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Determinants of female fecundity in a simultaneous hermaphrodite: the role of polyandry and food availability

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Abstract

Classical sexual selection theory assumes that the reproductive success of females is primarily limited by the resources available for egg production rather than by the number of mating partners. However, there is now accumulating evidence that multiple mating can entail fitness costs or benefits for females. In this study we investigated the effect of polyandry (i.e., the mating with different mating partners) and food availability on the reproductive output of the female sex function in an outcrossing simultaneous hermaphrodite, the free-living flatworm Macrostomum lignano. We exposed virgin worms to different group sizes, a treatment that has previously been shown to affect the level of polyandry in this species. Moreover, we manipulated the food availability throughout the subsequent egg laying period, during which the worms were kept in isolation. The number of offspring produced was used as an estimate of female fecundity. We found that food availability, but not group size, had a significant effect on female fecundity. Additionally, female fecundity was positively correlated with the number of stored sperm in the female sperm-storage organ at the time of isolation, but it was not correlated with body or ovary size of the worms. Our results suggest that female fecundity in M. lignano is primarily determined by the resources available for egg production, and not by the level of polyandry, confirming classic sexual selection theory for simultaneous hermaphrodites.

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References

  • Andersen RA, Berges JA, Harrison PJ, Watanabe MM (2005) Recipes for freshwater and seawater media. In: Andersen RA (ed) Algal culturing techniques. Elsevier, Amsterdam, pp 429–538

    Chapter  Google Scholar 

  • Andersson M (2005) Evolution of classical polyandry: three steps to female emancipation. Ethology 111:1–23

    Article  Google Scholar 

  • Anthes N, Putz A, Michiels NK (2005) Gender trading in a hermaphrodite. Curr Biol 15:R792–R793

    Article  CAS  PubMed  Google Scholar 

  • Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164

    Article  PubMed  Google Scholar 

  • Baker RH, Ashwell RIS, Richards TA, Fowler K, Chapman T, Pomiankowski A (2001) Effects of multiple mating and male eye span on female reproductive output in the stalk-eyed fly, Cyrtodiopsis dalmanni. Behav Ecol 12:732–739

    Article  Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  PubMed  Google Scholar 

  • Bedhomme S, Bernasconi G, Koene JM, Lankinen A, Arathi HS, Michiels NK, Anthes N (2009) How does breeding system variation modulate sexual antagonism? Biol Lett 5:717–720

    Article  PubMed  Google Scholar 

  • Birkhead TR, Biggins JD (1998) Sperm competition mechanisms in birds: models and data. Behav Ecol 9:253–260

    Article  Google Scholar 

  • Brauer VS, Schärer L, Michiels NK (2007) Phenotypically flexible sex allocation in a simultaneous hermaphrodite. Evolution 61:216–222

    Article  PubMed  Google Scholar 

  • Breslow NE, Clayton DG (1993) Approximate inference in generalized linear mixed models. J Am Stat Assoc 88:9–25

    Article  Google Scholar 

  • Bybee LF, Millar JG, Paine TD, Campbell K, Hanlon CC (2005) Effects of single versus multiple mates: monogamy results in increased fecundity for the beetle Phoracantha semipunctata. J Insect Behav 18:513–527

    Article  Google Scholar 

  • Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory-gland products. Nature 373:241–244

    Article  CAS  PubMed  Google Scholar 

  • Charnov EL (1979) Simultaneous hermaphroditism and sexual selection. Proc Natl Acad Sci USA 76:2480–2484

    Article  CAS  PubMed  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 

  • Crudgington HS, Siva-Jothy MT (2000) Genital damage, kicking and early death—the battle of the sexes takes a sinister turn in the bean weevil. Nature 407:855–856

    Article  CAS  PubMed  Google Scholar 

  • Daly M (1978) Cost of mating. Am Nat 112:771–774

    Article  Google Scholar 

  • Diaz SA, Haydon DT, Lindstrom J (2010) Sperm-limited fecundity and polyandry-induced mortality in female nematodes Caenorhabditis remanei. Biol J Linn Soc 99:362–369

    Article  Google Scholar 

  • Dunn DW, Sumner JP, Goulson D (2005) The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae). Behav Ecol Sociobiol 58:128–135

    Article  Google Scholar 

  • Engqvist L (2007) Nuptial food gifts influence female egg production in the scorpionfly Panorpa cognata. Ecol Entomol 32:327–332

    Article  Google Scholar 

  • Evans JP, Magurran AE (2000) Multiple benefits of multiple mating in guppies. Proc Natl Acad Sci USA 97:10074–10076

    Article  CAS  PubMed  Google Scholar 

  • Evans JP, Marshall DJ (2005) Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59:106–112

    PubMed  Google Scholar 

  • Fedorka KM, Mousseau TA (2002) Material and genetic benefits of female multiple mating and polyandry. Anim Behav 64:361–367

    Article  Google Scholar 

  • Fischer EA (1980) The relationship between mating system and simultaneous hermaphroditism in the coral-reef fish, Hypoplectrus nigricans (Serranidae). Anim Behav 28:620–633

    Article  Google Scholar 

  • Fisher DO, Double MC, Moore BD (2006) Number of mates and timing of mating affect offspring growth in the small marsupial Antechinus agilis. Anim Behav 71:289–297

    Article  Google Scholar 

  • Fjerdingstad EJ, Boomsma JJ (1998) Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens. Behav Ecol Sociobiol 42:257–261

    Article  Google Scholar 

  • Green K, Tregenza T (2009) The influence of male ejaculates on female mate search behaviour, oviposition and longevity in crickets. Anim Behav 77:887–892

    Article  Google Scholar 

  • Gwynne DT (1984) Courtship feeding increases female reproductive success in bush-crickets. Nature 307:361–363

    Article  Google Scholar 

  • Hosken DJ, Stockley P (2003) Benefits of polyandry: a life history perspective. Evol Biol 33:173–194

    Google Scholar 

  • House CM, Walling CA, Stamper CE, Moore AJ (2009) Females benefit from multiple mating but not multiple mates in the burying beetle Nicrophorus vespilloides. J Evol Biol 22:1961–1966

    Article  CAS  PubMed  Google Scholar 

  • Janicke T, Schärer L (2009a) Determinants of mating and sperm-transfer success in a simultaneous hermaphrodite. J Evol Biol 22:405–415

    Article  CAS  PubMed  Google Scholar 

  • Janicke T, Schärer L (2009b) Sex allocation predicts mating rate in a simultaneous hermaphrodite. Proc R Soc B-Biol Sci 276:4247–4253

    Article  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  CAS  PubMed  Google Scholar 

  • Klemme I, Eccard JA, Ylonen H (2007) Why do female bank voles, Clethrionomys glareolus, mate multiply? Anim Behav 73:623–628

    Article  Google Scholar 

  • Koene JM, Montagne-Wajer K, Ter Maat A (2006) Effects of frequent mating on sex allocation in the simultaneously hermaphroditic great pond snail (Lymnaea stagnalis). Behav Ecol Sociobiol 60:332–338

    Article  Google Scholar 

  • Koene JM, Brouwer A, Hoffer JNA (2009) Reduced egg laying caused by a male accessory gland product opens the possibility for sexual conflict in a simultaneous hermaphrodite. Anim Biol 59:435–448

    Article  Google Scholar 

  • LaDage LD, Gutzke WHN, Simmons RA, Ferkin MH (2008) Multiple mating increases fecundity fertility and relative clutch mass in the female leopard gecko (Eublepharis macularius). Ethology 114:512–520

    Article  Google Scholar 

  • Ladurner P, Schärer L, Salvenmoser W, Rieger RM (2005) A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano, n. sp. (Rhabditophora, Macrostomorpha). J Zool Syst Evol Res 43:114–126

    Article  Google Scholar 

  • Leonard JL (2005) Bateman’s principle and simultaneous hermaphrodites: a paradox. Integr Comp Biol 45:856–873

    Article  Google Scholar 

  • Leonard JL (2006) Sexual selection: lessons from hermaphrodite mating systems. Integr Comp Biol 46:349–367

    Article  Google Scholar 

  • Leonard JL, Lukowiak K (1991) Sex and the simultaneous hermaphrodite—testing models of male-female conflict in a sea slug, Navanax inermis (Opisthobranchia). Anim Behav 41:255–266

    Article  Google Scholar 

  • Levitan DR, Petersen C (1995) Sperm limitation in the sea. Trends Ecol Evol 10:228–231

    Article  Google Scholar 

  • Marshall DJ, Evans JP (2007) Context-dependent genetic benefits of polyandry in a marine hermaphrodite. Biol Lett 3:685–688

    Article  PubMed  Google Scholar 

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

    Chapter  Google Scholar 

  • Michiels NK, Koene JM (2006) Sexual selection favors harmful mating in hermaphrodites more than in gonochorists. Integr Comp Biol 46:473–480

    Article  Google Scholar 

  • Ojanguren AF, Evans JP, Magurran AE (2005) Multiple mating influences offspring size in guppies. J Fish Biol 67:1184–1188

    Article  Google Scholar 

  • Orsetti DM, Rutowski RL (2003) No material benefits, and a fertilization cost, for multiple mating by female leaf beetles. Anim Behav 66:477–484

    Article  Google Scholar 

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

    Chapter  Google Scholar 

  • Pitnick S (1993) Operational sex-ratios and sperm limitation in populations of Drosophila pachea. Behav Ecol Sociobiol 33:383–391

    Article  Google Scholar 

  • Priest NK, Roach DA, Galloway LF (2008) Cross-generational fitness benefits of mating and male seminal fluid. Biol Lett 4:6–8

    Article  PubMed  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing, 2.10.1. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reinhardt K, Naylor RA, Siva-Jothy MT (2009) Ejaculate components delay reproductive senescence while elevating female reproductive rate in an insect. Proc Natl Acad Sci USA 106:21743–21747

    Article  CAS  PubMed  Google Scholar 

  • Reinhold K, Kurtz J, Engqvist L (2002) Cryptic male choice: sperm allocation strategies when female quality varies. J Evol Biol 15:201–209

    Article  Google Scholar 

  • Reynolds JD (1996) Animal breeding systems. Trends Ecol Evol 11:A68–A72

    Article  Google Scholar 

  • Rolff J, Siva-Jothy MT (2002) Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc Natl Acad Sci USA 99:9916–9918

    Article  CAS  PubMed  Google Scholar 

  • Ronkainen K, Kaitala A, Kivelä SM (2010) Polyandry, multiple mating, and female fitness in a water strider Aquarius paludum. Behav Ecol Sociobiol 64:657–664

    Article  Google Scholar 

  • Rowe L (1994) The costs of mating and mate choice in water striders. Anim Behav 48:1049–1056

    Article  Google Scholar 

  • Schärer L (2009) Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution 63:1377–1405

    Article  PubMed  Google Scholar 

  • Schärer L, Ladurner P (2003) Phenotypically plastic adjustment of sex allocation in a simultaneous hermaphrodite. Proc R Soc B-Biol Sci 270:935–941

    Article  Google Scholar 

  • Schärer L, Joss G, Sandner P (2004) Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck. Mar Biol 145:373–380

    Article  Google Scholar 

  • Schärer L, Sandner P, Michiels NK (2005) Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp. J Evol Biol 18:396–404

    Article  PubMed  Google Scholar 

  • Schwartz SK, Peterson MA (2006) Strong material benefits and no longevity costs of multiple mating in an extremely polyandrous leaf beetle, Chrysochus cobaltinus (Coleoptera: Chrysomelidae). Behav Ecol 17:1004–1010

    Article  Google Scholar 

  • Sella G (1985) Reciprocal egg trading and brood care in a hermaphroditic polychaete worm. Anim Behav 33:938–944

    Article  Google Scholar 

  • Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst 36:125–146

    Article  Google Scholar 

  • Sprenger D, Anthes N, Michiels NK (2008) Multiple mating affects offspring size in the opisthobranch Chelidonura sandrana. Mar Biol 153:891–897

    Article  Google Scholar 

  • SPSS Inc. (2008) SPSS for windows, version 17.0. SPSS Inc, Chicago

    Google Scholar 

  • Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788

    Article  Google Scholar 

  • Thrall PH, Antonovics J, Bever JD (1997) Sexual transmission of disease and host mating systems: within-season reproductive success. Am Nat 149:485–506

    Article  Google Scholar 

  • Tregenza T, Wedell N (1998) Benefits of multiple mates in the cricket Gryllus bimaculatus. Evolution 52:1726–1730

    Article  Google Scholar 

  • Vahed K (1998) The function of nuptial feeding in insects: review of empirical studies. Biol Rev 73:43–78

    Article  Google Scholar 

  • van Duivenboden YA, Pieneman AW, Termaat A (1985) Multiple mating suppresses fecundity in the hermaphrodite freshwater snail Lymnaea stagnalis—a laboratory study. Anim Behav 33:1184–1191

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Google Scholar 

  • Venables WN, Ripley BD (2010) MASS: main package of Venables and Ripley’s MASS, R package, version 7.3-5

  • Vizoso DB, Rieger G, Schärer L (2010) Goings-on inside a worm: functional hypotheses derived from sexual conflict thinking. Biol J Linn Soc 99:370–383

    Article  Google Scholar 

  • Vreys C, Michiels NK (1998) Sperm trading by volume in a hermaphroditic flatworm with mutual penis intromission. Anim Behav 56:777–785

    Article  PubMed  Google Scholar 

  • Waage JK (1979) Dual function of the damselfly penis—sperm removal and transfer. Science 203:916–918

    Article  CAS  PubMed  Google Scholar 

  • Wagner WE, Kelley RJ, Tucker KR, Harper CJ (2001) Females receive a life-span benefit from male ejaculates in a field cricket. Evolution 55:994–1001

    Article  PubMed  Google Scholar 

  • Watson PJ (1991) Multiple paternity as genetic bet-hedging in female Sierra Dome Spiders, Linyphia litigiosa (Linyphiidae). Anim Behav 41:343–360

    Article  Google Scholar 

  • Yasui Y (1997) A ‘‘good-sperm’’ model can explain the evolution of costly multiple mating by females. Am Nat 149:573–584

    Article  Google Scholar 

  • Yasui Y (1998) The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol Evol 13:246–250

    Article  Google Scholar 

  • Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc B-Biol Sci 263:1711–1717

    Article  Google Scholar 

  • Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc B-Biol Sci 264:69–75

    Article  Google Scholar 

  • Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063

    Article  Google Scholar 

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Acknowledgments

We thank Dita B. Vizoso for technical assistance. Ralph Dobler and two anonymous referees provided constructive comments on an earlier version of the manuscript. We also thank Lucas Marie-Orléach and Matthew D. Hall for statistical advice. Finally, we are grateful to Jürgen Hottinger, Viktor Mislin and Urs Stiefel for technical support. This study was funded by grants from the Swiss National Science Foundation to L.S. (3100A0-113708 and 3100A0-127503).

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Janicke, T., Sandner, P. & Schärer, L. Determinants of female fecundity in a simultaneous hermaphrodite: the role of polyandry and food availability. Evol Ecol 25, 203–218 (2011). https://doi.org/10.1007/s10682-010-9402-5

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