Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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

Nature Ecology & Evolution volume 4, pages 745–752 (2020)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

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.

References

  1. Edward, D. A. & Chapman, T. The evolution and significance of male mate choice. Trends Ecol. Evol. 26, 647–654 (2011).

    Article  PubMed  Google Scholar 

  2. West-Eberhard, M. J. Sexual selection, social competition, and evolution. Proc. Am. Phil. Soc. 123, 222–234 (1979).

    Google Scholar 

  3. Rowell., J. T. & Servedio, M. R. Gentlemen prefer blondes: the evolution of mate preference among strategically allocated males. Am. Nat. 173, 12–25 (2009).

    Article  PubMed  Google Scholar 

  4. Venner, S., Bernstein, C., Dray, S. & Bel-Venner, M.-C. Make love not war: when should less competitive males choose low-quality but defendable females? Am. Nat. 175, 650–661 (2010).

    Article  PubMed  Google Scholar 

  5. Wedell, N., Gage, M. J. & Parker, G. A. Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17, 313–320 (2002).

    Article  Google Scholar 

  6. Härdling, R., Gosden, T. & Aguilée, R. Male mating constraints affect mutual mate choice: prudent male courting and sperm-limited females. Am. Nat. 172, 259–271 (2008).

    Article  PubMed  Google Scholar 

  7. 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).

    Article  PubMed  Google Scholar 

  8. Carazo, P., Tan, C. K. W., Allen, F., Wigby, S. & Pizzari, T. Within-group male relatedness reduces harm to females in Drosophila. Nature 505, 672–675 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chippindale, A. K., Berggren, M., Alpern, J. H. M. & Montgomerie, R. Does kin selection moderate sexual conflict in Drosophila? Proc. Biol. Sci. 282, 20151417 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hollis, B., Kawecki, T. J. & Keller, L. No evidence that within‐group male relatedness reduces harm to females in Drosophila. Ecol. Evol. 5, 979–983 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Martin, E. S. & Long, T. A. F. Are flies kind to kin? The role of intra- and inter-sexual relatedness in mediating reproductive conflict. Proc. Biol. Sci. 282, 20151991 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Le Page, S. et al. Male relatedness and familiarity are required to modulate male-induced harm to females in Drosophila. Proc. Biol. Sci. 284, 20170441 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Lymbery, S. J. & Simmons, L. W. Males harm females less when competing with familiar relatives. Proc. Biol. Sci. 284, 20171984 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Daniel, M. J. & Rodd, F. H. Female guppies can recognize kin but only avoid incest when previously mated. Behav. Ecol. 27, 55–61 (2016).

    Article  Google Scholar 

  15. Hamilton, W. D. The genetical evolution of social behaviour. II. J. Theor. Biol. 7, 17–52 (1964).

    Article  CAS  PubMed  Google Scholar 

  16. West, S. A. & Gardner, A. Altruism, spite, and greenbeards. Science 327, 1341–1344 (2010).

    Article  CAS  PubMed  Google Scholar 

  17. Staddon, J. E. R. Adaptive Behavior and Learning (Cambridge Univ. Press, 1983).

  18. Sargent, R. C., Gross, M. R. & Van Den Berghe, E. P. Male mate choice in fishes. Anim. Behav. 34, 545–550 (1986).

    Article  Google Scholar 

  19. Price, A. C. & Rodd, F. H. The effect of social environment on male–male competition in guppies (Poecilia reticulata). Ethology 112, 22–32 (2006).

    Article  Google Scholar 

  20. Houde, A. E. Sex, Color, and Mate Choice in Guppies (Princeton Univ. Press, 1997).

  21. Dosen, L. D. & Montgomerie, R. Female size influences mate preferences of male guppies. Ethology 110, 245–255 (2004).

    Article  Google Scholar 

  22. Hain, T. J. A. & Neff, B. D. Multiple paternity and kin recognition mechanisms in a guppy population. Mol. Ecol. 16, 3938–3946 (2007).

    Article  PubMed  Google Scholar 

  23. Farr, J. A. Male rarity or novelty, female choice behavior, and sexual selection in the guppy, Poecilia reticulata Peters (Pisces: Poeciliidae). Evolution 31, 162–168 (1977).

    Article  PubMed  Google Scholar 

  24. Hughes, K. A., Du, L., Rodd, F. H. & Reznick, D. N. Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Anim. Behav. 58, 907–916 (1999).

    Article  CAS  PubMed  Google Scholar 

  25. Eakley, A. L. & Houde, A. E. Possible role of female discrimination against ‘redundant’ males in the evolution of colour pattern polymorphism in guppies. Proc. Biol. Sci. 271, S299–S301 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Zajitschek, S. R. & Brooks, R. C. Distinguishing the effects of familiarity, relatedness, and color pattern rarity on attractiveness and measuring their effects on sexual selection in guppies (Poecilia reticulata). Am. Nat. 172, 843–854 (2008).

    Article  PubMed  Google Scholar 

  27. Hampton, K. J., Hughes, K. A. & Houde, A. E. The allure of the distinctive: reduced sexual responsiveness of female guppies to ‘redundant’ male colour patterns. Ethology 115, 475–481 (2009).

    Article  Google Scholar 

  28. Hughes, K. A., Houde, A. E., Price, A. C. & Rodd, F. H. Mating advantage for rare males in wild guppy populations. Nature 503, 108–110 (2013).

    Article  CAS  PubMed  Google Scholar 

  29. Graber, R. E., Senagolage, M., Ross, E., Houde, A. E. & Hughes, K. A. Mate preference for novel phenotypes: a fresh face matters. Ethology 121, 17–25 (2015).

    Article  Google Scholar 

  30. Daniel, M. J., Koffinas, L. & Hughes, K. A. Habituation underpins preference for mates with novel phenotypes in the guppy. Proc. Biol. Sci. 286, 20190435 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Mann, K. D., Turnell, E. R., Atema, J. & Gerlach, G. Kin recognition in juvenile zebrafish (Danio rerio) based on olfactory cues. Biol. Bull. 205, 224–225 (2003).

    Article  CAS  PubMed  Google Scholar 

  32. Mehlis, M., Bakker, T. C. M. & Frommen, J. G. Smells like sib spirit: kin recognition in three-spined sticklebacks (Gasterosteus aculeatus) is mediated by olfactory cues. Anim. Cogn. 11, 643–650 (2008).

    Article  PubMed  Google Scholar 

  33. Olsén, K. H. in Fish Chemoreception (ed. Hara, T. J.) Ch. 11 (Springer, 1992).

  34. Griffiths, S. W. & Magurran, A. E. Familiarity in schooling fish: how long does it take to acquire? Anim. Behav. 53, 945–949 (1997).

    Article  Google Scholar 

  35. Mariette, M. M., Zajitschek, S. R. K., Garcia, C. M. & Brooks, R. C. The effects of familiarity and group size on mating preferences in the guppy, Poecilia reticulata. J. Evol. Biol. 23, 1772–1782 (2010).

    Article  CAS  PubMed  Google Scholar 

  36. Piyapong, C. et al. Kin assortment in juvenile shoals in wild guppy populations. Heredity (Edinb) 106, 749–756 (2011).

    Article  CAS  Google Scholar 

  37. Villinger, J. & Waldman, B. Self-referent MHC type matching in frog tadpoles. Proc. Biol. Sci. 275, 1225–1230 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Mateo, J. M. Self-referent phenotype matching and long-term maintenance of kin recognition. Anim. Behav. 80, 929–935 (2010).

    Article  Google Scholar 

  39. Neff, B. D. & Sherman, P. W. In vitro fertilization reveals offspring recognition via self‐referencing in a fish with paternal care and cuckoldry. Ethology 111, 425–438 (2005).

    Article  Google Scholar 

  40. Hain, T. J. A. & Neff, B. D. Promiscuity drives self-referent kin recognition. Curr. Biol. 16, 1807–1811 (2006).

    Article  CAS  PubMed  Google Scholar 

  41. Gerlach, G., Hodgins-Davis, A., Avolio, C. & Schunter, C. Kin recognition in zebrafish: a 24-hour window for olfactory imprinting. Proc. Biol. Sci. 275, 2165–2170 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Bisazza, A., Novarini, N. & Pilastro, A. Male body size and male–male competition: interspecific variation in poeciliid fishes. Ital. J. Zool. 63, 365–369 (1996).

    Article  Google Scholar 

  43. Horth, L. Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki). Proc. Biol. Sci. 270, 1033–1040 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Paterson, I. G., Crispo, E., Kinnison, M. T., Hendry, A. P. & Bentzen, P. Characterization of tetranucleotide microsatellite markers in guppy (Poecilia reticulata). Mol. Ecol. Notes 5, 269–271 (2005).

    Article  CAS  Google Scholar 

  45. Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. & Shipley, P. micro‐checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538 (2004).

    Article  CAS  Google Scholar 

  46. Jones, A. G. gerud 2.0: a computer program for the reconstruction of parental genotypes from half‐sib progeny arrays with known or unknown parents. Mol. Ecol. Notes 5, 708–711 (2005).

    Article  CAS  Google Scholar 

  47. Sefc, K. M. & Koblmüller, S. Assessing parent numbers from offspring genotypes: the importance of marker polymorphism. J. Hered. 100, 197–205 (2009).

    Article  CAS  PubMed  Google Scholar 

  48. Pitcher, T. E., Neff, B. D., Rodd, F. H. & Rowe, L. Multiple mating and sequential mate choice in guppies: females trade up. Proc. Biol. Sci. 270, 1623–1629 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Rousset, F. & Billiard, S. A theoretical basis for measures of kin selection in subdivided populations: finite populations and localized dispersal. J. Evol. Biol. 13, 814–825 (2000).

    Article  Google Scholar 

  50. Krupp, D. B. & Taylor, P. D. Enhanced kin recognition through population estimation. Am. Nat. 181, 707–714 (2013).

    Article  PubMed  Google Scholar 

  51. Queller, D. C. Genetic relatedness in viscous populations. Evol. Ecol. 8, 70–73 (1994).

    Article  Google Scholar 

  52. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018); https://www.R-project.org/

  53. Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.4-5 https://cran.r-project.org/web/packages/vegan/index.html (2017).

  54. Legendre, P., Legendre, L. Numerical Ecology (Elsevier, 2012).

  55. Huang, Y., Xu, H., Calian, V. & Hsu, J. C. To permute or not to permute. Bioinformatics 22, 2244–2248 (2006).

    Article  CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada

    Mitchel J. Daniel

  2. Department of Biological Science, Florida State University, Tallahassee, FL, USA

    Mitchel J. Daniel

  3. Department of Computer Science and Software Engineering, Rose-Hulman Institute of Technology, Terre Haute, IN, USA

    Robert J. Williamson

Authors
  1. Mitchel J. Daniel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert J. Williamson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Mitchel J. Daniel.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

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

Reporting Summary

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-020-1152-3

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing