Ancient metapopulations and extreme sex-biased demography revealed by ABC inference and X-Chromosome diversity in Indo-Pacific reef sharks

Abstract

Reconstructing demographic histories in marine species is challenged by extensive geographic distributions, dispersal barriers, high site fidelity, and sex-biased movement. The grey reef shark Carcharhinus amblyrhynchos exemplifies these difficulties: despite limited long-distance dispersal, its Indo-Pacific range spans major oceanographic barriers, leading to competing hypotheses of continuous isolation-by-distance versus hierarchical metapopulation structure. We test these alternatives with a new Approximate Bayesian Computation framework and integrate sex chromosome diversity and differentiation analyses. We find strong support for two ancient, deeply separated Indo-Pacific metapopulations that only recently experienced limited secondary contact. X-chromosome diversity shows extreme reductions relative to autosomes (Q{pi}{approx} 0.18-0.30 in the central/western Indian Ocean and 0.37-0.46 elsewhere), and QFST estimates far below neutral expectations of 0.75. This signature is markedly stronger than in some other carcharhinids and consistent with a reduced effective size of the X chromosome under strong sex-biased dispersal, likely amplified during sequential colonisation events during the last range expansion. Combined evidence of ancient divergence, reduced genetic diversity and extreme depletion of X chromosome diversity supports designating the Western and Central Indian Ocean populations as Evolutionary Significant Units. Our results demonstrate how integrating simulation-based inference with chromosome-specific diversity resolves complex metapopulation histories and reveal how sex-biased dispersal shapes genomic diversity across evolutionary timescales.