Advertisement

Marine Biology

, Volume 159, Issue 4, pp 749–756 | Cite as

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

  • Rosemary J. ByrneEmail author
  • John C. Avise
Original Paper

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.

Keywords

Clutch Size Multiple Mating Multiple Paternity Female Fitness Female Body Size 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

References

  1. Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  2. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368CrossRefGoogle Scholar
  3. Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299:389–392CrossRefGoogle Scholar
  4. Birkhead T (2000) Promiscuity—an evolutionary history of sperm competition. Harvard University Press, CambridgeGoogle Scholar
  5. Birkhead T, Moller AP (1998) Sperm competition and sexual selection. Academic Press, LondonGoogle Scholar
  6. 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 13:3261–3273CrossRefGoogle Scholar
  7. Carrier JC, Pratt HL, Martin LK (1994) Group reproductive behaviors in free-living nurse sharks, Ginglymostoma cirratum. Copeia 1994:646–656CrossRefGoogle Scholar
  8. Castro JI (1983) The sharks of North American waters. A&M University Press, College StationGoogle Scholar
  9. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47CrossRefGoogle Scholar
  10. 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 13:1965–1974CrossRefGoogle Scholar
  11. Chesser RK, Baker RJ (1996) Effective sizes and dynamics of uniparentally and diparentally inherited genes. Genetics 114:1225–1235Google Scholar
  12. Chevolot M, Ellis JR, Rijnsdorp AD, Stam WT, Olsen JL (2007) Multiple paternity analysis in the thornback ray Raja clavata L. J Hered 98:712–715CrossRefGoogle Scholar
  13. Compagno LJV (1984) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2. FAO Fish Synop 125:410–412Google Scholar
  14. Conrath CL, Musick JA (2002) Reproductive biology of the smooth dogfish, Mustelus canis, in the northwest Atlantic Ocean. Environ Biol Fish 64:367–377CrossRefGoogle Scholar
  15. Cortés E (2000) Life history patterns and correlations in sharks. Rev Fish Sci 8:299–344Google Scholar
  16. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509CrossRefGoogle Scholar
  17. 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 76:419–424CrossRefGoogle Scholar
  18. 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 403:225–267CrossRefGoogle Scholar
  19. 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 17:783–795CrossRefGoogle Scholar
  20. 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 17:3337–3351CrossRefGoogle Scholar
  21. Dodd JM (1983) Reproduction in cartilaginous fishes (Chondrichthyes). In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol 9A. New York, Academic PressGoogle Scholar
  22. 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 77:1505–1525CrossRefGoogle Scholar
  23. Feldheim KA, Gruber SH, Ashley MV (2001) Multiple paternity of a lemon shark litter (Chondrichthyes: Carcharhinidae). Copeia 2001:781–786CrossRefGoogle Scholar
  24. Feldheim KA, Gruber SH, Ashley MV (2004) Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58:2332–2342Google Scholar
  25. 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 27:500–507Google Scholar
  26. Harvey PH, May RM (1989) Out for the sperm count. Nature 337:508–509CrossRefGoogle Scholar
  27. Hauswaldt JS, Glenn TC (2003) Miccrosatellite DNA loci from the diamondback terrapin (Malaclemys terrapin). Mol Ecol Notes 3:174–176CrossRefGoogle Scholar
  28. Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612CrossRefGoogle Scholar
  29. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64CrossRefGoogle Scholar
  30. 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 5:708–711CrossRefGoogle Scholar
  31. Karl SA (2008) The effect of multiple paternity on the genetically effective size of a population. Mol Ecol 17:3973–3977CrossRefGoogle Scholar
  32. Keller L, Reeve HK (1995) Why do females mate with multiple males: the sexually selected sperm hypothesis. Adv Stud Behav 24:291–315CrossRefGoogle Scholar
  33. Klimley AP (1985) Schooling in the large predator, Sphyrna lewini, a species with low risk of predation: a non-egalitarian state. Z Tierpsychol 70:297–319Google Scholar
  34. 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 73:2068–2074CrossRefGoogle Scholar
  35. Manire CA, Gruber SH (1990) Many sharks may be headed toward extinction. Conserv Biol 4:10–11CrossRefGoogle Scholar
  36. Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155CrossRefGoogle Scholar
  37. Musick JA, Burgess G, Cailliet G, Camhi M, Fordham S (2000) Management of sharks and their relatives (Elasmobranchii). Fisheries 25:9–13CrossRefGoogle Scholar
  38. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283CrossRefGoogle Scholar
  39. Neff BD, Pitcher TE (2002) Assessing the statistical power of genetic analyses to detect multiple mating in fishes. J Fish Biol 61:739–750CrossRefGoogle Scholar
  40. Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341CrossRefGoogle Scholar
  41. Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252CrossRefGoogle Scholar
  42. 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 73:782–792CrossRefGoogle Scholar
  43. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58CrossRefGoogle Scholar
  44. 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 16:187–197CrossRefGoogle Scholar
  45. Pratt HL Jr (1993) The storage of spermatozoa in the oviducal glands of western North Atlantic sharks. Environ Biol Fish 38:139–149CrossRefGoogle Scholar
  46. 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 60:157–188CrossRefGoogle Scholar
  47. Ramakrishnan U, Storz JF, Taylor BL, Lande R (2004) Estimation of genetically effective breeding numbers using a rejection algorithm approach. Mol Ecol 13:3283–3292CrossRefGoogle Scholar
  48. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  49. Rowe S, Hutchings JA (2003) Mating systems and the conservation of commercially exploited marine fish. Trends Ecol Evol 18:567–572CrossRefGoogle Scholar
  50. Saville KJ, Lindley AM, Maries EG, Carrier JC, Pratt HL (2002) Multiple paternity in the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 63:347–351CrossRefGoogle Scholar
  51. 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 2:117–124CrossRefGoogle Scholar
  52. 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 16:624–634CrossRefGoogle Scholar
  53. Smith SE, Au DW, Show C (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Mar Freshw Res 49:663–678CrossRefGoogle Scholar
  54. 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 269:1308–1324CrossRefGoogle Scholar
  55. Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155Google Scholar
  56. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027CrossRefGoogle Scholar
  57. Van Oosterhout C, Hutchinson WF, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  58. 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 102:88–93CrossRefGoogle Scholar
  59. Watson PJ (1991) Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linphia litigosa (Linyphiidae). Anim Behav 41:343–360CrossRefGoogle Scholar
  60. Whitney NM, Pratt HL, Carrier JC (2004) Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus. Anim Behav 68:1435–1442CrossRefGoogle Scholar
  61. Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Amer Zool 17:379–410Google Scholar
  62. Yasui Y (1998) The “genetic benefits” of female multiple mating reconsidered. Trends Ecol Evol 13:246–250CrossRefGoogle Scholar
  63. Zeh JA, Zeh DW (1996) The evolution of polyandry I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717CrossRefGoogle Scholar
  64. Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc Lond B 264:69–75CrossRefGoogle Scholar
  65. Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063CrossRefGoogle Scholar
  66. Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary Biology, 321 Steinhaus HallUniversity of California, IrvineIrvineUSA

Personalised recommendations