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Sex-specific response to nutrient limitation and its effects on female mating success in a gift-giving butterfly

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Abstract

Animals with complex life cycles respond to early food limitation by altering the way resources are allocated in the adult stage. Response to food limitation should differ between males and females, especially in organisms whose mating systems include nutritional nuptial gifts. In these organisms, males are predicted to keep their allocation to reproduction (sperm and nuptial gift production) constant, while females are predicted to sacrifice allocation to reproduction (egg production) since they can compensate by acquiring nuptial gifts when mating. In this study, we investigated how dietary nitrogen limitation during the larval stage affects sex-specific resource allocation in Pieris rapae butterflies. Also, we tested whether nutrient-limited females increased nuptial gift acquisition as a way to compensate for low allocation to reproduction. We found that as predicted females, but not males, sacrifice allocation to reproduction when larval dietary nitrogen is limited. However, females were unable to compensate for this low reproductive allocation by increasing their mating rate to acquire additional gifts. Females reared on low nitrogen diets also reduced wing coloration, a potential signal of female fecundity status. We suggest that female mating frequency is constrained by male mate choice based on females’ wing coloration. This study provides new insights into how larval dietary nitrogen, a key nutritional resource for all herbivores, alters male and female allocation to reproduction as well as to ornamentation.

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References

  • Andersson M (1986) Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40:804–816

    Article  Google Scholar 

  • Bauerfield SS, Fischer K (2005) Effects of food stress and density in different life stages on reproduction in a butterfly. Oikos 111:514–524

    Article  Google Scholar 

  • Bergström J, Wiklund C (2002) Effects of size and nuptial gifts on butterfly reproduction: can females compensate for a smaller size through male-derived nutrients? Behav Ecol Sociobiol 52:296–302

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Boggs CL (1981) Nutritional and life-history determinants of resource allocation in holometabolous insects. Am Nat 117:692–709

    Article  Google Scholar 

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

    Google Scholar 

  • Boggs CL (2009) Understanding insect life histories and senescence through a resource allocation lens. Funct Ecol 23:27–37

    Article  Google Scholar 

  • Boggs CL, Freeman KD (2005) Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144:353–361

    Article  PubMed  Google Scholar 

  • Boggs CL, Ross CL (1993) The effect of adult food limitation on life history traits in Speyria mormonia (Lepidoptera: Nymphalidae). Ecology 74:433–441

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bonduriansky R (2007) The evolution of condition-dependent sexual dimorphism. Am Nat 169:9–19

    Article  PubMed  Google Scholar 

  • Butlin RK, Woodhatch CW, Hewitt GM (1987) Male spermatophore investment increases female fecundity in a grasshopper. Evolution 41:221–225

    Article  Google Scholar 

  • Clarebrough C, Mira A, Raubenheimer D (2000) Sex-specific differences in nitrogen intake and investment by feral and laboratory-cultural cockroaches. J Insect Physiol 46:677–684

    Article  PubMed  CAS  Google Scholar 

  • Collins NC (1980) Developmental responses to food limitation as indicators of environmental conditions for Ephydra cinerea Jones (Diptera). Ecology 61:650–661

    Article  Google Scholar 

  • Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B 271:771–783

    Article  Google Scholar 

  • Drummond BB (1984) Multiple mating and sperm competition in the Lepidoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, London, pp 547–572

    Google Scholar 

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

    PubMed  Google Scholar 

  • Elser JJ, Fagan WF, Denno RF et al (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580

    Article  PubMed  CAS  Google Scholar 

  • Fedina TY, Lewis SM (2006) Female influence over offspring paternity in the red flour beetle Tribolium castaneum. Proc R Soc Lond B 271:1393–1399

    Article  Google Scholar 

  • Gwynne DT (2001) Katydids and bush-crickets: reproductive behavior and evolution of the Tettigoniidae. Cornell University Press, New York

    Google Scholar 

  • Gwynne DT (2004) Sexual differences in response to larval food stress in two nuptial feeding orthopterans-implications for sexual selection. Oikos 105:619–625

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hunt J, Brooks R, Jennions MD et al (2004) High-quality male field crickets invest heavily in sexual display but die young. Nature 432:1024–1027

    Article  PubMed  CAS  Google Scholar 

  • Jannot JE, Bruneau E, Wissinger SA (2007) Effects of larval energetic resources on life history and adult allocation patterns in a caddisfly (Trichoptera: Phryganeidae). Ecol Entomol 32:376–383

    Article  Google Scholar 

  • Kaitala A, Wiklund C (1994) Polyandrous female butterflies forage for matings. Behav Ecol Sociobiol 35:385–388

    Article  Google Scholar 

  • Kandori I, Ohsaki N (1996) Male mating behavior in relation to spermatophore transfer in the white cabbage butterfly. Res Pop Ecol 38:225–230

    Article  Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

  • Karlsson B (1998) Nuptial gifts, resource budgets, and reproductive output in a polyandrous butterfly. Ecology 79:2931–2940

    Article  Google Scholar 

  • Karlsson B, Leimar O, Wiklund C (1997) Unpredictable environments, nuptial gifts and the evolution of sexual size dimorphism in insects: an experiment. Proc R Soc Lond B 264:475–479

    Article  Google Scholar 

  • Kemp DJ, Rutowski RL (2007) Condition dependence, quantitative genetics, and the potential signal content of iridescent ultraviolet butterfly coloration. Evolution 61:168–183

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Leimar O, Karlsson B, Wiklund C (1994) Unpredictable food and sexual size dimorphism in insects. Proc R Soc Lond B 258:121–125

    Article  CAS  Google Scholar 

  • Lewis S, South A (2012) Evolution of animal nuptial gifts. Adv Study Behav 44:53–97

    Article  Google Scholar 

  • Magwere T, Chapman T, Partridge L (2004) Sex differences in the effect of dietary restriction on life span and mortality rates in female and male Drosophila melanogaster. J Gerontol 59A:3–9

    Google Scholar 

  • Maklakov AA, Simpson SJ, Zajitschek F et al (2008) Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr Biol 18:1062–1066

    Article  PubMed  CAS  Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • Moczek AP (1998) Horn polyphenism in the beetle Onthophgus taurus: larval diet quality and plasticity in parental investment determine adult body size and male horn morphology. Behav Ecol 9:636–641

    Article  Google Scholar 

  • Morehouse NI (2009) Sexually selected male color ornament advertises direct and indirect benefits in a butterfly. Limiting nutrients, female choice, and male color. PhD thesis, Arizona State University

  • Morehouse NI, Rutowski RL (2010a) In the eyes of the beholders: female choice and avian predation risk associated with an exaggerated male butterfly color. Am Nat 176:768–784

    Article  PubMed  Google Scholar 

  • Morehouse NI, Rutowski RL (2010b) Developmental responses to variable diet composition in the cabbage white butterfly, Pieris rapae: the role of nitrogen, carbohydrates and genotype. Oikos 199:636–645

    Article  Google Scholar 

  • Morehouse NI, Vukusic P, Rutowski R (2007) Pterin pigment granules are responsible for both broadband light scattering and wavelength selective absorption in the wing scales of pierid butterflies. Proc R Soc Lond B 274:359–366

    Article  CAS  Google Scholar 

  • Morehouse NI, Nakazawa T, Booher CM et al (2010) Sex in a material world: why the study of sexual reproduction and sex-specific traits should become more nutritionally-explicit. Oikos 119:766–778

    Article  Google Scholar 

  • Mullins D, Keil C, White RH (1992) Maternal and paternal nitrogen investment in Blattella germanica (Dictyoptera: Blattellidae). J Exp Biol 162:55–72

    PubMed  CAS  Google Scholar 

  • Nylin S, Gotthard K (1998) Plasticity in life history-traits. Annu Rev Entomol 43:63–83

    Article  PubMed  CAS  Google Scholar 

  • O’Brien DM, Boggs CL, Fogel ML (2004) Making eggs from nectar: the role of life history and dietary carbon turnover in butterfly reproductive resource allocation. Oikos 105:279–291

    Article  Google Scholar 

  • Obara Y, Majerus MEN (2000) Initial mate recognition in the British cabbage butterfly, Pieris rapae rapae. Zool Sci 17:725–730

    Article  Google Scholar 

  • Obara Y, Ozawa G, Fukano Y et al (2008) Mate preference in males of the cabbage butterfly, Pieris rapae crucivora, changes seasonally with the change in female UV color. Zool Sci 25:1–5

    Article  PubMed  Google Scholar 

  • Ringo J (1996) Sexual receptivity in insects. Annu Rev Entomol 41:473–494

    Article  PubMed  CAS  Google Scholar 

  • Shapiro AM (1970) The role of sexual behavior in density-related dispersal of pierid butterflies. Am Nat 104:367–372

    Article  Google Scholar 

  • Slansky F Jr, Feeny P (1977) Stabilization of the rate of nitrogen accumulation by larvae of the cabbage white butterfly on wild and cultivated food plants. Ecol Monogr 47:209–228

    Article  Google Scholar 

  • Slansky F Jr, Rodriguez JG (1987) Nutritional ecology of insects, mites, spiders and related invertebrates: an overview. In: Slansky F Jr, Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley, London, pp 1–69

    Google Scholar 

  • Stillwell RC, Davidowitz G (2010) Sex differences in phenotypic plasticity of a mechanism that controls body size: implications for sexual dimorphism. Proc R Soc Lond B 277:3819–3826

    Article  Google Scholar 

  • Sugawara T (1979) Stretch reception in the bursa copulatrix of the butterfly Pieris rapae crucivora and its role in behavior. J Comp Physiol 130:191–199

    Article  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 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Watanabe M, Ando S (1993) Influence of mating frequency on lifetime fecundity in wild females of the small white Pieris rapae (Lepidoptera, Pieridae). Jpn J Entomol 61:691–696

    Google Scholar 

  • Wedell N, Cook PA (1998) Determinants of paternity in a butterfly. Proc R Soc Lond B 265:625–630

    Article  Google Scholar 

  • Wheeler D (1996) The role of nourishment in oogenesis. Annu Rev Entomol 41:407–431

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Nathan Morehouse and Francie Chew for many helpful discussions throughout this Project, and to Wilson Andres Acuna and Diana Lu for help with data collection. This research was supported by an NSF REU award, and Sigma Xi and Tufts Graduate School Research awards to N.T.

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Correspondence to Natasha Tigreros.

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Tigreros, N., Sass, E.M. & Lewis, S.M. Sex-specific response to nutrient limitation and its effects on female mating success in a gift-giving butterfly. Evol Ecol 27, 1145–1158 (2013). https://doi.org/10.1007/s10682-013-9647-x

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