Abstract
The oceanic whitetip shark, Carcharhinus longimanus, is a Critically Endangered, circumtropical, and highly migratory, pelagic shark. Yet, little information exists on its population genetic dynamics to guide conservation management practice. We present a first worldwide, mitochondrial and nuclear DNA assessment of the population genetic status of this imperiled species based on sequences of the complete mitochondrial control region (n = 173) and partial ND4 gene (n = 172), and genotypes from 12 nuclear microsatellites (n = 164). Statistically significant mitochondrial and nuclear DNA population genetic differentiation was detected across all marker datasets between Western Atlantic and Indo-Pacific oceanic whitetip sharks. Additionally, our data, combined with previously published, partial (701-base pairs) mitochondrial control region sequences from additional locations in the Atlantic and Indian Oceans, confirmed significant matrilineal population structure between the Western and Eastern Atlantic. The combined data also provisionally (i.e., with FST but not ΦST) indicated differentiation between Western North and Central-South Atlantic sharks, pointing to the need for further assessment in this region. Matrilineal differentiation was also detected between Indian and Pacific Ocean sharks via pairwise analyses, albeit with the ND4 gene sequence only (ΦST = 0.051; FST = 0.092). Limited sampling in the Pacific leaves open questions about the connectivity dynamics in this large region. Despite the presence of geographic population genetic structure, the mitochondrial data showed no evidence of across ocean basin phylogeographic lineages. A provisional assessment of mitochondrial and nuclear genetic diversity indicated the oceanic whitetip shark’s status falls in the middle to upper ranges compared to other shark species, potentially lending some optimism for the present adaptability and resiliency of this species if strong conservation measures are effectively implemented.
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Data availability
All mitochondrial data underlying our analyses can be acessed at https://www.ncbi.nlm.nih.gov/ (GenBank Accession Numbers: OR490638-OR490690). Microsatellite genotypes are available from Dryad at https://doi.org/10.5061/dryad.ht76hdrp9.
References
Arévalo E, Davis SK, Sites JW Jr (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst Biol 43:387–418. https://doi.org/10.1093/sysbio/43.3.387
Ashe JL, Feldheim KA, Fields AT, Reyier EA, Brooks EJ, O’Connell MT, Skomal G, Gruber SH, Chapman DD (2015) Local population structure and context-dependent isolation by distance in a large coastal shark. Mar Ecol Prog Ser 520:203–216. https://doi.org/10.3354/meps11069
Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Benavides MT, Horn RL, Feldheim KA, Shivji MS, Clarke SC, Wintner S, Natanson L, Braccini M, Boomer JJ, Gulak SJB, Chapman DD (2011) Global phylogeography of the dusky shark Carcharhinus obscurus: implications for fisheries management and monitoring the shark fin trade. Endang Species Res 14:13–22. https://doi.org/10.3354/esr00337
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bernard AM, Feldheim KA, Heithaus MR, Wintner SP, Wetherbee BM, Shivji MS (2016) Global population genetic dynamics of a highly migratory, apex predator shark. Mol Ecol 25:5312–5329. https://doi.org/10.1111/mec.13845
Bernard AM, Horn RL, Chapman DD, Feldheim KA, Garla RC, Brooks EJ, Gore MA, Shivji MS (2017) Genetic connectivity of a coral reef ecosystem predator: the population genetic structure and evolutionary history of the Caribbean reef shark (Carcharhinus perezi). J Biogeogr 44:2488–2500. https://doi.org/10.1111/jbi.13062
Bernard AM, Richards VP, Stanhope MJ, Shivji MS (2018) Transcriptome-derived microsatellites demonstrate strong genetic differentiation in Pacific white sharks. J Hered 109:771–779. https://doi.org/10.1093/jhered/esy045
Bernard AM, Finnegan KA, Pavinski Bitar P, Stanhope MJ, Shivji MS (2021) Genomic assessment of global population structure in a highly migratory and habitat versatile apex predator, the tiger shark (Galeocerdo cuvier). J Hered 25:5312–5329. https://doi.org/10.1093/jhered/esab046
Bird CE, Karl SA, Smouse PE, Toonen RJ (2011) Detecting and measuring genetic differentiation. In: Koenemann S, Held C, Schubart C (eds) Phylogeography and population genetics in crustacea. CRC Press, Boca Raton, pp 31–55
Bonfil R, Clarke S, Nakano H (2008) The biology and ecology of the oceanic whitetip shark, Carcharhinus longimanus. In: Camhi MD, Pikitch EK, Babcock EA (eds) Sharks of the open ocean: biology, fisheries and conservation. Blackwell Science, Hoboken, pp 128–139
Briggs JC (2005) The marine East Indies: diversity and speciation. J Biogeogr 32:1517–1522. https://doi.org/10.1111/j.1365-2699.2005.01266.x
Buonaccorsi V, McDowell J, Graves J (2001) Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Mol Ecol 10:1179–1196. https://doi.org/10.1046/j.1365-294X.2001.01270.x
Camargo SM, Coelho R, Chapman D, Howey-Jordan L, Brooks EJ, Fernando D, Mendes NJ, Hazin FHV, Oliveira C, Santos MN, Foresti F, Mendonça FF (2016) Structure and genetic variability of the oceanic whitetip shark, Carcharhinus longimanus, determined using mitochondrial DNA. PLoS ONE 11:e0155623. https://doi.org/10.1371/journal.pone.0155623
Cardeñosa D, Shea SK, Zhang H, Fischer GA, Simpfendorfer CA, Chapman DD (2022) Two thirds of species in a global shark fin trade hub are threatened with extinction: conservation potential of international trade regulations for coastal sharks. Conserv Lett 15:e12910. https://doi.org/10.1111/conl.12910
Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 243:621–631. https://doi.org/10.1093/molbev/msl191
Clarke CR, Karl SA, Horn RL, Bernard AM, Lea JS, Hazin FH, Prodöhl PA, Shivji MS (2015) Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis. Mar Biol 162:945–955. https://doi.org/10.1007/s00227-015-2636-6
Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000. https://doi.org/10.1093/genetics/153.4.1989
Corrigan S, Lowther AD, Beheregaray LB, Bruce BD, Cliff G, Duffy CA, Foulis A, Francis MP, Goldsworthy SD, Hyde JR, Jabado RW, Kacev D, Marshall L, Mucientes GR, Naylor GJP, Pepperell JG, Queiroz N, White WT, Wintner SP, Rogers PJ (2018) Population connectivity of the highly migratory shortfin mako (Isurus oxyrinchus Rafinesque 1810) and implications for management in the southern hemisphere. Front Ecol Evol 6:187. https://doi.org/10.3389/fevo.2018.00187
da Silva L, Ferrette B, Coelho R, Peddemors VM, Ovenden JR, Alexandre De Franco B, Oliveira C, Foresti F, Mendonça FF (2021) Global phylogeography of the smooth hammerhead shark: glacial refugia and historical migration patterns. Aquat Conserv Mar Freshw Ecosyst 31:2348–2368. https://doi.org/10.1002/aqc.3629
Daley-Engel TS, Seraphin KD, Holland KN, Coffey JP, Nance HA, Toonen RJ, Bowen BW (2012) Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS ONE 7:e29986. https://doi.org/10.1371/journal.pone.0029986
DeWoody JA, Harder AM, Mathur S, Willoughby JR (2021) The long-standing significance of genetic diversity in conservation. Mol Ecol 30:4147–4154. https://doi.org/10.1111/mec.16051
Domingues RR, Hilsdorf AWS, Shivji MS, Hazin FVH, Gadig OBF (2018a) Effects of the Pleistocene on the mitochondrial population genetic structure and demographic history of the silky shark (Carcharhinus falciformis) in the western Atlantic. Rev Fish Biol Fish 28:213–227. https://doi.org/10.1007/s11160-017-9504-z
Domingues RR, Hilsdorf AWS, Gadig OBF (2018b) The importance of considering genetic diversity in shark and ray conservation policies. Conserv Genet 19:501–525. https://doi.org/10.1007/s10592-017-1038-3
Dulvy NK, Pacoureau N, Rigby CL, Pollom RA, Jabado RW, Ebert DA, Finucci B, Pollock CM, Cheok J, Derrick DH, Herman KB, Sherman CS, WanderWright WJ, Lawson JM, Walls RHL, Carlson JK, Charvet P, Bineesh KK, Fernando D, Ralph GM, Matsushiba JH, Hilton-Taylor C, Fordham SV, Simpfendorfer CA (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Curr Biol 31:4773–4787. https://doi.org/10.1016/j.cub.2021.08.062
Duncan KM, Martin AP, Bowen BW, Couet DE, HG, (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251. https://doi.org/10.1111/j.1365-294X.2006.02933.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 148:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491. https://doi.org/10.1093/genetics/131.2.479
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587. https://doi.org/10.1093/genetics/155.2.945
Ferrette BLdS, Coimbra RTF, Winter S, De Jong MJ, Williams SM, Coelho R, Rosa D, Rotundo MM, Arocha F, Mourato BL, Mendonça FF, Janke A (2023) Seascape genomics and phylogeography of the sailfish (Istiophorus platypterus). Genome Biol Evol. https://doi.org/10.1093/gbe/evad042
Feutry P, Kyne PM, Pillans RD, Chen X, Naylor GJ, Grewe PM (2014) Mitogenomics of the speartooth shark challenges ten years of control region sequencing. BMC Evol Biol 14:232. https://doi.org/10.1186/s12862-014-0232-x
Feutry P, Kyne PM, Pillans RD, Chen X, Marthick JR, Morgan DL, Grewe PM (2015) Whole mitogenome sequencing population structure of the critically endangered sawfish Pristis pristis. Mar Ecol Prog Ser 533:237–244. https://doi.org/10.3354/meps11354
Fluxus Engineering. Phylogenetic network software. https://www.fluxus-engineering.com/
Francis RM (2017) POPHELPER: an R package and web app to analyse and visualize population structure. Mol Ecol Resour 17:27–32. https://doi.org/10.1111/1755-0998.12509
Gibson AK (2022) Genetic diversity and disease: the past, present, and future of an old idea. Evolution 76:20–36. https://doi.org/10.1111/evo.14395
González MT, Sepúlveda FA, Zárate PM, Baeza JA (2020) Regional population genetics and global phylogeography of the endangered highly migratory shark Lamna nasus: implications for fishery management and conservation. Aquat Conserv Mar Freshw Ecosyst 31(3):620–634. https://doi.org/10.1002/aqc.3455
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
Hardenstine RS, He S, Cochran JEM, Braun CD, Cagua EF, Pierce SJ, Prebble CEM, Rohner CA, Saenz-Angudelo P, Sinclair-Taylor TH, Skomal GB, Thorrold SR, Watts AM, Zakroff CJ, Berumen ML (2022) Pieces in a global puzzle: population genetics at two whale shark aggregations in the western Indian Ocean. Ecol Evol 12:e8492. https://doi.org/10.1002/ece3.8492
Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318. https://doi.org/10.1111/j.1558-5646.1999.tb03767.x
Heist EJ, Musick JA, Graves JE (1996) Genetic population structure of the shortfin mako (Isurus oxyrinchus) inferred from restriction fragment length polymorphism analysis of mitochondrial DNA. Can J Fish Aquat Sci 53:583–588. https://doi.org/10.1139/f95-245
Hirschfeld M, Dudgeon C, Sheaves M, Barnett A (2021) Barriers in a sea of elasmobranchs: from fishing for populations to testing hypotheses in population genetics. Glob Ecol Biogeogr 30:2147–2163. https://doi.org/10.1111/geb.13379
Hoelzel RA, Shivji MS, Magnussen JE, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol Lett 2:639–642. https://doi.org/10.1098/rsbl.2006.0513
Howey-Jordan LA, Brooks EJ, Abercrombie DL, Jordan LKB, Brooks A, Williams S, Gospodarczyk E, Chapman DD (2013) Complex movements, philopatry and expanded depth range of a severely threatened pelagic shark, the oceanic whitetip (Carcharhinus longimanus) in the Western North Atlantic. PLoS ONE 8:e56588. https://doi.org/10.1371/journal.pone.0056588
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. https://doi.org/10.1111/j.1755-0998.2009.02591.x
Inoue JG, Miya M, Tsukamoto K, Nishida M (2001) A mitogenomic perspective on the basal teleostean phylogeny: resolving higher-level relationships with longer DNA sequences. Mol Phylogenet Evol 20:275–285. https://doi.org/10.1006/mpev.2001.0970
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x
Kalinowski ST (2005) HP-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. https://doi.org/10.1111/j.1471-8286.2004.00845.x
Kardos M, Armstrong EE, Fitzpatrick SW, Hauser S, Hedrick PW, Miller JM, Tallmon DA, Funk WC (2021) The crucial role of genome-wide genetic variation in conservation. PNAS 118:e2104642118. https://doi.org/10.1073/pnas.2104642118
Karl SA, Castro ALF, Lopez JA, Charvet P, Burgess GH (2011) Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conserv Genet 12:371–382. https://doi.org/10.1007/s10592-010-0145-1
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Klein JD, Bester-van der Merwe AE, Dicken ML, Mmonwa KL, Teske PR (2019) Reproductive philopatry in a coastal shark drives age-related population structure. Mar Biol 166:26. https://doi.org/10.1007/s00227-019-3467-7
Kottillil S, Rao C, Bowen BW, Shanker K (2023) Phylogeography of sharks and rays: a global review based on life history traits and biogeography partitions. PeerJ 11:e15396. https://doi.org/10.7717/peerj.15396
Kraft DW, Conklin EE, Barba EW, Hutchinson M, Toonen RJ, Forsman ZH, Bowen BW (2020) Genomics versus mtDNA for resolving stock structure in the silky shark (Carcharhinus falciformis). PeerJ 8:e10186. https://doi.org/10.7717/peerj.10186
Leigh JW, Bryant D (2015) POPART: Full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Li H, Xiang-Yu J, Dai G, Gu Z, Ming C, Yang Z, Ryder OA, Li W-H, Fu Y-X, Zhang Y-P (2016a) Large numbers of vertebrates began rapid population decline in the late 19th century. PNAS 113:14079–14084. https://doi.org/10.1073/pnas.1616804113
Li W, Dai X, Xu Q, Wu F, Gao C, Zhang Y (2016b) The complete mitochondrial genome sequence of oceanic whitetip shark, Carcharhinus longimanus (Carcharhiniformes: Carcharinidae). Mitochondrial DNA A 27:1775–1776. https://doi.org/10.3109/19401736.2014.963807
Lieber L, Hall G, Hall J, Berrow S, Johnston E, Gubili C, Sarginson J, Francis M, Duffy C, Wintner S, Doherty P, Godley B, Hawkes L, Witt M, Henderson SM, de Sabata E, Shivji M, Dawson D, Sims D, Jones C, Noble L (2020) Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters. Sci Rep 10:1661. https://doi.org/10.1038/s41598-020-58086-4
Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237. https://doi.org/10.1111/j.1523-1739.1998.96388.x
Madigan DJ, Brooks EJ, Bond ME, Gelsleichter J, Howey LA, Abercrombie DL, Brooks A, Chapman DD (2015) Diet shift and site-fidelity of oceanic whitetip sharks Carcharhinus longimanus along the Great Bahama Bank. Mar Ecol Prog Ser 529:185–197. https://doi.org/10.3354/meps11302
McClain MA, Hammerschlag N, Gallagher AJ, Drymon JM, Grubbs RD, Guttridge TL, Smukall MJ, Frazier BS, Daly-Engel TS (2022) Age-dependent dispersal and relatedness in tiger sharks (Galeocerdo cuvier). Front Mar Sci 9:900107. https://doi.org/10.3389/fmars.2022.900107
Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18. https://doi.org/10.1111/j.1755-0998.2010.02927.x
Nikolic N, Devloo-Delva F, Bailleul D, Noskova E, Rougeux C, Delord C, Borsa P, Liautard-Haag C, Hassan M, Marie AD, Feutry P, Grewe P, Davies C, Farley J, Fernando D, Biton-Porsmoguer S, Poisson F, Parker D, Leone A, Aulich J, Lansdell M, Marsac F, Arnaud-Haond S (2023) Stepping up to genome scan allows stock differentiation in the worldwide distributed blue shark Prionace glauca. Mol Ecol 32:1000–1019. https://doi.org/10.1111/mec.16822
O’Leary SJ, Feldheim KA, Fields AT, Natanson LJ, Wintner S, Hussey N, Shivji MS, Chapman DD (2015) Genetic diversity of white sharks, Carcharodon carcharias, in the Northwest Atlantic and Southern Africa. J Hered 106:258–265. https://doi.org/10.1093/jhered/esv001
Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65. https://doi.org/10.1046/j.1365-294X.2004.02008.x
Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. (Doctoral Thesis), University of Dublin, Ireland.
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418. https://doi.org/10.1111/j.1365-294X.2012.05635.x
Pinhal D, Domingues RR, Bruels CC, Ferrette BLS, Gadig OBF, Shivji MS, Martins C (2020) Restricted connectivity and population genetic fragility in a globally endangered Hammerhead shark. Rev Fish Biol Fish 30:501–517. https://doi.org/10.1007/s11160-020-09607-x
Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39. https://doi.org/10.1111/mec.12509
Piry S, Luikart G, Cornuet J-M (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503. https://doi.org/10.1093/jhered/90.4.502
Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539. https://doi.org/10.1093/jhered/esh074
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
R Core Team (2021) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Ramos-Onsins SE, Rozas J (2022) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201. https://doi.org/10.1073/pnas.94.17.9197
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573
Richards VP, Henning M, Witzell W, Shivji MS (2009) Species delineation and evolutionary history of the globally distributed spotted eagle ray (Aetobatus narinari). J Hered 100:273–283. https://doi.org/10.1093/jhered/esp005
Rigby CL, Barreto R, Carlson J, Fernando D, Fordham S, Francis MP, Herman K, Jabado RW, Liu KM, Marshall A, Pacoureau N, Romanov E, Sherley RB, Winker H (2019) Carcharhinus longimanus. The IUCN Red List of Threatened Species 2019: e.T39374A2911619. https://doi.org/10.2305/IUCN.UK.2019-3.RLTS.T39374A2911619.en
Rousset F (2008) Genepop’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Rozas J, Ferrer-Mata A, Sánchez-DelBarrrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP v6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302
Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386
Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602. https://doi.org/10.1111/j.1471-8286.2006.01378.x
Schmidt-Roach ACJ, Bruels CC, Barnett A, Miller AD, Sherman CDH, Ebert DA, Schmidt-Roach S, da Silva C, Wilke CG, Thorburn C, Mangel JC, Ezcurra JM, Irigoyen A, Jaureguizar AJ, Braccini M, Alfaro-Shigueto J, Duffy C, Shivji MS (2021) Evidence of historical isolation and genetic structuring among broadnose seventill sharks (Notorynchus cepedianus) from the world’s major oceanic regions. Rev Fish Biol Fish 30:433–447. https://doi.org/10.1007/s11160-021-09651-1
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234. https://doi.org/10.1038/72708
Sreelekshmi S, Sukumaran S, Kishor TG, Sebastian W, Gopalakrishnan A (2020) Population genetic structure of the oceanic whitetip shark, Carcharhinus longimanus, along the Indian coast. Mar Biodivers 50:78. https://doi.org/10.1007/s12526-020-01104-5
Thia JA (2023) Guidelines for standardizing the application of discriminant analysis of principal components. Mol Ecol Resour 23:523–538. https://doi.org/10.1111/1755-0998.13706
Tolotti MT, Bach P, Hazin F, Travassos P, Dagorn L (2015) Vulnerability of the oceanic whitetip shark to pelagic longline fisheries. PLoS ONE 10:e0141396. https://doi.org/10.1371/journal.pone.0141396
USA Federal Register (2018) Endangered and Threatened Wildlife and Plants: Listing the Oceanic Whitetip Shark as Threatened Under the Endangered Species Act, Vol. 83, No. 20. https://www.govinfo.gov/content/pkg/FR-2018-01-30/pdf/2018-01682.pdf
Veríssimo A, Sampaio I, McDowell JR, Alexandrino P, Mucientes G, Queiroz N, da Silva C, Jones CS, Noble LR (2017) World without borders—genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca). Ecol Evol 7:4768–4781. https://doi.org/10.1002/ece3.2987
Vignaud TM, Maynard JA, Leblois R, Meekan MG, Vázquez-Juárez R, Ramírez-Macías D, Pierce SJ, Rowat D, Berumen ML, Beeravolu C (2014) Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline. Mol Ecol 23:2590–2601. https://doi.org/10.1111/mec.12754
Villesen P (2007) FABOX: an online toolbox for FASTA sequences. Mol Ecol Notes 7:965–968. https://doi.org/10.1111/j.1471-8286.2007.01821.x
Wang J (2017) The computer program structure for assigning individuals to populations: easy to use but easier to misuse. Mol Ecol Resour 17:981–990. https://doi.org/10.1111/1755-0998.12650
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x
Whitney NM, Robbins WD, Schultz JK, Bowen BW, Holland KN (2012) Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage. J Biogeogr 39:1144–1156. https://doi.org/10.1111/j.1365-2699.2011.02660.x
Willoughby JR, Sundaram M, Wijayawardena BK, Kimble SJA, Ji Y, Fernandez NB, Antonides JD, Lamb MC, Marra NJ, DeWoody JA (2015) The reduction of genetic diversity in threatened vertebrates and new recommendations regarding IUCN conservation rankings. Biol Conserv 191:495–503. https://doi.org/10.1016/j.biocon.2015.07.025
Young CN, Carlson JK (2020) The biology and conservation status of the oceanic whitetip shark (Carcharhinus longimanus) and future directions for recovery. Rev Fish Biol Fish 30:293–312. https://doi.org/10.1007/s11160-020-09601-3
Acknowledgements
This work was funded by the Save Our Seas Foundation, Shark Foundation/Hai Stiftung, and Guy Harvey Foundation. We are very grateful to the following for contributing samples for this study: D. Abercrombie, F. Arocha, L. Beerkircher, D. Chapman, S. Clarke, M. Grace, S. Gulak, L. Hale, F. Hazin, E. Heist, V. Lin, D. McCauley, G. Mucientes, J. Vaudo, H.J. Walker, B. Wetherbee, T. White, and C. Wilson. We thank K. Finnegan and R. Horn for contributing to sequencing efforts. Shark samples from the Cayman Islands were exported under CITES Permit 2014/KY/000744 issued by the Ministry of Financial Services, Commerce & Environment, Government of Cayman Islands.
Funding
This study was supported by the Save Our Seas Foundation, Shark Foundation/Hai Stiftung, and Guy Harvey Foundation.
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CLR performed data collection, data analysis and writing the first draft of the manuscript. MSS led project conceptualization and design, supported writing of the initial draft of the manuscript and led manuscript revisions, and secured funding for the project. RSW performed sample collection and supported manuscript revisions. AMB supported project design and conceptualization, data analysis, writing the first draft of the manuscript, and manuscript revisions.
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Ruck, C.L., Shivji, M.S., Jabado, R.W. et al. Cross ocean-basin population genetic dynamics in a pelagic top predator of high conservation concern, the oceanic whitetip shark, Carcharhinus longimanus. Conserv Genet (2024). https://doi.org/10.1007/s10592-023-01596-1
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DOI: https://doi.org/10.1007/s10592-023-01596-1