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

Abstract

Marine species can manifest complex patterns of genetic structure due to factors including large geographic distribution ranges and dispersal barriers, sparse long-distance dispersal and high site fidelity. Understanding these connectivity patterns is vital to determine effective management units prioritising vulnerable or evolutionarily distinct populations. Here we investigate genetic differentiation and divergence among grey reef sharks (Carcharhinus amblyrhynchos), comparing western and central Indian Ocean populations on the one side, and eastern Indian Ocean and western Pacific populations on the other. Recent reports of very high differentiation of central and western Indian Ocean from eastern Indian and Pacific populations warranted investigation into whether central and western Indian Ocean populations represent cryptic species of Evolutionary Significant Units (ESUs). Using reduced representation data from 124 previously sequenced individuals, we confirm high differentiation across the Indo-West Pacific (FST ≈ 0.4). Through demographic reconstruction, we show considerably lower effective population sizes and genetic diversity in the western and central Indian Ocean and strong isolation: migration rates to the central-west Indian Ocean are on the scale of 1–4 migrants per 10 generations, which, nevertheless, may still be sufficient to allow adaptive connectivity, i.e. the spread of adaptive alleles between populations maintaining species cohesiveness. Current levels of divergence, however, are well within the range of observed within-species divergence for marine organisms. Although simulations revealed that net divergence between ocean basins is unlikely to reach the levels of the “grey zone of speciation”, these highly differentiated Indian Ocean populations fulfil several requirements of ESUs, and will benefit from targeted management approaches considering their low genetic diversity and the alarming population declines of Carcharhinids.