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Antagonistic pleiotropy for carbon use is rare in new mutations

Pleiotropic effects of mutations underlie diverse biological phenomena such as ageing and specialization. In particular, antagonistic pleiotropy (“AP”: when a mutation has opposite fitness effects in different environments) generates tradeoffs, which may constrain adaptation. Models of adaptation ty...

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Autores principales: Sane, Mrudula, Miranda, Joshua John, Agashe, Deepa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6203952/
https://www.ncbi.nlm.nih.gov/pubmed/30095155
http://dx.doi.org/10.1111/evo.13569
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author Sane, Mrudula
Miranda, Joshua John
Agashe, Deepa
author_facet Sane, Mrudula
Miranda, Joshua John
Agashe, Deepa
author_sort Sane, Mrudula
collection PubMed
description Pleiotropic effects of mutations underlie diverse biological phenomena such as ageing and specialization. In particular, antagonistic pleiotropy (“AP”: when a mutation has opposite fitness effects in different environments) generates tradeoffs, which may constrain adaptation. Models of adaptation typically assume that AP is common ‐ especially among large‐effect mutations ‐ and that pleiotropic effect sizes are positively correlated. Empirical tests of these assumptions have focused on de novo beneficial mutations arising under strong selection. However, most mutations are actually deleterious or neutral, and may contribute to standing genetic variation that can subsequently drive adaptation. We quantified the incidence, nature, and effect size of pleiotropy for carbon utilization across 80 single mutations in Escherichia coli that arose under mutation accumulation (i.e., weak selection). Although ∼46% of the mutations were pleiotropic, only 11% showed AP; among beneficial mutations, only ∼4% showed AP. In some environments, AP was more common in large‐effect mutations; and AP effect sizes across environments were often negatively correlated. Thus, AP for carbon use is generally rare (especially among beneficial mutations); is not consistently enriched in large‐effect mutations; and often involves weakly deleterious antagonistic effects. Our unbiased quantification of mutational effects therefore suggests that antagonistic pleiotropy may be unlikely to cause maladaptive tradeoffs.
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spelling pubmed-62039522018-10-27 Antagonistic pleiotropy for carbon use is rare in new mutations Sane, Mrudula Miranda, Joshua John Agashe, Deepa Evolution Original Articles Pleiotropic effects of mutations underlie diverse biological phenomena such as ageing and specialization. In particular, antagonistic pleiotropy (“AP”: when a mutation has opposite fitness effects in different environments) generates tradeoffs, which may constrain adaptation. Models of adaptation typically assume that AP is common ‐ especially among large‐effect mutations ‐ and that pleiotropic effect sizes are positively correlated. Empirical tests of these assumptions have focused on de novo beneficial mutations arising under strong selection. However, most mutations are actually deleterious or neutral, and may contribute to standing genetic variation that can subsequently drive adaptation. We quantified the incidence, nature, and effect size of pleiotropy for carbon utilization across 80 single mutations in Escherichia coli that arose under mutation accumulation (i.e., weak selection). Although ∼46% of the mutations were pleiotropic, only 11% showed AP; among beneficial mutations, only ∼4% showed AP. In some environments, AP was more common in large‐effect mutations; and AP effect sizes across environments were often negatively correlated. Thus, AP for carbon use is generally rare (especially among beneficial mutations); is not consistently enriched in large‐effect mutations; and often involves weakly deleterious antagonistic effects. Our unbiased quantification of mutational effects therefore suggests that antagonistic pleiotropy may be unlikely to cause maladaptive tradeoffs. John Wiley and Sons Inc. 2018-09-13 2018-10 /pmc/articles/PMC6203952/ /pubmed/30095155 http://dx.doi.org/10.1111/evo.13569 Text en © 2018 The Author(s). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Sane, Mrudula
Miranda, Joshua John
Agashe, Deepa
Antagonistic pleiotropy for carbon use is rare in new mutations
title Antagonistic pleiotropy for carbon use is rare in new mutations
title_full Antagonistic pleiotropy for carbon use is rare in new mutations
title_fullStr Antagonistic pleiotropy for carbon use is rare in new mutations
title_full_unstemmed Antagonistic pleiotropy for carbon use is rare in new mutations
title_short Antagonistic pleiotropy for carbon use is rare in new mutations
title_sort antagonistic pleiotropy for carbon use is rare in new mutations
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6203952/
https://www.ncbi.nlm.nih.gov/pubmed/30095155
http://dx.doi.org/10.1111/evo.13569
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