Fitness trade-offs result in the illusion of social success

Jason B. Wolf, Jennifer A. Howie, Katie Parkinson, Nicole Gruenheit, Diogo Melo, Daniel Rozen, Christopher R L Thompson

Research output: Contribution to journalArticle

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Abstract

Cooperation is ubiquitous across the tree of life, from simple microbes to the complex social systems of animals [1]. Individuals cooperate by engaging in costly behaviors that can be exploited by other individuals who benefit by avoiding these associated costs. Thus, if successful exploitation of social partners during cooperative interactions increases relative fitness, then we expect selection to lead to the emergence of a single optimal winning strategy in which individuals maximize their gain from cooperation while minimizing their associated costs [2]. Such social "cheating" appears to be widespread in nature [3], including in several microbial systems [4-11], but despite the fitness advantages favoring social cheating, populations tend to harbor significant variation in social success rather than a single optimal winning strategy. Using the social amoeba Dictyostelium discoideum, we provide a possible explanation for the coexistence of such variation. We find that genotypes typically designated as "cheaters" [12] because they produce a disproportionate number of spores in chimeric fruiting bodies do not actually gain higher fitness as a result of this apparent advantage because they produce smaller, less viable spores than putative "losers." As a consequence of this trade-off between spore number and viability, genotypes with different spore production strategies, which give the appearance of differential social success, ultimately have similar realized fitness. These findings highlight the limitations of using single fitness proxies in evolutionary studies and suggest that interpreting social trait variation in terms of strategies like cheating or cooperating may be misleading unless these behaviors are considered in the context of the true multidimensional nature of fitness. If exploitation of social partners increases fitness, then selection should favor one optimal winning strategy. However, cheaters and losers often coexist. Here, Wolf etal. show that different social strategies can coexist in the social amoeba D.discoideum due to trade-offs between social traits, meaning that simple views of cheating may be illusory.

Original languageEnglish
Pages (from-to)1086-1090
Number of pages6
JournalCurrent Biology
Volume25
Issue number8
Early online date26 Mar 2015
DOIs
Publication statusPublished - 20 Apr 2015

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Spores
spores
Amoeba
Ports and harbors
Costs
Animals
Genotype
Costs and Cost Analysis
Dictyostelium discoideum
Dictyostelium
genotype
Proxy
wolves
fruiting bodies
cooperatives
viability
microorganisms
Population
animals
Sociological Factors

Cite this

Wolf, J. B., Howie, J. A., Parkinson, K., Gruenheit, N., Melo, D., Rozen, D., & Thompson, C. R. L. (2015). Fitness trade-offs result in the illusion of social success. Current Biology, 25(8), 1086-1090. https://doi.org/10.1016/j.cub.2015.02.061

Fitness trade-offs result in the illusion of social success. / Wolf, Jason B.; Howie, Jennifer A.; Parkinson, Katie; Gruenheit, Nicole; Melo, Diogo; Rozen, Daniel; Thompson, Christopher R L.

In: Current Biology, Vol. 25, No. 8, 20.04.2015, p. 1086-1090.

Research output: Contribution to journalArticle

Wolf, JB, Howie, JA, Parkinson, K, Gruenheit, N, Melo, D, Rozen, D & Thompson, CRL 2015, 'Fitness trade-offs result in the illusion of social success', Current Biology, vol. 25, no. 8, pp. 1086-1090. https://doi.org/10.1016/j.cub.2015.02.061
Wolf JB, Howie JA, Parkinson K, Gruenheit N, Melo D, Rozen D et al. Fitness trade-offs result in the illusion of social success. Current Biology. 2015 Apr 20;25(8):1086-1090. https://doi.org/10.1016/j.cub.2015.02.061
Wolf, Jason B. ; Howie, Jennifer A. ; Parkinson, Katie ; Gruenheit, Nicole ; Melo, Diogo ; Rozen, Daniel ; Thompson, Christopher R L. / Fitness trade-offs result in the illusion of social success. In: Current Biology. 2015 ; Vol. 25, No. 8. pp. 1086-1090.
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