A single-nucleotide change underlies the genetic assimilation of a plastic trait

Paul Vigne; Clotilde Gimond; Céline Ferrari; Anne Vielle; Johan Hallin; Ania Pino-Querido; Sonia El Mouridi; Laure Mignerot; Christian Frøkjær-Jensen; Thomas Boulin; Henrique Teotónio; Christian Braendle

doi:10.1126/sciadv.abd9941

A single-nucleotide change underlies the genetic assimilation of a plastic trait

Paul Vigne, Clotilde Gimond, Céline Ferrari, Anne Vielle, Johan Hallin, Ania Pino-Querido, Sonia El Mouridi, Laure Mignerot, Christian Frøkjær-Jensen, Thomas Boulin, Henrique Teotónio, Christian Braendle

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21 Scopus citations

Abstract

Genetic assimilation—the evolutionary process by which an environmentally induced phenotype is made constitutive—represents a fundamental concept in evolutionary biology. Thought to reflect adaptive phenotypic plasticity, matricidal hatching in nematodes is triggered by maternal nutrient deprivation to allow for protection or resource provisioning of offspring. Here, we report natural Caenorhabditis elegans populations harboring genetic variants expressing a derived state of near-constitutive matricidal hatching. These variants exhibit a single amino acid change (V530L) in KCNL-1, a small-conductance calcium-activated potassium channel subunit. This gain-of-function mutation causes matricidal hatching by strongly reducing the sensitivity to environmental stimuli triggering egg-laying. We show that reestablishing the canonical KCNL-1 protein in matricidal isolates is sufficient to restore canonical egg-laying. While highly deleterious in constant food environments, KCNL-1 V530L is maintained under fluctuating resource availability. A single point mutation can therefore underlie the genetic assimilation—by either genetic drift or selection—of an ancestrally plastic trait.

Original language	English (US)
Pages (from-to)	eabd9941
Journal	Science advances
Volume	7
Issue number	6
DOIs	https://doi.org/10.1126/sciadv.abd9941
State	Published - Feb 3 2021

Bibliographical note

KAUST Repository Item: Exported on 2021-02-05
Acknowledgements: For helpful discussions and pointing out the curious phenotype of JU751, we would like to thank M.-A. Félix. For help with experimental work and data analysis, we thank B. Billard, S. Fausett, N. Poullet, G. Bouzouida, N. Schwartz-Tamoglia, N. Callemeyn-Torre, J.-A. Lepesant, R. Salle, J. Costa, and F. Mallard. For advice and helpful comments on previous versions of the manuscript, we thank E. Abouheif, L. Noble, and three anonymous reviewers. Strains and materials were provided by M.-A. Félix, the C. elegans Natural Diversity Resource (CeNDR), and the Caenorhabditis Genetics Center (CGC), which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440).

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10.1126/sciadv.abd9941

https://repository.kaust.edu.sa/bitstream/10754/667218/1/eabd9941.full.pdf

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@article{6d979328e08341e48f7e4ff898c97d5b,

title = "A single-nucleotide change underlies the genetic assimilation of a plastic trait",

abstract = "Genetic assimilation—the evolutionary process by which an environmentally induced phenotype is made constitutive—represents a fundamental concept in evolutionary biology. Thought to reflect adaptive phenotypic plasticity, matricidal hatching in nematodes is triggered by maternal nutrient deprivation to allow for protection or resource provisioning of offspring. Here, we report natural Caenorhabditis elegans populations harboring genetic variants expressing a derived state of near-constitutive matricidal hatching. These variants exhibit a single amino acid change (V530L) in KCNL-1, a small-conductance calcium-activated potassium channel subunit. This gain-of-function mutation causes matricidal hatching by strongly reducing the sensitivity to environmental stimuli triggering egg-laying. We show that reestablishing the canonical KCNL-1 protein in matricidal isolates is sufficient to restore canonical egg-laying. While highly deleterious in constant food environments, KCNL-1 V530L is maintained under fluctuating resource availability. A single point mutation can therefore underlie the genetic assimilation—by either genetic drift or selection—of an ancestrally plastic trait.",

author = "Paul Vigne and Clotilde Gimond and C{\'e}line Ferrari and Anne Vielle and Johan Hallin and Ania Pino-Querido and {El Mouridi}, Sonia and Laure Mignerot and Christian Fr{\o}kj{\ae}r-Jensen and Thomas Boulin and Henrique Teot{\'o}nio and Christian Braendle",

note = "KAUST Repository Item: Exported on 2021-02-05 Acknowledgements: For helpful discussions and pointing out the curious phenotype of JU751, we would like to thank M.-A. F{\'e}lix. For help with experimental work and data analysis, we thank B. Billard, S. Fausett, N. Poullet, G. Bouzouida, N. Schwartz-Tamoglia, N. Callemeyn-Torre, J.-A. Lepesant, R. Salle, J. Costa, and F. Mallard. For advice and helpful comments on previous versions of the manuscript, we thank E. Abouheif, L. Noble, and three anonymous reviewers. Strains and materials were provided by M.-A. F{\'e}lix, the C. elegans Natural Diversity Resource (CeNDR), and the Caenorhabditis Genetics Center (CGC), which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440).",

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AU - Vigne, Paul

AU - Gimond, Clotilde

AU - Ferrari, Céline

AU - Vielle, Anne

AU - Hallin, Johan

AU - Pino-Querido, Ania

AU - El Mouridi, Sonia

AU - Mignerot, Laure

AU - Frøkjær-Jensen, Christian

AU - Boulin, Thomas

AU - Teotónio, Henrique

AU - Braendle, Christian

N1 - KAUST Repository Item: Exported on 2021-02-05 Acknowledgements: For helpful discussions and pointing out the curious phenotype of JU751, we would like to thank M.-A. Félix. For help with experimental work and data analysis, we thank B. Billard, S. Fausett, N. Poullet, G. Bouzouida, N. Schwartz-Tamoglia, N. Callemeyn-Torre, J.-A. Lepesant, R. Salle, J. Costa, and F. Mallard. For advice and helpful comments on previous versions of the manuscript, we thank E. Abouheif, L. Noble, and three anonymous reviewers. Strains and materials were provided by M.-A. Félix, the C. elegans Natural Diversity Resource (CeNDR), and the Caenorhabditis Genetics Center (CGC), which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440).

PY - 2021/2/3

Y1 - 2021/2/3

N2 - Genetic assimilation—the evolutionary process by which an environmentally induced phenotype is made constitutive—represents a fundamental concept in evolutionary biology. Thought to reflect adaptive phenotypic plasticity, matricidal hatching in nematodes is triggered by maternal nutrient deprivation to allow for protection or resource provisioning of offspring. Here, we report natural Caenorhabditis elegans populations harboring genetic variants expressing a derived state of near-constitutive matricidal hatching. These variants exhibit a single amino acid change (V530L) in KCNL-1, a small-conductance calcium-activated potassium channel subunit. This gain-of-function mutation causes matricidal hatching by strongly reducing the sensitivity to environmental stimuli triggering egg-laying. We show that reestablishing the canonical KCNL-1 protein in matricidal isolates is sufficient to restore canonical egg-laying. While highly deleterious in constant food environments, KCNL-1 V530L is maintained under fluctuating resource availability. A single point mutation can therefore underlie the genetic assimilation—by either genetic drift or selection—of an ancestrally plastic trait.

AB - Genetic assimilation—the evolutionary process by which an environmentally induced phenotype is made constitutive—represents a fundamental concept in evolutionary biology. Thought to reflect adaptive phenotypic plasticity, matricidal hatching in nematodes is triggered by maternal nutrient deprivation to allow for protection or resource provisioning of offspring. Here, we report natural Caenorhabditis elegans populations harboring genetic variants expressing a derived state of near-constitutive matricidal hatching. These variants exhibit a single amino acid change (V530L) in KCNL-1, a small-conductance calcium-activated potassium channel subunit. This gain-of-function mutation causes matricidal hatching by strongly reducing the sensitivity to environmental stimuli triggering egg-laying. We show that reestablishing the canonical KCNL-1 protein in matricidal isolates is sufficient to restore canonical egg-laying. While highly deleterious in constant food environments, KCNL-1 V530L is maintained under fluctuating resource availability. A single point mutation can therefore underlie the genetic assimilation—by either genetic drift or selection—of an ancestrally plastic trait.

UR - http://hdl.handle.net/10754/667218

UR - https://advances.sciencemag.org/lookup/doi/10.1126/sciadv.abd9941

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DO - 10.1126/sciadv.abd9941

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VL - 7

SP - eabd9941

JO - Science advances

JF - Science advances

IS - 6

ER -

A single-nucleotide change underlies the genetic assimilation of a plastic trait

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