origin of the sampling sites: Indian Ocean (IND, yellow), Coral Sea (COR, red), and Central Pacific Ocean (CPA, blue).

FIGURE 2

Demographic scenarios investigated in all populations with n ≥ 7 through an approximate Bayesian computation (ABC) framework. N _anc, Ancestral effective population size; T _c , Time of effective population size change (NS only); N _mod, Modern effective population size (NS only); T _col, Colonization time of the array of demes (FIM and SST); D _1‐100: Demes (FIM and SST). Arrows represent the migrants exchanged (Nm) between demes. Details on each scenario are presented in the main text.

FIGURE 3

Correlation map between genetic diversity (θ_π) and least cost (LC) distances when considering Pacific Ocean sampling sites only. Each cell is colored according to the correlation coefficient value computed between θ_π and the LC distance from the putative origin of the range expansion (RE). Black dots represent the sampling sites considered.

FIGURE 4

Variation of the effective population size (Ne) through time and its 75% confidence interval estimated by the stairwayplot for sampling sites of n ≥ 7 in IND (a), COR (b), and CPA (c) regions

FIGURE 5

Individual‐based population structure analyses. Ancestry proportions retrieved using the sNMF algorithm with K = 2 and K = 3 ancestral populations (a) and principal component analysis (b)

FIGURE 6

Population‐based population structure analyses computed with populations of n ≥ 5. Heat map representing the pairwise F _ST values between sampling sites (a) and isolation by distance (IBD) plot considering Pacific sampling sites only (b)