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Sperm and sex peptide stimulate aggression in female Drosophila

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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Figure 1: Two proposed pathways for mating-induced female aggression.
Figure 2: Mated females spend more time fighting than virgins but do not win more fights.
Figure 3: Effects of male ejaculate components, female egg production and sex peptide receptor on total contest duration.

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References

  1. Stockley, P. & Bro-Jørgensen, J. Female competition and its evolutionary consequences in mammals. Biol. Rev. Camb. Phil. Soc. 86, 341–366 (2011).

    Article  Google Scholar 

  2. Clutton-Brock, T. & Huchard, E. Social competition and its consequences in female mammals. J. Zool. 289, 151–171 (2013).

    Article  Google Scholar 

  3. 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).

    Article  Google Scholar 

  4. 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).

    Article  CAS  Google Scholar 

  5. 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).

    Article  Google Scholar 

  6. 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).

    Article  CAS  Google Scholar 

  7. 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).

    Article  Google Scholar 

  8. 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).

    Article  Google Scholar 

  9. 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).

    Article  Google Scholar 

  10. 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).

    Article  Google Scholar 

  11. Stockley, P. & Campbell, A. Female competition and aggression: interdisciplinary perspectives. Phil. Trans. R. Soc. B 368, 20130073 (2013).

    Article  Google Scholar 

  12. 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).

    Article  Google Scholar 

  13. 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).

    Article  Google Scholar 

  14. 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).

    Article  Google Scholar 

  15. Kubli, E. & Bopp, D. Sexual behavior: how sex peptide flips the postmating switch of female flies. Curr. Biol. 22, R520–R522 (2012).

    Article  CAS  Google Scholar 

  16. Gittleman, J. L. & Thompson, D. Energy allocation in mammalian reproduction. Integr. Comp. Biol. 28, 863–875 (1988).

    Google Scholar 

  17. Wade, G. N. & Schneider, J. E. Metabolic fuels and reproduction in female mammals. Neurosci. Biobehav. Rev. 16, 235–272 (1992).

    Article  CAS  Google Scholar 

  18. 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).

    Article  CAS  Google Scholar 

  19. Arnqvist, G. & Rowe, L. Sexual Conflict (Princeton Univ. Press, 2005).

    Book  Google Scholar 

  20. Sgrò, C. M. & Partridge, L. A delayed wave of death from reproduction in Drosophila. Science 286, 2521–2524 (1999).

    PubMed  Google Scholar 

  21. Wheeler, D. The role of nourishment in oogenesis. Annu. Rev. Entomol. 41, 407–4731 (1996).

    Article  CAS  Google Scholar 

  22. 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).

    Article  CAS  Google Scholar 

  23. 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).

    Article  Google Scholar 

  24. 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).

    Article  Google Scholar 

  25. 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).

    Article  CAS  Google Scholar 

  26. Ueda, A. & Kidokoro, Y. Aggressive behaviours of female Drosophila melanogaster are influenced by their social experience and food resources. Physiol. Entomol. (2002).

  27. 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).

    Article  CAS  Google Scholar 

  28. 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).

    CAS  Google Scholar 

  29. 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).

    Article  CAS  Google Scholar 

  30. Peng, J. et al. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr. Biol. 15, 207–213 (2005).

    Article  CAS  Google Scholar 

  31. Boswell, R. E. & Mahowald, A. P. tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43, 97–104 (1985).

    Article  CAS  Google Scholar 

  32. 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).

    Article  Google Scholar 

  33. 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).

    Article  Google Scholar 

  34. Pilpel, N., Nezer, I., Applebaum, S. W. & Heifetz, Y. Mating-increases trypsin in female Drosophila hemolymph. Insect Biochem. Mol. Biol. 38, 320–330 (2008).

    Article  CAS  Google Scholar 

  35. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  37. 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).

    Article  CAS  Google Scholar 

  38. 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).

    Article  CAS  Google Scholar 

  39. 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).

    Article  Google Scholar 

  40. 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).

    Article  CAS  Google Scholar 

  41. Moshitzky, P. et al. Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch. Insect Biochem. Physiol. 32, 363–374 (1996).

    Article  CAS  Google Scholar 

  42. Soller, M., Bownes, M. & Kubli, E. Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208, 337–351 (1999).

    Article  CAS  Google Scholar 

  43. Scott, M. P. Resource defense and juvenile hormone: the ‘challenge hypothesis’ extended to insects. Horm. Behav. 49, 276–281 (2006).

    Article  CAS  Google Scholar 

  44. 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).

    Article  CAS  Google Scholar 

  45. Tibbetts, E. A., Vernier, C. & Jinn, J. Juvenile hormone influences precontest assessment behaviour in Polistes dominulus paper wasps. Anim. Behav. 85, 1177–1181 (2013).

    Article  Google Scholar 

  46. 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).

    Article  Google Scholar 

  47. 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).

    Article  Google Scholar 

  48. Clutton-Brock, T. et al. Infanticide and expulsion of females in a cooperative mammal. Proc. Biol. Sci. 265, 2291–2295 (1998).

    Article  CAS  Google Scholar 

  49. 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).

    Article  CAS  Google Scholar 

  50. Tibbetts, E. A. Resource value and the context dependence of receiver behaviour. Proc. Biol. Sci. 275, 2201–2206 (2008).

    Article  Google Scholar 

  51. Gillott, C. Male accesory gland secretions: Modulators of Female Reproductive Physiology and Behavior. Annu. Rev. Entomol. 48, 163–184 (2003).

    Article  CAS  Google Scholar 

  52. Mcgraw, L. A., Suarez, S. S. & Wolfner, M. F. On a matter of seminal importance. BioEssays 37, 142–147 (2015).

    Article  Google Scholar 

  53. Kapusta, J. & Marchlewska-Koj, A. Interfemale aggression in adult bank voles (Clethrionomys glareolus). Aggress. Behav. 24, 53–61 (1998).

    Article  Google Scholar 

  54. Ratto, M. H. et al. The nerve of ovulation-inducing factor in semen. Proc. Natl Acad. Sci. USA 109, 15042–15047 (2012).

    Article  CAS  Google Scholar 

  55. 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).

    Article  CAS  Google Scholar 

  56. Barton Browne, L. in Regulatory Mechanisms in Insect Feeding (eds Chapman, R. F. & de Boer, G. ) 307–342 (Chapman & Hall, 1995).

    Book  Google Scholar 

  57. 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).

    Article  CAS  Google Scholar 

  58. Wigby, S. & Chapman, T. Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution 58, 1028–1037 (2004).

    Article  Google Scholar 

  59. Clancy, D. J. & Kennington, W. J. A simple method to achieve consistent larval density in bottle cultures. Drosoph. Inf. Serv. 84, 168–169 (2001).

    Google Scholar 

  60. Lewis, E. A new standard food medium. Drosoph. Inf. Serv. 34, 117–118 (1960).

    Google Scholar 

  61. Xue, L. & Noll, M. Drosophila female sexual behavior induced by sterile males showing copulation complementation. Proc. Natl Acad. Sci. USA 97, 3272–3275 (2000).

    Article  CAS  Google Scholar 

  62. 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).

    Article  CAS  Google Scholar 

  63. Perry, J. C. et al. Experimental evolution under hyper-promiscuity in Drosophila melanogaster. BMC Evol. Biol. 16, 131 (2016).

    Article  Google Scholar 

  64. Blumenstein, D ., Evans, C & Daniels, J. C. Jwatcher 1.0 (2006); http://www.jwatcher.ucla.edu

  65. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012).

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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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Authors

Contributions

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.

Corresponding author

Correspondence to Eleanor Bath.

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The authors declare no competing financial interests.

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Supplementary Figures 1–4 (PDF 272 kb)

Supplementary Video 1

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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