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Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora

Phenotypic plasticity in ancestral populations is hypothesized to facilitate adaptation, but evidence is piecemeal and often contradictory. Further, whether ancestral plasticity increases the probability of parallel adaptive changes has not been explored. The most general finding is that ancestral r...

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Autores principales: Wood, Daniel P., Holmberg, Jon A., Osborne, Owen G., Helmstetter, Andrew J., Dunning, Luke T., Ellison, Amy R., Smith, Rhian J., Lighten, Jackie, Papadopulos, Alexander S. T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9998271/
https://www.ncbi.nlm.nih.gov/pubmed/36702857
http://dx.doi.org/10.1038/s41559-022-01975-w
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author Wood, Daniel P.
Holmberg, Jon A.
Osborne, Owen G.
Helmstetter, Andrew J.
Dunning, Luke T.
Ellison, Amy R.
Smith, Rhian J.
Lighten, Jackie
Papadopulos, Alexander S. T.
author_facet Wood, Daniel P.
Holmberg, Jon A.
Osborne, Owen G.
Helmstetter, Andrew J.
Dunning, Luke T.
Ellison, Amy R.
Smith, Rhian J.
Lighten, Jackie
Papadopulos, Alexander S. T.
author_sort Wood, Daniel P.
collection PubMed
description Phenotypic plasticity in ancestral populations is hypothesized to facilitate adaptation, but evidence is piecemeal and often contradictory. Further, whether ancestral plasticity increases the probability of parallel adaptive changes has not been explored. The most general finding is that ancestral responses to a new environment are reversed following adaptation (known as reversion). We investigated the contribution of ancestral plasticity to adaptive evolution of gene expression in two independently evolved lineages of zinc-tolerant Silene uniflora. We found that the general pattern of reversion is driven by the absence of a widespread stress response in zinc-adapted plants compared with zinc-sensitive plants. We show that ancestral plasticity that moves expression closer to the optimum value in the new environment influences the evolution of gene expression among genes that are likely to be involved in adaptation and increases the chance that genes are recruited repeatedly during adaptation. However, despite convergence in gene expression levels between independently adapted lineages, ancestral plasticity does not influence how similar expression values of adaptive genes become. Surprisingly, we also observed that ancestral plasticity that increases fitness often becomes genetically determined and fixed, that is, genetically assimilated. These results emphasize the important role of ancestral plasticity in parallel adaptation.
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spelling pubmed-99982712023-03-11 Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora Wood, Daniel P. Holmberg, Jon A. Osborne, Owen G. Helmstetter, Andrew J. Dunning, Luke T. Ellison, Amy R. Smith, Rhian J. Lighten, Jackie Papadopulos, Alexander S. T. Nat Ecol Evol Article Phenotypic plasticity in ancestral populations is hypothesized to facilitate adaptation, but evidence is piecemeal and often contradictory. Further, whether ancestral plasticity increases the probability of parallel adaptive changes has not been explored. The most general finding is that ancestral responses to a new environment are reversed following adaptation (known as reversion). We investigated the contribution of ancestral plasticity to adaptive evolution of gene expression in two independently evolved lineages of zinc-tolerant Silene uniflora. We found that the general pattern of reversion is driven by the absence of a widespread stress response in zinc-adapted plants compared with zinc-sensitive plants. We show that ancestral plasticity that moves expression closer to the optimum value in the new environment influences the evolution of gene expression among genes that are likely to be involved in adaptation and increases the chance that genes are recruited repeatedly during adaptation. However, despite convergence in gene expression levels between independently adapted lineages, ancestral plasticity does not influence how similar expression values of adaptive genes become. Surprisingly, we also observed that ancestral plasticity that increases fitness often becomes genetically determined and fixed, that is, genetically assimilated. These results emphasize the important role of ancestral plasticity in parallel adaptation. Nature Publishing Group UK 2023-01-26 2023 /pmc/articles/PMC9998271/ /pubmed/36702857 http://dx.doi.org/10.1038/s41559-022-01975-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Wood, Daniel P.
Holmberg, Jon A.
Osborne, Owen G.
Helmstetter, Andrew J.
Dunning, Luke T.
Ellison, Amy R.
Smith, Rhian J.
Lighten, Jackie
Papadopulos, Alexander S. T.
Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora
title Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora
title_full Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora
title_fullStr Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora
title_full_unstemmed Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora
title_short Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in Silene uniflora
title_sort genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in silene uniflora
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9998271/
https://www.ncbi.nlm.nih.gov/pubmed/36702857
http://dx.doi.org/10.1038/s41559-022-01975-w
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