Skip to main content
Log in

Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Although an understanding of mating systems is thought to be an important component of long-term population management, these life history characteristics are poorly known in sharks. Here, we employ polymorphic microsatellite markers to test for the occurrence and prevalence of multiple paternity in a population of the brown smoothhound shark, Mustelus henlei. We analyzed litters from 14 females sampled from the Pacific coast of Baja California Sur. The minimum number of sires ranged from one to three with an average of 2.3 sires per litter. Regression analyses did not indicate a relationship between female body size and number of sires, or female body size and size of the litter. A review of the existing literature on genetic mating systems in sharks suggests that polyandry may be common and that reproductive behavior may have evolved from conflicting selection pressures between the sexes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  Google Scholar 

  • Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299:389–392

    Article  CAS  Google Scholar 

  • Birkhead T (2000) Promiscuity—an evolutionary history of sperm competition. Harvard University Press, Cambridge

    Google Scholar 

  • Birkhead T, Moller AP (1998) Sperm competition and sexual selection. Academic Press, London

    Google Scholar 

  • Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273

    Article  CAS  Google Scholar 

  • Carrier JC, Pratt HL, Martin LK (1994) Group reproductive behaviors in free-living nurse sharks, Ginglymostoma cirratum. Copeia 1994:646–656

    Article  Google Scholar 

  • Castro JI (1983) The sharks of North American waters. A&M University Press, College Station

    Google Scholar 

  • Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47

    Article  Google Scholar 

  • Chapman DD, Prodohl PA, Gelsleichter J, Manire CA, Shivji MS (2004) Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation. Mol Ecol 13:1965–1974

    Article  CAS  Google Scholar 

  • Chesser RK, Baker RJ (1996) Effective sizes and dynamics of uniparentally and diparentally inherited genes. Genetics 114:1225–1235

    Google Scholar 

  • Chevolot M, Ellis JR, Rijnsdorp AD, Stam WT, Olsen JL (2007) Multiple paternity analysis in the thornback ray Raja clavata L. J Hered 98:712–715

    Article  CAS  Google Scholar 

  • Compagno LJV (1984) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2. FAO Fish Synop 125:410–412

    Google Scholar 

  • Conrath CL, Musick JA (2002) Reproductive biology of the smooth dogfish, Mustelus canis, in the northwest Atlantic Ocean. Environ Biol Fish 64:367–377

    Article  Google Scholar 

  • Cortés E (2000) Life history patterns and correlations in sharks. Rev Fish Sci 8:299–344

    Google Scholar 

  • Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

    Article  CAS  Google Scholar 

  • Daly-Engel TS, Grubbs RD, Holland KN, Toonen RJ, Bowen BW (2006) Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii. Environ Biol Fish 76:419–424

    Article  Google Scholar 

  • Daly-Engel TS, Grubbs RD, Feldheim KA, Bowen BW, Toonen RJ (2010) Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog Squalus mitsukurii. Mar Ecol Prog Ser 403:225–267

    Article  Google Scholar 

  • DiBattista JD, Feldheim KA, Gruber SH, Hendry AP (2008a) Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Mol Ecol 17:783–795

    Article  Google Scholar 

  • DiBattista JD, Feldheim KA, Thibert-Plante X, Gruber SH, Hendry AP (2008b) A genetic assessment of polyandry and breeding-site fidelity in lemon sharks. Mol Ecol 17:3337–3351

    Article  Google Scholar 

  • Dodd JM (1983) Reproduction in cartilaginous fishes (Chondrichthyes). In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol 9A. New York, Academic Press

    Google Scholar 

  • Farrell ED, Mariani S, Clarke MW (2010) Reproductive biology of the starry smooth hound shark Mustelus asterias: geographic variation and implications for sustainable exploitation. J Fish Biol 77:1505–1525

    Article  CAS  Google Scholar 

  • Feldheim KA, Gruber SH, Ashley MV (2001) Multiple paternity of a lemon shark litter (Chondrichthyes: Carcharhinidae). Copeia 2001:781–786

    Article  Google Scholar 

  • Feldheim KA, Gruber SH, Ashley MV (2004) Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58:2332–2342

    CAS  Google Scholar 

  • Hamilton MB, Pincus EL, Di Fiore A, Flescher RC (1999) Universal linker and ligation procedures for construction of genomic DNA libraries enriched for microsatellites. Biotechniques 27:500–507

    CAS  Google Scholar 

  • Harvey PH, May RM (1989) Out for the sperm count. Nature 337:508–509

    Article  CAS  Google Scholar 

  • Hauswaldt JS, Glenn TC (2003) Miccrosatellite DNA loci from the diamondback terrapin (Malaclemys terrapin). Mol Ecol Notes 3:174–176

    Article  CAS  Google Scholar 

  • Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612

    Article  CAS  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  CAS  Google Scholar 

  • Jones AG (2005) GERUD 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known and unknown parents. Mol Ecol Notes 5:708–711

    Article  CAS  Google Scholar 

  • Karl SA (2008) The effect of multiple paternity on the genetically effective size of a population. Mol Ecol 17:3973–3977

    Article  Google Scholar 

  • Keller L, Reeve HK (1995) Why do females mate with multiple males: the sexually selected sperm hypothesis. Adv Stud Behav 24:291–315

    Article  Google Scholar 

  • Klimley AP (1985) Schooling in the large predator, Sphyrna lewini, a species with low risk of predation: a non-egalitarian state. Z Tierpsychol 70:297–319

    Google Scholar 

  • Lage CR, Petersen CW, Forest D, Barnes D, Kornfield I, Wray C (2008) Evidence of multiple paternity in spiny dogfish (Squalus acanthias) broods based on microsatellite analysis. J Fish Biol 73:2068–2074

    Article  Google Scholar 

  • Manire CA, Gruber SH (1990) Many sharks may be headed toward extinction. Conserv Biol 4:10–11

    Article  Google Scholar 

  • Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155

    Article  CAS  Google Scholar 

  • Musick JA, Burgess G, Cailliet G, Camhi M, Fordham S (2000) Management of sharks and their relatives (Elasmobranchii). Fisheries 25:9–13

    Article  Google Scholar 

  • Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283

    Article  CAS  Google Scholar 

  • Neff BD, Pitcher TE (2002) Assessing the statistical power of genetic analyses to detect multiple mating in fishes. J Fish Biol 61:739–750

    Article  Google Scholar 

  • Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341

    Article  Google Scholar 

  • Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252

    Article  CAS  Google Scholar 

  • Pérez-Jiménez JC, Sosa-Nishizaki O (2008) Reproductive biology of the brown smoothhound shark Mustelus henlei, in the northern Gulf of California, Mexico. J Fish Biol 73:782–792

    Article  Google Scholar 

  • Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58

    Article  CAS  Google Scholar 

  • Portnoy DS, Piercy AN, Musick JA, Burgess GH, Graves JE (2007) Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico. Mol Ecol 16:187–197

    Article  CAS  Google Scholar 

  • Pratt HL Jr (1993) The storage of spermatozoa in the oviducal glands of western North Atlantic sharks. Environ Biol Fish 38:139–149

    Article  Google Scholar 

  • Pratt HL Jr, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 60:157–188

    Article  Google Scholar 

  • Ramakrishnan U, Storz JF, Taylor BL, Lande R (2004) Estimation of genetically effective breeding numbers using a rejection algorithm approach. Mol Ecol 13:3283–3292

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Google Scholar 

  • Rowe S, Hutchings JA (2003) Mating systems and the conservation of commercially exploited marine fish. Trends Ecol Evol 18:567–572

    Article  Google Scholar 

  • Saville KJ, Lindley AM, Maries EG, Carrier JC, Pratt HL (2002) Multiple paternity in the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 63:347–351

    Article  Google Scholar 

  • Schmid JV, Chen C–C, Sheikh SI, Meekan MG, Norman BM, Joung S-J (2010) Paternity analysis in a litter of whale shark embryos. Endang Species Res 2:117–124

    Article  Google Scholar 

  • Simmons LW (2003) The evolution of polyandry: patterns of genotypic variation in female mating frequency, male fertilization success and a test of the sex-sperm hypothesis. J Evol Biol 16:624–634

    Article  CAS  Google Scholar 

  • Smith SE, Au DW, Show C (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Mar Freshw Res 49:663–678

    Article  Google Scholar 

  • Storrie MT, Walker TI, Laurenson LJ, Hamlett WC (2008) Microscopic organization of the sperm storage tubules in the oviducal gland of the female gummy shark (Mustelus antarcticus), with observations on sperm distribution and storage. J Morphol 269:1308–1324

    Article  Google Scholar 

  • Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155

    CAS  Google Scholar 

  • Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Veríssimo A, Grubbs D, McDowell J, Musick J, Portnoy D (2011) Frequency of multiple paternity in the spiny dogfish Squalus acanthias in the western north Atlantic. J Hered 102:88–93

    Article  Google Scholar 

  • Watson PJ (1991) Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linphia litigosa (Linyphiidae). Anim Behav 41:343–360

    Article  Google Scholar 

  • Whitney NM, Pratt HL, Carrier JC (2004) Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus. Anim Behav 68:1435–1442

    Article  Google Scholar 

  • Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Amer Zool 17:379–410

    Google Scholar 

  • Yasui Y (1998) The “genetic benefits” of female multiple mating reconsidered. Trends Ecol Evol 13:246–250

    Article  CAS  Google Scholar 

  • Zeh JA, Zeh DW (1996) The evolution of polyandry I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717

    Article  Google Scholar 

  • Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc Lond B 264:69–75

    Article  Google Scholar 

  • Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063

    Article  Google Scholar 

  • Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the American Museum of Natural History to RJB, by the National Science Foundation (NSF Grant DGE-0638751), and by the University of California, Irvine. We thank Felipe Galván-Magaña (Fish Ecology Laboratory at CICIMAR-IPN, La Paz, Baja California Sur, Mexico) and the commercial fishermen of Las Barrancas, Baja California Sur, Mexico, who kindly allowed sampling of their catches, as well as Andrey Tatarenkov and Jin-Xian Liu for thoughtful review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosemary J. Byrne.

Additional information

Communicated by T. Reusch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Byrne, R.J., Avise, J.C. Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Mar Biol 159, 749–756 (2012). https://doi.org/10.1007/s00227-011-1851-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1851-z

Keywords

Navigation