Piercing the partner's skin influences sperm uptake in the earthworm Lumbricus terrestris

  • Joris M. Koene
  • Tina Pförtner
  • Nico K. Michiels
Original Article

Abstract

Sexual conflict between mating partners can give rise to strategies that are advantageous for one sex but harmful to the opposite sex. Usually, sperm donors develop (offensive) traits to enhance their chances in sperm competition, while sperm recipients evolve (defensive) traits that allow them to stay in control of who fathers their offspring. Here, we demonstrate that these processes are also at work in simultaneous hermaphrodites. The hermaphroditic earthworm Lumbricus terrestris uses 40 to 44 copulatory setae to pierce into its partner's skin, causing damage and injecting a substance from its setal glands. Experimental injection of the gland substance indicates that a refractory period may be induced. More importantly, removal of the copulatory setae shows that they influence the partner's sperm uptake. When the setae are present, more sperm are taken up and sperm are distributed more equally over the four spermathecae. We interpret this as a strategy that stacks the odds for the donor's sperm in fertilizing cocoons.

Keywords

Hermaphrodite Sexual conflict Sperm competition Allohormone Manipulation 

Notes

Acknowledgments

We thank J. Lange, G. Sundermann, C. Mehlis and C. Levesque for technical assistance and H. Schulenburg, L. Schärer, T. d'Souza, S. Field and A. Ter Maat for valuable comments. This research was partly funded by a fellowship from the Alexander von Humboldt Foundation to JMK

References

  1. Bishop JDD, Jones CS, Noble LR (1996) Female control of paternity in the internally fertilizing compound ascidian Diplosoma listerianum. II. Investigation of male mating success using RAPD markers. Proc R Soc Lond B 263:401–407CrossRefGoogle Scholar
  2. Breidenbach J (2002) Normalanatomie und -histologie des Lumbriciden Lumbricus terrestris L. (Annelida, Oligochaeta). Ph.D. Thesis, University of Muenster (Germany)Google Scholar
  3. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47CrossRefGoogle Scholar
  4. Cuadrado S, Martínez-Ansemil E (2001) External structures used during attachment and sperm transfer in tubificids (Annelida, Oligochaeta). Hydrobiologia 463:107–113CrossRefGoogle Scholar
  5. Darwin C (1871) The descent of man, and selection in relation to sex. Murray, LondonGoogle Scholar
  6. Fedina TY, Lewis SM. (2004) Female influence over offspring paternity in the red flour beetle Tribolium castaneum. Proc R Soc Lond B 271:1393–1399CrossRefGoogle Scholar
  7. Feldkamp J (1924) Untersuchungen über die Geschlechtsmerkmale und die Begattung der Regenwurmer. Zool Jahrb Anat 46:609–632Google Scholar
  8. Grove AJ (1925) On the reproductive process of the earthworm, Lumbricus terrestris. Q J Microsc Sci 69:245–290Google Scholar
  9. Haase M, Baur B (1995) Variation in spermathecal morphology and storage of spermatozoa in the simultaneous hermaphroditic land snail Arianta arbustorum (Gastropoda: Pulmonata: Stylommatophora). Invert Reprod Develop 28:33–41Google Scholar
  10. Hellriegel B, Ward PI (1998) Complex female reproductive tract morphology: Its possible use in postcopulatory female choice. J Theor Biol 190:179–186CrossRefGoogle Scholar
  11. Hellriegel B, Bernasconi G (2000) Female-mediated differential sperm storage in a fly with complex spermathecae, Scathophaga stercoraria. Anim Behav 59:311–317CrossRefPubMedGoogle Scholar
  12. Johnstone RA, Keller L (2000) How males can gain by harming their mates: Sexual conflict, seminal toxins, and the cost of mating. Am Nat 156:368–377CrossRefGoogle Scholar
  13. Koene JM (2004) Immunomodulation, allohormones and fertility. Med Hyp 63:1084–1085CrossRefGoogle Scholar
  14. Koene JM (2005) Love darts of land snails. Invert Biol 124:1Google Scholar
  15. Koene JM, Chase R (1998) Changes in the reproductive system of the snail Helix aspersa caused by mucus from the love dart. J Exp Biol 201:2313–2319PubMedGoogle Scholar
  16. Koene JM, Schulenburg H (2005) Shooting darts: Co-evolution and counter-adaptation in hermaphroditic snails. BMC Evol Biol 5:25PubMedCrossRefGoogle Scholar
  17. Koene JM, Sundermann G, Michiels NK (2002) On the function of body piercing during copulation in earthworms. Invert Reprod Develop 41:35–40Google Scholar
  18. Koene JM, Ter Maat A (2001) “Allohormones”: A class of bioactive substances favoured by sexual selection. J Comp Physiol A 187:323–326CrossRefPubMedGoogle Scholar
  19. Koene JM, Ter Maat A (2002) The distinction between pheromones and allohormones. J Comp Physiol A 188:163–164CrossRefGoogle Scholar
  20. Koene JM, Ter Maat A (2004) Energy budgets in the simultaneously hermaphroditic pond snail, Lymnaea stagnalis: A trade-off between growth and reproduction during development. Belgian J Zool 134:41–45Google Scholar
  21. Landolfa MA, Green DM, Chase R (2001) Dart shooting influences paternal reproductive success in the snail Helix aspersa (Pulmonata, Stylommatophora). Behav Ecol 12:773–777CrossRefGoogle Scholar
  22. Michiels NK (1998) Mating conflicts and sperm competition in simultaneous hermaphrodites. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press Ltd., pp. 219–254Google Scholar
  23. Michiels NK, Hohner A, Vorndran IC (2001) Dangerous liaisons in the earthworm Lumbricus terrestris: The importance of precopulatory mate assessment in relation to body size. Behav Ecol 12:612–618CrossRefGoogle Scholar
  24. Morgan MT (1994) Models of sexual selection in hermaphrodites, especially plants. Am Nat 144:S100–S125CrossRefGoogle Scholar
  25. Nuutinen V, Butt KR (1997) The mating behaviour of the earthworm Lumbricus terrestris (Oligochaeta: Lumbricidae). J Zool Lond 242:783–798CrossRefGoogle Scholar
  26. Olsson M, Shine R, Madsen T, Gullberg A, Tegelström H (1996) Sperm selection in females. Nature 383:585CrossRefGoogle Scholar
  27. Oumi T, Ukena K, Matsushima O, Ikeda T, Fujita T, Minakata H, Nomoto K (1996) Annetocin, an annelid oxytocin-related peptide, inducing egg-laying behavior in the earthworm, Eisenia foetida. J Exp Zool 276:151–156CrossRefPubMedGoogle Scholar
  28. Prosser CL, Zimmermann GL (1943) Effects of drugs on the heart of Arenicola and Lumbricus. Physiol Zool 16:77–83Google Scholar
  29. Rogers D, Chase R (2001) Dart receipt promotes sperm storage in the garden snail Helix aspersa. Behav Ecol Sociobiol 50:122–127CrossRefGoogle Scholar
  30. Rogers D, Chase R (2002) Determinants of paternity in the garden snail Helix aspersa. Behav Ecol Sociobiol 52:289–295CrossRefGoogle Scholar
  31. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, NJGoogle Scholar
  32. Sims RW, Gerard BM (1999) Earthworms, notes for the identification of British species. In: Barnes RSK, Crothers JH (eds) Synopses of the British fauna (new series), no. 31 revised. Field Studies Council, ShrewsburyGoogle Scholar
  33. Ward PI (1993) Females influence sperm storage and use in the yellow dung fly, Scathophaga stercoraria (L.). Behav Ecol Sociobiol 32:313–319CrossRefGoogle Scholar
  34. Ward PI (2000) Cryptic female choice in the yellow dung fly Scathophaga stercoraria (L). Evolution 54:1680–1686PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Joris M. Koene
    • 1
    • 2
  • Tina Pförtner
    • 2
  • Nico K. Michiels
    • 2
    • 3
  1. 1.Faculty of Earth and Life SciencesVrije UniversiteitAmsterdamThe Netherlands
  2. 2.Department of Evolutionary BiologyWestfaelische Wilhelms UniversitaetMuensterGermany
  3. 3.Animal Evolutionary EcologyZoological InstituteTübingenGermany

Personalised recommendations