Abstract
Many shark species are at risk of overexploitation due to their high economic value, slow maturation, and low recruitment compared to most teleosts. However, there is insufficient knowledge about population structure at different spatial scales necessary to optimise fisheries models. We used single-nucleotide polymorphisms (SNPs) obtained through complexity-reduction genome sequencing to quantify the population structure of two highly mobile and commercially fished shark species: bronze whalers (Carcharhinus brachyurus) and dusky sharks (C. obscurus). We applied a comprehensive approach to test several population-structure hypotheses and signal consistency across methods and marker type. We found that C. obscurus was panmictic across Australia and Indonesia and across the Indian Ocean to South Africa based on neutral loci, whereas for C. brachyurus, the westernmost Australian samples appeared to be separate from the rest. The southernmost east Australian samples indicated some difference from the rest of Australia and New Zealand based on candidate loci for C. brachyurus, and potentially also C. obscurus; however, the lack of a reference genome makes the interpretation difficult. Despite similar patterns in both species, subtle and potentially important structure differences emphasise the importance of studying each target species independently rather than assuming similar patterns from closely related species with similar dispersal abilities, as well as considering different marker types in future studies. We found evidence of connectivity across the regions sampled, suggesting that the cumulative effects of regional fisheries and the potential for cross-jurisdictional fishery assessments and management should be considered for Australian, Indonesian, and New Zealand populations.
Similar content being viewed by others
References
Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323
Ashe JL, Feldheim KA, Fields AT, Reyier EA, Brooks EJ, O’Connell MT, Skomal G, Gruber SH, Chapman CC (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
Bailleul D, Mackenzie A, Sacchi O, Poisson F, Bierne N, Arnaud-Haond S (2018) Large-scale genetic panmixia in the blue shark (Prionace glauca): a single worldwide population, or a genetic lag-time effect of the “grey zone” of differentiation? Evol Appl 11:614–630
Barbosa SS, Klanten SO, Puritz JB, Toonen RJ, Byrne M (2013) Very fine-scale population genetic structure of sympatric asterinid sea stars with benthic and pelagic larvae: influence of mating system and dispersal potential. Biol J Linn Soc 108:821–833. https://doi.org/10.1111/bij.12006
Barnes TC, Junge C, Myers SA, Taylor MD, Rogers PJ, Ferguson GJ, Lieschke JA, Donnellan SC, Gillanders BM (2015) Population structure in a wide-ranging coastal teleost (Argyrosomus japonicus, Sciaenidae) reflects marine biogeography across southern Australia. Mar Freshw Res 67:8. https://doi.org/10.1071/MF15044
Benavides MT, Feldheim KA, Duffy CA, Wintner S, Braccini M, Boomer J, Huveneers C, Rogers P, Mangel JC, Alfaro-Shigueto J, Cartamil DP, Chapman DD (2011a) Phylogeography of the copper shark (Carcharhinus brachyurus) in the southern hemisphere: implications for the conservation of a coastal apex predator. Mar Freshw Res 62:861–869. https://doi.org/10.1071/mf10236
Benavides MT, Horn RL, Feldheim KA, Shivji MS, Clarke SC, Wintner S, Natanson L, Braccini M, Boomer JJ, Gulak SJB, Chapman DD (2011b) Global phylogeography of the dusky shark Carcharhinus obscurus: implications for fisheries management and monitoring the shark fin trade. Endanger Species Res 14:13–22. https://doi.org/10.3354/esr00337
Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R, Bernatchez L (2015) RAD-genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species; the American lobster (Homarus americanus). Mol Ecol 24:3299–3315. https://doi.org/10.1111/mec.13245
Blaber SJM, Dichmont CM, White W, Buckworth R, Sadiyah L, Iskandar B, Nurhakim S, Pillans R, Andamari R, Dharmadi Fahmi (2009) Elasmobranchs in southern Indonesian fisheries: the fisheries, the status of the stocks and management options. Rev Fish Biol Fisher 19:367–391
Bonfil R, Meyer M, Scholl MC, Johnson R, O’Brien S, Oosthuizen H, Swanson S, Kotze D, Paterson M (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310:100–103. https://doi.org/10.1126/science.1114898
Braccini M, Johnson G, Rogers P, Hansen S, Peddemors V (2016) Dusky Whaler (Carcharhinus obscurus). In: Stewardson C, Andrews J, Ashby C, Haddon M, Hartmann K, Hone P, Horvat P, Mayfield S, Roelofs A, Sainsbury K, Saunders T, Stewart J, Stobutzki I, Wise B (eds) 2016, Status of Australian fish stocks reports 2016. FRDC, Canberra
Bradshaw CJA, Field IC, McMahon CR, Johnson GJ, Meekan MG, Buckworth RC (2013) More analytical bite in estimating targets for shark harvest. Mar Ecol Prog Ser 488:221–232. https://doi.org/10.3354/meps10375
Bradshaw CJA, Prowse TAA, Drew M, Gillanders BM, Donnellan SC, Huveneers C (2018) Predicting sustainable shark harvests when stock assessments are lacking. ICES J Mar Sci 75:1591–1601. https://doi.org/10.1093/icesjms/fsy031
Case RAJ, Hutchinson WF, Hauser L, Van Oosterhout C, Carvalho GR (2005) Macro- and micro-geographic variation in pantophysin (PanI) allele frequencies in NE Atlantic cod Gadus morhua. Mar Ecol Prog Ser 301:267–278. https://doi.org/10.3354/meps301267
Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annu Rev Mar Sci 7:547–570. https://doi.org/10.1146/annurev-marine-010814-015730
Cliff G, Dudley SFJ (1992) Sharks caught in the protective gill nets off Natal, South Africa. 6. The copper shark Carcharhinus brachyurus (Günther). S Afr J Marine Sci 12:663–674. https://doi.org/10.2989/02577619209504731
Cruz VMV, Kilian A, Dierig DA (2013) Development of DArT marker platforms and genetic diversity assessment of the US collection of the new oilseed crop Lesquerella and related species. PLoS One 8:e64062. https://doi.org/10.1371/journal.pone.0064062
Deschamps S, Llaca V, May GD (2012) Genotyping-by-sequencing in plants. Biology 1:460–483
Dichmont CM, Ovenden JR, Berry O, Welch DJ, Buckworth RC (2012) Scoping current and future genetic tools, their limitations and their applications for wild fisheries management. CSIRO, Brisbane, p 129
Donnellan SC, Foster R, Junge C, Huveneers C, Rogers P, Kilian A, Bertozzi T (2015) Fiddling with the proof: the magpie fiddler ray is a colour pattern variant of the common southern fiddler ray (Rhinobatidae: Trygonorrhina). Zootaxa 3981:367–384
Drew M, Rogers P, Huveneers C (2017) Slow life-history traits of a neritic predator, the bronze whaler (Carcharhinus brachyurus). Mar Freshw Res 68:461–472
Dudgeon CL, Blower DC, Broderick D, Giles JL, Holmes BJ, Kashiwagi T, Krück NC, Morgan AT, Tillett BJ, Ovenden JR (2012) A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. J Fish Biol 80:1789–1843. https://doi.org/10.1111/j.1095-8649.2012.03265.x
Dudley SFJ, Cliff G, Zungu MP, Smale MJ (2005) Sharks caught in the protective gill nets off KwaZulu-Natal, South Africa. 10. The dusky shark Carcharhinus obscurus (Lesueur 1818). Afr J Mar Sci 27:107–127. https://doi.org/10.2989/18142320509504072
Duffy C, Gordon I (2003a) Carcharhinus brachyurus (SSG Australia & Oceania Regional Workshop, March 2003). The IUCN Red List of Threatened Species version 20143 online: http://iucnredlist.org/
Duffy C, Gordon I (2003b) Carcharhinus brachyurus. In: Cavanagh Rachel D, Kyne PM, Fowler SL, Musick JA, Bennett MB (ed) The conservation status of Australian chondrichthyans: report of the IUCN Shark Specialist Group Australia and Oceania Regional Red List Workshop. The University of Queensland, School of Biomedical Sciences, Brisbane, Australia, vol x + 170, pp 106–109
Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LNK, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LJV, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti S, White WT (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590
Dulvy NK, Simpfendorfer CA, Davidson LNK, Fordham SV, Bräutigam A, Sant G, Welch DJ (2017) Challenges and priorities in shark and ray conservation. Curr Biol 27:R565–R572
Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
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
Field IC, Meekan MG, Buckworth RC, Bradshaw CJ (2009) Susceptibility of sharks, rays and chimaeras to global extinction. Adv Mar Biol 56:275–363
Flood MSI, Andrews J, Ashby C, Begg G, Fletcher R, Gardner C, Georgeson L, Hansen S, Hartmann K, Hone P, Horvat P, Maloney L, McDonald B, Moore A, Roelofs A, Sainsbury K, Saunders T, Smith T, Stewardson C, Stewart J, Wise B (eds) (2014) Status of key Australian fish stocks reports 2014. FRDC, Canberra
Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993. https://doi.org/10.1534/genetics.108.092221
Frisk MG, Miller TJ, Dulvy NK (2005) Life histories and vulnerability to exploitation of elasmobranchs: inferences from elasticity, perturbation and phylogenetic analyses. J Northwest Atl Fish Sci 35:27–45
Gaggiotti OE, Bekkevold D, Jørgensen HBH, Foll M, Carvalho GR, Andre C, Ruzzante DE (2009) Disentangling the effects of evolutionary, demographic, and environmental factors influeing genetic structure of natural populations: Atlantic herring as a case study. Evolution 63:2939–2951. https://doi.org/10.1111/j.1558-5646.2009.00779.x
Geraghty PT, Macbeth WG, Harry AV, Bell JE, Yerman MN, Williamson JE (2013) Age and growth parameters for three heavily exploited shark species off temperate eastern Australia. ICES J Mar Sci 71:559–573. https://doi.org/10.1093/icesjms/fst164
Geraghty PT, Williamson JE, Macbeth WG, Blower DC, Morgan JAT, Johnson G, Ovenden JR, Gillings MR (2014) Genetic structure and diversity of two highly vulnerable carcharhinids in Australian waters. Endanger Species Res 24:45–60. https://doi.org/10.3354/esr00580
Geraghty P, Macbeth W, Williamson J (2015) Aspects of the reproductive biology of dusky, spinner and sandbar sharks (Family Carcharhinidae) from the Tasman Sea. Mar Freshw Res 67:513–525
Gore MA, Rowat D, Hall J, Gell FR, Ormond RF (2008) Transatlantic migration and deep mid-ocean diving by basking shark. Biol Lett 4:395–398
Guo BC, DeFaveri J, Sotelo G, Nair A, Merilä J (2015) Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks. BMC Biol 13:19. https://doi.org/10.1186/s12915-015-0130-8
Hastings A (1993) Complex interactions between dispersal and dynamics: lessons from coupled logistic equations. Ecology 74:1362–1372
Hemmer-Hansen J, Therkildsen NO, Meldrup D, Nielsen EE (2014) Conserving marine biodiversity: insights from life-history trait candidate genes in Atlantic cod (Gadus morhua). Conserv Genet 15:213–228. https://doi.org/10.1007/s10592-013-0532-5
Hess JE, Campbell NR, Close DA, Docker MF, Narum SR (2013) Population genomics of Pacific lamprey: adaptive variation in a highly dispersive species. Mol Ecol 22:2898–2916. https://doi.org/10.1111/mec.12150
Hoenner X, Huveneers C, Steckenreuter A, Simpfendorfer C, Tattersall K, Jaine F, Atkins N, Babcock R, Brodie S, Burgess J (2018) Australia’s continental-scale acoustic tracking database and its automated quality control process. Sci Data 5:170206
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
Hussey NE, McCarthy ID, Dudley SF, Mann BQ (2009) Nursery grounds, movement patterns and growth rates of dusky sharks, Carcharhinus obscurus: a long-term tag and release study in South African waters. Mar Fresh Res 60:571–583
Huveneers C, Rogers PJ, Drew M (2014) Monitoring shark species of conservation concern within the Adelaide metropolitan and Gulf St Vincent regions. Final report to the Adelaide and Mount Lofty ranges natural resources management board. SARDI research report series No. 754, SARDI Aquatic Sciences, Adelaide, Australia
Izzo C, Huveneers C, Drew M, Bradshaw CJ, Donnellan SC, Gillanders BM (2016) Vertebral chemistry demonstrates movement and population structure of bronze whaler. Mar Ecol Prog Ser 556:195–207
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 Genetics 11:94. https://doi.org/10.1186/1471-2156-11-94
Jones GK (2008) Review of the fishery status for whaler sharks (Carcharhinus spp.) in South Australian and adjacent waters. FRDC Project 2004/067. SARDI Aquatic Sciences
Junge C, Vøllestad LA, Barson NJ, Haugen TO, Otero J, Sætre G-P, Primmer CR (2011) Strong gene flow and lack of stable population structure in the face of rapid adaptation to local temperature in a spring-spawning salmonid, the European grayling (Thymallus thymallus). Heredity 106:460–471. https://doi.org/10.1038/hdy.2010.160
Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, Caig V, Heller-Uszynska K, Jaccoud D, Hopper C, Aschenbrenner-Kilian M, Evers M, Peng K, Cayla C, Hok P, Uszynski G (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. In: Pompanon F, Bonin A (eds) Data production and analysis in population genomics, vol 888. Methods in Molecular Biology. Humana Press, New York, pp 67–89. https://doi.org/10.1007/978-1-61779-870-2_5
Kohler NE, Casey JG, Turner PA (1998) NMFS cooperative shark tagging program, 1962-93: an atlas of shark tag and recapture data. Mar Fish Rev 60:1–87
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Krück NC, Innes DI, Ovenden JR (2013) New SNPs for population genetic analysis reveal possible cryptic speciation of eastern Australian sea mullet (Mugil cephalus). Mol Ecol Resour 13:715–725. https://doi.org/10.1111/1755-0998.12112
Lamichhaney S, Martinez Barrio A, Rafati N, Sundström G, Rubin C-J, Gilbert ER, Berglund J, Wetterbom A, Laikre L, Webster MT, Grabherr M, Ryman N, Andersson L (2012) Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proc Natl Acad Sci USA 109:19345–19350. https://doi.org/10.1073/pnas.1216128109
Lea JSE, Wetherbee BM, Queiroz N, Brunie N, Aming C, Sousa LL, Muceintes GR, Humphries NE, Harvey GM, Sims DW, Shivji MS (2015) Repeated, long-distance migrations by a philopatric predator targeting highly contrasting ecosystems. Sci Rep 5:11202. https://doi.org/10.1038/srep11202
Leigh DM, Lischer HEL, Grossen C, Keller LF (2018) Batch effects in a multiyear sequencing study: false biological trends due to changes in read lengths. Mol Eco Resour 18(4):778–788
Limborg MT et al (2012) Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol Ecol 21:3686–3703. https://doi.org/10.1111/j.1365-294X.2012.05639.x
Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994
Macbeth WG, Geraghty PT, Peddemors VM, Gray CA (2009) Observer-based study of targeted commercial fishing for large shark species in waters off northern New South Wales. Industry & Investment NSW—Fisheries Final Report Series 114
McAuley RB, Simpfendorfer CA, Hall NG (2007) A method for evaluating the impacts of fishing mortality and stochastic influences on the demography of two long-lived shark stocks. ICES J Mar Sci 64:1710–1722. https://doi.org/10.1093/icesjms/fsm146
Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231. https://doi.org/10.1111/mec.13243
Meirmans PG, Van Tienderen PH (2004) Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Milano I, Babbucci M, Cariani A, Atanassova M, Bekkevold D, Carvalho GR, Espiñeira M, Florentino F, Garofalo G, Geffen AJ, Hansen JH, Helyar SJ, Nielsen EE, Ogden R, Patarnello T, Stagioni M, FishPopTrace Consortium, Tinti F, Bargelloni L (2014) Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Mol Ecol 23:118–135
Miller MR, Dunham JP, Amores A, Cresko WA, Johnson EA (2007) Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res 17:240–248. https://doi.org/10.1101/gr.5681207
Moore J-S, Bourret V, Dionne M, Bradbury I, O’Reilly P, Kent M, Chaput G, Bernatchez L (2014) Conservation genomics of anadromous Atlantic salmon across its North American range: outlier loci identify the same patterns of population structure as neutral loci. Mol Ecol 23:5680–5697. https://doi.org/10.1111/mec.12972
Musick JA, Grubbs RD, Baum J, Cortés E (2009) Carcharhinus obscurus. The IUCN red list of threatened species 2009:e.T3852A10127245. https://doi.org/10.2305/IUCN.UK.2009-2.RLTS.T3852A10127245.en
Narum SR, Hess JE (2011) Comparison of FST outlier tests for SNP loci under selection. Mol Ecol Resour 11:184–194
Otway NM, Bradshaw CJA, Harcourt RG (2004) Estimating the rate of quasi-extinction of the Australian grey nurse shark (Carcharias taurus) population using deterministic age- and stage-classified models. Biol Conserv 119:341–350. https://doi.org/10.1016/j.biocon.2003.11.017
Ovenden JR (2013) Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations. Mar Freshw Res 64:201–207. https://doi.org/10.1071/mf12314
Ovenden J, Kashiwagi T, Broderick D, Giles J, Salini J (2009) The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evol Biol 9:1–15. https://doi.org/10.1186/1471-2148-9-40
Ovenden JR, Berry O, Welch DJ, Buckworth RC, Dichmont CM (2015) Ocean’s eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries. Fish Fish 16:125–159. https://doi.org/10.1111/faf.12052
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
Pérez-Figueroa A, García-Pereira MJ, Saura M, Rolán-Alvarez E, Caballero A (2010) Comparing three different methods to detect selective loci using dominant markers. J Evol Biol 23:2267–2276. https://doi.org/10.1111/j.1420-9101.2010.02093.x
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Quintela M, Skaug HJ, Ølen N, Haug T, Seliussen BB, Solvang HK, Pampoulie C, Kanda N, Pastene LA, Glover KA (2014) Investigating population genetic structure in a highly mobile marine organism: the minke whale Balaenoptera acutorostrata in the North East Atlantic. PLoS One 9:e108640. https://doi.org/10.1371/journal.pone.0108640
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Roberts CD, Stewart AL, Struthers CD (eds) (2015) The fishes of New Zealand. In four volumes. Te Papa Press, Wellington
Rogers PJ, Huveneers C, Goldsworthy SD, Cheung WWL, Jones GK, Mitchell JG, Seuront L (2013a) Population metrics and movement of two sympatric carcharhinids: a comparison of the vulnerability of pelagic sharks of the southern Australian gulfs and shelves. Mar Freshw Res 64:20–30. https://doi.org/10.1071/MF11234
Rogers PJ, Huveneers C, Goldsworthy SD, Mitchell JG, Seuront L (2013b) Broad-scale movements and pelagic habitat of the dusky shark Carcharhinus obscurus off southern Australia determined using pop-up satellite archival tags. Fish Oceanogr 22:102–112. https://doi.org/10.1111/fog.12009
Romine J, Musick J, Burgess G (2009) Demographic analyses of the dusky shark, Carcharhinus obscurus, in the Northwest Atlantic incorporating hooking mortality estimates and revised reproductive parameters. Environ Biol Fish 84:277–289. https://doi.org/10.1007/s10641-008-9435-6
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
Roy D, Hardie DC, Treble MA, Reist JD, Ruzzante DE (2014) Evidence supporting panmixia in Greenland halibut (Reinhardtius hippoglossoides) in the Northwest Atlantic. Can J Fish Aquat Sci 71:763–774. https://doi.org/10.1139/cjfas-2014-0004
Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602
Sellas AB, Bassos-Hull K, Pérez-Jiménez JC, Angulo-Valdés JA, Bernal MA, Hueter RE (2015) Population structure and seasonal migration of the spotted eagle ray, Aetobatus narinari. J Hered 106:266–275. https://doi.org/10.1093/jhered/esv011
Simpfendorfer CA, McAuley R, Chidlow J, Lenanton R, Hall N, Bastow T (1999) Biology and stock assessment of western Australia’s commercially important shark species. Final Report. FRDC, ISBN 0 7309 8448 6, Canberra, Australia
Skomal GB, Zeeman SI, Chisholm JH, Summers EL, Walsh HJ, McMahon KW, Thorrold SR (2009) Transequatorial migrations by basking sharks in the Western Atlantic Ocean. Curr Biol 19:1019–1022. https://doi.org/10.1016/j.cub.2009.04.019
Smart JJ, Chin A, Tobin AJ, White WT, Kumasi B, Simpfendorfer CA (2017) Stochastic demographic analyses of the silvertip shark (Carcharhinus albimarginatus) and the common blacktip shark (Carcharhinus limbatus) from the Indo-Pacific. Fish Res 191:95–107
Smith SE, Au DW, Show C (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Mar Freshwater Res 49:663–678. https://doi.org/10.1071/MF97135
Veríssimo A, Sampaio Í, 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
Walker TI (1998) Can shark resources be harvested sustainably? A question revisited with a review of shark fisheries. Mar Freshw Res 49:553–572
Walter JP, Ebert DA (1991) Preliminary estimates of age of the bronze whaler Carcharhinus brachyurus (Chondrichthyes: Carcharhinidae) from southern Africa, with a review of some life history parameters. S Afr J Mar Sci 10:37–44. https://doi.org/10.2989/02577619109504617
Waples RS, Punt AE, Cope JM (2008) Integrating genetic data into management of marine resources: how can we do it better? Fish Fish 9:423–449. https://doi.org/10.1111/j.1467-2979.2008.00303.x
Warnes G, Leisch F (2006) Genetics: population genetics. R Package, version 1.2.1
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity arrays technology (DArT) for whole-genome profiling of barley. Proc Natl Acad Sci USA 101:9915–9920. https://doi.org/10.1073/pnas.0401076101
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer Science & Business Media, Berlin
Wright D, Bishop JM, Matthee CA, von der Heyden S (2015) Genetic isolation by distance reveals restricted dispersal across a range of life histories: implications for biodiversity conservation planning across highly variable marine environments. Divers Distrib 21:698–710. https://doi.org/10.1111/ddi.12302
Acknowledgements
We thank W White, M Scott, S Tindale, J Ovenden, and Auckland museum for providing samples, R Keane for the distance estimations, A Loi for help in the lab, and JCA Pistevos for the shark artwork in Figs. 3 and 4. The project received funding from the Australian Research Council (LP120100652), the Neiser Foundation, and the Nature Foundation of South Australia. BMG and CJAB were supported by ARC Future Fellowships FT100100767 and FT110100306, respectively). Unpublished acoustic tracking data was sourced from the Acoustic Tracking Database (animaltracking.aodn.org.au) of the Integrated Marine Observing System (IMOS; www.imos.org.au)—IMOS is a national collaborative research infrastructure supported by Australian Government.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
No sharks were sacrificed for this study. All tissue samples were approximately 2 × 2 cm and were taken from pectoral fins (unless otherwise indicated). All samples were obtained legally (see Electronic Supplementary Material 10).
Conflict of interest
All authors declare that they have no conflict of interest and all applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Additional information
Responsible Editor: J. Raeymaekers.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by P. Hablützel and an undisclosed expert.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Junge, C., Donnellan, S.C., Huveneers, C. et al. Comparative population genomics confirms little population structure in two commercially targeted carcharhinid sharks. Mar Biol 166, 16 (2019). https://doi.org/10.1007/s00227-018-3454-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-018-3454-4