Genome analysis reveals three distinct lineages of the cosmopolitan white shark.

Abstract

The white shark (Carcharodon carcharias) (Linnaeus, 1758), an iconic apex predator occurring in all oceans,^1,2 is classified as Vulnerable globally³-with global abundance having dropped to 63% of 1970s estimates,⁴-and as Critically Endangered in Europe.⁵ Identification of evolutionary significant units and their management are crucial for conservation,⁶ especially as the white shark is facing various but often region-specific anthropogenic threats.^7,8,9,10,11 Assessing connectivity in a cosmopolitan marine species requires worldwide sampling and high-resolution genetic markers.¹² Both are lacking for the white shark, with studies to date typified by numerous but geographically limited sampling, and analyses relying largely on relatively small numbers of nuclear microsatellites,^{13,14,15,16,17,18,19} which can be plagued by various genotyping artefacts and thus require cautious interpretation.²⁰ Sequencing and computational advances are finally allowing genomes^21,22,23 to be leveraged into population studies,^24,25,26,27 with datasets comprising thousands of single-nucleotide polymorphisms (SNPs). Here, combining target gene capture (TGC)²⁸ sequencing (89 individuals, 4,000 SNPs) and whole-genome re-sequencing (17 individuals, 391,000 SNPs) with worldwide sampling across most of the distributional range, we identify three genetically distinct allopatric lineages (North Atlantic, Indo-Pacific, and North Pacific). These diverged 100,000-200,000 years ago during the Penultimate Glaciation, when low sea levels, different ocean currents, and water temperatures produced significant biogeographic barriers. Our results show that without high-resolution genomic analyses of samples representative of a species' range,¹² the true extent of diversity, presence of past and contemporary barriers to gene flow, subsequent speciation, and local evolutionary events will remain enigmatic.