Population genetic analyses reveal female reproductive philopatry in the oviparous Port Jackson shark
Joanna Day A B C , Jennalee A. Clark B , Jane E. Williamson B , Culum Brown B and Michael Gillings BA Taronga Conservation Society Australia, Bradleys Head Road, Mosman, NSW 2088, Australia.
B Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia.
C Corresponding author. Email: jday@zoo.nsw.gov.au
Marine and Freshwater Research 70(7) 986-994 https://doi.org/10.1071/MF18255
Submitted: 14 July 2018 Accepted: 16 November 2018 Published: 21 January 2019
Abstract
Restricted gene flow and reproductive philopatry are increasingly being described in marine predators such as sharks. However, observing shark reproductive behaviour in situ is problematic because of issues associated with sampling in the marine environment. As such, molecular tools have become fundamental to unravelling complex mating behaviours. In this study, we examined patterns of genetic structure in the oviparous Port Jackson shark (Heterodontus portusjacksoni) using 10 microsatellite loci and the mitochondrial (mt)DNA control region. Patterns of genetic structure were investigated between breeding aggregations in Sydney and Jervis Bay, as well as between two sites within Jervis Bay. Significant genetic differentiation was detected between Sydney and Jervis Bay using mtDNA, but no structure was observed within Jervis Bay. No significant genetic differentiation was found with microsatellites within or between aggregations. Mean assignment index values were significantly higher for females than males in Jervis Bay, but not in Sydney. Both females and males migrate inshore during the Austral winter for breeding, but it appears females may exhibit higher levels of reproductive philopatry than males. This is the first study to document reproductive philopatry in an oviparous shark, highlighting the importance of conserving and appropriately managing breeding sites for H. portusjacksoni and potentially other oviparous shark species.
Additional keywords: elasmobranch, Heterodontus portusjacksoni, mating system, microsatellite, mtDNA.
References
Baker, C. S., Steel, D., Calambokidis, J., Falcone, E., González-Peral, U., Barlow, J., Burdin, A. M., Clapham, P. J., Ford, J. K. B., Gabriele, C. M., Mattila, D., Rojas-Bracho, L., Straley, J. M., Taylor, B. L., Urbán, J., Wade, P. R., Weller, D., Witteveen, B. H., and Yamaguchi, M. (2013). Strong maternal fidelity and natal philopatry shape genetic structure in North Pacific humpback whales. Marine Ecology Progress Series 494, 291–306.| Strong maternal fidelity and natal philopatry shape genetic structure in North Pacific humpback whales.Crossref | GoogleScholarGoogle Scholar |
Barker, A. M., Nosal, A. P., Lewallen, E. A., and Burton, R. S. (2015). Genetic structure of leopard shark (Triakis semifasciata) populations along the Pacific coast of North America. Journal of Experimental Marine Biology and Ecology 472, 151–157.
| Genetic structure of leopard shark (Triakis semifasciata) populations along the Pacific coast of North America.Crossref | GoogleScholarGoogle Scholar |
Bass, N. C., Mourier, J., Knott, N. A., Day, J., Guttridge, T., and Brown, C. (2017). Long-term migration patterns and bisexual philopatry in a benthic shark species. Marine and Freshwater Research 68, 1414–1421.
| Long-term migration patterns and bisexual philopatry in a benthic shark species.Crossref | GoogleScholarGoogle Scholar |
Bird, C. E., Karl, S. A., Smouse, P. E., and Toonen, R. J. (2011). Detecting and measuring genetic differentiation. In ‘Phylogenetics and Population Genetics in Crustacea’. (Eds C. Held, S. Koenemann, and C. D. Schubart.) pp. 31–55. (Taylor and Francis: Boca Raton, FL, USA.)
Blower, D. C., Pandolfi, J. M., Bruce, B. D., Gomez-Cabrera Md, C., and Ovenden, J. R. (2012). Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes. Marine Ecology Progress Series 455, 229–244.
| Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes.Crossref | GoogleScholarGoogle Scholar |
Braccini, J. M., Walker, T. I., and Gason, A. S. (2009). ‘GHATF Shark Survey of Population Abundance and Population Size Composition for Target, Byproduct and Bycatch Species.’ (Department of Primary Industries, Fisheries Research Branch: Queenscliff, Vic., Australia.)
Bravington, M. V., Skaug, H. J., and Anderson, E. C. (2016). Close-kin mark–recapture. Statistical Science 31, 259–274.
| Close-kin mark–recapture.Crossref | GoogleScholarGoogle Scholar |
Castro, A. L., Stewart, B. S., Wilson, S. G., Hueter, R. E., Meekan, M. G., Motta, P. J., Bowen, B. W., and Karl, S. A. (2007). Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus). Molecular Ecology 16, 5183–5192.
| Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus).Crossref | GoogleScholarGoogle Scholar | 18092992PubMed |
Chapman, D. D., Feldheim, K. A., Papastamatiou, Y. P., and Hueter, R. E. (2015). There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annual Review of Marine Science 7, 547–570.
| There and back again: a review of residency and return migrations in sharks, with implications for population structure and management.Crossref | GoogleScholarGoogle Scholar | 25251267PubMed |
Chesser, R. K., and Baker, R. J. (1996). Effective sizes and dynamics of uniparental and biparentally inherited genes. Genetics 144, 1225–1235.
| 8913763PubMed |
Clark, J. A., Brown, C., Gillings, M. R., Gardner, M., Williamson, J. E., Izzo, C., and Day, J. (2017). Characterization of 12 polymorphic microsatellite loci in the Port Jackson shark, Heterodontus portusjacksoni (Meyer, 1793). Marine Biodiversity , .
| Characterization of 12 polymorphic microsatellite loci in the Port Jackson shark, Heterodontus portusjacksoni (Meyer, 1793).Crossref | GoogleScholarGoogle Scholar |
Clarke, C. R., Karl, S. A., Horn, R. L., Bernard, A. M., Lea, J. S., Hazin, F. H., Prodöhl, P. A., and Shivji, M. S. (2015). Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis. Marine Biology 162, 945–955.
| Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis.Crossref | GoogleScholarGoogle Scholar |
Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 11050560PubMed |
Corrigan, S., Huveneers, C., Stow, A., and Beheregaray, L. B. (2016). A multilocus comparative study of dispersal in three codistributed demersal sharks from eastern Australia. Canadian Journal of Fisheries and Aquatic Sciences 73, 406–415.
| A multilocus comparative study of dispersal in three codistributed demersal sharks from eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Daly-Engel, T. S., Seraphin, K. D., Holland, K. N., Coffey, J. P., Nance, H. A., Toonen, R. J., and Bowen, B. W. (2012). Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS One 7, e29986.
| Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini).Crossref | GoogleScholarGoogle Scholar | 22253848PubMed |
Dudgeon, C. L., Blower, D. C., Broderick, D., Giles, J. L., Holmes, B. J., Kashiwagi, T., Krück, N. C., Morgan, J. A. T., Tillett, B. J., and Ovenden, J. R. (2012). A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. Journal of Fish Biology 80, 1789–1843.
| A review of the application of molecular genetics for fisheries management and conservation of sharks and rays.Crossref | GoogleScholarGoogle Scholar | 22497408PubMed |
Earl, D. A., and von Holdt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
| STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |
Engelhaupt, D., Hoelzel, A. R., Nicholson, C., Frantzis, A., Mesnick, S. L., Gero, S., Whitehead, H., Rendell, L., Miller, P., De Stefanis, R., Cañadas, A., Airoldi, S., and Mignucci-Giannoni, A. A. (2009). Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus). Molecular Ecology 18, 4193–4205.
| Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus).Crossref | GoogleScholarGoogle Scholar | 19769692PubMed |
Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
| Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 15969739PubMed |
Excoffier, L., and Lischer, H. E. L. (2010). ARLEQUIN suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| ARLEQUIN suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |
Falush, D., Stephens, M., and Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
| 12930761PubMed |
Favre, L., Balloux, F., Goudet, J., and Perrin, N. (1997). Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proceedings of the Royal Society of London. Series B, Biological Sciences 264, 127–132.
| Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns.Crossref | GoogleScholarGoogle Scholar |
Feldheim, K. A., Gruber, S. H., DiBattista, J. D., Babcock, E. A., Kessel, S. T., Hendry, A. P., Pikitch, E. K., Ashley, M. V., and Chapman, D. D. (2014). Two decades of genetic profiling yields first evidence of natal philopatry and long‐term fidelity to parturition sites in sharks. Molecular Ecology 23, 110–117.
| Two decades of genetic profiling yields first evidence of natal philopatry and long‐term fidelity to parturition sites in sharks.Crossref | GoogleScholarGoogle Scholar | 24192204PubMed |
Geraghty, P. T., Williamson, J. E., Macbeth, W. G., Wintner, S. P., Harry, A. V., Ovenden, J. R., and Gillings, M. R. (2013). Population expansion and genetic structure in Carcharhinus brevipinna in the southern Indo-Pacific. PLoS One 8, e75169.
| Population expansion and genetic structure in Carcharhinus brevipinna in the southern Indo-Pacific.Crossref | GoogleScholarGoogle Scholar | 24086462PubMed |
Gilbert, K. J., Andrew, R. L., Bock, D. G., Franklin, M. T., Kane, N. C., Moore, J.-S., Moyers, B. T., Renaut, S., Rennison, D. J., Veen, T., and Vines, T. H. (2012). Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program STRUCTURE. Molecular Ecology 21, 4925–4930.
| Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program STRUCTURE.Crossref | GoogleScholarGoogle Scholar | 22998190PubMed |
Goudet, J. (1995). FSTAT (version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
| FSTAT (version 1.2): a computer program to calculate F-statistics.Crossref | GoogleScholarGoogle Scholar |
Greenwood, P. (1980). Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28, 1140–1162.
| Mating systems, philopatry and dispersal in birds and mammals.Crossref | GoogleScholarGoogle Scholar |
Heist, E. J. (2009). Molecular markers and genetic population structure of pelagic sharks. In ‘Sharks of the Open Ocean: Biology, Fisheries and Conservation’. (Eds T. J. Pitcher, M. D. Camhi, E. K. Pikitch, and E. A. Babcock.) pp. 323–333. (Blackwell Publishing: Oxford, UK.)
Hernández, S., Daley, R., Walker, T., Braccini, J. M., Varela, A., Francis, M. P., and Ritchie, P. A. (2015). Demographic history and the South Pacific dispersal barrier for school shark (Galeorhinus galeus) inferred by mitochondrial DNA and microsatellite DNA mark. Fisheries Research 167, 132–142.
| Demographic history and the South Pacific dispersal barrier for school shark (Galeorhinus galeus) inferred by mitochondrial DNA and microsatellite DNA mark.Crossref | GoogleScholarGoogle Scholar |
Hochberg, Y. (1988). A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75, 800–802.
| A sharper Bonferroni procedure for multiple tests of significance.Crossref | GoogleScholarGoogle Scholar |
Holmes, B. J., Williams, S. M., Otway, N. M., Nielsen, E. E., Maher, S. L., Bennett, M. B., and Ovenden, J. R. (2017). Population structure and connectivity of tiger sharks (Galeocerdo cuvier) across the Indo-Pacific Ocean basin. Royal Society Open Science 4, 170309.
| Population structure and connectivity of tiger sharks (Galeocerdo cuvier) across the Indo-Pacific Ocean basin.Crossref | GoogleScholarGoogle Scholar | 29291060PubMed |
Hubisz, M., Falush, D., Stephens, M., and Pritchard, J. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 1322–1332.
| Inferring weak population structure with the assistance of sample group information.Crossref | GoogleScholarGoogle Scholar | 21564903PubMed |
Huveneers, C., and Simpfendorfer, C. (2015). Port Jackson Shark Heterodontus portusjacksoni. In ‘The IUCN Red List of Threatened Species 2015’, e.T39334A68625721. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/39334/68625721 [Verified 8 January 2019].
Jost, L. O. U. (2008). GST and its relatives do not measure differentiation. Molecular Ecology 17, 4015–4026.
| GST and its relatives do not measure differentiation.Crossref | GoogleScholarGoogle Scholar |
Kalinowski, S. T., Wagner, A. P., and Taper, M. L. (2006). ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes 6, 576–579.
| ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship.Crossref | GoogleScholarGoogle Scholar |
Karl, S. A., Castro, A. L. F., Lopez, J. A., Charvet, P., and Burgess, G. H. (2011). Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conservation Genetics 12, 371–382.
| Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA.Crossref | GoogleScholarGoogle Scholar |
Keeney, D. B., Heupel, M. R., Hueter, R. E., and Heist, E. J. (2005). Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Molecular Ecology 14, 1911–1923.
| Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea.Crossref | GoogleScholarGoogle Scholar | 15910315PubMed |
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.
| MEGA X: molecular evolutionary genetics analysis across computing platforms.Crossref | GoogleScholarGoogle Scholar | 29722887PubMed |
Last, P. R., and Stevens, J. D. (2009) ‘Sharks and Rays of Australia’, 2nd edn. (CSIRO Publishing: Melbourne, Vic., Australia.)
Lee, P. L., Luschi, P., and Hays, G. C. (2007). Detecting female precise natal philopatry in green turtles using assignment methods. Molecular Ecology 16, 61–74.
| Detecting female precise natal philopatry in green turtles using assignment methods.Crossref | GoogleScholarGoogle Scholar | 17181721PubMed |
Manly, B. F. J. (1997). ‘RT, a Program for Randomisation Testing, Version 2.1.’ (Centre for Applications of Statistics and Mathematics, University of Otago: Otago, New Zealand.)
Mourier, J., and Planes, S. (2013). Direct genetic evidence for reproductive philopatry and associated fine-scale migrations in female blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia. Molecular Ecology 22, 201–214.
| Direct genetic evidence for reproductive philopatry and associated fine-scale migrations in female blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia.Crossref | GoogleScholarGoogle Scholar | 23130666PubMed |
Mourier, J., Buray, N., Schultz, J. K., Clua, E., and Planes, S. (2013). Genetic network and breeding patterns of a sicklefin lemon shark (Negaprion acutidens) population in the Society Islands, French Polynesia. PLoS One 8, e73899.
| Genetic network and breeding patterns of a sicklefin lemon shark (Negaprion acutidens) population in the Society Islands, French Polynesia.Crossref | GoogleScholarGoogle Scholar | 23967354PubMed |
Nosal, A. P., Caillat, A., Kisfaludy, E. K., Royer, M. A., and Wegner, N. C. (2014). Aggregation behavior and seasonal philopatry in male and female leopard sharks Triakis semifasciata along the open coast of southern California, USA. Marine Ecology Progress Series 499, 157–175.
| Aggregation behavior and seasonal philopatry in male and female leopard sharks Triakis semifasciata along the open coast of southern California, USA.Crossref | GoogleScholarGoogle Scholar |
O’Gower, A. K., and Nash, A. R. (1978). Dispersion of the Port Jackson shark in Australian waters. In ‘Sensory Biology of Sharks, Skates, and Rays’. (Eds E. S. Hodgson and R. F. Mathewson.) pp. 529–544. (Office of Naval Research, Department of the Navy: Arlington, VA, USA.)
Ovenden, J. R., Kashiwagi, T., Broderick, D., Giles, J., and Salini, J. (2009). The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evolutionary Biology 9, 40.
| The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago.Crossref | GoogleScholarGoogle Scholar | 19216767PubMed |
Pardini, A. T., Jones, C. S., Noble, L. R., Kreiser, B., Malcolm, H., Bruce, B. D., Stevens, J. D., Cliff, G., Scholl, M. C., Francis, M., Duffy, C. A. J., and Martin, A. P. (2001). Sex-biased dispersal of great white sharks. Nature 412, 139.
| Sex-biased dispersal of great white sharks.Crossref | GoogleScholarGoogle Scholar | 11449258PubMed |
Peakall, R., and Smouse, P. E. (2006). GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Peakall, R., and Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.
| GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update.Crossref | GoogleScholarGoogle Scholar | 22820204PubMed |
Perrin, N., and Mazalov, V. (2000). Local competition, inbreeding, and the evolution of sex-biased dispersal. American Naturalist 155, 116–127.
| 10657181PubMed |
Piry, S., Alapetite, A., Cornuet, J., Paetkau, D., Baudouin, L., and Estoup, A. (2004). GeneClass2: a software for genetic assignment and first-generation migrant detection. The Journal of Heredity 95, 536–539.
| GeneClass2: a software for genetic assignment and first-generation migrant detection.Crossref | GoogleScholarGoogle Scholar | 15475402PubMed |
Portnoy, D. S., and Heist, E. J. (2012). Molecular markers: progress and prospects for understanding reproductive ecology in elasmobranchs. Journal of Fish Biology 80, 1120–1140.
| Molecular markers: progress and prospects for understanding reproductive ecology in elasmobranchs.Crossref | GoogleScholarGoogle Scholar | 22497375PubMed |
Portnoy, D. S., McDowell, J. R., Heist, E. J., Musick, J. A., and Graves, J. E. (2010). World phylogeography and male‐mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Molecular Ecology 19, 1994–2010.
| World phylogeography and male‐mediated gene flow in the sandbar shark, Carcharhinus plumbeus.Crossref | GoogleScholarGoogle Scholar | 20406387PubMed |
Portnoy, D. S., Puritz, J. B., Hollenbeck, C. M., Gelsleichter, J., Chapman, D., and Gold, J. R. (2015). Selection and sex-biased dispersal in a coastal shark: the influence of philopatry on adaptive variation. Molecular Ecology 24, 5877–5885.
| Selection and sex-biased dispersal in a coastal shark: the influence of philopatry on adaptive variation.Crossref | GoogleScholarGoogle Scholar | 26518727PubMed |
Powter, D. M. (2006). Conservation biology of the Port Jackson shark, Heterodontus portusjacksoni in New South Wales. Ph.D. Thesis, University of Newcastle, Newcastle, NSW, Australia.
Powter, D. M., and Gladstone, W. (2009). Habitat-mediated use of space by juvenile and mating adult Port Jackson sharks, Heterodontus portusjacksoni, in eastern Australia. Pacific Science 63, 1–14.
| Habitat-mediated use of space by juvenile and mating adult Port Jackson sharks, Heterodontus portusjacksoni, in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 10835412PubMed |
Prugnolle, F., and de Meeus, T. (2002). Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88, 161–165.
| Inferring sex-biased dispersal from population genetic tools: a review.Crossref | GoogleScholarGoogle Scholar | 11920116PubMed |
Rannala, B., and Mountain, J. L. (1997). Detecting immigration by using multi-locus genotypes. Proceedings of the National Academy of Sciences of the United States of America 94, 9197–9201.
| Detecting immigration by using multi-locus genotypes.Crossref | GoogleScholarGoogle Scholar | 9256459PubMed |
Raymond, M., and Rousset, F. (1995). Population genetics software for exact tests and ecumenicism. The Journal of Heredity 86, 248–249.
| Population genetics software for exact tests and ecumenicism.Crossref | GoogleScholarGoogle Scholar |
Ryman, N., and Palm, S. (2006). POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Molecular Ecology Notes 6, 600–602.
| POWSIM: a computer program for assessing statistical power when testing for genetic differentiation.Crossref | GoogleScholarGoogle Scholar |
Schultz, J. K., Feldheim, K. A., Gruber, S. H., Ashley, M. V., McGovern, T. M., and Bowen, B. W. (2008). Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Molecular Ecology 17, 5336–5348.
| Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion).Crossref | GoogleScholarGoogle Scholar | 19121001PubMed |
Shulman, M. J., and Bermingham, E. (1995). Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49, 897–910.
| Early life histories, ocean currents, and the population genetics of Caribbean reef fishes.Crossref | GoogleScholarGoogle Scholar | 28564869PubMed |
Speed, C. W., Field, I. C., Meekan, M. G., and Bradshaw, C. J. A. (2010). Complexities of coastal shark movements and their implications for management. Marine Ecology Progress Series 408, 275–293.
| Complexities of coastal shark movements and their implications for management.Crossref | GoogleScholarGoogle Scholar |
Springer, S. (1967). Social organization of shark populations. In ‘Sharks, Skates and Rays’. (Eds P. W. Guilbert, R. F. Mathewson, and D. P. Rall.) pp. 149–174. (John Hopkins Press: Baltimore, MD, USA.)
Sunnucks, P., and Hales, D. F. (1996). Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510–524.
| Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae).Crossref | GoogleScholarGoogle Scholar | 8742640PubMed |
Taguchi, M., King, J. R., Wetklo, M., Withler, R. E., and Yokawa, K. (2015). Population genetic structure and demographic history of Pacific blue sharks (Prionace glauca) inferred from mitochondrial DNA analysis. Marine and Freshwater Research 66, 267–275.
| Population genetic structure and demographic history of Pacific blue sharks (Prionace glauca) inferred from mitochondrial DNA analysis.Crossref | GoogleScholarGoogle Scholar |
Tamura, K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition–transversion and G+C-content biases. Molecular Biology and Evolution 9, 678–687.
| 1630306PubMed |
Templeton, A. R., Crandall, K. A., and Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
| 1385266PubMed |
Tillett, B. J., Meekan, M. G., Field, I. C., Thorburn, D. C., and Ovenden, J. R. (2012). Evidence for reproductive philopatry in the bull shark Carcharhinus leucas. Journal of Fish Biology 80, 2140–2158.
| Evidence for reproductive philopatry in the bull shark Carcharhinus leucas.Crossref | GoogleScholarGoogle Scholar | 22551174PubMed |
Tovar-Ávila, J., Day, R. W., and Walker, T. I. (2010). Using rapid assessment and demographic methods to evaluate the effects of fishing on Heterodontus portusjacksoni off far-eastern Victoria, Australia. Journal of Fish Biology 77, 1564–1578.
| Using rapid assessment and demographic methods to evaluate the effects of fishing on Heterodontus portusjacksoni off far-eastern Victoria, Australia.Crossref | GoogleScholarGoogle Scholar | 21078019PubMed |
Trochet, A., Courtois, E. A., Stevens, V. M., Baguette, M., Chaine, A., Schmeller, D. S., Clobert, J., and Wiens, J. J. (2016). Evolution of sex-biased dispersal. The Quarterly Review of Biology 91, 297–320.
| Evolution of sex-biased dispersal.Crossref | GoogleScholarGoogle Scholar | 29558614PubMed |
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotypic errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
| MICRO-CHECKER: software for identifying and correcting genotypic errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar |
Vignaud, T. M., Maynard, J. A., Leblois, R., Meekan, M. G., Vazquez-Juarez, R., Ramirez-Macias, D., Pierce, S. J., Rowat, D., Berumen, M. L., Beeravolu, C., Baksay, S., and Planes, S. (2014). Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline. Molecular Ecology 23, 2590–2601.
| Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline.Crossref | GoogleScholarGoogle Scholar | 24750370PubMed |
Walker, T. I., Hudson, R. J., and Gason, A. S. (2005). Catch evaluation of target, by-product and by-catch species taken by gillnets and longlines in the shark fishery of south-eastern Australia. Journal of Northwest Atlantic Fishery Science 35, 505–530.
| Catch evaluation of target, by-product and by-catch species taken by gillnets and longlines in the shark fishery of south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Waples, R. S. (1998). Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. The Journal of Heredity 89, 438–450.
| Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species.Crossref | GoogleScholarGoogle Scholar |