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Marine Biology

, Volume 151, Issue 1, pp 53–61 | Cite as

Multiple paternity and female sperm usage along egg-case strings of the knobbed whelk, Busycon carica (Mollusca; Melongenidae)

  • DeEtte Walker
  • Alan J. Power
  • Mary Sweeney-Reeves
  • John C. Avise
Research Article

Abstract

We used genotypic data from three highly polymorphic microsatellite loci (two autosomal and one sex-linked) to examine micro-spatial and temporal arrangements of genetic paternity for more than 1,500 embryos housed along 12 egg-case strings of the knobbed whelk, Busycon carica. Multiple paternity proved to be the norm in these single-dam families, with genetic contributions of several sires (at least 3.5 on average) being represented among embryos within individual egg capsules as well as along the string. Two strings were studied in much greater detail; five and seven fathers were identified, none of which was among the several males found in consort with the female at her time of egg-laying. Each deduced sire had fathered roughly constant proportions of embryos along most of the string, but those proportions differed consistently among fathers. A few significant paternity shifts at specifiable positions along an egg-case string were also observed. Although the precise physical mechanisms inside a female whelk’s reproductive tract remain unknown, our genetic findings indicate that successive fertilization events (and/or depositions of zygotes into egg capsules) normally occur as near-random draws from a well-but-not-perfectly blended pool of gametes (or zygotes) stemming from stored ejaculates, perhaps in different titers, of a dam’s several mates.

Keywords

Multiple Paternity Seminal Receptacle Sperm Storage Bursa Copulatrix Progeny Array 
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

Work was supported by a Pew Foundation Fellowship in Marine Conservation to JCA and by the Marine Extension Service to AJP. Rebecca Green, Dodie Thompson, and Randal Walker provided field assistance. John N. Kraeuter and an anonymous reviewer provided helpful comments that improved the manuscript greatly. All experiments comply with current US laws.

References

  1. Ankel WF (1925) Zur befruchtungsfrage bei Viviparus viviparus L. nebst bemerkungen uber die erste reifungsteilung des Eies. Senckenbergiana 7:37–54Google Scholar
  2. Avise JC (1996) Three fundamental contributions of molecular genetics to avian ecology and evolution. Ibis 138:16–25CrossRefGoogle Scholar
  3. Avise JC (ed) (2001) DNA-based profiling of genetic mating systems and reproductive behaviors in poikilothermic vertebrates. J Hered (special issue) 92:99–211Google Scholar
  4. Avise JC, Jones AG, Walker D, et al (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45CrossRefGoogle Scholar
  5. Avise JC, Power AJ, Walker D (2004) Genetic sex determination, gender identification, and pseudohermaphroditism in the knobbed whelk, Busycon carica (Mollusca; Melongenidae). Proc R Soc Lond B 271:641–646CrossRefGoogle Scholar
  6. Birkhead TR, Møller AP (eds) (1992) Sperm competition in birds. Academic, LondonGoogle Scholar
  7. Bishop JDD, Pemberton AJ, Noble LR (2000) Sperm precedence in a novel context: mating in a sessile marine invertebrate with dispersing sperm. Proc R Soc Lond B 267:1107–1113CrossRefGoogle Scholar
  8. Brockmann HJ, Nguyen C, Potts W (2000) Paternity in horseshoe crabs when spawning in multiple-male groups. Anim Behav 60:837–849CrossRefGoogle Scholar
  9. Buresch KM, Hanlon RT, Maxwell MR, Ring S (2001) Microsatellite DNA markers indicate a high frequency of multiple paternity within individual field-collected egg capsules of the squid Loligo pealeii. Mar Ecol Prog Ser 210:161–165CrossRefGoogle Scholar
  10. Burton RS (1985) Mating system of the intertidal copepod Tigriopus californicus. Mar Biol 86:247–252CrossRefGoogle Scholar
  11. Castagna M, Kraeuter JN (1994) Age, growth rate, sexual dimorphism and fecundity of knobbed whelk Busycon carica (Gmelin 1791) in a western mid-Atlantic lagoon system, Virginia. J Shellfish Res 13:581–585Google Scholar
  12. Coe WR (1942) The reproductive organs of the prosobranch mollusk Crepidula onyx and their transformation during the change from male to female phase. J Morphol 70:501–512CrossRefGoogle Scholar
  13. Emery AM, Wilson IJ, Craig S, Boyle PR, Noble LR (2001) Assignment of paternity groups without access to parental genotypes: multiple mating and developmental plasticity in squid. Mol Ecol 10:1265–1278CrossRefGoogle Scholar
  14. Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, LondonGoogle Scholar
  15. Gaffney PM, McGee B (1992) Multiple paternity in Crepidula fornicata (Linnaeus). Veliger 35:12–15Google Scholar
  16. Gloor G, Engels W (1992) Single-fly preps for PCR. Drosoph Inf Serv 71:148–149Google Scholar
  17. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372CrossRefGoogle Scholar
  18. Halliday T, Arnold SJ (1987) Multiple mating by females: a perspective from quantitative genetics. Anim Behav 35:939–941CrossRefGoogle Scholar
  19. Jones AG (2003) GERUD 1.0: a computer program for the reconstruction of parental genotypes from progeny arrays using multilocus DNA data. Mol Ecol 1:215–218CrossRefGoogle Scholar
  20. Jones AG, Avise JC (1997) Microsatellite analysis of maternity and the mating system in the Gulf pipefish, Syngnathus scovelli, a species with male pregnancy and sex-role reversal. Mol Ecol 6:203–213CrossRefGoogle Scholar
  21. Jones AG, Rosenqvist G, Berglund A, Avise JC (1999) Clustered microsatellite mutations in the pipefish Syngnathus typhle. Genetics 152:1057–1063PubMedPubMedCentralGoogle Scholar
  22. Kellogg KA, Markert JA, Stauffer JR, Kocher TD (1998) Intraspecific brood mixing and reduced polyandry in a maternal mouth-brooding cichlid. Behav Ecol 9:309–312CrossRefGoogle Scholar
  23. Martel A, Larrivee D, Himmelman J (1986) Behaviour and timing of copulation and egg-laying in the neogastropod Buccinum undatum L. J Exp Mar Biol Ecol 96:27–42CrossRefGoogle Scholar
  24. Murray J (1964) Multiple mating and effective population size in Cepaea nemoralis. Evolution 18:283–291CrossRefGoogle Scholar
  25. Oppliger A, Naciti-Graven Y, Ribi G, Hosken DJ (2003) Sperm length influences fertilization success during sperm competition in the snail Viviparus ater. Mol Ecol 12:485–492CrossRefGoogle Scholar
  26. Paterson IG, Partridge V, Buckland-Nicks JB (2001) Multiple paternity in Littorina obtusata (Gastropoda, Littorinidae) revealed by microsatellite analysis. Biol Bull 200:261–267CrossRefGoogle Scholar
  27. Pearse DE, Eckerman CM, Janzen FJ, Avise JC (2001) A genetic analogue of ‘mark-recapture’ methods for estimating population size: an approach based on molecular parentage assessments. Mol Ecol 10:2711–2718CrossRefGoogle Scholar
  28. Power AJ, Keegan BF (2001) Seasonal patterns in the reproductive activity of the red whelk, Neptunea antiqua (Mollusca: Prosobranchia) in the Irish Sea. J Mar Biol Assoc UK 81:243–250CrossRefGoogle Scholar
  29. Power AJ, Covington E, Recicar T, Walker RL, Eller N (2002) Observations on the egg capsules and hatchlings of the knobbed whelk, Busycon carica (Gmelin, 1791) in coastal Georgia. J Shellfish Res 21:769–775Google Scholar
  30. Raymond M, Rousset F (1995) GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  31. Reed SE (1995) Reproductive anatomy and biology of the genus Strombus in the Caribbean. II. Females. J Shellfish Res 14:331–336Google Scholar
  32. Rogers DW, Chase R (2002) Determinants of paternity in the garden snail Helix aspersa. Behav Ecol Sociobiol 52:289–295CrossRefGoogle Scholar
  33. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  34. Selvin S (1980) Probability of nonpaternity determined by multiple allele codominant systems. Am J Hum Genet 32:276–278PubMedPubMedCentralGoogle Scholar
  35. Shaw PW, Boyle PR (1997) Multiple paternity within the brood of single females of Loligo forbesi (Cephalopoda: Loliginidae), demonstrated with microsatellite DNA markers. Mar Ecol Prog Ser 160:279–282CrossRefGoogle Scholar
  36. Simmons LW, Siva-Jothy MT (1998) Sperm competition in insects: mechanisms and the potential for selection. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp. 341–434CrossRefGoogle Scholar
  37. Smith RL (ed) (1984) Sperm competition and the evolution of animal mating systems. Academic, New YorkGoogle Scholar
  38. Sokal RR, Rohlf FJ (1969) Biometry. W.H. Freeman and Co., San FranciscoGoogle Scholar
  39. Urbani N, Sainte-Marie B, Sévigny J-M, Zadworthy D, Kuhnlein U (1998) Sperm competition and paternity assurance during the first breeding period of female snow crab (Chionoecetes opilio) (Brachyura: Majidae). Can J Fish Aquat Sci 55:1104–1113CrossRefGoogle Scholar
  40. Walker D, Porter BA, Avise JC (2002) Genetic parentage assessment in the crayfish Orconectes placidus, a high-fecundity invertebrate with extended maternal brood care. Mol Ecol 11:2115–2122CrossRefGoogle Scholar
  41. Walker D, Power AJ, Avise JC (2005) Sex-linked markers facilitate genetic parentage analyses in knobbed whelk broods. J Hered 96:1–6CrossRefGoogle Scholar
  42. Westneat DF, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369Google Scholar
  43. Woodruff RC, Thompson JN Jr (1992) Have premeiotic clusters of mutation been overlooked in evolutionary theory? J Evol Biol 5:457–464CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • DeEtte Walker
    • 1
  • Alan J. Power
    • 2
  • Mary Sweeney-Reeves
    • 2
  • John C. Avise
    • 3
  1. 1.Georgia Institute of Technology AtlantaUSA
  2. 2.Marine Extension ServiceUniversity of GeorgiaSavannahUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA

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