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Developmental constraints enforce altruism and avert the tragedy of the commons in a social microbe

Belcher, Laurence J; Madgwick, Philip G; Kuwana, Satoshi; Stewart, Balint; Thompson, Christopher RL; Wolf, Jason B; (2022) Developmental constraints enforce altruism and avert the tragedy of the commons in a social microbe. Proceedings of the National Academy of Sciences of the United States of America , 119 (29) , Article e2111233119. 10.1073/pnas.2111233119. Green open access

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Abstract

Organisms often cooperate through the production of freely available public goods. This can greatly benefit the group but is vulnerable to the “tragedy of the commons” if individuals lack the motivation to make the necessary investment into public goods production. Relatedness to groupmates can motivate individual investment because group success ultimately benefits their genes’ own self-interests. However, systems often lack mechanisms that can reliably ensure that relatedness is high enough to promote cooperation. Consequently, groups face a persistent threat from the tragedy unless they have a mechanism to enforce investment when relatedness fails to provide adequate motivation. To understand the real threat posed by the tragedy and whether groups can avert its impact, we determine how the social amoeba Dictyostelium discoideum responds as relatedness decreases to levels that should induce the tragedy. We find that, while investment in public goods declines as overall within-group relatedness declines, groups avert the expected catastrophic collapse of the commons by continuing to invest, even when relatedness should be too low to incentivize any contribution. We show that this is due to a developmental buffering system that generates enforcement because insufficient cooperation perturbs the balance of a negative feedback system controlling multicellular development. This developmental constraint enforces investment under the conditions expected to be most tragic, allowing groups to avert a collapse in cooperation. These results help explain how mechanisms that suppress selfishness and enforce cooperation can arise inadvertently as a by-product of constraints imposed by selection on different traits.

Type: Article
Title: Developmental constraints enforce altruism and avert the tragedy of the commons in a social microbe
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1073/pnas.2111233119
Publisher version: http://dx.doi.org/10.1073/pnas.2111233119
Language: English
Additional information: © 2022 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (https://creativecommons.org/licenses/by/4.0/).
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Genetics, Evolution and Environment
URI: https://discovery.ucl.ac.uk/id/eprint/10187630
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