Abstract
Female aggression towards other females is associated with reproduction in many taxa, and traditionally thought to be related to the protection or provisioning of offspring, such as through increased resource acquisition. However, the underlying reproductive factors causing aggressive behaviour in females remain unknown. Here we show that female aggression in the fruit fly Drosophila melanogaster is strongly stimulated by the receipt of sperm at mating, and in part by an associated seminal fluid protein, the sex peptide. We further show that the post-mating increase in female aggression is decoupled from the costs of egg production and from post-mating decreases in sexual receptivity. Our results indicate that male ejaculates can have a surprisingly direct influence on aggression in recipient females. Male ejaculate traits thus influence the female social competitive environment, with potentially far-reaching ecological and evolutionary consequences.
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References
Stockley, P. & Bro-Jørgensen, J. Female competition and its evolutionary consequences in mammals. Biol. Rev. Camb. Phil. Soc. 86, 341–366 (2011).
Clutton-Brock, T. & Huchard, E. Social competition and its consequences in female mammals. J. Zool. 289, 151–171 (2013).
Cain, K. E. & Ketterson, E. D. Competitive females are successful females; phenotype, mechanism and selection in a common songbird. Behav. Ecol. Sociobiol. 66, 241–252 (2012).
Dloniak, S. M., French, J. A. & Holekamp, K. E. Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas. Nature 440, 1190–1193 (2006).
Huchard, E. & Cowlishaw, G. Female–female aggression around mating: an extra cost of sociality in a multimale primate society. Behav. Ecol. 22, 1003–1011 (2011).
Seebacher, F., Ward, A. J. W. & Wilson, R. S. Increased aggression during pregnancy comes at a higher metabolic cost. J. Exp. Biol. 216, 771–776 (2013).
Müller, J. K. & Eggert, A.-K. Time-dependent shifts between infanticidal and parental behavior in female burying beetles: a mechanism of indirect mother-offspring recognition. Behav. Ecol. Sociobiol. 27, 11–16 (1990).
Elias, D. O., Botero, C. A., Andrade, M. C. B., Mason, A. C. & Kasumovic, M. M. High resource valuation fuels ‘desperado’ fighting tactics in female jumping spiders. Behav. Ecol. 21, 868–875 (2010).
Papadopoulos, N. T., Carey, J. R., Liedo, P., Müller, H.-G. & Sentürk, D. Virgin females compete for mates in the male lekking species Ceratitis capitata. Physiol. Entomol. 34, 238–245 (2009).
Tobias, J. A., Montgomerie, R. & Lyon, B. E. The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Phil. Trans. R. Soc. Lond. B 367, 2274–2293 (2012).
Stockley, P. & Campbell, A. Female competition and aggression: interdisciplinary perspectives. Phil. Trans. R. Soc. B 368, 20130073 (2013).
Robinson, M. R. & Kruuk, L. E. B. Function of weaponry in females: the use of horns in intrasexual competition for resources in female Soay sheep. Biol. Lett. 3, 651–654 (2007).
Eggert, A.-K. & Müller, J. K. Timing of oviposition enables dominant female burying beetles to destroy brood-parasitic young. Anim. Behav. 82, 1227–1233 (2011).
Haney, M., DeBold, J. F. & Miczek, K. A. Maternal aggression in mice and rats towards male and female conspecifics. Aggress. Behav. 15, 443–453 (1989).
Kubli, E. & Bopp, D. Sexual behavior: how sex peptide flips the postmating switch of female flies. Curr. Biol. 22, R520–R522 (2012).
Gittleman, J. L. & Thompson, D. Energy allocation in mammalian reproduction. Integr. Comp. Biol. 28, 863–875 (1988).
Wade, G. N. & Schneider, J. E. Metabolic fuels and reproduction in female mammals. Neurosci. Biobehav. Rev. 16, 235–272 (1992).
Avila, F. W., Sirot, L. K., LaFlamme, B. A., Rubinstein, C. D. & Wolfner, M. F. Insect seminal fluid proteins: identification and function. Annu. Rev. Entomol. 56, 21–40 (2011).
Arnqvist, G. & Rowe, L. Sexual Conflict (Princeton Univ. Press, 2005).
Sgrò, C. M. & Partridge, L. A delayed wave of death from reproduction in Drosophila. Science 286, 2521–2524 (1999).
Wheeler, D. The role of nourishment in oogenesis. Annu. Rev. Entomol. 41, 407–4731 (1996).
Walker, S. J., Corrales-Carvajal, V. M. & Ribeiro, C. Postmating circuitry modulates salt taste processing to increase reproductive output in Drosophila. Curr. Biol. 25, 2621–2630 (2015).
Faas, M. M., Melgert, B. N. & De Vos, P. A brief review on how pregnancy and sex hormones interfere with taste and food intake. Chemosens. Percept. 3, 51–56 (2010).
Wertheim, B., Allemand, R., Vet, L. E. M. & Dicke, M. Effects of aggregation pheromone on individual behaviour and food web interactions: a field study on Drosophila. Ecol. Entomol. 31, 216–226 (2006).
Markow, T. A. Reproductive behavior of Drosophila melanogaster and Drosophila nigrospiracula in the field and in the laboratory. J. Comp. Psychol. 102, 169–173 (1988).
Ueda, A. & Kidokoro, Y. Aggressive behaviours of female Drosophila melanogaster are influenced by their social experience and food resources. Physiol. Entomol. (2002).
Nilsen, S. P., Chan, Y.-B., Huber, R. & Kravitz, E. A. Gender-selective patterns of aggressive behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 101, 12342–12347 (2004).
Vrontou, E., Nilsen, S. P., Demir, E., Kravitz, E. A. & Dickson, B. J. fruitless regulates aggression and dominance in Drosophila. Nat. Neurosci. 9, 1469–1471 (2006).
Liu, H. & Kubli, E. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 100, 9929–9933 (2003).
Peng, J. et al. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr. Biol. 15, 207–213 (2005).
Boswell, R. E. & Mahowald, A. P. tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43, 97–104 (1985).
Yapici, N., Kim, Y.-J., Ribeiro, C. & Dickson, B. J. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451, 33–37 (2008).
Sirot, L. K., Buehner, N. A., Fiumera, A. C. & Wolfner, M. F. Seminal fluid protein depletion and replenishment in the fruit fly, Drosophila melanogaster: an ELISA-based method for tracking individual ejaculates. Behav. Ecol. Sociobiol. 63, 1505–1513 (2009).
Pilpel, N., Nezer, I., Applebaum, S. W. & Heifetz, Y. Mating-increases trypsin in female Drosophila hemolymph. Insect Biochem. Mol. Biol. 38, 320–330 (2008).
Ram, K. R. & Wolfner, M. F. A network of interactions among seminal proteins underlies the long-term postmating response in Drosophila. Proc. Natl Acad. Sci. USA 106, 15384–15389 (2009).
Wigby, S. & Chapman, T. Sex peptide causes mating costs in female Drosophila melanogaster. Curr. Biol. 15, 316–321 (2005).
Chapman, T., Liddle, L. & Kalb, J. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241–244 (1995).
Fricke, C., Bretman, A. & Chapman, T. Female nutritional status determines the magnitude and sign of responses to a male ejaculate signal in Drosophila melanogaster. J. Evol. Biol. 23, 157–165 (2010).
Haussmann, I., Hemani, Y., Wijesekera, T., Dauwalder, B. & Soller, M. Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours. Proc. Biol. Sci. 280, 20131938 (2013).
Fan, Y. et al. Common functional elements of Drosophila melanogaster seminal peptides involved in reproduction of Drosophila melanogaster and Helicoverpa armigera females. Insect Biochem. Mol. Biol. 30, 805–812 (2000).
Moshitzky, P. et al. Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch. Insect Biochem. Physiol. 32, 363–374 (1996).
Soller, M., Bownes, M. & Kubli, E. Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208, 337–351 (1999).
Scott, M. P. Resource defense and juvenile hormone: the ‘challenge hypothesis’ extended to insects. Horm. Behav. 49, 276–281 (2006).
Kou, R., Chou, S. Y., Chen, S. C. & Huang, Z. Y. Juvenile hormone and the ontogeny of cockroach aggression. Horm. Behav. 56, 332–338 (2009).
Tibbetts, E. A., Vernier, C. & Jinn, J. Juvenile hormone influences precontest assessment behaviour in Polistes dominulus paper wasps. Anim. Behav. 85, 1177–1181 (2013).
Barnes, A. I., Wigby, S., Boone, J. M., Partridge, L. & Chapman, T. Feeding, fecundity and lifespan in female Drosophila melanogaster. Proc. Biol. Sci. 275, 1675–1683 (2008).
Connolly, K. & Cook, R. Rejection responses by female Drosophila melanogaster: their ontogeny, causality and effects upon the behaviour of the courting male. Behaviour 44, 142–165 (1973).
Clutton-Brock, T. et al. Infanticide and expulsion of females in a cooperative mammal. Proc. Biol. Sci. 265, 2291–2295 (1998).
Bowler, C. M., Cushing, B. S. & Carter, C. S. Social factors regulate female–female aggression and affiliation in prairie voles. Physiol. Behav. 76, 559–566 (2002).
Tibbetts, E. A. Resource value and the context dependence of receiver behaviour. Proc. Biol. Sci. 275, 2201–2206 (2008).
Gillott, C. Male accesory gland secretions: Modulators of Female Reproductive Physiology and Behavior. Annu. Rev. Entomol. 48, 163–184 (2003).
Mcgraw, L. A., Suarez, S. S. & Wolfner, M. F. On a matter of seminal importance. BioEssays 37, 142–147 (2015).
Kapusta, J. & Marchlewska-Koj, A. Interfemale aggression in adult bank voles (Clethrionomys glareolus). Aggress. Behav. 24, 53–61 (1998).
Ratto, M. H. et al. The nerve of ovulation-inducing factor in semen. Proc. Natl Acad. Sci. USA 109, 15042–15047 (2012).
Bogle, O. A., Ratto, M. H. & Adams, G. P. Evidence for the conservation of biological activity of ovulation-inducing factor in seminal plasma. Reproduction 142, 277–283 (2011).
Barton Browne, L. in Regulatory Mechanisms in Insect Feeding (eds Chapman, R. F. & de Boer, G. ) 307–342 (Chapman & Hall, 1995).
Oliver, B., Perrimon, N. & Mahowald, A. P. The ovo locus is required for sex-specific germ line maintenance in Drosophila. Genes Dev. 1, 913–923 (1987).
Wigby, S. & Chapman, T. Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution 58, 1028–1037 (2004).
Clancy, D. J. & Kennington, W. J. A simple method to achieve consistent larval density in bottle cultures. Drosoph. Inf. Serv. 84, 168–169 (2001).
Lewis, E. A new standard food medium. Drosoph. Inf. Serv. 34, 117–118 (1960).
Xue, L. & Noll, M. Drosophila female sexual behavior induced by sterile males showing copulation complementation. Proc. Natl Acad. Sci. USA 97, 3272–3275 (2000).
Dean, R., Perry, J. C., Pizzari, T., Mank, J. E. & Wigby, S. Experimental evolution of a novel sexually antagonistic allele. PLoS Genet. 8, e1002917 (2012).
Perry, J. C. et al. Experimental evolution under hyper-promiscuity in Drosophila melanogaster. BMC Evol. Biol. 16, 131 (2016).
Blumenstein, D ., Evans, C & Daniels, J. C. Jwatcher 1.0 (2006); http://www.jwatcher.ucla.edu
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012).
Acknowledgements
This study was funded by NERC (NE/J018937/1) and BBSRC (BB/K014544/1) fellowships to S.W. and scholarships from the Rhodes Trust and St John’s College, Oxford to E.B.
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E.B., S.W. and N.S conceived the project. E.B. and S.W. designed the experiments, with S.F.G. providing additional advice on experimental design for later experiments. E.B., S.B., C.P. and A.R. performed the behavioural experiments and scored the behavioural data. E.B. analysed the data and wrote the manuscript. S.W., S.F.G., N.S., E.E.-C. and J.A.T. discussed the results and contributed to the manuscript.
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Annotated examples of female aggressive behaviour as observed and scored in this study. (MP4 28465 kb)
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Bath, E., Bowden, S., Peters, C. et al. Sperm and sex peptide stimulate aggression in female Drosophila. Nat Ecol Evol 1, 0154 (2017). https://doi.org/10.1038/s41559-017-0154
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DOI: https://doi.org/10.1038/s41559-017-0154
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