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Do male seminal donations shape female post-mating receptivity in a usually monandrous moth?

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Abstract

Male ejaculates in insects include a complex array of substances other than sperm whose proximate functions have proven to be diverse. Some function as allohormones that manipulate post-mating female physiology and behaviour. As each sex pursues their own reproductive interests to maximise fitness, seminal allohormones are expected to promote outcomes ranging from reproductive cooperation to sexual conflict and antagonistic coevolution. Most research on the evolutionary importance of male seminal donations has targeted highly polyandrous species, and more research is needed on usually monandrous species. Here, we explore in the mostly monandrous moth Lobesia botrana if there is variation among males in their ability to influence female post-mating receptivity (PMR), if the trait covariates with the polyandry level of the parental strain and if it could be mediated by ejaculate composition when taking into account spermatophore size. To do this, we conducted controlled reciprocal crosses between field-collected mostly monandrous strains and laboratory-selected highly polyandrous strains. We found that laboratory strain males were significantly less efficient than field strain males at inhibiting female PMR, and that such variation covariate with the polyandry level of the parental strain. Male strain also influenced the duration of the female refractory period, fecundity and fertility being high and roughly similar. Between-strain differences in the ability of males to influence female PMR suggest an effect of seminal fluid composition and its underlying genetic variation in male strains. Further research is needed to assess whether male donations that regulate female PMR are widespread in monandrous insect species to better understand the wider evolutionary significance of these findings in L. botrana.

Significance statement

The available evidence suggests that male-donated allohormonal substances (including parasperm) can influence/manipulate female PMR in insects. Most research on this issue has targeted polyandrous species, as it is often implicitly assumed that in monandrous species eupyrene sperm itself plays the key role in inhibiting female PMR. We studied whether male donations could have some allohormonal effect on female PMR in the usually monandrous moth Lobesia botrana. Controlled crosses between field-collected mostly monandrous strains and artificially selected highly polyandrous strains suggest that there is genetic variation in ejaculate composition-mediated male ability to influence/manipulate female PMR.

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References

  • Al-Wathiqui N, Fallon TR, South A, Weng JK, Lewis SM (2016) Molecular characterization of firefly nuptial gifts: a multi-omics approach sheds light on postcopulatory sexual selection. Sci Rep 6:38556

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andrés JA, Maroja LS, Bogdanowicz SM, Swanson WJ, Harrison RG (2006) Molecular evolution of seminal proteins in field crickets. Mol Biol Evol 23:1574–1584

    PubMed  Google Scholar 

  • Arnqvist G, Edvardsson M, Friberg U, Nilsson T (2000) Sexual conflict promotes speciation in insects. Proc Natl Acad Sci U S A 97:10460–10464

    CAS  PubMed  PubMed Central  Google Scholar 

  • Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56:21–40

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bissoondath CJ, Wiklund C (1995) Protein content of spermatophores in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 37:365–371

    Google Scholar 

  • Cook PA, Wedell N (1999) Non-fertile sperm delay female remating. Nature 397:486

    CAS  Google Scholar 

  • Cordero C (1995) Ejaculate substances that affects female insect reproductive physiology and behavior: honest or arbitrary traits? J Theor Biol 174:453–461

    CAS  Google Scholar 

  • Drummond BA (1984) Multiple mating and sperm competition in the Lepidoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, New York, pp 291–370

    Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Friberg U, Lew TA, Byrne PG, Rice WR (2005) Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation. Evolution 59:1540–1551

    PubMed  Google Scholar 

  • Gage MJG (1994) Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc R Soc Lond B 258:247–254

    Google Scholar 

  • Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184

    CAS  PubMed  Google Scholar 

  • Gwynne DT (2008) Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 53:83–101

    CAS  PubMed  Google Scholar 

  • Harano T, Miyatake T (2005) Heritable variation in polyandry in Callosobruchus chinensis. Anim Behav 70:299–304

    Google Scholar 

  • Harano T, Miyatake T (2007) Interpopulation variation in female remating is attributable to female and male effects in Callosobruchus chinensis. J Ethol 25:49–55

    Google Scholar 

  • Heller KS, Faltin S, Fleischmann P, Helversen OV (1998) The chemical composition of the spermatophore in some species of phaneropterid bushcrickets (Orthoptera: Tettigonioidea). J Insect Physiol 44:1001–1008

    CAS  PubMed  Google Scholar 

  • Holman L, Head ML, Lanfear R, Jennions MD (2015) Evidence of experimental bias in the life sciences: why we need blind data recording. PLoS Biol 13:e1002190

    PubMed  PubMed Central  Google Scholar 

  • Hosken DJ, Ward PI (2001) Experimental evidence for testis size evolution via sperm competition. Ecol Lett 4:10–13

    Google Scholar 

  • Karlsson B (1995) Resource allocation and mating systems in butterflies. Evolution 49:955–961

    PubMed  Google Scholar 

  • Karlsson B (1996) Male reproductive reserves in relation to mating system in butterflies: a comparative study. Proc R Soc Lond B 263:187–192

    CAS  Google Scholar 

  • Lewis SM, Vahed K, Koene JM, Engqvist L, Bussière LF, Perry JC, Gwynne D, Lehmann GUC (2014) Emerging issues in the evolution of animal nuptial gifts. Biol Lett 10:20140336

    PubMed  PubMed Central  Google Scholar 

  • Meslin C, Cherwin TS, Plakke MS, Hill J, Small BS, Goetz BJ, Wheat CW, Morehouse NI, Clark NL (2017) Structural complexity and molecular heterogeneity of a butterfly ejaculate reflect a complex history of selection. Proc Natl Acad Sci U S A 114:E5406–E5413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moreau J, Thiéry D, Troussard JP, Benrey B (2007) Grape variety affects female but also male reproductive success in wild European grapevine moths. Ecol Entomol 32:747–753

    Google Scholar 

  • Muller K, Thiéry D, Moret Y, Moreau J (2015) Male larval nutrition affects adult reproductive success in wild European grapevine moth (Lobesia botrana). Behav Ecol Sociobiol 69:39–47

    Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–568

    Google Scholar 

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

    Google Scholar 

  • Perry JC, Sirot L, Wigby S (2013) The seminal symphony: how to compose an ejaculate. Trends Ecol Biol 28:414–422

    Google Scholar 

  • Poiani A (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60:289–310

    Google Scholar 

  • Ridley M (1989) The timing and frequency of mating in insects. Anim Behav 37:535–545

    Google Scholar 

  • Rowe L, Cameron E, Day T (2003) Detecting sexually antagonistic coevolution with population crosses. Proc R Soc Lond B 270:2009–2016

    Google Scholar 

  • Shuker DM, Phillimore AJ, Burton-Chellew MN, Hodge SE, West SA (2007) The quantitative genetic basis of polyandry in the parasitoid wasp, Nasonia vitripennis. Heredity 98:69–73

    CAS  PubMed  Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton

    Google Scholar 

  • Simmons LW, Parker GA (1989) Nuptial feeding in insects: mating effort versus paternal investment. Ethology 81:332–343

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman and Co, New York

    Google Scholar 

  • Solymar BD, Cade WH (1990) Heritable variation for female mating frequency in field crickets, Gryllus integer. Behav Ecol Sociobiol 26:73–76

    Google Scholar 

  • Stockel J, Roehrich R, Carles JP, Nadaud A (1989) Technique d’élevage pour l’obtention programmée d’adultes vierges d’Eudémis. Phytoma 412:45–47

    Google Scholar 

  • Svärd L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402

    Google Scholar 

  • Swallow JG, Wilkinson GS (2002) The long and short of sperm polymorphisms in insects. Biol Rev 77:153–182

    PubMed  Google Scholar 

  • Thorburn DMJ, Knell RJ, Parrett JM (2018) Sperm morph and remating frequency in the Indian meal moth, Plodia interpunctella. Biol Lett 14:20180304

    PubMed  PubMed Central  Google Scholar 

  • Torres-Vila LM (2013) Polyandry-fecundity relationship in insects: methodological and conceptual problems. J Evol Biol 26:325–334

    CAS  PubMed  Google Scholar 

  • Torres-Vila LM, Jennions MD (2005) Male mating history and female fecundity in the Lepidoptera: do male virgins make better partners? Behav Ecol Sociobiol 57:318–326

    Google Scholar 

  • Torres-Vila LM, Rodríguez-Molina MC (2013) Host plant-mediated reaction norms in the European grapevine moth: evidence for evolutionary host shift from daphne to vine. Arth-Plant Int 7:125–136

    Google Scholar 

  • Torres-Vila LM, Stockel J, Roehrich R (1995) Le potentiel reproducteur et ses variables biotiques associées chez le mâle de l’Eudémis de la vigne Lobesia botrana. Entomol Exp Appl 77:105–119

    Google Scholar 

  • Torres-Vila LM, Stockel J, Rodríguez-Molina MC (1997) Physiological factors regulating polyandry in Lobesia botrana (Lepidoptera: Tortricidae). Physiol Entomol 22:387–393

    Google Scholar 

  • Torres-Vila LM, Rodríguez-Molina MC, Roehrich R, Stockel J (1999) Vine phenological stage during larval feeding affects male and female reproductive output of Lobesia botrana (Lepidoptera: Tortricidae). Bull Entomol Res 89:549–556

    Google Scholar 

  • Torres-Vila LM, Rodríguez-Molina MC, Gragera J, Bielza-Lino P (2001) Polyandry in Lepidoptera: a heritable trait in Spodoptera exigua Hübner. Heredity 86:177–183

    CAS  PubMed  Google Scholar 

  • Torres-Vila LM, Gragera J, Rodríguez-Molina MC, Stockel J (2002) Heritable variation for female remating in Lobesia botrana, a usually monandrous moth. Anim Behav 64:899–907

    Google Scholar 

  • Torres-Vila LM, Rodríguez-Molina MC, McMinn M, Rodríguez-Molina A (2005) Larval food source promotes cyclic seasonal variation in polyandry in the moth Lobesia botrana. Behav Ecol 16:114–122

    Google Scholar 

  • Välimäki P, Kaitala A (2010) Properties of male ejaculates do not generate geographical variation in female mating tactics in a butterfly Pieris napi. Anim Behav 79:1173–1179

    Google Scholar 

  • Wedell N, Wiklund C, Cook PA (2002) Monandry and polyandry as alternative lifestyles in a butterfly. Behav Ecol 13:450–455

    Google Scholar 

  • Wedell N, Wiklund C, Bergström J (2009) Coevolution of non-fertile sperm and female receptivity in a butterfly. Biol Lett 5:678–681

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to all colleagues who provided technical assistance in the field and laboratory, especially Paco Ponce, Álvaro Sánchez and Juanjo Ferrero. We also recognize the valuable comments and suggestions made by Michael D. Jennions and two anonymous reviewers.

Funding

This research was supported by the Servicio de Sanidad Vegetal (SSV, Junta de Extremadura).

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Correspondence to Luis M. Torres-Vila.

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The experiments conducted conform to the normative of the institution, region and country in which they were performed.

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Communicated by D. J. Hosken

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Torres-Vila, L.M., Mendiola-Díaz, F.J. & Echave-Sanabria, A.C. Do male seminal donations shape female post-mating receptivity in a usually monandrous moth?. Behav Ecol Sociobiol 73, 163 (2019). https://doi.org/10.1007/s00265-019-2776-7

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