Population expansion and genetic structure in Carcharhinus brevipinna in the southern Indo-Pacific

Abstract

Background: Quantifying genetic diversity and metapopulation structure provides insights into the evolutionary history of a species and helps develop appropriate management strategies. We provide the first assessment of genetic structure in spinner sharks (Carcharhinus brevipinna), a large cosmopolitan carcharhinid, sampled from eastern and northern Australia and South Africa.

Methods and findings: Sequencing of the mitochondrial DNA NADH dehydrogenase subunit 4 gene for 430 individuals revealed 37 haplotypes and moderately high haplotype diversity (h = 0.6770 ±0.025). While two metrics of genetic divergence (ΦST and F ST) revealed somewhat different results, subdivision was detected between South Africa and all Australian locations (pairwise ΦST, range 0.02717-0.03508, p values ≤ 0.0013; pairwise F ST South Africa vs New South Wales = 0.04056, p = 0.0008). Evidence for fine-scale genetic structuring was also detected along Australia's east coast (pairwise ΦST = 0.01328, p < 0.015), and between south-eastern and northern locations (pairwise ΦST = 0.00669, p < 0.04).

Conclusions: The Indian Ocean represents a robust barrier to contemporary gene flow in C. brevipinna between Australia and South Africa. Gene flow also appears restricted along a continuous continental margin in this species, with data tentatively suggesting the delineation of two management units within Australian waters. Further sampling, however, is required for a more robust evaluation of the latter finding. Evidence indicates that all sampled populations were shaped by a substantial demographic expansion event, with the resultant high genetic diversity being cause for optimism when considering conservation of this commercially-targeted species in the southern Indo-Pacific.

Figure 1. Collection locations for tissues included in genetic structure and diversity analyses.

Sample numbers for each putative population are in parentheses. GoC = Gulf of Carpentaria.

Figure 2. Length-frequency distribution of individuals from which tissues were sampled.

Figure 3. Maximum likelihood phylogenetic tree for Carcharhinus brevipinna haplotypes.

Nodal bootstrap support is displayed where ≥ 70%. Scale represents the proportion of polymorphic sites between haplotypes.

Figure 4. Rarefaction exact curves for sample locations.

Figure 5. Carcharhinus brevipinna mitochondrial DNA ND4 haplotype network.

Sizes of circles correspond to the number of individuals displaying each haplotype. Shading indicates the proportion observed from each of the four putative populations. (−) = mutational steps/missing haplotypes.

Figure 6. Likelihood of pairwise result contradicting that of the original analysis.

Likelihoods computed based on 10,000 replicate random re-samples of the NSW population at varying sample sizes. Y-intercept represents original NSW population (n = 208).

Figure 7. Pairwise Φ_st and p value distributions following random re-sampling simulations.

NSW versus QLD and NT pairwise distributions based on 10,000 replicate random re-samples of the NSW population at n = 150, 100 and 60. Grey and black zones on p value distributions represent p ≤ 0.05 and p > 0.05 respectively. Dotted lines denote upper and lower 95% confidence intervals around sample means. Dashed lines indicate pairwise Φ_ST and p values generated by the original analysis.