Behavioral Ecology and Sociobiology

, Volume 60, Issue 3, pp 359–367 | Cite as

Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana

Original Article

Abstract

Costs and benefits associated with matings and the effects of mating frequency on fitness commonly differ between the sexes. As a result, outcrossing simultaneous hermaphrodites may prefer to copulate in the more rewarding sex role, generating conflicts over sperm donation and sperm receipt between mates. Because recent sex role preference models remain controversial, we contrast here some of their assumptions and predictions in the sea slug Chelidonura sandrana. For this hermaphrodite with sperm storage and internal fertilisation, risk-averse models assume that fitness pay-offs are constantly higher in the female than in the male function in any single mating. Moreover, excluding mutual partner assessment, these models predict male mating behaviour to be independent of receiver traits. The competing gender ratio hypothesis assumes that relative fitness pay-offs, and thus the preferred mating roles, vary and may reverse between matings and predicts that ejaculation strategies co-vary with receiver quality. We found that field mating rates of C. sandrana substantially exceeded what is required to maintain female fertility and fecundity, indicating large variation in direct female benefits between matings. We further demonstrate that male copulation duration adaptively increased with partner body size (i.e. fecundity) but decreased with recent partner promiscuity. These findings are compatible with the gender ratio hypothesis but contradict risk-averse models.

Keywords

Fertility Male choice Partner quality Sexual conflict Sperm competition intensity 

Notes

Acknowledgements

S. Tyler and M. Hooge kindly identified the food flatworms of C. sandrana. L. Angeloni, S.G. Field, M. Haase, J.M. Koene, H. Schulenburg and anonymous referees made helpful suggestions to previous versions of the manuscript. The Great Barrier Reef Marine Park Authority (GBRMPA) supplied the permit (G02/2868.1) for field and laboratory work. The authors received funding from the German Science Foundation (DFG; grant Mi 482/7-2,3 to N.K.M.) and the German Academic Exchange Service (DAAD; grant D/03/36804 to A.P.).

References

  1. Angeloni L (2003) Sexual selection in a simultaneous hermaphrodite with hypodermic insemination: body size, allocation to sexual roles and paternity. Anim Behav 66:417–426 DOI 10.1006/anbe.2003.2255CrossRefGoogle Scholar
  2. Angeloni L, Bradbury J (1999) Body size influences mating strategies in a simultaneously hermaphroditic sea slug, Aplysia vaccaria. Ethol Ecol Evol 11:187–195Google Scholar
  3. Angeloni L, Bradbury J, Charnov EL (2002) Body size and sex allocation in simultaneously hermaphroditic animals. Behav Ecol 13:419–426 DOI 10.1093/beheco/13.3.419CrossRefGoogle Scholar
  4. Angeloni L, Bradbury JW, Burton RS (2003) Multiple mating, paternity, and body size in a simultaneous hermaphrodite, Aplysia californica. Behav Ecol 14:554–560 DOI 10.1093/beheco/arg033CrossRefGoogle Scholar
  5. Anthes N, Michiels NK (2005) Do “sperm trading” simultaneous hermaphrodites always trade sperm? Behav Ecol 16:188–195 DOI 10.1093/beheco/arh150CrossRefGoogle Scholar
  6. Anthes N, Putz A, Michiels NK (2005) Gender trading in a hermaphrodite. Curr Biol 15:R792–R793PubMedCrossRefGoogle Scholar
  7. Anthes N, Putz A, Michiels NK (2006) Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework. Anim Behav (in press)Google Scholar
  8. Arnold SJ (1994) Bateman’s principles and the measurement of sexual selection in plants and animals. Am Nat 144:S126–S149CrossRefGoogle Scholar
  9. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164 DOI 10.1006/anbe.2000.1446PubMedCrossRefGoogle Scholar
  10. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonGoogle Scholar
  11. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368PubMedCrossRefGoogle Scholar
  12. Baur B (1998) Sperm competition in molluscs. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 255–305CrossRefGoogle Scholar
  13. Baur B, Baur A (1992) Effect of courtship and repeated copulation on egg production in the simultaneously hermaphroditic land snail Arianta arbustorum. Invert Repr Dev 21:201–206Google Scholar
  14. Beeman RD (1970) An autoradiographic study of sperm exchange and storage in a sea hare, Phyllaplysia taylori, a hermaphroditic gastropod (Opisthobranchia: Anaspidea). J Exp Zool 175:125–132CrossRefGoogle Scholar
  15. Chaine A, Angeloni L (2005) Size-dependent mating and gender choice in a simultaneous hermaphrodite, Bulla gouldiana. Behav Ecol Sociobiol 59:58–68 DOI 10.1007/s00265-005-0009-8CrossRefGoogle Scholar
  16. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47CrossRefGoogle Scholar
  17. DeBoer P, Jansen RF, TerMaat A (1996) Copulation in the hermaphroditic snail Lymnaea stagnalis: a review. Invert Repr Dev 30:167–176Google Scholar
  18. Dillon RT (2000) The ecology of freshwater molluscs. Cambridge University Press, CambridgeGoogle Scholar
  19. Greeff JM, Michiels NK (1999) Sperm digestion and reciprocal sperm transfer can drive hermaphrodite sex allocation to equality. Am Nat 153:421–430CrossRefGoogle Scholar
  20. Greeff JM, Parker GA (2000) Spermicide by females: what should males do? Proc R Soc Lond B Biol Sci 267:1759–1763 DOI 10.1098/rspb.2000.1207CrossRefGoogle Scholar
  21. Haase M, Karlsson A (2004) Mate choice in a hermaphrodite: you won’t score with a spermatophore. Anim Behav 67:287–291 DOI 10.1016/j.anbehav.2003.06.009CrossRefGoogle Scholar
  22. Hughes RN, Manríquez PH, Bishop JDD (2002) Female investment is retarded pending reception of allosperm in a hermaphroditic colonial invertebrate. Proc Natl Acad Sci USA 99:14884–14886 DOI 10.1073/pnas.162339699PubMedCrossRefGoogle Scholar
  23. Jennions MP, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  24. Karlsson A, Haase M (2002) The enigmatic mating behaviour and reproduction of a simultaneous hermaphrodite, the nudibranch Aeolidiella glauca (Gastropoda, Opisthobranchia). Can J Zool 80:260–270CrossRefGoogle Scholar
  25. 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. Belg J Zool 134:41–45Google Scholar
  26. Koene JM, Ter Maat A (2005) Sex role alternation in the simultaneous hermaphroditic pond snail Lymnaea stagnalis is determined by the availability of seminal fluid. Anim Behav 69:845–850 DOI 10.1016/j.anbehav.2004.07.012CrossRefGoogle Scholar
  27. Koene JM, Pförtner T, Michiels NK (2005) Piercing the partner’s skin influences sperm uptake in the earthworm Lumbricus terrestris. Behav Ecol Sociobiol 59:243–249 DOI 10.1007/s00265-005-0030-yCrossRefGoogle Scholar
  28. Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc R Soc Lond B Biol Sci 270:646–653 DOI 10.1098/rspb.2002.2235CrossRefGoogle Scholar
  29. Leonard JL (1990) The hermaphrodite’s dilemma. J Theor Biol 147:361–372PubMedCrossRefGoogle Scholar
  30. Leonard JL (1999) Modern portfolio theory and the prudent hermaphrodite. Invert Repr Dev 36:129–135Google Scholar
  31. Leonard JL (2005) Bateman’s principle and simultaneous hermaphrodites: a paradox. Integr Comp Biol 45:856–873CrossRefGoogle Scholar
  32. Leonard JL, Lukowiak K (1984) Male–female conflict in a simultaneous hermaphrodite resolved by sperm trading. Am Nat 124:282–286CrossRefGoogle Scholar
  33. Lüscher A, Wedekind C (2002) Size-dependent discrimination of mating partners in the simultaneous hermaphroditic cestode Schistocephalus solidus. Behav Ecol 13:254–259 DOI 10.1093/beheco/13.2.254CrossRefGoogle Scholar
  34. McCartney MA (1997) Sex allocation and male fitness gain in a colonial, hermaphroditic marine invertebrate. Evolution 51:127–140CrossRefGoogle Scholar
  35. Michiels NK (1998) Mating conflicts and sperm competition in simultaneous hermaphrodites. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 219–254CrossRefGoogle Scholar
  36. Michiels NK, Hohner A, Vorndran IC (2001) Precopulatory mate assessment in relation to body size in the earthworm Lumbricus terrestris: avoidance of dangerous liaisons? Behav Ecol 12:612–618 DOI 10.1093/beheco/12.5.612CrossRefGoogle Scholar
  37. Michiels NK, Raven-Yoo-Heufes A, Kleine Brockmann K (2003) Sperm trading and sex roles in the hermaphroditic opisthobranch sea slug Navanax inermis: eager females or opportunistic males? Biol J Linn Soc 78:105–116 DOI 10.1046/j.1095-8312.2003.00135.xCrossRefGoogle Scholar
  38. Norton CG, Bronson JM (2005) The relationship of body size and growth to egg production in the hermaphroditic freshwater snail, Helisoma trivolvis. J Molluscan Stud DOI 10.1093/mollus/eyi057Google Scholar
  39. Ohbayashi-Hodoki K, Ishihama F, Shimada M (2004) Body size-dependent gender role in a simultaneous hermaphrodite freshwater snail, Physa acuta. Behav Ecol 15:976–981, DOI 10.1093/beheco/arh101CrossRefGoogle Scholar
  40. Otsuka C, Rouger Y, Tobach E (1980) A possible relationship between size and reproductive behaviour in a population of Aplysia punctata Cuvier, 1803. Veliger 23:159–163Google Scholar
  41. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos Trans R Soc Lond B Biol Sci 361:235–259 DOI 10.1098/rstb.2005.1785PubMedCrossRefGoogle Scholar
  42. Pongratz N, Michiels NK (2003) High multiple paternity and low last-male sperm precedence in a hermaphroditic planarian flatworm: consequences for reciprocity patterns. Mol Ecol 12:1425–1433 DOI 10.1046/j.1365-294X.2003.01844.xPubMedCrossRefGoogle Scholar
  43. Rice WR, Stewart AD, Morrow EH, Linder JE, Orteiza N, Byrne PG (2006) Assessing sexual conflict in the Drosophila melanogaster laboratory model system. Philos Trans R Soc Lond B Biol Sci 361:287–299 DOI 10.1098/rstb.2005.1787PubMedCrossRefGoogle Scholar
  44. Rowe L, Cameron E, Day T (2005) Escalation, retreat, and female indifference as alternative outcomes of sexually antagonistic coevolution. Am Nat 165:S5–S18 DOI 10.1086/429395PubMedCrossRefGoogle Scholar
  45. Rudman WB (1973) On some species of Chelidonura (Opisthobranchia: Aglajidae) from Zanzibar and Fiji. Zool J Linn Soc 52:201–215CrossRefGoogle Scholar
  46. Rudman WB (1974) A comparison of Chelidonura, Navanax and Aglaja with other genera of the Aglajidae (Opisthobranchia: Gastropoda). Zool J Linn Soc 54:185–212CrossRefGoogle Scholar
  47. Schärer L, Joss G, Sandner P (2004) Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck. Mar Biol 145:373–380 DOI 10.1007/s00227-004-1314-xCrossRefGoogle Scholar
  48. Schleicherova D, Lorenzi MC, Sella G (2006) How outcrossing hermaphrodites sense the presence of conspecifics and suppress female allocation. Behav Ecol 17:1–5 DOI 10.1093/beheco/ari093CrossRefGoogle Scholar
  49. Sella G, Lorenzi MC (2003) Increased sperm allocation delays body growth in a protandrous simultaneous hermaphrodite. Biol J Linn Soc 78:149–154. DOI 10.1046/j.1095-8312.2003.00167.xCrossRefGoogle Scholar
  50. Siva-Jothy MT, Stutt AD (2003) A matter of taste: direct detection of female mating status in the bedbug. Proc R Soc Lond B Biol Sci 270:649–652. DOI 10.1098/rspb.2002.2260CrossRefGoogle Scholar
  51. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 163–179Google Scholar
  52. Tsitrone A, Jarne P, David P (2003) Delayed selfing and resource reallocations in relation to mate availability in the freshwater snail Physa acuta. Am Nat 162:474–488PubMedCrossRefGoogle Scholar
  53. Uhia E, Cordero Rivera A (2005) Male damselflies detect female mating status: importance for postcopulatory sexual selection. Anim Behav 69:797–804 DOI 10.1016/j.anbehav.2004.08.005CrossRefGoogle Scholar
  54. Vreys C, Michiels NK (1995) The influence of body size on immediate reproductive success in Dugesia gonocephala (Tricladida, Paludicola). Hydrobiologia 305:113–117CrossRefGoogle Scholar
  55. Vreys C, Michiels NK (1997) Flatworms flatten to size up each other. Proc R Soc Lond B Biol Sci 264:1559–1564CrossRefGoogle Scholar
  56. Wedell N, Cook PA (1999) Butterflies tailor their ejaculate in response to sperm competition risk and intensity. Proc R Soc Lond B Biol Sci 266:1033–1039CrossRefGoogle Scholar
  57. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320CrossRefGoogle Scholar
  58. Wethington AR, Dillon RT (1996) Gender choice and gender conflict in a non-reciprocally mating simultaneous hermaphrodite, the freshwater snail, Physa. Anim Behav 51:1107–1118 DOI 10.1006/anbe.1996.0112CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Animal Evolutionary Ecology, Zoological InstituteEberhard Karls-Universität TübingenTübingenGermany
  2. 2.Institute for Pharmaceutical Biology and BiotechnologyHeinrich Heine Universität DüsseldorfDüsseldorfGermany

Personalised recommendations