Males optimally balance selfish and kin-selected strategies of sexual competition in the guppy

Abstract

Resolving the strategies by which organisms compete for limited resources is key to understanding behavioural and social evolution. When competing for matings, males in many species allocate mating effort preferentially towards higher-quality females. How males balance this against avoiding competition with rival males, who should also prefer high-quality females, is poorly understood. Kin selection theory further complicates these dynamics: males should avoid competition with close relatives especially because of added, indirect fitness costs. However, whether between-male relatedness modulates the intensity of intrasexual competition is equivocal. Here, we develop and test an analytical model describing how males should optimally allocate their mating efforts in response to information about differences in female quality, competitor presence/absence and competitor relatedness. Using freely interacting groups of Trinidadian guppies (Poecilia reticulata), we show concordance between observed and predicted mating effort allocation across all combinations of these factors. Thus, male mating effort is sensitive to variation in female quality, competitor presence and competitor relatedness, which is consistent with a kin-selected strategy of male–male competition. The fit of our model’s predictions demonstrates that males integrate assessments of female quality and competitive context in a quantitatively meaningful way, implicating a competitive strategy that has been fine-tuned to maximize inclusive fitness gains.

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Fig. 1: The profitability (that is, brood size divided by the estimated sire number) and standard length of wild-caught females (n = 36).
Fig. 2: The rate at which focal males (n = 50) attempted copulation with small, medium and large females that were unattended, attended by a non-kin rival or attended by a brother rival.
Fig. 3: Average predicted and corrected observed proportions of mating effort (that is, following time) that focal males (n = 50) allocated towards small, medium and large females, when no rival, a non-kin rival or a brother rival was pursuing the same female.

Data availability

Data supporting this study are available as Excel spreadsheets as part of the Supplementary Data.

Code availability

The source code for the simulated behavioural trials can be found at https://github.com/williarj/GuppySim2017.

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Acknowledgements

We thank A. De Serrano, A. Li and many undergraduate assistants for their help in rearing the fish. A. De Serrano, A. Li, L. Rowe, D. McLennan, A. Agrawal, J. Levine, D. Punzalan, F. H. Rodd, K. Hughes and A. Wardlaw provided comments on our experimental design, model and/or analyses. T. Paton, T. Harrison and S. Wright assisted with genotyping. We also thank I. Ramnarine and the Government of Trinidad and Tobago for permission to collect the guppies. This work was supported by funding from the National Sciences and Engineering Research Council to M.J.D. (grant no. CGSM-427283-2012).

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M.J.D. designed the experiment and analytical model, and conducted and analysed the behavioural and molecular work. R.J.W. designed the individual-based model. M.J.D. wrote the article with input from R.J.W.

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Correspondence to Mitchel J. Daniel.

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Supplementary Information

Supplementary Methods, discussion, Figs. 1–6 and Tables 1–6.

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Supplementary Data

Excel spreadsheets containing the data supporting the article’s empirical experiments: (1) wild-caught female profitabilities, (2) male–male relatedness behavioural experiment and (3) male colour pattern behavioural experiment.

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Daniel, M.J., Williamson, R.J. Males optimally balance selfish and kin-selected strategies of sexual competition in the guppy. Nat Ecol Evol 4, 745–752 (2020). https://doi.org/10.1038/s41559-020-1152-3

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