Pleiotropic constraints promote the evolution of cooperation in cellular groups

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. These cell lineages occur within microbial communities, and multicellular organisms in the form of tumours and cancer. In contrast to an earlier study, here we show how...

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Main Authors: Bentley, MA, Yates, CA, Hein, J, Preston, GM, Foster, KR
Format: Journal article
Language:English
Published: Public Library of Science 2022
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author Bentley, MA
Yates, CA
Hein, J
Preston, GM
Foster, KR
author_facet Bentley, MA
Yates, CA
Hein, J
Preston, GM
Foster, KR
author_sort Bentley, MA
collection OXFORD
description The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. These cell lineages occur within microbial communities, and multicellular organisms in the form of tumours and cancer. In contrast to an earlier study, here we show how the evolution of pleiotropic genetic architectures—which link the expression of cooperative and private traits—can protect against cheater lineages and allow cooperation to evolve. We develop an age-structured model of cellular groups and show that cooperation breaks down more slowly within groups that tie expression to a private trait than in groups that do not. We then show that this results in group selection for pleiotropy, which strongly promotes cooperation by limiting the emergence of cheater lineages. These results predict that pleiotropy will rapidly evolve, so long as groups persist long enough for cheater lineages to threaten cooperation. Our results hold when pleiotropic links can be undermined by mutations, when pleiotropy is itself costly, and in mixed-genotype groups such as those that occur in microbes. Finally, we consider features of multicellular organisms—a germ line and delayed reproductive maturity—and show that pleiotropy is again predicted to be important for maintaining cooperation. The study of cancer in multicellular organisms provides the best evidence for pleiotropic constraints, where abberant cell proliferation is linked to apoptosis, senescence, and terminal differentiation. Alongside development from a single cell, we propose that the evolution of pleiotropic constraints has been critical for cooperation in many cellular groups.
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spelling oxford-uuid:b3f07537-3646-4290-95f9-b0af8b2195672022-06-23T13:45:23ZPleiotropic constraints promote the evolution of cooperation in cellular groupsJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:b3f07537-3646-4290-95f9-b0af8b219567EnglishSymplectic ElementsPublic Library of Science2022Bentley, MAYates, CAHein, JPreston, GMFoster, KRThe evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. These cell lineages occur within microbial communities, and multicellular organisms in the form of tumours and cancer. In contrast to an earlier study, here we show how the evolution of pleiotropic genetic architectures—which link the expression of cooperative and private traits—can protect against cheater lineages and allow cooperation to evolve. We develop an age-structured model of cellular groups and show that cooperation breaks down more slowly within groups that tie expression to a private trait than in groups that do not. We then show that this results in group selection for pleiotropy, which strongly promotes cooperation by limiting the emergence of cheater lineages. These results predict that pleiotropy will rapidly evolve, so long as groups persist long enough for cheater lineages to threaten cooperation. Our results hold when pleiotropic links can be undermined by mutations, when pleiotropy is itself costly, and in mixed-genotype groups such as those that occur in microbes. Finally, we consider features of multicellular organisms—a germ line and delayed reproductive maturity—and show that pleiotropy is again predicted to be important for maintaining cooperation. The study of cancer in multicellular organisms provides the best evidence for pleiotropic constraints, where abberant cell proliferation is linked to apoptosis, senescence, and terminal differentiation. Alongside development from a single cell, we propose that the evolution of pleiotropic constraints has been critical for cooperation in many cellular groups.
spellingShingle Bentley, MA
Yates, CA
Hein, J
Preston, GM
Foster, KR
Pleiotropic constraints promote the evolution of cooperation in cellular groups
title Pleiotropic constraints promote the evolution of cooperation in cellular groups
title_full Pleiotropic constraints promote the evolution of cooperation in cellular groups
title_fullStr Pleiotropic constraints promote the evolution of cooperation in cellular groups
title_full_unstemmed Pleiotropic constraints promote the evolution of cooperation in cellular groups
title_short Pleiotropic constraints promote the evolution of cooperation in cellular groups
title_sort pleiotropic constraints promote the evolution of cooperation in cellular groups
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AT yatesca pleiotropicconstraintspromotetheevolutionofcooperationincellulargroups
AT heinj pleiotropicconstraintspromotetheevolutionofcooperationincellulargroups
AT prestongm pleiotropicconstraintspromotetheevolutionofcooperationincellulargroups
AT fosterkr pleiotropicconstraintspromotetheevolutionofcooperationincellulargroups