Skip to main content
Log in

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

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

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.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ankel WF (1925) Zur befruchtungsfrage bei Viviparus viviparus L. nebst bemerkungen uber die erste reifungsteilung des Eies. Senckenbergiana 7:37–54

    Google Scholar 

  • Avise JC (1996) Three fundamental contributions of molecular genetics to avian ecology and evolution. Ibis 138:16–25

    Article  Google Scholar 

  • Avise JC (ed) (2001) DNA-based profiling of genetic mating systems and reproductive behaviors in poikilothermic vertebrates. J Hered (special issue) 92:99–211

    Google Scholar 

  • 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 36:19–45

    Article  CAS  Google Scholar 

  • 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 271:641–646

    Article  CAS  Google Scholar 

  • Birkhead TR, Møller AP (eds) (1992) Sperm competition in birds. Academic, London

  • 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 267:1107–1113

    Article  CAS  Google Scholar 

  • Brockmann HJ, Nguyen C, Potts W (2000) Paternity in horseshoe crabs when spawning in multiple-male groups. Anim Behav 60:837–849

    Article  CAS  Google Scholar 

  • 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 210:161–165

    Article  Google Scholar 

  • Burton RS (1985) Mating system of the intertidal copepod Tigriopus californicus. Mar Biol 86:247–252

    Article  Google Scholar 

  • 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 13:581–585

    Google Scholar 

  • 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 70:501–512

    Article  Google Scholar 

  • 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 10:1265–1278

    Article  CAS  Google Scholar 

  • Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, London

    Google Scholar 

  • Gaffney PM, McGee B (1992) Multiple paternity in Crepidula fornicata (Linnaeus). Veliger 35:12–15

    Google Scholar 

  • Gloor G, Engels W (1992) Single-fly preps for PCR. Drosoph Inf Serv 71:148–149

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  CAS  Google Scholar 

  • Halliday T, Arnold SJ (1987) Multiple mating by females: a perspective from quantitative genetics. Anim Behav 35:939–941

    Article  Google Scholar 

  • Jones AG (2003) GERUD 1.0: a computer program for the reconstruction of parental genotypes from progeny arrays using multilocus DNA data. Mol Ecol 1:215–218

    Article  Google Scholar 

  • 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 6:203–213

    Article  CAS  Google Scholar 

  • Jones AG, Rosenqvist G, Berglund A, Avise JC (1999) Clustered microsatellite mutations in the pipefish Syngnathus typhle. Genetics 152:1057–1063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kellogg KA, Markert JA, Stauffer JR, Kocher TD (1998) Intraspecific brood mixing and reduced polyandry in a maternal mouth-brooding cichlid. Behav Ecol 9:309–312

    Article  Google Scholar 

  • 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 96:27–42

    Article  Google Scholar 

  • Murray J (1964) Multiple mating and effective population size in Cepaea nemoralis. Evolution 18:283–291

    Article  Google Scholar 

  • 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 12:485–492

    Article  CAS  Google Scholar 

  • Paterson IG, Partridge V, Buckland-Nicks JB (2001) Multiple paternity in Littorina obtusata (Gastropoda, Littorinidae) revealed by microsatellite analysis. Biol Bull 200:261–267

    Article  CAS  Google Scholar 

  • 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 10:2711–2718

    Article  CAS  Google Scholar 

  • 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 81:243–250

    Article  Google Scholar 

  • 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 21:769–775

    Google Scholar 

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

    Article  Google Scholar 

  • Reed SE (1995) Reproductive anatomy and biology of the genus Strombus in the Caribbean. II. Females. J Shellfish Res 14:331–336

    Google Scholar 

  • Rogers DW, Chase R (2002) Determinants of paternity in the garden snail Helix aspersa. Behav Ecol Sociobiol 52:289–295

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Selvin S (1980) Probability of nonpaternity determined by multiple allele codominant systems. Am J Hum Genet 32:276–278

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 160:279–282

    Article  Google Scholar 

  • 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. 341–434

    Chapter  Google Scholar 

  • Smith RL (ed) (1984) Sperm competition and the evolution of animal mating systems. Academic, New York

  • Sokal RR, Rohlf FJ (1969) Biometry. W.H. Freeman and Co., San Francisco

    Google Scholar 

  • 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 55:1104–1113

    Article  Google Scholar 

  • 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 11:2115–2122

    Article  CAS  Google Scholar 

  • Walker D, Power AJ, Avise JC (2005) Sex-linked markers facilitate genetic parentage analyses in knobbed whelk broods. J Hered 96:1–6

    Article  Google Scholar 

  • Westneat DF, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369

    Google Scholar 

  • Woodruff RC, Thompson JN Jr (1992) Have premeiotic clusters of mutation been overlooked in evolutionary theory? J Evol Biol 5:457–464

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to DeEtte Walker.

Additional information

Communicated by P.W. Sammarco, Chauvin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Walker, D., Power, A.J., Sweeney-Reeves, M. et al. Multiple paternity and female sperm usage along egg-case strings of the knobbed whelk, Busycon carica (Mollusca; Melongenidae). Mar Biol 151, 53–61 (2007). https://doi.org/10.1007/s00227-006-0463-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0463-5

Keywords

Navigation