Multilevel selection analysis of a microbial social trait

Abstract The study of microbial communities often leads to arguments for the evolution of cooperation due to group benefits. However, multilevel selection models caution against the uncritical assumption that group benefits will lead to the evolution of cooperation. We analyze a microbial social tra...

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Main Authors: Laura de Vargas Roditi, Kerry E Boyle, Joao B Xavier
Format: Article
Language:English
Published: Springer Nature 2013-08-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.1038/msb.2013.42
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author Laura de Vargas Roditi
Kerry E Boyle
Joao B Xavier
author_facet Laura de Vargas Roditi
Kerry E Boyle
Joao B Xavier
author_sort Laura de Vargas Roditi
collection DOAJ
description Abstract The study of microbial communities often leads to arguments for the evolution of cooperation due to group benefits. However, multilevel selection models caution against the uncritical assumption that group benefits will lead to the evolution of cooperation. We analyze a microbial social trait to precisely define the conditions favoring cooperation. We combine the multilevel partition of the Price equation with a laboratory model system: swarming in Pseudomonas aeruginosa. We parameterize a population dynamics model using competition experiments where we manipulate expression, and therefore the cost‐to‐benefit ratio of swarming cooperation. Our analysis shows that multilevel selection can favor costly swarming cooperation because it causes population expansion. However, due to high costs and diminishing returns constitutive cooperation can only be favored by natural selection when relatedness is high. Regulated expression of cooperative genes is a more robust strategy because it provides the benefits of swarming expansion without the high cost or the diminishing returns. Our analysis supports the key prediction that strong group selection does not necessarily mean that microbial cooperation will always emerge.
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spelling doaj-art-576ebcb8a11a49d38931e7f130cae5fe2025-08-20T03:46:37ZengSpringer NatureMolecular Systems Biology1744-42922013-08-019111210.1038/msb.2013.42Multilevel selection analysis of a microbial social traitLaura de Vargas Roditi0Kerry E Boyle1Joao B Xavier2Program in Computational Biology, Memorial Sloan‐Kettering Cancer CenterProgram in Computational Biology, Memorial Sloan‐Kettering Cancer CenterProgram in Computational Biology, Memorial Sloan‐Kettering Cancer CenterAbstract The study of microbial communities often leads to arguments for the evolution of cooperation due to group benefits. However, multilevel selection models caution against the uncritical assumption that group benefits will lead to the evolution of cooperation. We analyze a microbial social trait to precisely define the conditions favoring cooperation. We combine the multilevel partition of the Price equation with a laboratory model system: swarming in Pseudomonas aeruginosa. We parameterize a population dynamics model using competition experiments where we manipulate expression, and therefore the cost‐to‐benefit ratio of swarming cooperation. Our analysis shows that multilevel selection can favor costly swarming cooperation because it causes population expansion. However, due to high costs and diminishing returns constitutive cooperation can only be favored by natural selection when relatedness is high. Regulated expression of cooperative genes is a more robust strategy because it provides the benefits of swarming expansion without the high cost or the diminishing returns. Our analysis supports the key prediction that strong group selection does not necessarily mean that microbial cooperation will always emerge.https://doi.org/10.1038/msb.2013.42conflictcooperationmetabolic prudencePseudomonas aeruginosaswarming
spellingShingle Laura de Vargas Roditi
Kerry E Boyle
Joao B Xavier
Multilevel selection analysis of a microbial social trait
Molecular Systems Biology
conflict
cooperation
metabolic prudence
Pseudomonas aeruginosa
swarming
title Multilevel selection analysis of a microbial social trait
title_full Multilevel selection analysis of a microbial social trait
title_fullStr Multilevel selection analysis of a microbial social trait
title_full_unstemmed Multilevel selection analysis of a microbial social trait
title_short Multilevel selection analysis of a microbial social trait
title_sort multilevel selection analysis of a microbial social trait
topic conflict
cooperation
metabolic prudence
Pseudomonas aeruginosa
swarming
url https://doi.org/10.1038/msb.2013.42
work_keys_str_mv AT lauradevargasroditi multilevelselectionanalysisofamicrobialsocialtrait
AT kerryeboyle multilevelselectionanalysisofamicrobialsocialtrait
AT joaobxavier multilevelselectionanalysisofamicrobialsocialtrait