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Male larval nutrition affects adult reproductive success in wild European grapevine moth (Lobesia botrana)

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Abstract

In Lepidoptera, males transfer a spermatophore to females containing sperm and accessory gland secretions that are reinvested into female reproduction, providing a fitness gain to females. One of the key factors shaping male spermatophore size is certainly the resources that males have acquired as larvae. In this study, we investigate how male larval food contributes to shaping the spermatophore quantity and quality and how it affects female reproduction in the European grapevine moth (Lobesia botrana). Specifically, we examined the effect of male origin (cultivar or geographical site) on their mating success by scoring individual motivation to mate, male spermatophore size and amount of sperm, and finally female fecundity and fertility. A strong effect of larval cultivar was found on spermatophore size and amount of fertilizing sperm produced by males. These male characteristics had important repercussions on female reproductive output. Females mating with males producing the biggest spermatophore and more fertilizing sperm were the most fecund and fertile. Finally, females were able to recognize males of different quality during the precopulatory phase and changed their mating behavior accordingly. The present results suggest that male nutritional quality could have an important implication for population dynamics.

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References

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Ann Rev Entomol 47:817–844

    Article  CAS  Google Scholar 

  • Barbosa F (2011) Copulation duration in the soldier fly: the roles of cryptic male choice and sperm competition risk. Behav Ecol 22:1332–1336

    Article  Google Scholar 

  • Bissoondath CJ, Wiklund C (1996) Effect of male mating history and body size on ejaculate size and quality in two polyandrous butterflies, Pieris napi and Pieris rapae (Lepidoptera: Pieridae). Funct Ecol 10:457–464

    Article  Google Scholar 

  • Boggs CL (1990) A general model of the role of male-donated nutrients in female insects' reproduction. Am Nat 136:598–617

    Article  Google Scholar 

  • Boggs CL (1995) Male nuptial gifts: phenotypic consequences and evolutionary implications. In: Leather SR, Hardie J (eds) Insect reproduction. CRC Press Inc, Florida, pp 215–242

    Google Scholar 

  • Cahenzli F, Erhardt A (2012) Nectar sugars enhance fitness in male Coenonympha pamphilus butterflies by increasing longevity or realized reproduction. Oikos 121:1417–1423

    Article  Google Scholar 

  • Cardoso MZ, Gilbert LE (2007) A male gift to its partner? Cyanogenic glycosides in the spermatophore of longwing butterflies (Heliconius). Naturwissenschaften 94:39–42

    Article  CAS  PubMed  Google Scholar 

  • Carrière Y (1992) Host plant exploitation within a population of a generalist herbivore, Choristoneura rosaceana. Entomol Exp Appl 65:1–10

    Article  Google Scholar 

  • Carroll AL (1994) Interactions between body size and mating history influence the reproductive success of males of a tortricid moth, Zeiraphera canadensis. Can J Zool 72:2124–2132

    Article  Google Scholar 

  • Cook PA, Gage MJ (1995) Effects of risks of sperm competition on the numbers of eupyrene and apyrene sperm ejaculated by the moth Plodia interpunctella (Lepidoptera: Pyralidae). Behav Ecol Sociobiol 36:261–268

    Article  Google Scholar 

  • Cook PA, Wedell N (1996) Ejaculate dynamics in butterflies: a strategy for maximizing fertilization success? Proc R Soc Lond 263:1047–1051

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Delisle J, Bouchard A (1995) Male larval nutrition in Choristoneura rosaceana (Lepidoptera: Tortricidae): an important factor in reproductive success. Oecologia 104:508–517

    Article  Google Scholar 

  • Delisle J, Hardy M (1997) Male larval nutrition influences the reproductive success of both sexes of the spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Funct Ecol 11:451–463

    Article  Google Scholar 

  • Eichhorn KW, Lorenz DH (1977) Phaenologische Entwicklungsstadien der Rebe. Nachr bl. Dtsch Pflanzenschutzd 29:119–120

    Google Scholar 

  • Eisner T, Meinwald J (1995) The chemistry of sexual selection. Proc Natl Acad Sci U S A 92:50–55

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Foster SP, Ayers RH (1996) Multiple mating and its effects in the lightbrown apple moth, Epiphyas postvittana (Walker). J Insect Physiol 42:657–667

    Article  CAS  Google Scholar 

  • Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse. Behav Ecol Sociobiol 65:47–55

    Article  PubMed Central  PubMed  Google Scholar 

  • Friedländer M (1997) Control of the eupyrene–apyrene sperm dimorphism in Lepidoptera. J Insect Physiol 43:1085–1092

    Article  PubMed  Google Scholar 

  • Friedländer M, Seth RK, Reynolds SE (2005) Eupyrene and apyrene sperm: dichotomous spermatogenesis in Lepidoptera. Adv Insect Physiol 32:206–308

    Article  Google Scholar 

  • Gage MJG, Cook PA (1994) Sperm size or numbers? Effects of nutritional stress upon eupyrene and apyrene sperm production strategies in the moth Plodia interpunctella (Lepidoptera: Pyralidae). Funct Ecol 8:594–599

    Article  Google Scholar 

  • González A, Rossini C, Eisner M, Eisner T (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A 96:5570–5574

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Harari AR, Zahavi T, Thiéry D (2011) Fitness cost of pheromone production in signaling female moths. Evol 65:1572–1582

    Article  Google Scholar 

  • He Y, Miyata T (1997) Variations in sperm number in relation to larval crowding and spermatophore size in the armyworm, Pseudaletia separata. Ecol Entomol 22:41–46

    Article  Google Scholar 

  • Hunt J, Breuker CJ, Sadowski JA, Moore AJ (2009) Male–male competition, female mate choice and their interaction: determining total sexual selection. J Evol Biol 22:13–26

    Article  PubMed  Google Scholar 

  • Jervis MA, Boggs CL, Ferns PN (2007) Egg maturation strategy and survival trade‐offs in holometabolous insects: a comparative approach. Biol J Linnean Soc 90:293–302

    Article  Google Scholar 

  • Khan NR, Musgrave AJ (1969) Observations on the functional anatomy of the reproductive organs of Sitophilus (Coleoptera: Curculionidae). Can J Zool 47:665–669

    Article  Google Scholar 

  • LaMunyon CW, Eisner T (1994) Spermatophore size as determinant of paternity in an arctiid moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A 91:7081–7084

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lederhouse RC, Ayres MP, Scriber JM (1990) Adult nutrition affects male virility in Papilio glaucus L. Funct Ecol 4:743–751

    Article  Google Scholar 

  • Leopold RA (1976) The role of male accessory glands in insect reproduction. Ann Rev Entomol 21:199–221

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Article  Google Scholar 

  • Lewis Z, Wedell N (2007) Effect of adult feeding on male mating behaviour in the butterfly, Bicyclus anynana (Lepidoptera: Nymphalidae). J Insect Behav 20:201–213

    Article  Google Scholar 

  • Lewis Z, Sasaki H, Miyatake T (2011) Sex starved: do resource-limited males ensure fertilization success at the expense of precopulatory mating success? Anim Behav 81:579–583

    Article  Google Scholar 

  • Mann T (1984) Spermatophores: development, structure, biochemical attributes and role in the transfer of spermatozoa. Springer, Berlin

    Book  Google Scholar 

  • Marshall LD, McNeil JN (1989) Spermatophore mass as an estimate of male nutrient investment: a closer look in Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae). Funct Ecol 3:605–612

    Article  Google Scholar 

  • McNamara KB, Elgar MA, Jones TM (2009) Large spermatophores reduce female receptivity and increase male paternity success in the almond moth, Cadra cautella. Anim Behav 77:931–936

    Article  Google Scholar 

  • Mevi-Schütz J, Erhardt A (2005) Amino acids in nectar enhance butterfly fecundity: a long‐awaited link. Am Nat 165:411–419

    Article  PubMed  Google Scholar 

  • Milonas PG, Farrell SL, Andow DA (2011) Experienced males have higher mating success than virgin males despite fitness costs to females. Behav Ecol Sociobiol 65:1249–1256

    Article  Google Scholar 

  • Moreau J, Benrey B, Thiéry D (2006a) Grape variety affects larval performance and also female reproductive performance of the European grapevine moth (Lobesia botrana). Bull Entomol Res 96:205–212

    Article  CAS  PubMed  Google Scholar 

  • Moreau J, Benrey B, Thiéry D (2006b) Assessing larval food quality for phytophagous insects: are facts as simple as it appears? Funct Ecol 20:592–600

    Article  Google Scholar 

  • Moreau J, Arruego X, Benrey B, Thiery D (2006c) Differences in nutritional quality of parts of Vitis vinifera berries affect fitness of the European grapevine moth. Entomol Exp Appl 119:93–99

    Article  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

    Article  Google Scholar 

  • Oberhauser KS (1988) Male monarch butterfly spermatophore mass and mating strategies. Anim Behav 36:1384–1388

    Article  Google Scholar 

  • Oberhauser KS (1989) Effects of spermatophores on male and female monarch butterfly reproductive success. Behav Ecol Sociobiol 25:237–246

    Article  Google Scholar 

  • Phelan PL, Baker TC (1990) Comparative study of courtship in twelve phycitine moths (Lepidoptera: Pyralidae). J Insect Behav 3:303–326

    Article  Google Scholar 

  • Phillips DM (1970) Insect sperm: their structure and morphogenesis. J Cell Biol 44:243–277

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Royer L, McNeil JN (1993) Male investment in the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae): impact on female longevity and reproductive performance. Funct Ecol 7:209–215

    Article  Google Scholar 

  • Savopoulou-Soultani M, Nikolaou N, Milonas PG (1999) Influence of maturity stage of the grape berries on the development of Lobesia botrana (Lepidoptera: Tortricidae) larvae. J Econ Entomol 92:551–556

    Google Scholar 

  • Silberglied RE, Shepherd JG, Dickinson JL (1984) Eunuchs: the role of apyrene sperm in Lepidoptera? Am Nat 123:255–265

    Article  Google Scholar 

  • South A, Lewis SM (2011) The influence of male ejaculate quantity on female fitness: a meta‐analysis. Biol Rev 86:299–309

    Article  PubMed  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

    Article  Google Scholar 

  • Thiéry D, Moreau J (2005) Relative performance of European grapevine moth (Lobesia botrana) on grapes and other hosts. Oecologia 143:548–557

    Article  PubMed  Google Scholar 

  • Tigreros N (2013) Linking nutrition and sexual selection across life stages in a model butterfly system. Funct Ecol 27:145–154

    Article  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

    Article  Google Scholar 

  • Torres-Vila LM, Rodriguez-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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Velde LV, Schtickzelle N, Van Dyck H (2013) Effect of larval food stress on male adult behaviour, morphology and reproductive investment in the butterfly Pararge aegeria. Evol Ecol 27:221–234

    Article  Google Scholar 

  • Virkki N (1969) Sperm bundles and phylogenesis. Z Zellforsch Mikrosk Anat 101:13–27

    Article  CAS  PubMed  Google Scholar 

  • Warton DI, Hui FK (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Wedell N, Cook PA (1999) Strategic sperm allocation in the small white butterfly Pieris rapae (Lepidoptera: Pieridae). Funct Ecol 13:85–93

    Article  Google Scholar 

  • Wedell N, Karlsson B (2003) Paternal investment directly affects female reproductive effort in an insect. Proc R Soc Lond 270:2065–2071

    Article  CAS  Google Scholar 

  • Whittier TS, Nam FY, Shelly TE, Kaneshiro KY (1994) Male courtship success and female discrimination in the Mediterranean fruit fly (Diptera: Tephritidae). J Insect Behav 7:159–170

    Article  Google Scholar 

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Acknowledgments

We thank L. Delbac, J. Oustric, D. Richy, and M. Guisset for their valuable experimental assistance. This study was supported by the CNRS and grants from the ANR (ANR-07-JCJC-0134 and ANR-08-JCJC-0006). We also thank the Conseil Régional of Aquitaine, the Conseil Régional of Bourgogne, and the Chambre d’Agriculture des Bouches-du-Rhône, du Gard et des Pyrénées-Orientales. Second author belongs to the Labex Cote research program.

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Authors and Affiliations

  1. Equipe Ecologie Evolutive, UMR CNRS 6282 Biogéosciences, Université de Bourgogne, 6 Bd Gabriel, 21000, Dijon, France

    Karen Muller, Yannick Moret & Jérôme Moreau

  2. Institut des Science de la Vigne et du Vin, INRA UMR 1065 Santé et Agroécologie du Vignoble, Ave E. Bourleaux, 33883, Villenave d’Ornon Cedex, France

    Denis Thiéry

  3. Université de Bordeaux, INRA UMR 1065, Save, Bordeaux Sciences Agro, Ave E. Bourleaux, 33883, Villenave d’Ornon Cedex, France

    Denis Thiéry

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  1. Karen Muller
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  4. Jérôme Moreau
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Correspondence to Karen Muller.

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Communicated by N. Wedell

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Muller, K., Thiéry, D., Moret, Y. et al. Male larval nutrition affects adult reproductive success in wild European grapevine moth (Lobesia botrana). Behav Ecol Sociobiol 69, 39–47 (2015). https://doi.org/10.1007/s00265-014-1815-7

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  • DOI: https://doi.org/10.1007/s00265-014-1815-7

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