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Large donors transfer more sperm, but depletion is faster in a promiscuous hermaphrodite

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Abstract

Males are limited in sperm and seminal fluid, which can lead to prudent sperm allocation across consecutive matings. While sperm depletion is usually considered a population characteristic, we investigated an individual size-related variation in sperm depletion in the promiscuous sea slug Chelidonura sandrana. We found that sperm counts substantially declined across four successive copulations, indicating sperm depletion. Sperm depletion occurred at a disproportionally fast rate in larger sperm donors. Based on our finding of body size-dependent sperm depletion, we further investigated whether this translates into prudent sperm allocation across ejaculates. We found no evidence that slugs adjusted the number of delivered sperm in response to partner body weight, a tight proxy of fecundity. Instead, sperm counts increased with sperm donor body weight. Sperm donation independent of partner body size and—as found in previous work—partner novelty leaves scope for currently unidentified traits like the sperm competition environment to affect male sperm allocation. Alternatively, we propose that, in C. sandrana, a low optimal male mating rate close to the female optimum as indicated by our data may ultimately render indiscriminate sperm allocation the most beneficial male mating strategy.

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References

  • Anthes N (2010) Mate choice and reproductive conflict in simultaneous hermaphrodites. In: Kappeler PM (ed) Animal behaviour: evolution and mechanisms. Springer, Heidelberg, pp 329–357

    Chapter  Google Scholar 

  • Anthes N, Michiels NK (2005) Do “sperm trading” simultaneous hermaphrodites always trade sperm? Behav Ecol 16:188–195

    Article  Google Scholar 

  • Anthes N, Michiels NK (2007) Reproductive morphology, mating behaviour, and spawning ecology of cephalaspid sea slugs (Aglajidae and Gastropteridae). Invert Biol 126:335–365

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Arnqvist G, Danielsson I (1999) Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider. Behav Ecol 10:358–365

    Article  Google Scholar 

  • Arnqvist G, Rowe L, Krupa JJ, Sih A (1996) Assortative mating by size: a meta-analysis of mating patterns in water striders. Evol Ecol 10:265–284

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using S4 classes. In: R package version 0.999999-2. http://cran.r-project.org/web/packages/lme4/index.html. Accessed 15 Jun 2013

  • Baur B, Locher R, Baur A (1998) Sperm allocation in the simultaneously hermaphroditic land snail Arianta arbustorum. Anim Behav 56:839–845

    Article  PubMed  Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London

    Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339

    Article  CAS  PubMed  Google Scholar 

  • Byrne PG, Rice WR (2006) Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proc R Soc Lond B 273:917–922

    Article  Google Scholar 

  • Charnov EL (1982) The theory of Sex allocation. Princeton University Press, Princeton

    Google Scholar 

  • Crespi BJ (1989) Causes of assortative mating in arthropods. Anim Behav 38:980–1000

    Article  Google Scholar 

  • DelBarco-Trillo J (2011) Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. J Evol Biol 24:1706–1714

    Article  CAS  PubMed  Google Scholar 

  • Dewsbury DA (1981) Effects of novelty on copulatory behavior: the Coolidge effect and related phenomena. Psychol Bull 89:464–482

    Article  Google Scholar 

  • Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610

    Article  Google Scholar 

  • Dillen L, Jordaens K, van Dongen S, Backeljau T (2010) Effects of body size on courtship role, mating frequency and sperm transfer in the land snail Succinea putris. Anim Behav 79:1125–1133

    Article  Google Scholar 

  • Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654

    Article  PubMed  Google Scholar 

  • Howard R, Martens R, Innis S, Drnevich J, Hale J (1998) Mate choice and mate competition influence male body size in Japanese medaka. Anim Behav 55:1151–1163

    Article  PubMed  Google Scholar 

  • Kelly CD, Jennions MD (2011) Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol Rev 86:863–884

    Article  PubMed  Google Scholar 

  • Kendall MS, Wolcott DL, Wolcott TG, Hines AH (2002) Influence of male size and mating history on sperm content of ejaculates of the blue crab Callinectes sapidus. Mar Ecol Progr Ser 230:235–240

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lange R, Beninde J, Reichel V, Werminghausen J, Gerlach T, Anthes N (2012) Copulation duration does not predict sperm transfer in a marine hermaphrodite. Anim Behav 83:469–472

    Article  Google Scholar 

  • Locher R, Baur B (1999) Effects of intermating interval on spermatophore size and sperm number in the simultaneously hermaphroditic land snail Arianta arbustorum. Ethol 105:839–849

    Article  Google Scholar 

  • Locher R, Baur B (2000) Mating frequency and resource allocation to male and female function in the simultaneous hermaphrodite land snail Arianta arbustorum. J Evol Biol 13:607–614

    Article  Google Scholar 

  • Loose MJ, Koene JM (2008) Sperm transfer is affected by mating history in the simultaneously hermaphroditic snail Lymnaea stagnalis. Invert Biol 127:162–167

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Parker G (1990) Sperm competition games: raffles and roles. Proc R Soc Lond B 242:120–126

    Article  Google Scholar 

  • Parker GA, Simmons LW (1994) Evolution of phenotypic optima and copula duration in dungflies. Nature 370:53–56

    Article  Google Scholar 

  • Pitnick S, Markow TA (1994) Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc Natl Acad Sci U S A 91:9277–9281

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pizzari T, Cornwallis CK, Birkhead TR, Løvlie H, Jakobsson S (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74

    Article  CAS  PubMed  Google Scholar 

  • Preston BT, Stevenson IR, Pemberton JM, Wilson K (2001) Dominant rams lose out by sperm depletion. Nature 409:681–682

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 13 May 2013

  • Rudman WB (1973) On some species of Chelidonura (Opisthobranchia: Aglajidae) from Zanzibar and Fiji. Zool J Linn Soc 52:201–215

    Article  Google Scholar 

  • Sato T, Ashidate M, Wada S, Goshima S (2005) Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab Paralithodes brevipes. Mar Ecol Progr Ser 296:251–262

    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 

  • Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20:416–420

    Article  PubMed  Google Scholar 

  • Spence R, Reichard M, Smith C (2013) Strategic sperm allocation and a Coolidge effect in an externally fertilizing species. Behav Ecol 24:82–88

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sprenger D, Lange R, Anthes N (2011) Population density and group size effects on reproductive behavior in a simultaneous hermaphrodite. BMC Evol Biol 11:107

    Article  PubMed Central  PubMed  Google Scholar 

  • Svärd L, Wiklund C (1986) Different ejaculate delivery strategies in first versus subsequent matings in the swallowtail butterfly Papilio machaon L. Behav Ecol Sociobiol 18:325–330

    Article  Google Scholar 

  • Teuschl Y, Reim C, Meister B, Egger J, Blanckenhorn WU (2010) Strategic ejaculation in the black scavenger fly Sepsis cynipsea revisited: copula duration as a function of sperm depletion and body size. Ethol 116:1118–1126

    Article  Google Scholar 

  • Turner LM, Wilson NG (2012) The Chelidonura tsurugensis–sandrana (Gastropoda: Cephalaspidea) species complex: do reproductive decisions maintain colour polymorphism? J Moll Stud 78:166–172

    Article  Google Scholar 

  • van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137

    Article  Google Scholar 

  • van Son TC, Thiel M (2006) Mating behaviour of male rock shrimp, Rhynchocinetes typus (Decapoda: Caridea): effect of recent mating history and predation risk. Anim Behav 71:61–70

    Article  Google Scholar 

  • Velando A, Eiroa J, Domínguez J (2008) Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners. Proc R Soc Lond B 275:1067–1072

    Article  Google Scholar 

  • Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320

    Article  Google Scholar 

  • Werminghausen J, Lange R, Anthes N (2013) Seeking a sex-specific Coolidge Effect in a simultaneous hermaphrodite. Ethol 119:541–551

    Article  Google Scholar 

  • Wiernasz DC, Sater AK, Abell AJ, Cole BJ (2001) Male size, sperm transfer, and colony fitness in the western harvester ant, Pogonomyrmex occidentals. Evol 55:324–329

    CAS  Google Scholar 

  • Yusa Y (1994) Factors regulating sperm transfer in an hermaphroditic sea hare, Aplysia parvula Mörch, 1863 (Gastropoda: Opisthobranchia). J Exp Mar Biol Ecol 181:213–221

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. In: Gail M, Krickeberg K, Samet JM, Tsiatis A, Wong W (eds) Statistics for biology and health. Springer, New York

    Google Scholar 

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Acknowledgments

We thank the staff of Lizard Island Research Station, Australia, for excellent support during field work. Field and laboratory work were carried out with permission from the Great Barrier Reef Marine Park Authority (GBRMPA permit no. G09/30973.1 to Rolanda Lange). Constructive suggestions by two anonymous referees helped improving the presentation of our data. We received funding by the German Academic Exchange Service (DAAD) to JW and the Deutsche Forschungsgemeinschaft (DFG) to NA (AN 549/2-1).

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Correspondence to Nils Anthes.

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Communicated by N. Wedell

Nils Anthes and Rolanda Lange equally contributed to this work.

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Anthes, N., Werminghausen, J. & Lange, R. Large donors transfer more sperm, but depletion is faster in a promiscuous hermaphrodite. Behav Ecol Sociobiol 68, 477–483 (2014). https://doi.org/10.1007/s00265-013-1662-y

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