Duration of sperm storage in the simultaneous hermaphrodite Lymnaea stagnalis

Journal of Molluscan Studies

Volumn 80, Issue 1, 2014, Pages 1-7

  Nakadera, Yumi ^a   Blom, Christiaan ^a   Koene, Joris M ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BODY SIZE; GENETIC MARKER; HERMAPHRODITE; LONGEVITY; PATERNITY; REPRODUCTIVE SUCCESS; SEXUAL SELECTION; SNAIL; SPERM;

EID: 84893051839     PISSN: 02601230     EISSN: 14643766     Source Type: Journal    
DOI: 10.1093/mollus/eyt049     Document Type: Article

References (69)

1. ANGELONI, L. 2003. Sexual selection in a simultaneous hermaphrodite with hypodermic insemination: body size, allocation to sexual roles and paternity. Animal Behaviour, 66: 417-426.
2. ANTHES, N., DAVID, P., AULD, J.R., HOFFER, J.N.A., JARNE, P., KOENE, J.M., KOKKO, H., LORENZI, M.C., PÉ LISSIÉ , B., SPRENGER, D., STAIKOU, A. & SCHARER, L. 2010. Bateman gradients in hermaphrodites: An extended approach to quantify sexual selection. American Naturalist, 176: 249-263.
3. ARNOLD, S.J. 1994. Bateman principles and the measurement of sexual selection in plants and animals. American Naturalist, 144: S126-S149.
4. ARNOLD, S.J. & DUVALL, D. 1994. Animal mating systems-a synthesis based on selection theory. American Naturalist, 143: 317-348.
5. BATEMAN, A.J. 1948. Intra-sexual selection in Drosophila melanogaster. Heredity, 2: 277-277.
6. BAUR, B. 1994. Multiple paternity and individual variation in sperm precedence in the simultaneously hermaphroditic land snail Arianta arbustorum. Behavioral Ecology and Sociobiology, 35: 413-421.
7. BAUR, B. 1998. Sperm competition in molluscs. In: Sperm competition and sexual selection (T.R. Birkhead & A.P. Møller, eds), pp. 255-305.
8. Academic Press, San Diego. BIRKHEAD, T.R. & MØLLER, A.P. 1993. Sexual selection and the temporal separation of reproductive events-sperm storage data from reptiles, birds and mammals. Biological Journal of the Linnean Society, 50: 295-311.
9. BIRKHEAD, T.R. & MØLLER, A.P. 1998. Sperm competition and sexual selection. Academic Press, San Diego
10. BOOMSMA, J.J., BAER, B. & HEINZE, J. 2005. The evolution of male traits in social insects. Annual Review of Entomology, 50: 395-420.
11. BOORMAN, E. & PARKER, G.A. 1976. Sperm (ejaculate) competition in Drosophila melanogaster, and reproductive value of females to males in relation to female age and mating status. Ecological Entomology, 1: 145-155.
12. CAIN, G.L. 1956. Studies on cross-fertilization and self-fertilization in Lymnaea stagnalis appressa Say. Biological Bulletin, 111: 45-52.
13. CHAPMAN, T. & DAVIES, S.J. 2004. Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies. Peptides, 25: 1477-1490.
14. CHASE, R. & BLANCHARD, K.C. 2006. The snail's love-dart delivers mucus to increase paternity. Proceedings of the Royal Society Series B, Biological Sciences, 273: 1471-1475.
15. COLLINS, A.M., WILLIAMS, V. & EVANS, J.D. 2004. Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Insect Molecular Biology, 13: 141-146.
16. COUTELLEC, M.A. & LAGADIC, L. 2006. Effects of selffertilization, environmental stress and exposure to xenobiotics on fitness-related traits of the freshwater snail Lymnaea stagnalis. Ecotoxicology, 15: 199-213.
17. DILLON, R.T., MCCULLOUGH, T.E. & EARNHARDT, C.E. 2005. Estimates of natural allosperm storage capacity and self-fertilization rate in the hermaphroditic freshwater pulmonate snail, Physa acuta. Invertebrate Reproduction&Development, 47: 111-115.
18. EBERHARD, W.G. 1996. Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton.
19. ESCOBAR, J.S., AULD, J.R., CORREA, A.C., ALONSO, J.M., BONY, Y.K., COUTELLEC, M.A., KOENE, J.M., POINTIER, J.P., JARNE, P. & DAVID, P. 2011. Patterns of mating-system evolution in hermaphroditic animals: correlations among selfing rate, inbreeding depression, and the timing of reproduction. Evolution, 65: 1233-1253.
20. GAREFALAKI, M.E., TRIANTAFYLLIDIS, A., ABATZOPOULOS, T.J. & STAIKOU, A. 2010. The outcome of sperm competition is affected by behavioural and anatomical reproductive traits in a simultaneously hermaphroditic land snail. Journal of Evolutionary Biology, 23: 966-976.
21. GILLOTT, C. 2003. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annual Review of Entomology, 48: 163-184.
22. HERMANN, P.M., GENEREUX, B. & WILDERING, W.C. 2009. Evidence for age-dependent mating strategies in the simultaneous hermaphrodite snail, Lymnaea stagnalis (L.). Journal of Experimental Biology, 212: 3164-3173.
23. HOFFER, J.N.A., ELLERS, J. & KOENE, J.M. 2010. Costs of receipt and donation of ejaculates in a simultaneous hermaphrodite. BMC Evolutionary Biology, 10: 393.
24. HOFFER, J.N.A., SCHWEGLER, D., ELLERS, J. & KOENE, J.M. 2012. Mating rate influences female reproductive investment in a simultaneous hermaphrodite, Lymnaea stagnalis. Animal Behaviour, 84: 523-529.
25. JANICKE, T., VELLNOW, N., SARDA, V. & DAVID, P. 2013. Sex-specific inbreeding depression depends on the strength of male- male competition. Evolution, 67: 2861-2875.
26. JARNE, P. & AULD, J.R. 2006. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution, 60: 1816-1824.
27. JARNE, P. & CHARLESWORTH, D. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annual Review of Ecology and Systematics, 24: 441-466.
28. JARNE, P., DAVID, P., POINTER, P.J. & KOENE, J.M. 2010. Basommatophoran gastropods. In: The evolution of primary sexual characters in animals (J.L. Leonard & A. Có rdoba-Aguilar, eds), pp.173-196. Oxford University Press, Oxford.
29. JARNE, P., VIANEY-LIAUD, M. & DELAY, B. 1993. Selfing and outcrossing in hermaphrodite fresh-water gastropods (Basommatophora)-where, when and why. Biological Journal of the Linnean Society, 49: 99-125.
30. JONES, A.G. 2009. On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution, 63: 1673-1684.
31. JORDAENS, K., DILLEN, L. & BACKELJAU, T. 2007. Effects of mating, breeding system and parasites on reproduction in hermaphrodites: pulmonate gastropods (Mollusca). Animal Biology, 57: 137-195.
32. KNOTT, K.E., PUURTINEN, M. & KAITALA, V. 2003. Primers for nine microsatellite loci in the hermaphroditic snail Lymnaea stagnalis. Molecular Ecology Notes, 3: 333-335.
33. KOENE, J.M., LOOSE, M.J. & WOLTERS, L. 2008. Mate choice is not affected by mating history in the simultaneously hermaphroditic snail Lymnaea stagnalis. Journal of Molluscan Studies, 74: 331-335.
34. KOENE, J.M., MONTAGNE-WAJER, K., ROELOFS, D. & TER MAAT, A. 2009. The fate of received sperm in the reproductive tract of a hermaphroditic snail and its implications for fertilisation. Evolutionary Ecology, 23: 533-543.
35. KOENE, J.M., SLOOT, W., MONTAGNE-WAJER, K., CUMMINS, S.F., DEGNAN, B.M., SMITH, J.S., NAGLE, G.T. & TER MAAT, A. 2010. Male accessory gland protein reduces egg laying in a simultaneous hermaphrodite. PLoS One, 5: e10117.
36. KOENE, J.M. & TER MAAT, A. 2004. Energy budgets in the simultaneously hermaphroditic pond snail, Lymnaea stagnalis: a trade-off between growth and reproduction during development. Belgian Journal of Zoology, 134: 41-45.
37. KOENE, J.M. & TER MAAT, A. 2005. Sex role alternation in the simultaneously hermaphroditic pond snail Lymnaea stagnalis is determined by the availability of seminal fluid. Animal Behaviour, 69: 845-850.
38. KOENE, J.M. & TER MAAT, A. 2007. Coolidge effect in pond snails: male motivation in a simultaneous hermaphrodite. BMC Evolutionary Biology, 7: 212.
39. KUPFERNAGEL, S. & BAUR, B. 2011. Sperm utilization in subadult and adult simultaneous hermaphrodite snails mating in the wild. Canadian Journal of Zoology, 89: 1041-1049.
40. LEONARD, J.L. & CO RDOBA-AGUILAR, A. 2010. The evolution of primary sexual characters in animals. Oxford University Press, Oxford
41. LOMBARDO, R.C., TAKESHITA, F., ABE, S. & GOSHIMA, S. 2013. Mate choice by males and paternity distribution in offspring of triple-mated females in Neptunea arthritica (Gastropoda: Buccinidae). Journal of Molluscan Studies, 78: 283-289.
42. LOOSE, M.J. & KOENE, J.M. 2008. Sperm transfer is affected by mating history in the simultaneously hermaphroditic snail Lymnaea stagnalis. Invertebrate Biology, 127: 162-167.
43. LÓ PEZ-SEPULCRE, A., GORDON, S.P., PATERSON, I.G., BENTZEN, P. & REZNICK, D.N. 2013. Beyond lifetime reproductive success: the posthumous reproductive dynamics of male Trinidadian guppies. Proceedings of the Royal Society Series B, Biological Sciences, 280: 20131116-0.
44. LUDWIG, A.N. & WALSH, P.J. 2004. Sperm storage and use in laboratory-reared Aplysia californica, a simultaneous hermaphrodite. Marine Biology, 145: 727-732.
45. NAKADERA, Y. & KOENE, J.M. 2013. Reproductive strategies in hermaphroditic gastropods: conceptual and empirical approaches. Canadian Journal of Zoology, 91: 367-381.
46. NEUBAUM, D.M. & WOLFNER, M.F. 1999. Wise, winsome, or weird? Mechanisms of sperm storage in female animals. Current Topics in Developmental Biology, 41: 67-97.
47. NOLAND, L.E. & CARRIKER, M.R. 1946. Observations on the biology of the snail Lymnaea stagnalis appressa during 20 generations in laboratory culture. American Midland Naturalist, 36: 467-493.
48. OLSSON, M., SCHWARTZ, T., ULLER, T. & HEALEY, M. 2007. Sons are made from old stores: sperm storage effects on sex ratio in a lizard. Biology Letters, 3: 491-493.
49. OLSSON, M., SCHWARTZ, T., ULLER, T. & HEALEY, M. 2009. Effects of sperm storage and male colour on probability of paternity in a polychromatic lizard. Animal Behaviour, 77: 419-424.
50. PAGE, R.E. 1986. Sperm utilization in social insects. Annual Review of Entomology, 31: 297-320.
51. PARKER, G.A. 1970. Sperm competition and its evolutionary consequences in insects. Biological Reviews of the Cambridge Philosophical Society, 45: 525-567.
52. PEARSE, D.E. & AVISE, J.C. 2001. Turtle mating systems: behavior, sperm storage, and genetic paternity. Journal of Heredity, 92: 206-211.
53. PÉ LISSIÉ , B., JARNE, P. & DAVID, P. 2012. Sexual selection without sexual dimorphism: Bateman gradients in a simultaneous hermaphrodite. Evolution, 66: 66-81.
54. PUURTINEN, M., KNOTT, K.E., SUONPAA, S., NISSINEN, K. & KAITALA, V. 2007. Predominance of outcrossing in Lymnaea stagnalis despite low apparent fitness costs of self-fertilization. Journal of Evolutionary Biology, 20: 901-912.
55. RACEY, P.A. 1979. Prolonged storage and survival of spermatozoa in Chiroptera. Journal of Reproduction and Fertility, 56: 391-402.
56. RAVI RAM, K. &WOLFNER,M.F. 2007. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integrative and Comparative Biology, 47: 427-445.
57. SCHARER, L. & PEN, I. 2013. Sex allocation and investment into preand postcopulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition. Philosophical Transactions of the Royal Society of London Series B, 368: 20120052.
58. SHUSTER, S.M., BRIGGS, W.R. & DENNIS, P.A. 2013. How multiple mating by females affects sexual selection. Philosophical Transactions of the Royal Society of London Series B, 368: 20120046.
59. SIMMONS, L.W. & SIVA-JOTHY, M.T. 1998. Sperm competition in insects: mechanisms and the potential for selection. In: Sperm competition and sexual selection (T.R. Birkhead & A.P. Møller, eds), pp. 341-432. Academic Press.
60. SWANSON, W.J. & VACQUIER, V.D. 2002. The rapid evolution of reproductive proteins. Nature Reviews Genetics, 3: 137-144.
61. TER MAAT, A., LODDER, J.C. & WILBRINK, M. 1983. Induction of egg-laying in the pond snail Lymnaea stagnalis by environmental stimulation of the release of ovulation hormone from the caudodorsal cells. International Journal of Invertebrate Reproduction, 6: 239-247.
62. TER MAAT, A., PIENEMAN, A.W. & KOENE, J.M. 2012. The effect of light on induced egg laying in the simultaneous hermaphrodite Lymnaea stagnalis. Journal of Molluscan Studies, 78: 262-267.
63. ULLER, T., SCHWARTZ, T., KOGLIN, T. & OLSSON, M. 2013. Sperm storage and sperm competition across ovarian cycles in the dragon lizard, Ctenophorus fordi. Journal of Experimental Zoology Part A-Ecological Genetics and Physiology, 319: 404-408.
64. VAN DUIVENBODEN, Y.A. & TER MAAT, A. 1985. Masculinity and receptivity in the hermaphrodite pond snail, Lymnaea stagnalis. Animal Behaviour, 33: 885-891.
65. VIANEY-LIAUD, M., JOLY, D. & DUSSART, G. 1996. Sperm competition in the simultaneous hermaphrodite freshwater snail Biomphalaria glabrata (Gastropoda: Pulmonata). Journal of Molluscan Studies, 62: 451-457.
66. WADE, M.J. 1979. Sexual selection and variance in reproductive success. American Naturalist, 114: 742-747.
67. WOLFNER, M.F. 2011. Precious essences: female secretions promote sperm storage in Drosophila. PLoS Biology, 9: e1001191.
68. ZAMUDIO, K.R. & SINERVO, E. 2000. Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. Proceedings of the National Academy of Sciences of the USA, 97: 14427-14432.
69. ZONNEVELD, C. & KOOIJMAN, S.A.L.M. 1989. Application of a dynamic energy budget model to Lymnaea stagnalis (L). Functional Ecology, 3: 269-278.