The paradox of cooperation among selfish cancer cells

Abstract It is traditionally assumed that during cancer development, tumor cells abort their initially cooperative behavior (i.e., cheat) in favor of evolutionary strategies designed solely to enhance their own fitness (i.e., a “selfish” life style) at the expense of that of the multicellular organi...

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Main Authors: Jean‐Pascal Capp, Frédéric Thomas, Andriy Marusyk, Antoine M. Dujon, Sophie Tissot, Robert Gatenby, Benjamin Roche, Beata Ujvari, James DeGregori, Joel S. Brown, Aurora M. Nedelcu
Format: Article
Language:English
Published: Wiley 2023-07-01
Series:Evolutionary Applications
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Online Access:https://doi.org/10.1111/eva.13571
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author Jean‐Pascal Capp
Frédéric Thomas
Andriy Marusyk
Antoine M. Dujon
Sophie Tissot
Robert Gatenby
Benjamin Roche
Beata Ujvari
James DeGregori
Joel S. Brown
Aurora M. Nedelcu
author_facet Jean‐Pascal Capp
Frédéric Thomas
Andriy Marusyk
Antoine M. Dujon
Sophie Tissot
Robert Gatenby
Benjamin Roche
Beata Ujvari
James DeGregori
Joel S. Brown
Aurora M. Nedelcu
author_sort Jean‐Pascal Capp
collection DOAJ
description Abstract It is traditionally assumed that during cancer development, tumor cells abort their initially cooperative behavior (i.e., cheat) in favor of evolutionary strategies designed solely to enhance their own fitness (i.e., a “selfish” life style) at the expense of that of the multicellular organism. However, the growth and progress of solid tumors can also involve cooperation among these presumed selfish cells (which, by definition, should be noncooperative) and with stromal cells. The ultimate and proximate reasons behind this paradox are not fully understood. Here, in the light of current theories on the evolution of cooperation, we discuss the possible evolutionary mechanisms that could explain the apparent cooperative behaviors among selfish malignant cells. In addition to the most classical explanations for cooperation in cancer and in general (by‐product mutualism, kin selection, direct reciprocity, indirect reciprocity, network reciprocity, group selection), we propose the idea that “greenbeard” effects are relevant to explaining some cooperative behaviors in cancer. Also, we discuss the possibility that malignant cooperative cells express or co‐opt cooperative traits normally expressed by healthy cells. We provide examples where considerations of these processes could help understand tumorigenesis and metastasis and argue that this framework provides novel insights into cancer biology and potential strategies for cancer prevention and treatment.
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spelling doaj.art-40f663a816d647f3bbcfcd57342f99de2023-07-24T07:47:08ZengWileyEvolutionary Applications1752-45712023-07-011671239125610.1111/eva.13571The paradox of cooperation among selfish cancer cellsJean‐Pascal Capp0Frédéric Thomas1Andriy Marusyk2Antoine M. Dujon3Sophie Tissot4Robert Gatenby5Benjamin Roche6Beata Ujvari7James DeGregori8Joel S. Brown9Aurora M. Nedelcu10Toulouse Biotechnology Institute University of Toulouse, INSA, CNRS, INRAE Toulouse FranceCREEC, MIVEGEC University of Montpellier, CNRS, IRD Montpellier FranceDepartment of Cancer Physiology H Lee Moffitt Cancer Center and Research Institute Tampa Florida USACentre for Integrative Ecology, School of Life and Environmental Sciences Deakin University Geelong Victoria AustraliaDepartment of Biochemistry and Molecular Genetics University of Colorado Anschutz Medical Campus Aurora Colorado USADepartment of Cancer Physiology H Lee Moffitt Cancer Center and Research Institute Tampa Florida USADepartment of Biochemistry and Molecular Genetics University of Colorado Anschutz Medical Campus Aurora Colorado USACentre for Integrative Ecology, School of Life and Environmental Sciences Deakin University Geelong Victoria AustraliaDepartment of Biochemistry and Molecular Genetics University of Colorado Anschutz Medical Campus Aurora Colorado USADepartment of Cancer Physiology H Lee Moffitt Cancer Center and Research Institute Tampa Florida USADepartment of Biology University of New Brunswick Fredericton New Brunswick CanadaAbstract It is traditionally assumed that during cancer development, tumor cells abort their initially cooperative behavior (i.e., cheat) in favor of evolutionary strategies designed solely to enhance their own fitness (i.e., a “selfish” life style) at the expense of that of the multicellular organism. However, the growth and progress of solid tumors can also involve cooperation among these presumed selfish cells (which, by definition, should be noncooperative) and with stromal cells. The ultimate and proximate reasons behind this paradox are not fully understood. Here, in the light of current theories on the evolution of cooperation, we discuss the possible evolutionary mechanisms that could explain the apparent cooperative behaviors among selfish malignant cells. In addition to the most classical explanations for cooperation in cancer and in general (by‐product mutualism, kin selection, direct reciprocity, indirect reciprocity, network reciprocity, group selection), we propose the idea that “greenbeard” effects are relevant to explaining some cooperative behaviors in cancer. Also, we discuss the possibility that malignant cooperative cells express or co‐opt cooperative traits normally expressed by healthy cells. We provide examples where considerations of these processes could help understand tumorigenesis and metastasis and argue that this framework provides novel insights into cancer biology and potential strategies for cancer prevention and treatment.https://doi.org/10.1111/eva.13571cancercheatingcooperationgreenbeardselfishness
spellingShingle Jean‐Pascal Capp
Frédéric Thomas
Andriy Marusyk
Antoine M. Dujon
Sophie Tissot
Robert Gatenby
Benjamin Roche
Beata Ujvari
James DeGregori
Joel S. Brown
Aurora M. Nedelcu
The paradox of cooperation among selfish cancer cells
Evolutionary Applications
cancer
cheating
cooperation
greenbeard
selfishness
title The paradox of cooperation among selfish cancer cells
title_full The paradox of cooperation among selfish cancer cells
title_fullStr The paradox of cooperation among selfish cancer cells
title_full_unstemmed The paradox of cooperation among selfish cancer cells
title_short The paradox of cooperation among selfish cancer cells
title_sort paradox of cooperation among selfish cancer cells
topic cancer
cheating
cooperation
greenbeard
selfishness
url https://doi.org/10.1111/eva.13571
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