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Within-group male relatedness reduces harm to females in Drosophila

Nature volume 505, pages 672–675 (2014)Cite this article

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Abstract

To resolve the mechanisms that switch competition to cooperation is key to understanding biological organization1. This is particularly relevant for intrasexual competition, which often leads to males harming females2. Recent theory proposes that kin selection may modulate female harm by relaxing competition among male relatives3,4,5. Here we experimentally manipulate the relatedness of groups of male Drosophila melanogaster competing over females to demonstrate that, as expected, within-group relatedness inhibits male competition and female harm. Females exposed to groups of three brothers unrelated to the female had higher lifetime reproductive success and slower reproductive ageing compared to females exposed to groups of three males unrelated to each other. Triplets of brothers also fought less with each other, courted females less intensively and lived longer than triplets of unrelated males. However, associations among brothers may be vulnerable to invasion by minorities of unrelated males: when two brothers were matched with an unrelated male, the unrelated male sired on average twice as many offspring as either brother. These results demonstrate that relatedness can profoundly affect fitness through its modulation of intrasexual competition, as flies plastically adjust sexual behaviour in a manner consistent with kin-selection theory.

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Figure 1: The effect of male–male relatedness on female fitness.
Figure 2: The effect of male–male relatedness on male sexual behaviour and longevity.
Figure 3: Unrelated males outcompete brothers.

References

  1. Bourke, A. F. G. Principles of Social Evolution (Oxford Univ. Press, Oxford, 2011)

    Google Scholar 

  2. Parker, G. A. Sexual conflict over mating and fertilization: an overview. Phil. Trans. R. Soc. Lond. B 361, 235–259 (2006)

    CAS  Google Scholar 

  3. Rankin, D. J. Kin selection and the evolution of sexual conflict. J. Evol. Biol. 24, 71–81 (2011)

    CAS  PubMed  Google Scholar 

  4. Wild, G., Pizzari, T. & West, S. A. Sexual conflict in viscous populations: the effect of the timing of dispersal. Theor. Popul. Biol. 80, 298–316 (2011)

    PubMed  MATH  Google Scholar 

  5. Pizzari, T. & Gardner, A. The sociobiology of sex: inclusive fitness consequences of inter-sexual interactions. Phil. Trans. R. Soc. B 367, 2314–2323 (2012)

    PubMed  PubMed Central  Google Scholar 

  6. Edward, D. A., Fricke, C., Gerrard, D. T. & Chapman, T. Quantifying the life-history response to male exposure in female Drosophila melanogaster. Evolution 65, 564–573 (2011)

    PubMed  Google Scholar 

  7. 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)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chapman, T. et al. The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc. Natl Acad. Sci. USA 100, 9923–9928 (2003)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  10. 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)

    CAS  PubMed  Google Scholar 

  11. Anxolabéhère, D. Heterosis overdominance and frequency-dependent selection in Drosophila melanogaster at the sepia locus. Evolution 30, 523–534 (1976)

    PubMed  Google Scholar 

  12. Fu, W. & Noll, M. The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. Genes Dev. 11, 2066–2078 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Partridge, L. & Fowler, K. Non-mating costs of exposure to males in female Drosophila melanogaster. J. Insect Physiol. 36, 419–425 (1990)

    Google Scholar 

  14. Tan, C. K. W. et al. Sex-specific responses to sexual familiarity, and the role of olfaction in Drosophila. Proc. R. Soc. Lond. B 280, 20131691 (2013)

    Google Scholar 

  15. Le Galliard, J. F. et al. Sex ratio bias, male aggression, and population collapse in lizards. Proc. Natl Acad. Sci. USA 102, 18231–18236 (2005)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  16. Rankin, D. J. & Kokko, H. Sex, death and tragedy. Trends Ecol. Evol. 21, 225–226 (2006)

    PubMed  Google Scholar 

  17. Rankin, D. J., Dieckmann, U. & Kokko, H. Sexual conflict and the tragedy of the commons. Am. Nat. 177, 780–791 (2011)

    PubMed  Google Scholar 

  18. Fedorka, K. M. & Zuk, M. Sexual conflict and female immune suppression in the cricket, Allonemobious socius. J. Evol. Biol. 18, 1515–1522 (2005)

    PubMed  Google Scholar 

  19. McInnis, D. O., Schaffer, H. E. & Mettler, L. E. Field dispersal and population sizes of native Drosophila from North Carolina. Am. Nat. 119, 319–330 (1982)

    Google Scholar 

  20. Robinson, S. P., Kennington, W. J. & Simmons, L. W. Preference for related mates in the fruit fly, Drosophila melanogaster. Anim. Behav. 84, 1169–1176 (2012)

    Google Scholar 

  21. Hamilton, W. D. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 193–232 (1972)

    Google Scholar 

  22. Bourke, A. F. G. & Frank, N. R. Social Evolution in Ants (Princeton Univ. Press, 1995)

    Google Scholar 

  23. Packer, C. & Pusey, A. E. Cooperation and competition within coalitions of male lions: kin selection or game theory. Nature 296, 740–742 (1982)

    ADS  Google Scholar 

  24. McDonald, D. B. & Potts, W. K. Cooperative display and relatedness among males in a lek-mating bird. Science 266, 1030–1032 (1994)

    ADS  CAS  PubMed  Google Scholar 

  25. Petrie, M., Krupa, A. & Burke, T. Peacocks lek with relatives even in the absence of social and environmental cues. Nature 401, 155–157 (1999)

    ADS  CAS  Google Scholar 

  26. Krakauer, A. H. Kin selection and cooperative courtship in wild turkeys. Nature 434, 69–72 (2005)

    ADS  CAS  PubMed  Google Scholar 

  27. Den Boer, S., Baer, B. & Boomsma, J. J. Seminal fluid mediates ejaculate competition in social insects. Science 327, 1506–1509 (2010)

    ADS  CAS  PubMed  Google Scholar 

  28. Moore, A. J. & Pizzari, T. Quantitative genetic models of sexual conflict based on interacting phenotypes. Am. Nat. 165, S88–S97 (2005)

    PubMed  Google Scholar 

  29. Eldakar, O. T., Dlugos, M., Pepper, J. W. & Wilson, D. S. Population structure mediates sexual conflict in water striders. Science 326, 816 (2009)

    ADS  CAS  PubMed  Google Scholar 

  30. Buckling, A. & Brockhurst, M. A. Kin selection and the evolution of virulence. Heredity 100, 484–488 (2008)

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  32. Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for Biologists. (Cambridge Univ. Press, 2002)

    Google Scholar 

  33. Kleinbaum, D. G. & Klein, M. Survival analysis: A self-learning text. 3rd edn (Springer, 2012)

    MATH  Google Scholar 

  34. Charlesworth, B. Selection in populations with overlapping generations. I. The use of Malthusian parameters in population genetics. Theor. Popul. Biol. 1, 352–370 (1970)

    MathSciNet  CAS  PubMed  MATH  Google Scholar 

  35. Prout, T. & McChesney, F. Competition among immatures affects their adult fertility: population-dynamics. Am. Nat. 126, 521–558 (1985)

    Google Scholar 

  36. McGraw, J. B. & Caswell, H. Estimation of individual fitness from life-history data. Am. Nat. 147, 47–64 (1996)

    Google Scholar 

  37. Bastock, M. & Manning, A. The courtship behaviour of Drosophila melanogaster. Behaviour 8, 85–111 (1955)

    Google Scholar 

  38. Chen, S., Lee, A. Y., Bowens, N. M., Huber, R. & Kravitz, E. A. Fighting fruit flies: A model system for the study of aggression. Proc. Natl Acad. Sci. USA 99, 5664–5668 (2002)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  39. Jacobs, M. E. Influence of light on mating of Drosophila melanogaster. Ecology 41, 182–188 (1960)

    Google Scholar 

  40. Dierick, H. A. A method for quantifying aggression in male Drosophila melanogaster. Nature Protocols 2, 2712–2718 (2007)

    CAS  PubMed  Google Scholar 

  41. Nilsen, S. P., Chan, Y.-B., Huber, R. & Kravitz, E. A. Gender-selective patterns of aggressive behaviour in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 101, 12342–12347 (2004)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  42. McCullagh, P. & Nelder, J. A. Generalized Linear Models. 2nd edn (Chapman & Hall, 1989)

    MATH  Google Scholar 

  43. Liggett, R. E. & Delwiche, J. F. The beta-binomial model: variability in overdispersion across methods and over time. J. Sens. Stud. 20, 48–61 (2005)

    Google Scholar 

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Acknowledgements

We thank the following funding agencies: Marie Curie fellowship (PIEF-GA-2010-273010 to P.C.), the Wellcome Trust VIP award and NERC fellowship (to S.W.), NERC research grant and the Leverhulme Trust (to T.P.). We thank C. Garroway, J. Perry and S. Michaelides for technical help; and M. Bonsall, A. Buckling, G. McDonald, D. Noble, J. Perry, P. Pizzari, R. Snook and S. West for helpful discussions.

Author information

Author notes

  1. Pau Carazo and Cedric K. W. Tan: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Zoology, Edward Grey Institute, University of Oxford, Oxford OX1 3PS, UK,

    Pau Carazo, Cedric K. W. Tan, Felicity Allen, Stuart Wigby & Tommaso Pizzari

Authors
  1. Pau Carazo
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  2. Cedric K. W. Tan
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  3. Felicity Allen
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  4. Stuart Wigby
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Contributions

Experiment 1 was designed by P.C., S.W. and T.P., conducted by P.C. and F.A., and analysed by P.C. Experiment 2 was designed by P.C., C.K.W.T., S.W. and T.P., and conducted and analysed by P.C. Experiment 3 was designed and conducted by S.W. and P.C., and analysed by P.C. Experiment 4 was designed by C.K.W.T., T.P. and S.W., and conducted and analysed by C.K.W.T. The article was conceived and written by T.P. with input from P.C., C.K.W.T. and S.W.

Corresponding author

Correspondence to Tommaso Pizzari.

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Competing interests

The authors declare no competing financial interests.

Additional information

Data have been deposited in the Dryad Digital Repository at http://dx.doi.org/10.5061/dryad.9c7bq.

Extended data figures and tables

Extended Data Figure 1

a, Rate-sensitive estimates of individual female fitness (wind) over a gradient in population growth rates (r). Female fitness was estimated to be higher under high within-group male relatedness for values of r ranging from −0.1 to 0 (dark shaded area), a similar non-significant (0.05 < P < 0.08) pattern was extended for r = −0.2 and r = 0.1 (light shaded area). b, The effect of within-group male relatedness on population fitness. The relative fitness cost of reducing within-group male relatedness at different population growth rates (r). The dashed line identifies relative fitness of 1, where reduction in within-group male relatedness has no fitness cost. Reducing within-group male relatedness is always costly over the range of population growth rates explored, but particularly so with smaller growth rates.

Extended Data Table 1 Female rate-insensitive fitness measures in experiment 2
Full size table
Extended Data Table 2 Female post-mating responses in experiment 3
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Extended Data Table 3 Summary of statistical tests in experiment 4
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Extended Data Table 4 Effect of genotype of A male and genotype of B male on the response variable
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Carazo, P., Tan, C., Allen, F. et al. Within-group male relatedness reduces harm to females in Drosophila. Nature 505, 672–675 (2014). https://doi.org/10.1038/nature12949

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