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Elevated temperature changes female costs and benefits of reproduction

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Abstract

Despite obvious benefits, reproduction also imposes severe costs on females. Such costs and benefits are highly sensitive to environmental factors. Rapidly changing conditions may thus disturb a finely poised balance between the two and pose a challenge to natural populations. A more complete understanding of reproduction and population fitness across different environments is, hence, crucial. In particular, sexual selection could either be beneficial or detrimental when conditions change abruptly. Here Tribolium castaneum females were subjected to mating treatments with or without sexual selection (virginity, monogamy, polyandry) replicated at standard versus elevated temperatures. We found a substantial survival cost of reproduction at the standard, but not at the elevated temperature. Reproductive success was similar across mating treatments at the standard temperature, but at elevated temperature we detected a significant benefit of polyandry compared to monogamy. These findings indicate that environmental heterogeneity can strongly influence the balance between costs and benefits when sexual selection is allowed to act. Furthermore, reproduction may be critically affected by changes in temperature with potentially profound consequences for population fitness.

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References

  • Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

    Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton

    Google Scholar 

  • Bale JS, Masters GJ, Hodkinson ID et al (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16

    Article  Google Scholar 

  • Blanckenhorn WU, Hosken DJ, Martin OY et al (2002) The costs of copulating in the dung fly Sepsis cynipsea. Behav Ecol 13:353–358

    Article  Google Scholar 

  • Candolin U, Heuschele J (2008) Is sexual selection beneficial during adaptation to environmental change? TREE 23:446–452

    PubMed  Google Scholar 

  • Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8:1–8

    Article  Google Scholar 

  • Chihrane J, Lauge G (1994) Effects of high-temperature shocks on male germinal cells of Trichogramma brassicae (Hymenoptera, Trichogrammatidae). Entomophaga 39:11–20

    Article  Google Scholar 

  • Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229

    Article  Google Scholar 

  • Cohet YA, David JR (1976) Deleterious effects of copulation in Drosophila females as a function of growth temperature of both sexes. Experientia 32:696–697

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Edvardsson M (2007) Female Callosobruchus maculatus mate when they are thirsty: resource-rich ejaculates as mating effort in a beetle. Anim Behav 74:183–188

    Article  Google Scholar 

  • Fedina TY, Lewis SM (2004) Female influence over offspring paternity in the red flour beetle Tribolium castaneum. Proc Roy Soc Lond B 271:1393–1399

    Article  Google Scholar 

  • Fedina TY, Lewis SM (2007) Female mate choice across mating stages and between sequential mates in flour beetles. J Evol Biol 20:2138–2143

    Article  PubMed  CAS  Google Scholar 

  • Fedina TY, Lewis SM (2008) An integrative view of sexual selection in Tribolium flour beetles. Biol Rev 83:151–171

    Article  PubMed  Google Scholar 

  • Fox CW (1993) Multiple mating, lifetime fecundity and female mortality of the bruchid beetle, Callosobruchus maculatus (Coleoptera, Bruchidae). Funct Ecol 7:203–208

    Article  Google Scholar 

  • Fox CW, Rauter CM (2003) Bet-hedging and the evolution of multiple mating. Evol Ecol Res 5:273–286

    Google Scholar 

  • Fricke C, Perry J, Chapman T et al (2009) The conditional economics of sexual conflict. Biol Lett 5:671–674

    Article  PubMed  Google Scholar 

  • Hadley NF (1994) Water relations of terrestrial arthropods. Academic Press, San Diego

    Google Scholar 

  • Holland B, Rice WR (1999) Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. PNAS 96:5083–5088

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Hosken DJ, Garner TWJ, Ward PI (2001) Sexual conflict selects for male and female reproductive characters. Curr Biol 11:489–493

    Article  PubMed  CAS  Google Scholar 

  • Hughes L (2000) Biological consequences of global warming: is the signal already apparent? TREE 15:56–61

    PubMed  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 

  • Hurst GDD, Sharpe RG, Broomfield AH et al (1995) Sexually-transmitted disease in a promiscuous insect, Adalia bipunctata. Ecol Entomol 20:230–236

    Article  Google Scholar 

  • Ingleby FC, Hunt J, Hosken DJ (2010) The role of genotype-by-environment interactions in sexual selection. J Evol Biol 23:2031–2045

    Article  PubMed  CAS  Google Scholar 

  • Ivy TM, Johnson JC, Sakaluk SK (1999) Hydration benefits to courtship feeding in crickets. Proc Roy Soc Lond B 266:1523–1527

    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  PubMed  CAS  Google Scholar 

  • Johnstone RA, Keller L (2000) How males can gain by harming their mates: sexual conflict, seminal toxins, and the cost of mating. Am Nat 156:368–377

    Article  Google Scholar 

  • Lewis SM, Jutkiewicz E (1998) Sperm precedence and sperm storage in multiply mated red flour beetles. Behav Ecol Sociobiol 43:365–369

    Article  Google Scholar 

  • Lewis SM, Kobel A, Fedina T et al (2005) Sperm stratification and paternity success in red flour beetles. Physiol Entomol 30:303–307

    Article  Google Scholar 

  • Maes D, Titeux N, Hortal J et al (2010) Predicted insect diversity declines under climate change in an already impoverished region. J Ins Conserv 14:485–498

    Article  Google Scholar 

  • Mahroof R, Zhu KY, Neven L et al (2005) Expression patterns of three heat shock protein 70 genes among developmental stages of the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Comp Biochem Physiol A 141:247–256

    Article  Google Scholar 

  • Martin OY, Hosken DJ (2003a) Costs and benefits of evolving under experimentally enforced polyandry or monogamy. Evolution 57:2765–2772

    PubMed  Google Scholar 

  • Martin OY, Hosken DJ (2003b) The evolution of reproductive isolation through sexual conflict. Nature 423:979–982

    Article  PubMed  CAS  Google Scholar 

  • Martin OY, Hosken DJ (2004) Copulation reduces male but not female longevity in Saltella sphondylli (Diptera: Sepsidae). J Evol Biol 17:357–362

    Article  PubMed  CAS  Google Scholar 

  • Meehl GA, Stocker TF, Collins WD et al (2007) Global climate projections. In: Solomon S, Qin D, Manning M et al (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 747–845

    Google Scholar 

  • Menendez R (2007) How are insects responding to global warming? Tijdschrift voor Entomol 150:355–365

    Google Scholar 

  • Michalczyk L, Martin OY, Millard AL et al (2010) Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum. Proc Roy Soc Lond B 277:3483–3491

    Article  Google Scholar 

  • Michalczyk L, Millard AL, Martin OY et al (2011) Experimental evolution exposes female and male responses to sexual selection and conflict in Tribolium castaneum. Evolution 65:713–724

    Article  PubMed  Google Scholar 

  • Morrow EH, Arnqvist G, Pitnick S (2003) Adaptation versus pleiotropy: why do males harm their mates? Behav Ecol 14:802–806

    Article  Google Scholar 

  • Narraway C, Hunt J, Wedell N et al (2010) Genotype-by-environment interactions for female preferences. J Evol Biol 23:2550–2557

    Article  PubMed  CAS  Google Scholar 

  • Nilsson T, Fricke C, Arnqvist G (2003) The effects of male and female genotype on variance in male fertilization success in the red flour beetle (Tribolium castaneum). Behav Ecol Sociobiol 53:227–233

    Article  Google Scholar 

  • Pai A, Bernasconi G (2008) Polyandry and female control: the red flour beetle Tribolium castaneum as a case study. J Exp Zool (Mol Dev Evol) 310B:148–159

    Article  Google Scholar 

  • Pai A, Yan GY (2003) Rapid female multiple mating in red flour beetles (Tribolium castaneum). Can J Zool 81:888–896

    Article  Google Scholar 

  • Partridge L, Farquhar M (1981) Sexual activity reduces lifespan of male fruitflies. Nature 294:580–582

    Article  Google Scholar 

  • Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Elsevier Academic Press, Burlington, pp 207–245

    Google Scholar 

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

    Article  Google Scholar 

  • Qazi MCB, Aprille JR, Lewis SM (1998) Female role in sperm storage in the red flour beetle, Tribolium castaneum. Comp Biochem Physiol A 120:641–647

    Article  Google Scholar 

  • Reed DH (2008) Effects of population size on population viability: from mutation to environmental catastrophes. In: Carroll SP, Fox CW (eds) Conservation biology: evolution in action. Oxford University Press, Oxford, pp 16–34

    Google Scholar 

  • Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232–234

    Article  PubMed  CAS  Google Scholar 

  • Sadd B, Holman L, Armitage H et al (2006) Modulation of sexual signalling by immune challenged male mealworm beetles (Tenebrio molitor L.): evidence for terminal investment and dishonesty. J Evol Biol 19:321–325

    Article  PubMed  CAS  Google Scholar 

  • Sokoloff A (1972) The biology of Tribolium with special emphasis on genetic aspects. Oxford University Press, Oxford

    Google Scholar 

  • Svard L, Mcneil JN (1994) Female benefit, male risk—polyandry in the true armyworm Pseudaletia unipuncta. Behav Ecol Sociobiol 35:319–326

    Article  Google Scholar 

  • Tanaka Y (1996) Sexual selection enhances population extinction in a changing environment. J Theor Biol 180:197–206

    Article  PubMed  CAS  Google Scholar 

  • Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148

    Article  PubMed  CAS  Google Scholar 

  • Ward PI, Vonwil J, Scholte EJ et al (2002) Field experiments on the distributions of eggs of different phosphoglucomutase (PGM) genotypes in the yellow dung fly Scathophaga stercoraria (L.). Mol Ecol 11:1781–1785

    Article  PubMed  CAS  Google Scholar 

  • Watson PJ, Arnqvist G, Stallmann RR (1998) Sexual conflict and the energetic costs of mating and mate choice in water striders. Am Nat 151:46–58

    Article  PubMed  CAS  Google Scholar 

  • West PM, Packer C (2002) Sexual selection, temperature, and the lion’s mane. Science 297:1339–1343

    Article  PubMed  CAS  Google Scholar 

  • Wigby S, Chapman T (2005) Sex peptide causes mating costs in female Drosophila melanogaster. Curr Biol 15:316–321

    Article  PubMed  CAS  Google Scholar 

  • Wiklund C, Karlsson B, Leimar O (2001) Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness. Proc Roy Soc Lond B 268:1661–1667

    Article  CAS  Google Scholar 

  • Williams SE, Shoo LP, Isaac JL et al (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol 6:2621–2626

    Article  PubMed  CAS  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 the SNF for support (standard research grant 31003A_125144/1, Ambizione grant PZ00P3_121777/1 to OYM), Sonja Sbilordo for help with the experiment and Marco Demont for statistical advice. We further thank Camillo Berenos, Luc Bussière, Niels Kerstes & Sara Goodacre for helpful comments and interesting discussions and Prof. Schmid-Hempel’s group for providing a stimulating research and social environment.

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Correspondence to Oliver Y. Martin.

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Grazer, V.M., Martin, O.Y. Elevated temperature changes female costs and benefits of reproduction. Evol Ecol 26, 625–637 (2012). https://doi.org/10.1007/s10682-011-9508-4

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