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Mutational Pleiotropy and the Strength of Stabilizing Selection Within and Between Functional Modules of Gene Expression

View ORCID ProfileJulie M. Collet, Katrina McGuigan, Scott L. Allen, Stephen F. Chenoweth and Mark W. Blows
Genetics April 1, 2018 vol. 208 no. 4 1601-1616; https://doi.org/10.1534/genetics.118.300776
Julie M. Collet
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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  • ORCID record for Julie M. Collet
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Katrina McGuigan
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Scott L. Allen
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Stephen F. Chenoweth
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Mark W. Blows
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Abstract

Variational modules, sets of pleiotropically covarying traits, affect phenotypic evolution, and therefore are predicted to reflect functional modules, such that traits within a variational module also share a common function. Such an alignment of function and pleiotropy is expected to facilitate adaptation by reducing the deleterious effects of mutations, and by allowing coordinated evolution of functionally related sets of traits. Here, we adopt a high-dimensional quantitative genetic approach using a large number of gene expression traits in Drosophila serrata to test whether functional grouping, defined by gene ontology (GO terms), predicts variational modules. Mutational or standing genetic covariance was significantly greater than among randomly grouped sets of genes for 38% of our functional groups, indicating that GO terms can predict variational modularity to some extent. We estimated stabilizing selection acting on mutational covariance to test the prediction that functional pleiotropy would result in reduced deleterious effects of mutations within functional modules. Stabilizing selection within functional modules was weaker than that acting on randomly grouped sets of genes in only 23% of functional groups, indicating that functional alignment can reduce deleterious effects of pleiotropic mutation but typically does not. Our analyses also revealed the presence of variational modules that spanned multiple functions.

  • modularity
  • pleiotropy
  • genotype–phenotype map
  • Drosophila serrata
  • gene expression
  • Received March 23, 2017.
  • Accepted January 30, 2018.
  • Copyright © 2018 by the Genetics Society of America
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Volume 208 Issue 4, April 2018

Genetics: 208 (4)

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Genetics of complex traits
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Mutational Pleiotropy and the Strength of Stabilizing Selection Within and Between Functional Modules of Gene Expression

View ORCID ProfileJulie M. Collet, Katrina McGuigan, Scott L. Allen, Stephen F. Chenoweth and Mark W. Blows
Genetics April 1, 2018 vol. 208 no. 4 1601-1616; https://doi.org/10.1534/genetics.118.300776
Julie M. Collet
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Julie M. Collet
  • For correspondence: j.collet@uq.edu.au
Katrina McGuigan
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Scott L. Allen
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Stephen F. Chenoweth
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Mark W. Blows
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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Citation

Mutational Pleiotropy and the Strength of Stabilizing Selection Within and Between Functional Modules of Gene Expression

View ORCID ProfileJulie M. Collet, Katrina McGuigan, Scott L. Allen, Stephen F. Chenoweth and Mark W. Blows
Genetics April 1, 2018 vol. 208 no. 4 1601-1616; https://doi.org/10.1534/genetics.118.300776
Julie M. Collet
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Julie M. Collet
  • For correspondence: j.collet@uq.edu.au
Katrina McGuigan
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Scott L. Allen
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
  • Find this author on Google Scholar
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  • Search for this author on this site
Stephen F. Chenoweth
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
  • Find this author on Google Scholar
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  • Search for this author on this site
Mark W. Blows
School of Biological Sciences, The University of Queensland, Brisbane 4072, Queensland, Australia
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  • Search for this author on this site

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