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Pleiotropy as a mechanism to stabilize cooperation

Nature volume 431, pages 693–696 (2004)Cite this article

Abstract

Most genes affect many traits1,2,3,4. This phenomenon, known as pleiotropy, is a major constraint on evolution because adaptive change in one trait may be prevented because it would compromise other traits affected by the same genes2,4. Here we show that pleiotropy can have an unexpected effect and benefit one of the most enigmatic of adaptations—cooperation. A spectacular act of cooperation occurs in the social amoeba Dictyostelium discoideum, in which some cells die to form a stalk that holds the other cells aloft as reproductive spores5,6. We have identified a gene, dimA7, in D. discoideum that has two contrasting effects. It is required to receive the signalling molecule DIF-1 that causes differentiation into prestalk cells. Ignoring DIF-1 and not becoming prestalk should allow cells to cheat by avoiding the stalk. However, we find that in aggregations containing the wild-type cells, lack of the dimA gene results in exclusion from spores. This pleiotropic linkage of stalk and spore formation limits the potential for cheating in D. discoideum because defecting on prestalk cell production results in an even greater reduction in spores. We propose that the evolution of pleiotropic links between cheating and personal costs can stabilize cooperative adaptations.

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Figure 1: dimA- cells occupy the prespore zone and behave like a cheater in chimaeras.
Figure 2: The dimA- mutant loses out in the fruiting body.
Figure 3: AX4/dimA- chimaeras produce the same number of spores as wild type (AX4) alone.
Figure 4: The majority of AX4 prestalk cells switch fate and become prespore cells when in chimaeras with dimA-.

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Acknowledgements

Thank you to N. Mehdiabadi and G. Velicer for helpful comments. This material is based upon work supported by the National Science Foundation, and C.R.L.T. was supported by a Wellcome Trust International Prize Travelling Research Fellowship.

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Author notes

  1. Kevin R. Foster and Chris R. L. Thompson: These authors contributed equally to this work.

Authors and Affiliations

  1. Ecology and Evolution, Rice University, Houston, Texas, 77005, USA

    Kevin R. Foster, Joan E. Strassmann & David C. Queller

  2. Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas, 77030, USA

    Gad Shaulsky & Chris R. L. Thompson

  3. School of Biological Sciences, University of Manchester, M13 9PT, Manchester, UK

    Chris R. L. Thompson

Authors
  1. Kevin R. Foster
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  2. Gad Shaulsky
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  5. Chris R. L. Thompson
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Correspondence to Kevin R. Foster or Chris R. L. Thompson.

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Foster, K., Shaulsky, G., Strassmann, J. et al. Pleiotropy as a mechanism to stabilize cooperation. Nature 431, 693–696 (2004). https://doi.org/10.1038/nature02894

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