Detecting natural selection in trait-trait coevolution

Abstract No phenotypic trait evolves independently of all other traits, but the cause of trait-trait coevolution is poorly understood. While the coevolution could arise simply from pleiotropic mutations that simultaneously affect the traits concerned, it could also result from multivariate natural s...

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Main Authors: Daohan Jiang, Jianzhi Zhang
Format: Article
Language:English
Published: BMC 2023-09-01
Series:BMC Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1186/s12862-023-02164-4
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author Daohan Jiang
Jianzhi Zhang
author_facet Daohan Jiang
Jianzhi Zhang
author_sort Daohan Jiang
collection DOAJ
description Abstract No phenotypic trait evolves independently of all other traits, but the cause of trait-trait coevolution is poorly understood. While the coevolution could arise simply from pleiotropic mutations that simultaneously affect the traits concerned, it could also result from multivariate natural selection favoring certain trait relationships. To gain a general mechanistic understanding of trait-trait coevolution, we examine the evolution of 220 cell morphology traits across 16 natural strains of the yeast Saccharomyces cerevisiae and the evolution of 24 wing morphology traits across 110 fly species of the family Drosophilidae, along with the variations of these traits among gene deletion or mutation accumulation lines (a.k.a. mutants). For numerous trait pairs, the phenotypic correlation among evolutionary lineages differs significantly from that among mutants. Specifically, we find hundreds of cases where the evolutionary correlation between traits is strengthened or reversed relative to the mutational correlation, which, according to our population genetic simulation, is likely caused by multivariate selection. Furthermore, we detect selection for enhanced modularity of the yeast traits analyzed. Together, these results demonstrate that trait-trait coevolution is shaped by natural selection and suggest that the pleiotropic structure of mutation is not optimal. Because the morphological traits analyzed here are chosen largely because of their measurability and thereby are not expected to be biased with regard to natural selection, our conclusion is likely general.
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spelling doaj.art-53f58e137ddb4facb8327f54e2ab43ae2023-11-19T12:10:50ZengBMCBMC Ecology and Evolution2730-71822023-09-0123111410.1186/s12862-023-02164-4Detecting natural selection in trait-trait coevolutionDaohan Jiang0Jianzhi Zhang1Department of Ecology and Evolutionary Biology, University of MichiganDepartment of Ecology and Evolutionary Biology, University of MichiganAbstract No phenotypic trait evolves independently of all other traits, but the cause of trait-trait coevolution is poorly understood. While the coevolution could arise simply from pleiotropic mutations that simultaneously affect the traits concerned, it could also result from multivariate natural selection favoring certain trait relationships. To gain a general mechanistic understanding of trait-trait coevolution, we examine the evolution of 220 cell morphology traits across 16 natural strains of the yeast Saccharomyces cerevisiae and the evolution of 24 wing morphology traits across 110 fly species of the family Drosophilidae, along with the variations of these traits among gene deletion or mutation accumulation lines (a.k.a. mutants). For numerous trait pairs, the phenotypic correlation among evolutionary lineages differs significantly from that among mutants. Specifically, we find hundreds of cases where the evolutionary correlation between traits is strengthened or reversed relative to the mutational correlation, which, according to our population genetic simulation, is likely caused by multivariate selection. Furthermore, we detect selection for enhanced modularity of the yeast traits analyzed. Together, these results demonstrate that trait-trait coevolution is shaped by natural selection and suggest that the pleiotropic structure of mutation is not optimal. Because the morphological traits analyzed here are chosen largely because of their measurability and thereby are not expected to be biased with regard to natural selection, our conclusion is likely general.https://doi.org/10.1186/s12862-023-02164-4FlyMorphologyMutationModularityPleiotropyYeast
spellingShingle Daohan Jiang
Jianzhi Zhang
Detecting natural selection in trait-trait coevolution
BMC Ecology and Evolution
Fly
Morphology
Mutation
Modularity
Pleiotropy
Yeast
title Detecting natural selection in trait-trait coevolution
title_full Detecting natural selection in trait-trait coevolution
title_fullStr Detecting natural selection in trait-trait coevolution
title_full_unstemmed Detecting natural selection in trait-trait coevolution
title_short Detecting natural selection in trait-trait coevolution
title_sort detecting natural selection in trait trait coevolution
topic Fly
Morphology
Mutation
Modularity
Pleiotropy
Yeast
url https://doi.org/10.1186/s12862-023-02164-4
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