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Social Epistasis Amplifies the Fitness Costs of Deleterious Mutations, Engendering Rapid Fitness Decline Among Modernized Populations

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Abstract

Deleterious mutations are typically understood exclusively in terms of their harmful effects on carrier organisms. But there are convincing reasons to think that such adverse effects are not confined to the individual level. We argue that in social species, interorganismal gene-gene interactions, which in previous literatures have been termed social epistasis, allow genomes carrying deleterious mutations to reduce via group-level pleiotropy the fitness of others, including noncarriers. This fitness reduction occurs by way of degradation of group-level processes that optimize the reproductive ecology of a population for intergroup competition through, among other mechanisms, suppression of free-riding. Such damage to group regulatory processes suggests a hidden role for the accumulation of behavior-altering "spiteful" mutations in the dynamics of the demographic transition—these mutations may have contributed to the maladaptive outcomes of this process, such as widespread subreplacement fertility. A structured population model is presented describing aspects of this social epistasis amplification model. This phenomenon is also considered as a potential explanation for the results of Calhoun’s mouse utopia experiments, which provide an opportunity to directly test a major prediction stemming from the model.

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Notes

  1. Mutation accumulation research involving the nematode Caenorhabditis elegans indicates that, even when there are no reductions in viability (Keightley and Caballero 1997), behavioral changes, such as degraded chemotaxis and locomotion, can nevertheless be observed (Ajie et al. 2005). On this basis, Lynch (2016) has speculated that in human populations, behavioral degradation via mutation accumulation may be occurring at a faster rate than intrinsic fitness loss.

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Acknowledgements

We are grateful to two anonymous reviewers for comments that substantially improved this manuscript. We are especially grateful also to Prof. AJ Figueredo and Dr. Bruce Charlton for detailed discussion of and commentary on several of the ideas put forward in the present work.

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Authors and Affiliations

  1. Technische Universität Chemnitz, Chemnitz, Germany

    Michael A. Woodley of Menie & Radomir N. Pestow

  2. Center Leo Apostel for Interdisciplinary Studies, Vrije Universiteit Brussel, Brussels, Belgium

    Michael A. Woodley of Menie

  3. Cornell University, Ithaca, NY, USA

    Matthew A. Sarraf

  4. Department of Psychology, University of Arizona, Tucson, AZ, USA

    Heitor B. F. Fernandes

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Woodley of Menie, M.A., Sarraf, M.A., Pestow, R.N. et al. Social Epistasis Amplifies the Fitness Costs of Deleterious Mutations, Engendering Rapid Fitness Decline Among Modernized Populations. Evolutionary Psychological Science 3, 181–191 (2017). https://doi.org/10.1007/s40806-017-0084-x

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