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

Laurence J. Belcher, Philip G. Madgwick, Satoshi Kuwana, Balint Stewart, Christopher R.L. Thompson, Jason B. Wolf

Research output: Contribution to journalArticlepeer-review

2 Citations (SciVal)

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.

Original languageEnglish
Article numbere2111233119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number29
DOIs
Publication statusPublished - 19 Jul 2022

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. This work was supported by a Natural Environment Research Council (NERC) GW4+ PhD Studentship to L.J.B., a Biotechnology and Biological Sciences Research Council (BBSRC) SWBio PhD Studentship to P.G.M., grants from the BBSRC (BB/M01035X/1 and BB/M007146/1) and NERC (NE/ V012002/1) to C.R.L.T. and J.B.W., and a Wellcome Trust Investigator Award (WT095643AIA) to C.R.L.T. Portions of the paper were developed from content that appeared in the PhD theses of L.J.B. and P.G.M. We thank two anonymous reviewers for comments that greatly improved the presentation of our work.

Keywords

  • altruism
  • Cooperation
  • developmental constraints
  • enforcement
  • tragedy of the commons

ASJC Scopus subject areas

  • General

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