Abstract
Contrary to many separate sex systems, the evolutionary ecology of polyandry in simultaneous hermaphrodites, and in particular in those with internal fertilization, has received little attention. Recent studies on the promiscuous gastropod Chelidonura sandrana showed that offspring size, an important determinant of offspring performance in many marine invertebrates, varies with the number of different mating partners. However, the source of this differential allocation by mothers remained unclear. Using a quantitative genetic model, we here tested for parental effects on offspring size and the importance of ‘good gene’ effects on early life history traits. Our analysis revealed no significant sire but strong dam effects for all investigated traits. Moreover, embryo viability tended to increase with egg capsule volume, thus linking offspring size with offspring performance. Our findings suggest that in C. sandrana (1) differential allocation is a maternal effect in response to the number of different partners, and that (2) additive genetic variance is of negligible importance in early life history traits.
Similar content being viewed by others
References
Allen RM, Buckley YM, Marshall DJ (2008) Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages. Am Nat 171:225–237. doi:10.1086/524952
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/arg033
Anthes N, Michiels NK (2005) Do “sperm trading” simultaneous hermaphrodites always trade sperm? Behav Ecol 16:188–195. doi:10.1093/beheco/arh150
Anthes N, Putz A, Michiels NK (2006) Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana. Behav Ecol Sociobiol 60:359–367. doi:10.1007/s00265-006-0173-5
Baur B (1998) Sperm competition in molluscs. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 255–305
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340. doi:10.1017/S0016672399004152
Charmantier A, Garant D (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc Lond B Biol Sci 272:1415–1425. doi:10.1098/rspb.2005.3117
Crnokrak P, Roff DA (1995) Dominance variance: associations with selection and fitness. Heredity 75:530–540. doi:10.1038/hdy.1995.169
Evanno G, Madec L, Arnaud J-F (2005) Multiple paternity and postcopulatory sexual selection in a hermaphrodite: what influences sperm precedence in the garden snail Helix aspersa?. Mol Ecol 14:805–812. doi:10.1111/j.1365-294X.2005.02449.x
Evans JP, Marshall DJ (2005) Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evol Int J Org Evol 59:106–112
Fox CW (1993) Maternal and genetic influences on egg size and larval performance in a seed beetle (Callosobruchus maculatus): multigenerational transmission of a maternal effect? Heredity 73:509–517. doi:10.1038/hdy.1994.149
Garcia L (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105:657–663. doi:10.1111/j.0030-1299.2004.13046.x
García-González F, Simmons LW (2005) The evolution of polyandry: intrinsic sire effects contribute to embryo viability. J Evol Biol 18:1097–1103. doi:10.1111/j.1420-9101.2005.00889.x
García-González F, Simmons L (2007) Paternal indirect genetic effects on offspring viability and the benefits of polyandry. Curr Biol 17:32–36. doi:10.1016/j.cub.2006.10.054
Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101. doi:10.1016/S0169-5347(99)01595-5
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21–64. doi:10.1017/S0006323199005423
Jennions MD, Drayton JM, Brooks R, Hunt J (2007) Do female black field crickets Teleogryllus commodus benefit from polyandry? J Evol Biol 20:1469–1477. doi:10.1111/j.1420-9101.2007.01333.x
Jordaens K, Dillen L, Backeljau T (2007) Effects of mating, breeding system and parasites on reproduction in hermaphrodites: pulmonate gastropods (Mollusca). Anim Biol 57:137–195. doi:10.1163/157075607780377965
Kotiaho JS, Simmons LW, Hunt J, Tomkins JL (2003) Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus. Am Nat 161:852–859. doi:10.1086/375173
Lessels CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland
Marshall DJ, Evans JP (2007) Context-dependent genetic benefits of polyandry in a marine hermaphrodite. Biol Lett 3:685–688. doi:10.1098/rsbl.2007.0438
Marshall DJ, Keough MJ (2003) Variation in the dispersal potential of non-feeding invertebrate larvae: the desperate larva hypothesis and larval size. Mar Ecol Prog Ser 255:145–153. doi:10.3354/meps255145
Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60. doi:10.1016/S0065-2881(07)53001-4
Marshall DJ, Uller TU (2007) When is a maternal effect adaptive? Oikos 116:1957–1963. doi:10.1111/j.2007.0030-1299.16203.x
Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109. doi:10.1038/sj.hdy.6885850
Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407. doi:10.1016/S0169-5347(98)01472-4
Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38. doi:10.1111/j.1365-294X.2004.02395.x
Poiani A (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60:289–310. doi:10.1007/s00265-006-0178-0
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.x
Roff DA, Emerson K (2006) Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evol Int J Org Evol 60:1981–1990
Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst 36:125–146. doi:10.1146/annurev.ecolsys.36.102403.112501
Sprenger D, Anthes N, Michiels NK (2008a) Multiple mating affects offspring size in the opisthobranch Chelidonura sandrana. Mar Biol (Berl) 153:891–897. doi:10.1007/s00227-007-0861-3
Sprenger D, Faber J, Michiels NK, Anthes N (2008b) Natural female mating rate maximizes hatchling size in a marine invertebrate. J Anim Ecol 77:696–701. doi:10.1111/j.1365-2656.2008.01376.x
Sprenger D, Lange R, Michiels NK, Anthes N (2009) The role of body size in early mating behavior in a simultaneous hermaphrodite, Chelidonura sandrana. Behav Ecol Sociobiol 63:953–958
Thompson TE (1976) Biology of opisthobranch molluscs. The Ray Society, London
Toonen RJ (2004) Genetic evidence of multiple paternity of broods in the intertidal crab Petrolisthes cinctipes. Mar Ecol Prog Ser 270:259–263. doi:10.3354/meps270259
Toonen R, Pawlik J (1994) Foundations of gregariousness. Nature 370:511–512. doi:10.1038/370511a0
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027. doi:10.1046/j.1365-294x.2000.00964.x
Verhoeven K, Simonsen K, McIntyre L (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647. doi:10.1111/j.0030-1299.2005.13727.x
Wedekind C, Müller R, Spicher H (2001) Potential genetic benefits of mate selection in whitefish. J Evol Biol 14:980–986. doi:10.1046/j.1420-9101.2001.00349.x
Wolf J, Brodie EI, Cheverud J, Moore A, Wade M (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69. doi:10.1016/S0169-5347(97)01233-0
Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility (invited article). Ethology 109:929–950. doi:10.1046/j.1439-0310.2003.00945.x
Zeh JA, Zeh DW (2006) Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females. Nature 439:201–203. doi:10.1038/nature04260
Acknowledgments
We thank Philippe Jarne, Hinrich Schulenburg, Kurt Jordaens and one anonymous referee for valuable comments on earlier drafts of this manuscript. We also thank the staff of Lizard Island Research Station for logistical support throughout this study. This work was funded by grants of the German Science Foundation (DFG) to N.K.M. and N.A. (DFG Mi 482/7-3 and Mi 482/7-4).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sprenger, D., Lange, R., Michiels, N.K. et al. Sources of phenotypic variance in egg and larval traits in a marine invertebrate. Evol Ecol 24, 185–194 (2010). https://doi.org/10.1007/s10682-009-9300-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-009-9300-x