First evidence of multiple paternity in the bull shark (Carcharhinus leucas)
Agathe Pirog A , Sébastien Jaquemet A B , Marc Soria C and Hélène Magalon A B DA Université de La Réunion, UMR 9220 ENTROPIE (Université de La Réunion/IRD/CNRS), 15 Avenue René Cassin, CS 92003, F-97744 Saint Denis Cedex 09, La Réunion, France.
B Laboratory of Excellence CORAIL, 58, Avenue Paul Alduy, F-66860 Perpignan Cedex, France.
C IRD Réunion, UMR 248 MARBEC, CS 41095 2 rue Joseph Wetzell, F-97492 Sainte-Clotilde, La Réunion, France.
D Corresponding author. Email: helene.magalon@univ-reunion.fr
Marine and Freshwater Research 68(1) 195-201 https://doi.org/10.1071/MF15255
Submitted: 6 July 2015 Accepted: 24 August 2015 Published: 6 November 2015
Abstract
The present study assessed the occurrence of multiple paternity in four litters of bull shark Carcharhinus leucas (n = 5, 8, 9 and 11 embryos) sampled at Reunion Island in the Western Indian Ocean. Using 21 microsatellite loci, we revealed that two litters were generated from two sires each, demonstrating for the first time multiple paternity for this species. We also reported a high paternal skew (10 : 1 in Litter 1 and 7 : 1 in Litter 3), which may be because of post-copulatory or post-zygotic selection processes. These results contribute to a better understanding of the reproductive behaviour of the bull shark, which remains poorly documented. The present study must be expanded to assess the frequency of multiple paternity in this species, and to test for genetic or cryptic benefits (convenience polyandry), which is important for long-term conservation and management plans.
Additional keywords: microsatellite, paternity test, polyandry.
References
Avise, J. C., Jones, A. G., Walker, D. E., and DeWoody, J. A. (2002). Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annual Review of Genetics 36, 19–45.| Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsleltQ%3D%3D&md5=35163245dcf77597ce67fc7a406bd3ecCAS | 12429685PubMed |
Branstetter, S., and Stiles, R. (1987). Age and growth estimates of the bull shark, Carcharhinus leucas, from the northern Gulf of Mexico. Environmental Biology of Fishes 20, 169–181.
| Age and growth estimates of the bull shark, Carcharhinus leucas, from the northern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Brunnschweiler, J. M., and Baensch, H. (2011). Seasonal and long-term changes in relative abundance of bull sharks from a tourist shark feeding site in Fiji. PLoS One 6, e16597.
| Seasonal and long-term changes in relative abundance of bull sharks from a tourist shark feeding site in Fiji.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhslyiu78%3D&md5=ffafd6cb71abbc05a6f20a3ae788826eCAS | 21346792PubMed |
Byrne, R. J., and Avise, J. C. (2012). Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Marine Biology 159, 749–756.
| Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species.Crossref | GoogleScholarGoogle Scholar |
Castro, J. I. (2011). ‘The Sharks of North America.’ (Oxford University Press: New York.)
Chabot, C., and Haggin, B. (2014). Frequency of multiple paternity varies between two populations of brown smoothhound shark, Mustelus henlei. Marine Biology 161, 797–804.
| Frequency of multiple paternity varies between two populations of brown smoothhound shark, Mustelus henlei.Crossref | GoogleScholarGoogle Scholar |
Chapman, D. D., Prodohl, P. A., Gelsleichter, J., Manire, C. A., and Shivji, M. S. (2004). Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation. Molecular Ecology 13, 1965–1974.
| Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFelu7Y%3D&md5=c8919fa6b5dc39a4bca93674e9645e99CAS | 15189217PubMed |
Chapman, D. D., Shivji, M. S., Louis, E., Sommer, J., Fletcher, H., and Prodohl, P. A. (2007). Virgin birth in a hammerhead shark. Biology Letters 3, 425–427.
| Virgin birth in a hammerhead shark.Crossref | GoogleScholarGoogle Scholar | 17519185PubMed |
Chapman, D. D., Firchau, B., and Shivji, M. S. (2008). Parthenogenesis in a large-bodied requiem shark, the blacktip shark Carcharhinus limbatus. Journal of Fish Biology 73, 1473–1477.
| Parthenogenesis in a large-bodied requiem shark, the blacktip shark Carcharhinus limbatus.Crossref | GoogleScholarGoogle Scholar |
Chapman, D. D., Wintner, S. P., Abercrombie, D. L., Ashe, J., Bernard, A. M., Shivji, M. S., and Feldheim, K. A. (2013). The behavioural and genetic mating system of the sand tiger shark, Carcharias taurus, an intrauterine cannibal. Biology Letters 9, 20130003.
| The behavioural and genetic mating system of the sand tiger shark, Carcharias taurus, an intrauterine cannibal.Crossref | GoogleScholarGoogle Scholar | 23637391PubMed |
Chapuis, M.-P., and Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.
| Microsatellite null alleles and estimation of population differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtleku7c%3D&md5=26e281717e3ceddbac87bdb2cd9bfb71CAS | 17150975PubMed |
Compagno, L. J. V. (1984). ‘FAO Species Catalogue: Vol 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2 – Carcharhiniformes.’ (FAO: Rome.)
Compagno, L. J. V. (1990). Alternative life-history styles of cartilaginous fishes in time and space. Environmental Biology of Fishes 28, 33–75.
| Alternative life-history styles of cartilaginous fishes in time and space.Crossref | GoogleScholarGoogle Scholar |
Compagno, L. J. V. (2001). ‘Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Volume 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes).’ (FAO: Rome.)
Conrath, C. L., Musick, J. A., Carrier, J. C., and Heithaus, M. R. (2012). Reproductive biology of elasmobranchs. In ‘Biology of Sharks and Their Relatives’, 2nd edn. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 291–311. (CRC Press, Taylor & Francis Group: Boca Raton, FL, USA.)
Dakin, E. E., and Avise, J. C. (2004). Microsatellite null alleles in parentage analysis. Heredity 93, 504–509.
| Microsatellite null alleles in parentage analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVWgs7o%3D&md5=778399440756af9167930ec294c6040dCAS | 15292911PubMed |
Daly, R., Froneman, P. W., and Smale, M. J. (2013). Comparative feeding ecology of bull sharks (Carcharhinus leucas) in the coastal waters of the Southwest Indian Ocean inferred from stable isotope analysis. PLoS One 8, e78229.
| Comparative feeding ecology of bull sharks (Carcharhinus leucas) in the coastal waters of the Southwest Indian Ocean inferred from stable isotope analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs12js7%2FP&md5=fbf16f52887846909558c7f5eaadc926CAS | 24205168PubMed |
Daly-Engel, T. S., Grubbs, R. D., Bowen, B. W., and Toonen, R. J. (2007). Frequency of multiple paternity in an unexploited tropical population of sandbar sharks (Carcharhinus plumbeus). Canadian Journal of Fisheries and Aquatic Sciences 64, 198–204.
| Frequency of multiple paternity in an unexploited tropical population of sandbar sharks (Carcharhinus plumbeus).Crossref | GoogleScholarGoogle Scholar |
DiBattista, J. D., Feldheim, K. A., Gruber, S. H., and Hendry, A. P. (2008a). Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Molecular Ecology 17, 783–795.
| Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks.Crossref | GoogleScholarGoogle Scholar | 18194167PubMed |
DiBattista, J. D., Feldheim, K. A., Thibert-Plante, X., Gruber, S. H., and Hendry, A. P. (2008b). A genetic assessment of polyandry and breeding-site fidelity in lemon sharks. Molecular Ecology 17, 3337–3351.
| A genetic assessment of polyandry and breeding-site fidelity in lemon sharks.Crossref | GoogleScholarGoogle Scholar | 18564083PubMed |
Dopazo, H., and Alberch, P. (1994). Preliminary results on optional viviparity and intrauterine siblicide in Salamandra salamandra populations from Northern Spain. Mertensiella 4, 125–137.
Dulvy, N. K., Baum, J. K., Clarke, S., Compagno, L. J. V., Cortes, E., Domingo, A., Fordham, S., Fowler, S., Francis, M. P., and Gibson, C. (2008). You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquatic Conservation: Marine and Freshwater Ecosystems 18, 459–482.
| You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays.Crossref | GoogleScholarGoogle Scholar |
Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L. N. K., Fordham, S. V., Francis, M. P., Pollock, C. M., Simpfendorfer, C. A., Burgess, G. H., Carpenter, K. E., Compagno, L. J. V., Ebert, D. A., Gibson, C., Heupel, M. R., Livingstone, S. R., Sanciangco, J. C., Stevens, J. D., Valenti, S., and White, W. T. (2014). Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590.
| Extinction risk and conservation of the world’s sharks and rays.Crossref | GoogleScholarGoogle Scholar | 24448405PubMed |
Ellegren, H. (2004). Microsatellites: simple sequences with complex evolution. Nature Reviews. Genetics 5, 435–445.
| Microsatellites: simple sequences with complex evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktV2rsrg%3D&md5=216fb5be8eade8e78967f52f878f01e7CAS | 15153996PubMed |
Engel, E. (1980). A new genetic concept: uniparental disomy and its potential effect, isodisomy. American Journal of Medical Genetics 6, 137–143.
| A new genetic concept: uniparental disomy and its potential effect, isodisomy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M%2Fotlaqsg%3D%3D&md5=be43e229a573a2fbcc1527ade44d6450CAS | 7192492PubMed |
Feldheim, K. A., Gruber, S. H., and Ashley, M. V. (2004). Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58, 2332–2342.
| Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVentLnL&md5=a3406940624296c8e4e4f21a64afdef5CAS | 15562694PubMed |
Ferretti, F., Worm, B., Britten, G. L., Heithaus, M. R., and Lotze, H. K. (2010). Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13, 1055–1071.
| Patterns and ecosystem consequences of shark declines in the ocean.Crossref | GoogleScholarGoogle Scholar | 20528897PubMed |
Fitzpatrick, J. L., Kempster, R. M., Daly-Engel, T. S., Collin, S. P., and Evans, J. P. (2012). Assessing the potential for post-copulatory sexual selection in elasmobranchs. Journal of Fish Biology 80, 1141–1158.
| Assessing the potential for post-copulatory sexual selection in elasmobranchs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rksVOkug%3D%3D&md5=a104e83c5146252d762efc273c72dbcaCAS | 22497376PubMed |
Frankham, R., Briscoe, D. A., and Ballou, J. D. (2010). ‘Introduction to Conservation Genetics’, 2nd edn. (Cambridge University Press: New York.)
Frisk, M. G., Miller, T. J., and Fogarty, M. J. (2001). Estimation and analysis of biological parameters in elasmobranch fishes: a comparative life history study. Canadian Journal of Fisheries and Aquatic Sciences 58, 969–981.
| Estimation and analysis of biological parameters in elasmobranch fishes: a comparative life history study.Crossref | GoogleScholarGoogle Scholar |
Griffiths, A. M., Jacoby, D. M. P., Casane, D., McHugh, M., Croft, D. P., Genner, M. J., and Sims, D. W. (2012). First analysis of multiple paternity in an oviparous shark, the small-spotted catshark (Scyliorhinus canicula L.). The Journal of Heredity 103, 166–173.
| First analysis of multiple paternity in an oviparous shark, the small-spotted catshark (Scyliorhinus canicula L.).Crossref | GoogleScholarGoogle Scholar | 22058410PubMed |
Heithaus, M. R., Frid, A., Wirsing, A. J., and Worm, B. (2008). Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23, 202–210.
| Predicting ecological consequences of marine top predator declines.Crossref | GoogleScholarGoogle Scholar |
Heupel, M. R., Simpfendorfer, C. A., Espinoza, M., Smoothey, A. F., Tobin, A., and Peddemors, V. (2015). Conservation challenges of sharks with continental scale migrations. Frontiers of Materials Science 2, .
| Conservation challenges of sharks with continental scale migrations.Crossref | GoogleScholarGoogle Scholar |
Holman, L., and Kokko, H. (2013). The consequences of polyandry for population viability, extinction risk and conservation. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 368, 20120053.
| The consequences of polyandry for population viability, extinction risk and conservation.Crossref | GoogleScholarGoogle Scholar | 23339244PubMed |
Hueter, R. E., Heupel, M. R., Heist, E. J., and Keeney, D. B. (2005). Evidence of philopatry in sharks and implications for the management of shark fisheries. Journal of Northwest Atlantic Fishery Science 35, 239–247.
| Evidence of philopatry in sharks and implications for the management of shark fisheries.Crossref | GoogleScholarGoogle Scholar |
Jennions, M. D., and Petrie, M. (2000). Why do females mate multiply? A review of the genetic benefits. Biological Reviews of the Cambridge Philosophical Society 75, 21–64.
| Why do females mate multiply? A review of the genetic benefits.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3gsFSltw%3D%3D&md5=b7d4b05f02b8cb318f0da6a238a6d13bCAS | 10740892PubMed |
Jenson, N. H. (1976). Reproduction of the Bull Shark, Carcharhinus leucas, in the Lake Nicaragua-Rio San Juan System. In ‘Investigations of the Ichtyofauna of Nicaraguan Lakes’. (Ed T. B. Thorson.) pp. 539–560. (School of Life Sciences University of Nebraska–Lincoln: Lincoln, NB, USA.)
Jones, O. R., and Wang, J. L. (2010). COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10, 551–555.
| COLONY: a program for parentage and sibship inference from multilocus genotype data.Crossref | GoogleScholarGoogle Scholar | 21565056PubMed |
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., and Heist, E. J. (2003). Characterization of microsatellite loci isolated from the blacktip shark and their utility in requiem and hammerhead sharks. Molecular Ecology Notes 3, 501–504.
| Characterization of microsatellite loci isolated from the blacktip shark and their utility in requiem and hammerhead sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks12nsw%3D%3D&md5=42c336811b9aa46ec64455150414b715CAS |
Kohler, N. E., and Turner, P. A. (2001). Shark tagging: a review of conventional methods and studies. Environmental Biology of Fishes 60, 191–224.
| Shark tagging: a review of conventional methods and studies.Crossref | GoogleScholarGoogle Scholar |
Marino, I. A. M., Riginella, E., Gristina, M., Rasotto, M. B., Zane, L., and Mazzoldi, C. (2015). Multiple paternity and hybridization in two smooth-hound sharks. Scientific Reports 5, 12 919.
| Multiple paternity and hybridization in two smooth-hound sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVKhsrbM&md5=c213ddf8c28170b7543de4f4767f270dCAS |
Martinez, J. L., Moran, P., Perez, J., De Gaudemar, B., Beall, E., and Garcia‐Vazquez, E. (2000). Multiple paternity increases effective size of southern Atlantic salmon populations. Molecular Ecology 9, 293–298.
| Multiple paternity increases effective size of southern Atlantic salmon populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3gtVOmuw%3D%3D&md5=8f5a12834f9ad65fcba9b933f71baabfCAS | 10736027PubMed |
Musick, J. A., Burgess, G., Cailliet, G., Camhi, M., and Fordham, S. (2000). Management of sharks and their relatives (Elasmobranchii). Fisheries (Bethesda, Md.) 25, 9–13.
| Management of sharks and their relatives (Elasmobranchii).Crossref | GoogleScholarGoogle Scholar |
Myers, R. A., and Worm, B. (2005). Extinction, survival or recovery of large predatory fishes. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 360, 13–20.
| Extinction, survival or recovery of large predatory fishes.Crossref | GoogleScholarGoogle Scholar | 15713586PubMed |
Myers, R. A., Bowen, K. G., and Barrowman, N. J. (1999). Maximum reproductive rate of fish at low population sizes. Canadian Journal of Fisheries and Aquatic Sciences 56, 2404–2419.
| Maximum reproductive rate of fish at low population sizes.Crossref | GoogleScholarGoogle Scholar |
Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P., and Peterson, C. H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.
| Cascading effects of the loss of apex predatory sharks from a coastal ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFSitrw%3D&md5=46fc872a3098aa00922b3337e654d3f0CAS | 17395829PubMed |
Neff, B. D., and Pitcher, T. E. (2002). Assessing the statistical power of genetic analyses to detect multiple mating in fishes. Journal of Fish Biology 61, 739–750.
| Assessing the statistical power of genetic analyses to detect multiple mating in fishes.Crossref | GoogleScholarGoogle Scholar |
Nevill, J. E. G., Bamboche, D., and Philoe, H. (2014). Record litter size for the bull shark, Carcharhinus leucas (Muller & Henle, 1839), documented in the Seychelles. Western Indian Ocean Journal of Marine Science 12, 85.
Nosal, A. P., Lewallen, E. A., and Burton, R. S. (2013). Multiple paternity in leopard shark (Triakis semifasciata) litters sampled from a predominantly female aggregation in La Jolla, California, USA. Journal of Experimental Marine Biology and Ecology 446, 110–114.
| Multiple paternity in leopard shark (Triakis semifasciata) litters sampled from a predominantly female aggregation in La Jolla, California, USA.Crossref | GoogleScholarGoogle Scholar |
Ortego, J., Aparicio, J. M., Cordero, P. J., and Calabuig, G. (2008). Characteristics of loci and individuals are associated with germline microsatellite mutation rates in lesser kestrels (Falco naumanni). Mutation Research. Fundamental and Molecular Mechanisms of Mutagenesis 648, 82–86.
| Characteristics of loci and individuals are associated with germline microsatellite mutation rates in lesser kestrels (Falco naumanni).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWmtL%2FN&md5=bdccd94b44a426aa7141a69e14d9a55dCAS | 18973763PubMed |
Parsons, G. R., Hoffmayer, E. R., Frank, J., and Bet-Sayad, W. V. (2008). A review of shark reproductive ecology: life history and evolutionary implications. In ‘Fish Reproduction’, 1st edn. (Eds M. J. Rocha, A. Aruke and B. G. Kapoor.) pp. 435–469. (CRC Press: Boca Raton, FL, USA.)
Pattillo, M. E., Czapla, T. E., Nelson, D. M., and Monaco, M. E. (1997). ‘Distribution and Abundance of Fisheries and Invertebrates in Gulf of Mexico Estuaries, Volume 2: Species Life History Summaries.’ ELMR Report 11. (NOAA/NOSS Strategic Environmental Assessments Division: Silver Spring, MD, USA.)
Pirog, A., Blaison, A., Jaquemet, S., Soria, M., and Magalon, H. (2015). Isolation and characterization of 20 microsatellite markers from Carcharhinus leucas (bull shark) and cross-amplification in Galeocerdo cuvier (tiger shark), Carcharhinus obscurus (dusky shark) and Carcharhinus plumbeus (sandbar shark). Conservation Genetics Resources 7, 121–124.
| Isolation and characterization of 20 microsatellite markers from Carcharhinus leucas (bull shark) and cross-amplification in Galeocerdo cuvier (tiger shark), Carcharhinus obscurus (dusky shark) and Carcharhinus plumbeus (sandbar shark).Crossref | GoogleScholarGoogle Scholar |
Portnoy, D. S., Piercy, A. N., Musick, J. A., Burgess, G. H., and Graves, J. E. (2007). Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico. Molecular Ecology 16, 187–197.
| Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1Cltbc%3D&md5=c1d61b5e7e57493dd6beca0fbdf8d8eeCAS | 17181730PubMed |
Portnoy, D. S., Hollenbeck, C. M., Johnston, J. S., Casman, H. M., and Gold, J. R. (2014). Parthenogenesis in a whitetip reef shark Triaenodon obesus involves a reduction in ploidy. Journal of Fish Biology 85, 502–508.
| Parthenogenesis in a whitetip reef shark Triaenodon obesus involves a reduction in ploidy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cjps1Wkuw%3D%3D&md5=1df0d2e2b276d295eec855ce1eb3daa8CAS | 24905881PubMed |
Pratt, H. L., and Carrier, J. C. (2001). A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environmental Biology of Fishes 60, 157–188.
| A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum.Crossref | GoogleScholarGoogle Scholar |
Rowe, L. (1992). Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Animal Behaviour 44, 189–202.
| Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration.Crossref | GoogleScholarGoogle Scholar |
Rowe, S., and Hutchings, J. A. (2003). Mating systems and the conservation of commercially exploited marine fish. Trends in Ecology & Evolution 18, 567–572.
| Mating systems and the conservation of commercially exploited marine fish.Crossref | GoogleScholarGoogle Scholar |
Simpfendorfer, C., and Burgess, G. H. (2009). Carcharhinus leucas (Bull Shark). In ‘The IUCN Red List of Threatened Species’, ver. 2015.1. (International Union for Conservation of Nature and Natural Resources.) Available at http://www.iucnredlist.org/details/39372/0 [Verified 1 May 2015].
Simpfendorfer, C. A., Freitas, G. G., Wiley, T. R., and Heupel, M. R. (2005). Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a southwest Florida estuary. Estuaries 28, 78–85.
| Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a southwest Florida estuary.Crossref | GoogleScholarGoogle Scholar |
Smith, S. E., Au, D. W., and Show, C. (1998). Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678.
| Intrinsic rebound potentials of 26 species of Pacific sharks.Crossref | GoogleScholarGoogle Scholar |
Sugg, D. W., and Chesser, R. K. (1994). Effective population sizes with multiple paternity. Genetics 137, 1147–1155.
| 1:STN:280:DyaK2M%2FntlKjsw%3D%3D&md5=44d8a48dabc20748c0e67db51c02830aCAS | 7982568PubMed |
Thiel, M., and Hinojosa, I. A. (2003). Mating behavior of female rock shrimp Rhynchocinetes typus (Decapoda: Caridea): indication for convenience polyandry and cryptic female choice. Behavioral Ecology and Sociobiology 55, 113–121.
| Mating behavior of female rock shrimp Rhynchocinetes typus (Decapoda: Caridea): indication for convenience polyandry and cryptic female choice.Crossref | GoogleScholarGoogle Scholar |
Thonhauser, K. E., Thoß, M., Musolf, K., Klaus, T., and Penn, D. J. (2014). Multiple paternity in wild house mice (Mus musculus musculus): effects on offspring genetic diversity and body mass. Ecology and Evolution 4, 200–209.
| Multiple paternity in wild house mice (Mus musculus musculus): effects on offspring genetic diversity and body mass.Crossref | GoogleScholarGoogle Scholar | 24558575PubMed |
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 | 1:STN:280:DC%2BC38jgs1SjsA%3D%3D&md5=8d7e6ed6c8e439d9e32428b232d8ce43CAS | 22551174PubMed |
Whitney, N. M., Pratt, H. L., and Carrier, J. C. (2004). Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus. Animal Behaviour 68, 1435–1442.
| Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus.Crossref | GoogleScholarGoogle Scholar |
Wintner, S. P., Dudley, S. F. J., Kistnasamy, N., and Everett, B. (2002). Age and growth estimates for the Zambezi shark, Carcharhinus leucas, from the east coast of South Africa. Environmental Biology of Fishes 53, 557–566.
| Age and growth estimates for the Zambezi shark, Carcharhinus leucas, from the east coast of South Africa.Crossref | GoogleScholarGoogle Scholar |
Wolff, J. O., and Macdonald, D. W. (2004). Promiscuous females protect their offspring. Trends in Ecology & Evolution 19, 127–134.
| Promiscuous females protect their offspring.Crossref | GoogleScholarGoogle Scholar |
Worm, B., Davis, B., Kettemer, L., Ward-Paige, C. A., Chapman, D., Heithaus, M. R., Kessel, S. T., and Gruber, S. H. (2013). Global catches, exploitation rates, and rebuilding options for sharks. Marine Policy 40, 194–204.
| Global catches, exploitation rates, and rebuilding options for sharks.Crossref | GoogleScholarGoogle Scholar |
Zeh, J. A., and Zeh, D. W. (1997). The evolution of polyandry II: post-copulatory defenses against genetic incompatibility. Proceedings of the Royal Society of London – B. Biological Sciences 264, 69–75.
| The evolution of polyandry II: post-copulatory defenses against genetic incompatibility.Crossref | GoogleScholarGoogle Scholar |
Zeh, J. A., and Zeh, D. W. (2001). Reproductive mode and the genetic benefits of polyandry. Animal Behaviour 61, 1051–1063.
| Reproductive mode and the genetic benefits of polyandry.Crossref | GoogleScholarGoogle Scholar |