Genome analysis reveals three distinct lineages of the cosmopolitan white shark

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The white shark (Carcharodon carcharias) (Linnaeus, 1758), an iconic apex predator occurring in all oceans,1Compagno L.J.V. FAO Species Catalogue. Volume 4. Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 1. Hexanchiformes to Lamniformes. Food and Agriculture Organization of the United Nations, Rome1984: 125-249Google Scholar,2Cortés E. Standardized diet compositions and trophic levels of sharks.ICES J. Mar. Sci. 1999; 56: 707-717https://doi.org/10.1006/jmsc.1999.0489Google Scholar is classified as Vulnerable globally3Rigby C.L. Barreto R. Carlson J. Fernando D. Fordham S. Francis M.P. Herman K. Jabado R.W. Liu K.M. Lowe C.G. et al.Carcharodon carcharias. The IUCN Red List of Threatened Species 2019, 2019https://doi.org/10.2305/IUCN.UK.2019-3.RLTS.T3855A2878674.enGoogle Scholar—with global abundance having dropped to 63% of 1970s estimates,4Pacoureau N. Rigby C.L. Kyne P.M. Sherley R.B. Winker H. Carlson J.K. Fordham S.V. Barreto R. Fernando D. Francis M. et al.Half a century of global decline in oceanic sharks and rays.Nature. 2021; 589: 567-571https://doi.org/10.1038/s41586-020-03173-9Google Scholar—and as Critically Endangered in Europe.5Soldo A. Bradai M.N. Walls R.H.L. Carcharodon carcharias. The IUCN red list of threatened species, 2016Google Scholar Identification of evolutionary significant units and their management are crucial for conservation,6Palsbøll P.J. Bérubé M. Allendorf F.W. Identification of management units using population genetic data.Trends Ecol. Evol. 2007; 22: 11-16https://doi.org/10.1016/j.tree.2006.09.003Google Scholar especially as the white shark is facing various but often region-specific anthropogenic threats.7Ferretti F. Myers R.A. Serena F. Lotze H.K. Loss of large predatory sharks from the Mediterranean Sea.Conserv. Biol. 2008; 22: 952-964https://doi.org/10.1111/j.1523-1739.2008.00938.xGoogle Scholar,8Towner A.V. Watson R.G.A. Kock A.A. Papastamatiou Y. Sturup M. Gennari E. Baker K. Booth T. Dicken M. Chivell W. et al.Fear at the top: killer whale predation drives white shark absence at South Africa’s largest aggregation site.Afr. J. Mar. Sci. 2022; 44: 139-152https://doi.org/10.2989/1814232X.2022.2066723Google Scholar,9Towner A.V. Kock A.A. Stopforth C. Hurwitz D. Elwen S.H. Direct Observation of Killer Whales Preying on White Sharks and Evidence of a Flight Response.Ecology. 2023; 104e3875https://doi.org/10.1002/ecy.3875Google Scholar,10Jorgensen S.J. Anderson S. Ferretti F. Tietz J.R. Chapple T. Kanive P. Bradley R.W. Moxley J.H. Block B.A. Killer whales redistribute white shark foraging pressure on seals.Sci. Rep. 2019; 9: 6153https://doi.org/10.1038/s41598-019-39356-2Google Scholar,11Davenport D. Butcher P. Andreotti S. Matthee C. Jones A. Ovenden J. Effective number of white shark (Carcharodon carcharias, Linnaeus) breeders is stable over four successive years in the population adjacent to eastern Australia and New Zealand.Ecol. Evol. 2021; 11: 186-198https://doi.org/10.1002/ece3.7007Google Scholar Assessing connectivity in a cosmopolitan marine species requires worldwide sampling and high-resolution genetic markers.12Choo L.Q. Spagliardi G. Malinsky M. Choquet M. Goetze E. Hoarau G. Peijnenburg K.T.C.A. Genome-wide phylogeography reveals cryptic speciation in the circumglobal planktonic calcifier Limacina bulimoides.Mol. Ecol. 2023; 32: 3200-3219https://doi.org/10.1111/mec.16931Google Scholar 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,13O’Leary S.J. Feldheim K.A. Fields A.T. Natanson L.J. Wintner S. Hussey N. Shivji M.S. Chapman D.D. Genetic diversity of white sharks, Carcharodon carcharias, in the Northwest Atlantic and Southern Africa.J. Hered. 2015; 106: 258-265https://doi.org/10.1093/jhered/esv001Google Scholar,14Bernard A.M. Richards V.P. Stanhope M.J. Shivji M.S. Transcriptome-derived microsatellites demonstrate strong genetic differentiation in pacific white sharks.J. Hered. 2018; 109: 771-779https://doi.org/10.1093/jhered/esy045Google Scholar,15Blower D.C. Pandolfi J.M. Bruce B.D. Gomez-Cabrera M.D.C. Ovenden J.R. Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes.Mar. Ecol. Prog. Ser. 2012; 455: 229-244https://doi.org/10.3354/meps09659Google Scholar,16Andreotti S. Von Der Heyden S. Henriques R. Rutzen M. Meÿer M. Oosthuizen H. Matthee C.A. New insights into the evolutionary history of white sharks, Carcharodon carcharias.J. Biogeogr. 2016; 43: 328-339https://doi.org/10.1111/jbi.12641Google Scholar,17Andreotti S. Rutzen M. Van Der Walt S. Von Der Heyden S. Henriques R. Meyer M. Oosthuizen C. Matthee C.A. An integrated mark-recapture and genetic approach to estimate the population size of white sharks in South Africa.Mar. Ecol. Prog. Ser. 2016; 552: 241-253https://doi.org/10.3354/meps11744Google Scholar,18Pardini A.T. Jones C.S. Noble L.R. Kreiser B. Malcolm H. Bruce B.D. Stevens J. Cliff G. Scholl M.C. Francis M. et al.Sex-biased dispersal of great white sharks.Nature. 2001; 412: 139-140https://doi.org/10.1038/35084125Google Scholar,19Saavedra-Sotelo N.C. Mendivil-Castro P. Oñate-González E.C. Nuclear genetic structure of the white shark (Carcharodon carcharias) from the Northeastern Pacific.Lat. Am. J.Aquat. Res. 2023; 51: 388-403https://doi.org/10.3856/vol51-issue3-fulltext-2984Google Scholar which can be plagued by various genotyping artefacts and thus require cautious interpretation.20Choquet M. Lizano A.M. Le Moan A. Ravinet M. Dhanasiri A.K. Hoarau G. Unmasking microsatellite deceptiveness and debunking hybridization with SNPs in four marine copepod species of Calanus.Mol. Ecol. 2023; 32: 6854-6873https://doi.org/10.1111/mec.17183Google Scholar Sequencing and computational advances are finally allowing genomes21Johri S. Doane M.P. Allen L. Dinsdale E.A. Taking advantage of the genomics revolution for monitoring and conservation of chondrichthyan populations.Diversity. 2019; 11: 49https://doi.org/10.3390/d11040049Google Scholar,22Pearce J. Fraser M.W. Sequeira A.M.M. Kaur P. State of Shark and Ray Genomics in an Era of Extinction.Front. Mar. Sci. 2021; 8744986https://doi.org/10.3389/fmars.2021.744986Google Scholar,23Marra N.J. Stanhope M.J. Jue N.K. Wang M. Sun Q. Bitar P.P. Richards V.P. Komissarov A. Rayko M. Kliver S. et al.White shark genome reveals ancient elasmobranch adaptations associated with wound healing and the maintenance of genome stability.P. Natl.Acad. Sci. USA. 2019; 116: 4446-4455https://doi.org/10.1073/pnas.1819778116Google Scholar to be leveraged into population studies,24Devloo-Delva F. Burridge C.P. Kyne P.M. Brunnschweiler J.M. Chapman D.D. Charvet P. Chen X. Cliff G. Daly R. Drymon J.M. et al.From rivers to ocean basins: The role of ocean barriers and philopatry in the genetic structuring of a cosmopolitan coastal predator.Ecol. Evol. 2023; 13e9837https://doi.org/10.1002/ece3.9837Google Scholar,25Bernard A.M. Finnegan K.A. Pavinski Bitar A. Stanhope M.J. Shivji M.S. Genomic assessment of global population structure in a highly migratory and habitat versatile apex predator, the tiger shark (Galeocerdo cuvier).J. Hered. 2021; 112: 497-507https://doi.org/10.1093/jhered/esab046Google Scholar,26Nikolic N. Devloo-Delva F. Bailleul D. Noskova E. Rougeux C. Delord C. Borsa P. Liautard-Haag C. Hassan M. Marie A.D. et al.Stepping up to genome scan allows stock differentiation in the worldwide distributed blue shark Prionace glauca.Mol. Ecol. 2023; 32: 1000-1019https://doi.org/10.1111/mec.16822Google Scholar,27Domingues R.R. Mastrochirico-Filho V.A. Mendes N.J. Hashimoto D.T. Coelho R. Antunes A. Foresti F. Mendonça F.F. Gene-associated markers as a genomic and transcriptomic resource for a highly migratory and apex predator shark (Isurus oxyrinchus).Mar. Biol. 2022; 169109https://doi.org/10.1007/s00227-022-04094-zGoogle Scholar with datasets comprising thousands of single-nucleotide polymorphisms (SNPs). Here, combining target gene capture (TGC)28Wagner C.I. Choquet M. Smolina I. Jones C.S. Noble L.R. Hoarau G. Genome-wide target capture baits for endangered shark species.Authorea. 2023; https://doi.org/10.22541/au.169812932.23834906/v1Google Scholar 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,12Choo L.Q. Spagliardi G. Malinsky M. Choquet M. Goetze E. Hoarau G. Peijnenburg K.T.C.A. Genome-wide phylogeography reveals cryptic speciation in the circumglobal planktonic calcifier Limacina bulimoides.Mol. Ecol. 2023; 32: 3200-3219https://doi.org/10.1111/mec.16931Google Scholar the true extent of diversity, presence of past and contemporary barriers to gene flow, subsequent speciation, and local evolutionary events will remain enigmatic.