Skip to main content
Log in

Among- and within-population variation in sperm quality in the simultaneously hermaphroditic land snail Arianta arbustorum

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Sperm competition models on the evolution of sperm size assume associations with another sperm quality trait, sperm longevity. Sperm length can also provide an indication of possible mechanisms affecting motility and thus fertilization success. Despite their importance, however, detailed mechanisms of sperm competition at the gamete level are poorly understood. In simultaneously hermaphroditic land snails, sperm traits and cryptic female choice are assumed to be crucial in determining fertilization success. We examined the variation in sperm length and number among individuals from four natural populations of the land snail Arianta arbustorum, a species with multiple mating and long-term sperm storage. We also assessed variation in velocity, motility and longevity of sperm in snails from two of the four populations. Independent of shell size, sperm length differed among populations and, to a minor extent, even among individuals within populations. Mean sperm length of a snail was not correlated with the number of sperm delivered in a spermatophore. The mean sperm velocity (=VCL) did not differ between snails from two populations. However, VCL varied among snails. Percentage motility and longevity of sperm differed between snails from the two populations. No correlations were found between length, velocity, percentage motility and longevity of sperm. To conclude, individual snails differed in sperm quality, and this variation may partly explain the differential fertilization success between A. arbustorum snails. Moreover, our findings did not support the positive association between sperm length and longevity assumed by sperm competition models for internally fertilizing species.

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
Fig. 4

Similar content being viewed by others

References

  • Anderson WA, Personne P (1976) The molluscan spermatozoon: dynamic aspects of its structure and function. Am Zool 16:292–313

    Google Scholar 

  • Baer B, Schmid-Hempel P, Høeg JT, Boomsma JJ (2003) Sperm length, sperm storage and mating system characteristics in bumblebees. Insectes Soc 50:101–108

    Article  Google Scholar 

  • Baminger H, Haase M (2001) Spermatophore formation in the simultaneously hermaphroditic land snail Arianta arbustorum (Pulmonata: Stylommatophora: Helicidae). Neth J Zool 51:347–360

    Article  Google Scholar 

  • Baur B (1984) Shell size and growth rate differences for alpine populations of Arianta arbustorum (L.) (Pulmonata: Helicidae). Rev Suisse Zool 91:37–46

    Google Scholar 

  • Baur B (1988a) Repeated mating and female fecundity in the simultaneously hermaphroditic land snail Arianta arbustorum. Invertebr Reprod Dev 14:197–204

    Google Scholar 

  • Baur B (1988b) Population regulation in the land snail Arianta arbustorum: density effects on adult size, clutch size and incidence of egg cannibalism. Oecologia 77:390–394

    Article  Google Scholar 

  • Baur B (1990) Seasonal changes in clutch size, egg size and mode of oviposition in Arianta arbustorum L. (Gastropoda) from alpine populations. Zool Anz 225:253–264

    Google Scholar 

  • Baur B (1994) Multiple paternity and individual variation in sperm precedence in the simultaneously hermaphroditic land snail Arianta arbustorum. Behav Ecol Sociobiol 35:413–421

    Article  Google Scholar 

  • Baur B (1998) Sperm competition in molluscs. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 255–305

    Chapter  Google Scholar 

  • Baur B, Baur A (1992) Effect of courtship and repeated copulation on egg production in the simultaneously hermaphroditic land snail Arianta arbustorum. Invertebr Reprod Dev 21:201–206

    Google Scholar 

  • Baur B, Raboud C (1988) Life history of the land snail Arianta arbustorum along an altitudinal gradient. J Anim Ecol 57:71–87

    Article  Google Scholar 

  • Baur B, Locher R, Baur A (1998) Sperm allocation in the simultaneously hermaphroditic land snail Arianta arbustorum. Anim Behav 56:839–845

    Article  PubMed  Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London

    Google Scholar 

  • Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764

    Article  CAS  Google Scholar 

  • Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H (2005) Genetic effects on sperm design in the zebra finch. Nature 434:383–387

    Article  PubMed  CAS  Google Scholar 

  • Bojat NC, Haase M (2002) Sperm storage in the simultaneously hermaphroditic land snail Arianta arbustorum. J Zool 258:497–503

    Article  Google Scholar 

  • Bojat NC, Sauder U, Haase M (2001) The spermathecal epithelium, sperm and their interactions in the hermaphroditic land snail Arianta arbustorum (Pulmonata, Stylommatophora). Zoomorphology 120:149–157

    Article  Google Scholar 

  • Bressac C, Hauschteck-Jungen E (1996) Drosophila subobscura females preferentially select long sperm for storage and use. J Insect Physiol 42:323–328

    Article  CAS  Google Scholar 

  • Burness G, Casselman SJ, Schulte-Hostedde AI, Moyes CD, Montgomerie R (2004) Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav Ecol Sociobiol 56:65–70

    Article  Google Scholar 

  • Chen XF, Baur B (1993) The effect of multiple mating on female reproductive success in the simultaneously hermaphroditic land snail Arianta arbustorum. Can J Zool 71:2431–2436

    Article  Google Scholar 

  • Dohmen MR (1983) Gametogenesis. In: Wilbur KM (ed) The Mollusca, vol 3. Academic, Orlando, pp 1–48

    Google Scholar 

  • Froman D (2003) Deduction of a model for sperm storage in the oviduct of the domestic fowl (Gallus domesticus). Biol Reprod 69:248–253

    Article  PubMed  CAS  Google Scholar 

  • Froman DP, Feltmann AJ, Rhoads ML, Kirby JD (1999) Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus). Biol Reprod 61:400–405

    Article  PubMed  CAS  Google Scholar 

  • Froman DP, Pizzari T, Feltmann AJ, Castillo-Juarez H, Birkhead TR (2002) Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc R Soc Lond B 269:607–612

    Article  Google Scholar 

  • Gage MJG, Macfarlane C, Yeates S, Shackleton R, Parker GA (2002) Relationships between sperm morphometry and sperm motility in the Atlantic salmon. J Fish Biol 61:1528–1539

    Article  Google Scholar 

  • Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47

    PubMed  CAS  Google Scholar 

  • Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc R Soc Lond B 243:181–185

    Article  CAS  Google Scholar 

  • Hayashi F (1998) Sperm co-operation in the fishfly, Parachauliodes japonicus. Funct Ecol 12:347–350

    Article  Google Scholar 

  • Healy JM (1996) Molluscan sperm ultrastructure: correlation with taxonomic units within the Gastropoda, Cephalopoda and Bivalvia. In: Taylor J (ed) Origin and evolutionary radiation of the Mollusca. Oxford Univ Press, Oxford, pp 99–113

    Google Scholar 

  • Hellriegel B, Blanckenhorn WU (2002) Environmental influences on the gametic investment of yellow dung fly males. Evol Ecol 16:505–522

    Article  Google Scholar 

  • Hofmann E (1923) Über den Begattungsvorgang von Arianta arbustorum (L.). Jena Z Med Naturwiss 59:363–400

    Google Scholar 

  • Hosken DJ, Garner TWJ, Ward PI (2001) Sexual conflict selects for male and female reproductive characters. Curr Biol 11:489–493

    Article  PubMed  CAS  Google Scholar 

  • Joly D, Cariou ML, Lachaise D (1991) Can sperm competition explain sperm polymorphism in Drosophila teissieri? Evol Biol 5:25–44

    Google Scholar 

  • Karr TL, Pitnick S (1996) The ins and outs of fertilization. Nature 379:405–406

    Article  PubMed  CAS  Google Scholar 

  • Katz DF, Drobnis EZ (1990) Analysis and interpretation of the forces generated by spermatozoa. In: Bavister BD, Cummins J, Roldan ERS (eds) Fertilization in mammals. Serono Symposia, Norwell, MA, pp 125–137

    Google Scholar 

  • Kerney MP, Cameron RAD (1979) A field guide to the land snails of Britain and northwest Europe. Collins, London

    Google Scholar 

  • Kubo-Irie M, Irie M, Nakazawa T, Mohri H (2003) Ultrastructure and function of long and short sperm in Cicadidae (Hemiptera). J Insect Physiol 49:983–991

    Article  PubMed  CAS  Google Scholar 

  • Kupriyanova E, Havenhand JN (2002) Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa. Invertebr Reprod Dev 41:21–26

    Google Scholar 

  • LaMunyon CW, Ward S (2002) Evolution of larger sperm in response to experimentally increased sperm competition in Caenorhabditis elegans. Proc R Soc Lond B 269:1125–1128

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Lind H (1973) The functional significance of the spermatophore and the fate of spermatozoa in the genital tract of Helix pomatia (Gastropoda: Stylommatophora). J Zool 169:39–64

    Article  Google Scholar 

  • Locher R, Baur B (1997) A new technique to assess the number of spermatozoa in spermatophores of stylommatophoran gastropods. J Molluscan Stud 63:555–556

    Article  Google Scholar 

  • Locher R, Baur B (1999) Effects of intermating interval on spermatophore size and sperm number in the simultaneously hermaphroditic land snail Arianta arbustorum. Ethology 105:839–849

    Article  Google Scholar 

  • Locher R, Baur B (2000) Sperm delivery and egg production of the simultaneously hermaphroditic land snail Arianta arbustorum exposed to an increased sperm competition risk. Invertebr Reprod Dev 38:53–60

    Google Scholar 

  • Locher R, Baur B (2002) Nutritional stress changes sex-specific reproductive allocation in the simultaneously hermaphroditic land snail Arianta arbustorum. Funct Ecol 16:623-632

    Article  Google Scholar 

  • Meisenheimer J (1912) Die Weinbergschnecke: Helix pomatia L. Klinkhardt LW, Leipzig

    Google Scholar 

  • Michiels NK (1998) Mating conflicts and sperm competition in simultaneous hermaphrodites. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 219-254

    Chapter  Google Scholar 

  • Miller GT, Pitnick S (2002) Sperm–female coevolution in Drosophila. Science 298:1230–1233

    Article  PubMed  CAS  Google Scholar 

  • Moore PJ, Harris WE, Montrose VT, Levin D, Moore AJ (2004) Constraints on evolution and postcopulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58:1773–1780

    PubMed  Google Scholar 

  • Oppliger A, Naciri-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  PubMed  CAS  Google Scholar 

  • Parker GA (1993) Sperm competition games: sperm size and sperm number under adult control. Proc R Soc Lond B 253:245–254

    Article  CAS  Google Scholar 

  • Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 3–54

    Chapter  Google Scholar 

  • Parker GA, Begon ME (1993) Sperm competition games: sperm size and number under gametic control. Proc R Soc Lond B 253:255–262

    Article  CAS  Google Scholar 

  • Peng J, Chen S, Büsser S, Liu HF, Honegger T, Kubli E (2005) Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr Biol 15:207–213

    Article  PubMed  CAS  Google Scholar 

  • Pitnick S, Miller GT, Reagan J, Holland B (2001) Males’ evolutionary responses to experimental removal of sexual selection. Proc R Soc Lond B 268:1071–1080

    Article  CAS  Google Scholar 

  • Pitnick S, Miller GT, Schneider K, Markow TA (2003) Ejaculate-female coevolution in Drosophila mojavensis. Proc R Soc Lond B 270:1507–1512

    Article  Google Scholar 

  • Radwan J (1996) Intraspecific variation in sperm competition success in the bulb mite: a role for sperm size. Proc R Soc Lond B 263:855–859

    Article  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 

  • Romeis B (1989) Mikroskopische Technik. 17 edn. Urban und Schwarzenberg, München

    Google Scholar 

  • Scheiner SM, Gurevitch J (1993) Design and analysis of ecological experiments. Chapman & Hall, New York

    Google Scholar 

  • Schulte-Hostedde AI, Millar JS (2004) Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav Ecol Sociobiol 55:272–277

    Article  Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton Univ. Press, Princeton, NJ

    Google Scholar 

  • Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53

    Article  PubMed  Google Scholar 

  • Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149:933–954

    Article  PubMed  CAS  Google Scholar 

  • Thompson TE (1973) Euthyneuran and other molluscan spermatozoa. Malacologia 14:167–206

    Google Scholar 

  • Thurston LM, Watson PF, Holt WV (1999) Sources of variation in the morphological characteristics of sperm subpopulations assessed objectively by a novel automated sperm morphology analysis system. J Reprod Fertil 117:271–280

    Article  PubMed  CAS  Google Scholar 

  • Thurston LM, Watson PF, Mileham AJ, Holt WV (2001) Morphologically distinct sperm subpopulations defined by Fourier shape descriptors in fresh ejaculates correlate with variation in boar semen quality following cryopreservation. J Androl 22:382–394

    PubMed  CAS  Google Scholar 

  • Ward PI (1998) Intraspecific variation in sperm size characters. Heredity 80:655–659

    Article  PubMed  Google Scholar 

  • Zschokke S (2003) BioPictViewer+, v1.10 for Macintosh, University of Basel

Download references

Acknowledgements

We thank K. Beese, M. Dürrenberger (Microscope Centre, University of Basel), M. Haase, R. Locher, A. Wacker, and S. Zschokke for advice and help. We are grateful to C. De Geyter (Univ. Hospital Basel) for providing access to the IVOS-semen analysis system, and M. Fusco (Bauman Medical AG) for technical support. G. A. Armbruster, A. Baur, K. Beese, J. Mevi-Schütz, P. Stoll, S. Zschokke and an anonymous referee provided valuable comments on the manuscript. Financial support was received from the Swiss National Science Foundation. We declare that our study is in accordance with the current Swiss laws.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicole Minoretti.

Additional information

Communicated by P. Moore

Rights and permissions

Reprints and permissions

About this article

Cite this article

Minoretti, N., Baur, B. Among- and within-population variation in sperm quality in the simultaneously hermaphroditic land snail Arianta arbustorum . Behav Ecol Sociobiol 60, 270–280 (2006). https://doi.org/10.1007/s00265-006-0165-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0165-5

Keywords

Navigation