Abstract
Cosmopolitan marine pelagic species display variable patterns of population connectivity among the world’s major oceans. While this information is crucial for informing management, information is lacking for many ecologically important species, including apex predators. In this study we examine patterns of genetic structure in the broadnose sevengill shark, Notorynchus cepedianus across its global distribution. We estimate patterns of connectivity among broadnose sevengill shark populations from three major oceanic regions (South Atlantic, Oceania and Eastern Pacific) by contrasting mitochondrial and nuclear DNA haplotype frequencies. We also produced time calibrated Bayesian Inference phylogenetic reconstructions to analyses global phylogeographic patterns and estimate divergence times among distinctive shark lineages. Our results demonstrate significant genetic differentiation among oceanic regions (ΦST = 0.9789, P < 0.0001) and a lack of genetic structuring within regions (ΦST = − 0.007; P = 0.479). Time calibrated Bayesian Inference phylogenetic reconstructions indicate that the observed patterns of genetic structure among oceanic regions are historical, with regional populations estimated to have diverged from a common ancestor during the early to mid-Pleistocene. Our results indicate significant genetic structuring and a lack of gene flow among broadnose sevengill shark populations from the South Atlantic, Oceania and Eastern Pacific regions. Evidence of deep lineage divergences coinciding with the early to mid-Pleistocene suggests historical glacial cycling has contributed to the vicariant divergence of broadnose sevengill shark populations from different ocean basins. These finding will help inform global management of broadnose sevengill shark populations, and provides new insights into historical and contemporary evolutionary processes shaping populations of this ecologically important apex predator.
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Data availability
The mtDNA and ITS2 sequence data have been submitted to the GenBank databases under accession number BankIt2397217: MW275497—MW275745 and MW310265—MW310319 respectively.
References
Anderson OF, Bagley NW, Hurst RJ, Francis MP, Clark MR, McMillan PJ (1998) Atlas of New Zealand fish and squid distributions from research bottom trawls. NIWA Technical Report 42.
Avise JC (2000) Phylogeography: The history and formation of species. Harvard University Press, Cambridge
Avise JC, Bowen BW, Ayala FJ (2016) In the light of evolution X: Comparative phylogeography PNAS 113
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mole Biol Evol 16:37–48
Barnett A, Abrantes KG, Stevens JD, Semmens JM (2011) Site fidelity and sex-specific migration in a mobile apex predator: implications for conservation and ecosystem dynamics. Anim Behav 81:1039–1048
Barnett A, Braccini JM, Awruch CA, Ebert DA (2012) An overview on the role of Hexanchiformes in marine ecosystems: biology, ecology and conservation status of a primitive order of modern sharks. J Fish Biol 80:966–990
Barnett A, Stevens JD, Frusher SD, Semmens JM (2010) Seasonal occurrence and population structure of the broadnose sevengill shark Notorynchus cepedianus in coastal habitats of south-east Tasmania. J Fish Biol 77:1688–1701. https://doi.org/10.1111/j.1095-8649.2010.02810.x
Benavides MT et al (2011) Phylogeography of the copper shark (Carcharhinus brachyurus) in the southern hemisphere: implications for the conservation of a coastal apex predator. Marine Freshwater Res 62:861–869
Bermingham E, McCafferty SS, Martin AP (1997) Fish Biogeography and Molecular Clocks: Perspectives from the Panamanian Isthmus. In: Kocher TD, Stepien CA (eds) Molecular Systematics of Fishes. Academic Press, San Diego, pp 113–128.
Bernard AM, Feldheim KA, Heithaus MR, Wintner SP, Wetherbee BM, Shivji MS (2016) Global population genetic dynamics of a highly migratory, apex predator shark. Mole Ecol 25:5312–5329
Bester-van der Merwe AE et al (2017) Population genetics of Southern Hemisphere tope shark (Galeorhinus galeus): Intercontinental divergence and constrained gene flow at different geographical scales. PLoS ONE 12:e0184481. https://doi.org/10.1371/journal.pone.0184481
Bouckaert R et al (2014) BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Comput Biol 10:e1003537
Bowen BW, Clark AM, Abereu-Grobois FA, Chaves A, Reichart HA, Ferl RJ (1998) Global phylogeography of the ridley sea turtles (Lepidochelys spp.) as inferred from mitochondrial DNA sequences. Genetica 101:179–189
Bowen BW et al (2016) Comparative phylogeography of the ocean planet. Proc Natl Acad Sci USA 113:7962–7969. https://doi.org/10.1073/pnas.1602404113
Camargo SM et al (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
Castro ALF et al (2007) Population genetic structure of earth’s largest fish, the whale shark (Rhincodon typus). Mole Ecol 16:5183–5192
Cheng J, Wang Z, Song N, Yanagimoto T, Gao T (2019) Phylogeographic analysis of the genus Platycephalus along the coastline of the northwestern Pacific inferred by mitochondrial DNA. BMC Evol Biol 19:159. https://doi.org/10.1186/s12862-019-1477-1
Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mole Ecol 15:3693–3705. https://doi.org/10.1111/j.1365-294X.2006.03043.x
Clarke CR et al (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
Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mole Ecol 9:1657–1660
Corrigan S, Huveneers C, Stow A, Beheregaray LB, Bradbury I (2016) A multilocus comparative study of dispersal in three codistributed demersal sharks from eastern Australia. Can J Fish Aquat Sci 73:406–415. https://doi.org/10.1139/cjfas-2015-0085
Costello MJ, Tsai P, Wong PS, Cheung AKL, Basher Z, Chaudhary C (2017) Marine biogeographic realms and species endemicity nature. Communications 8:1057. https://doi.org/10.1038/s41467-017-01121-2
da Silva C et al (2015) The current status and management of South Africa’s chondrichthyan fisheries. Afr J Mar Sci 37:233–248
Daly-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
Domingues RR, Hilsdorf AWS, Gadig OBF (2018) 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
Domingues RR, Hilsdorf AWS, Shivji MM, Hazin FVH, Gadig OBF (2017) Effects of the Pleistocene on the mitochondrial population genetic structure and demographic history of the silky shark (Carcharhinus falciformis) in the western Atlantic Ocean. Rev Fish Biol Fisheries. https://doi.org/10.1007/s11160-017-9504-z
Drummond AJ et al. (2008) Geneious v4.0
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biol 7:214
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973
Dudgeon CL, Broderick D, Ovenden JR (2009) IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific. Mol Ecol 18:248–261. https://doi.org/10.1111/j.1365-294X.2008.04025.x
Dulvy NK et al (2014) Extinction risk and conservation of the world’s sharks and rays. eLife. https://doi.org/10.7554/eLife.00590
Duncan KM, Martin AP, Bowen BW, De Couet G (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mole Ecol 15:2239–2251. https://doi.org/10.1111/j.1365-294X.2006.02933.x
Ebert DA (1989) Life history of the sevengill shark, Notorynchus cepedianus Peron, in two northern California bays. California Fish and Game 75:102–112
Ebert DA (1996) Biology of the sevengill shark Notorynchus cepedianus (Peron, 1807) in the temperate coastal waters of southern Africa. South African J Marine Sci 17:93–103. https://doi.org/10.2989/025776196784158545
Ferrari A et al (2018) Natural history and molecular evolution of demersal Mediterranean sharks and skates inferred by comparative phylogeographic and demographic analyses. PeerJ 6:e5560. https://doi.org/10.7717/peerj.5560
Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071
Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Geraghty PT et al (2014) Genetic structure and diversity of two highly vulnerable carcharhinids in Australian waters. Endang Species Res 24:45–60
Giles JL, Riginos C, Naylor GJP, Dharmadi OJR (2016) Genetic and phenotypic diversity in the wedgefish Rhynchobatus australiae, a threatened ray of high value in the shark fin trade. Marine Ecol Prog Series 548:165–180
Harrison S, Hastings A (1996) Genetic and evolutionary consequences of metapopulation structure. Trends Ecol Evol 11:180–183. https://doi.org/10.1016/0169-5347(96)20008-4
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174. https://doi.org/10.1007/BF02101694
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. Canadian J Fisheries Aquatic Sci 53:583–588. https://doi.org/10.1139/f95-245
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210
Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK (2014) Sizing up the ecological role of sharks as predators. Mar Ecol Prog Ser 495:291–298
Holmes BJ, Williams SM, Otway NM, Nielsen EE, Maher SL, Bennett MB, Ovenden JR (2017) Population structure and connectivity of tiger sharks (Galeocerdo cuvier) across the Indo-Pacific Ocean basin. Royal Soc Open Sci 4:170309
Karl SA, Castro ALF, Garla RC (2012) Population genetics of the nurse shark (Ginglymostoma cirratum) in the western. Atlantic Marine Biol 159:489–498. https://doi.org/10.1007/s00227-011-1828-y
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 Conservation. Genetics 12:371–382. https://doi.org/10.1007/s10592-010-0145-1
Keeney DB, Heist EJ (2006) Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal. Mole Ecol 15:3669–3679. https://doi.org/10.1111/j.1365-294X.2006.03036.x
Keeney DB, Heupel M, Hueter RE, Heist EJ (2003) Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the U.S. Atlantic and Gulf of Mexico Marine Biol 143:1039–1046. https://doi.org/10.1007/s00227-003-1166-9
Kenchington E, Heino M, Nielsen EE (2003) Managing marine genetic diversity: time for action? ICES J Mar Sci 60:1172–1176. https://doi.org/10.1016/S1054-3139(03)00136-X
Kraft S, Pérez-Álvarez M, Olavarría C, Poulin E (2020) Global phylogeography and genetic diversity of the long-finned pilot whale Globicephala melas, with new data from the southeastern Pacific. Sci Rep 10:1769. https://doi.org/10.1038/s41598-020-58532-3
Kriwet J, Kiessling W, Klug S (2009) Diversification trajectories and evolutionary life-history traits in early sharks and batoids. Proc Biol Sci 276:945–951. https://doi.org/10.1098/rspb.2008.1441
Kumar R, Kumar V (2018) A review of phylogeography: biotic and abiotic factors. Geol Ecol Landscap. https://doi.org/10.1080/24749508.2018.1452486
Labrado P, Rozas J (2009) DnaSP v5: A software for comprhensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lara-Lizardi F et al. (2020) Shark movements in the Revillagigedo Archipelago and connectivity with the Eastern Tropical Pacific bioRxiv: 2020.2003.2002.972844 doi:https://doi.org/10.1101/2020.03.02.972844
Larson S, Farrer D, Lowry D, Ebert DA (2015) Preliminary Observations of Population Genetics and Relatedness of the Broadnose Sevengill Shark Notorynchus cepedianus, in Two Northeast Pacific Estuaries. PLoS ONE 10:1–11. https://doi.org/10.1371/journal.pone.0129278
Larson SE, Daly-Engel TS, Phillips NM (2017) Chapter Three - Review of Current Conservation Genetic Analyses of Northeast Pacific Sharks. In: Larson SE, Lowry D (eds) Advances in Marine Biology, vol 77. Academic Press, pp 79–110
Lessios HA, Kessing BD, Robertson DR (1998) Massive gene flow across the world’s most potent marine biogeographic barrier. Proc Royal Soc B: Biol Sci 265:583–588. https://doi.org/10.1098/rspb.1998.0334
Lucifora LO, Menni RC, Escalante AH (2005) Reproduction, abundance and feeding habits of the broadnose sevengill shark Notorynchus cepedianus in north Patagonia. Argentina Marine Ecol Prog Series 289:237–244. https://doi.org/10.3354/meps289237
Luiz OJ, Madin JS, Robertson DR, Rocha LA, Wirtz P, Floeter SR (2012) Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes. Proc Royal Soc B: Biol Sci 279:1033–1040. https://doi.org/10.1098/rspb.2011.1525
Maisey JG (2012) What is an ‘elasmobranch’? The impact of palaeontology in understanding elasmobranch phylogeny and evolution. J Fish Biol 80:918–951
McClenachan L, Cooper AB, Carpenter KE, Dulvy NK (2012) Extinction risk and bottlenecks in the conservation of charismatic marine species. Conserv Lett 5:73–80. https://doi.org/10.1111/j.1755-263X.2011.00206.x
Miller AD, Versace VL, Matthews TG, Montgomery S, Bowie KC (2013) Ocean currents influence the genetic structure of an intertidal mollusc in southeastern Australia – implications for predicting the movement of passive dispersers across a marine biogeographic barrier. Ecol Evolut 3:1248–1261. https://doi.org/10.1002/ece3.535
O’Leary SJ et al (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
Palsbøll PJ, Berube M, Allendorf FW (2006) Identification of management units using population genetic data. Trends Ecol Evolut 22:11–16
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. https://doi.org/10.1146/annurev.es.25.110194.002555
Péron F (1807) Voyage de Découvertes aux Terres Australes, exécuté par ordre de sa majesté l’Empereur et Roi, sur les Corvettes la Géographe, la Naturaliste et la Goulette le Casuarina, pendant les années 1800, 1801, 1803 et 1804. Paris Voyage de Découvertes aux Terres Australes 1:1–496
Portnoy DS, McDowell JR, Heist EJ, Musick JA, Graves JE (2010) World phylogeography and male-mediated gene flow in the sandbar shark Carcharhinus plumbeus. Mol Ecol 19:1994–2010. https://doi.org/10.1111/j.1365-294X.2010.04626.x
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evolut 25:1253–1256. https://doi.org/10.1093/molbev/msn083
Quattro JM et al (2006) Genetic evidence of cryptic speciation within hammerhead sharks (Genus Sphyrna). Marine Biol. https://doi.org/10.1007/s00227-005-0151-x
Queiroz N et al (2019) Global spatial risk assessment of sharks under the footprint of fisheries. Nature 572:461–466. https://doi.org/10.1038/s41586-019-1444-4
Ramos-Onsins SE, Rozas J (2002) Statistical Properties of New Neutrality Tests Against Population Growth. Mol Biol Evol 19:2092–2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rus Hoelzel A, Mahmood SS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in basking shark (Cetorhinus maximus). Biol Lett 2:639–642. https://doi.org/10.1098/rsbl.2006.0513
Schmidt JV, Schmidt CL, Ozer F, Ernst RE, Feldheim KA, Ashley MV, Levine M (2009) Low genetic differentiation across three major ocean populations of the Whale shark Rhincodon typus. PLoS ONE 4:4988–4988
Schultz JK, Feldheim KA, Gruber SH, Ashley MV, McGovern TM, Bowen BW (2008) Global phylogeography and seascape genetics of the lemon shark (genus Negaprion). Mole Ecol 17:5336–5348. https://doi.org/10.1111/j.1365-294X.2008.04000.x
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464
Sherman CDH, Hunt A, Ayre DJ (2008) Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biol J Linnean Soc 95:106–116
Shivji MS, Clarke S, Pank M, Natanson LJ, Kohler N, Stanhope M (2002) Genetic identification of pelagic shark body parts for conservation and trade monitoring. Conserv Biol 16:1035–1039
Smith SE, Au DW, Show C (1999) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine Freshwater Res 49:663–678. https://doi.org/10.1071/MF97135
Städele V, Vigilant L (2016) Strategies for determining kinship in wild populations using genetic data. Ecol Evolut 6:6107–6120. https://doi.org/10.1002/ece3.2346
Stehfest KM, Patterson TA, Barnett A, Semmens JM (2014) Intraspecific differences in movement, dive behavior and vertical habitat preferences of a key marine apex predator. Marine Ecol Prog Series 495:249–262. https://doi.org/10.3354/meps10563
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochon- drial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Thompson KF, Patel S, Baker CS, Constantine R, Millar CD (2016) Bucking the trend: genetic analysis reveals high diversity, large population size and low differentiation in a deep ocean cetacean. Heredity 116:277–285. https://doi.org/10.1038/hdy.2015.99
Veríssimo A et al (2017) World without borders-genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca). Ecol Evolut. https://doi.org/10.1002/ece3.2987
Williams GD, Andrews KS, Katz SL, Moser ML, Tolimieri N, Farrer DA, Levin PS (2012) Scale and pattern of broadnose sevengill shark Notorynchus cepedianus movement in estuarine embayments. J Fish Biol 80:1380–1400. https://doi.org/10.1111/j.1095-8649.2011.03179.x
Acknowledgements
We thank P. Scott, Shark Dive NZ, DAFF and the RV Ellen Khuzwayo staff in South Africa for tissue collection. ASR thanks Prof. Jayson Semmens from the University of Tasmania for his PhD supervision and Prof. Gabriele Gerlach for her support and hospitality at the Carl von Ossietzky Universität Oldenburg. We would also like to thank the two anonymous reviewers for their constructive comments, which helped to improve the manuscript.
Funding
Mahmood S. Shivji and Christine C. Bruels were funded by the Save Our Seas Foundation, Guy Harvey Ocean Foundation, and Hai Stiftung/Shark Foundation. Adam Barnett secured funding from Sea World Research and Rescue Foundation Inc., Save Our Seas Foundation, Holsworth Wildlife Fund, Winnifred Violet Scott Trust, and National Geographic.
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AB and MSS conceived the project. CCB conducted lab work while ACJS-R and ADM analysed the data. The first draft of the manuscript was written by ACJS-R with assistance from AB, ADM, CDHS, MSS and CCB. All authors commented on previous versions of the manuscript. SS-R assisted with data analysis and figure presentation. Samples were provided by CS, DAE, CGW, CT, JCM, JME, AI, AJJ, MB, JA-S and CD. All authors read and approved the final manuscript.
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Schmidt-Roach, A.C.J., Bruels, C.C., Barnett, A. et al. Evidence of historical isolation and genetic structuring among broadnose sevengill sharks (Notorynchus cepedianus) from the world’s major oceanic regions. Rev Fish Biol Fisheries 31, 433–447 (2021). https://doi.org/10.1007/s11160-021-09651-1
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DOI: https://doi.org/10.1007/s11160-021-09651-1