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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.

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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.

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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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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
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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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