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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, Christian Frøkjær-Jensen, Thomas Boulin, Henrique Teotónio, Christian Braendle
doi: https://doi.org/10.1101/2020.06.29.176990
Paul Vigne
1Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France
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Clotilde Gimond
1Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France
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Céline Ferrari
1Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France
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Anne Vielle
1Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France
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Johan Hallin
1Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France
2Institut de Biologie Intégrative et des Systèmes, Département de Biologie, Université Laval, Québec, Canada
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Ania Pino-Querido
3IBENS, Département de Biologie, Ecole Normale Supérieure, CNRS, Inserm, PSL Research University, F-75005 Paris, France
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Sonia El Mouridi
4Institut NeuroMyoGène, CNRS, Inserm, Université de Lyon, Lyon, France
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Christian Frøkjær-Jensen
5King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Thuwal, Saudi Arabia
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Thomas Boulin
4Institut NeuroMyoGène, CNRS, Inserm, Université de Lyon, Lyon, France
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Henrique Teotónio
3IBENS, Département de Biologie, Ecole Normale Supérieure, CNRS, Inserm, PSL Research University, F-75005 Paris, France
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Christian Braendle
1Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France
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  • For correspondence: braendle@unice.fr
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Abstract

Genetic assimilation – the evolutionary process by which an ancestral environmentally sensitive phenotype is made constitutive – is a fundamental concept in biology. Its evolutionary relevance is debated, and our understanding of its prevalence, and underlying genetics and molecular mechanisms, is poor. Matricidal hatching is an extreme form of maternal provisioning induced by adverse conditions, which varies among Caenorhabditis elegans populations. We identified wild isolates, sampled from natural populations across multiple years and locations, that express a derived state of near-constitutive matricidal hatching. A single amino acid change in kcnl-1, encoding a small-conductance calcium-activated potassium channel subunit, explains most of this variation. A gain-of-function mutation altering the S6 transmembrane domain causes inappropriate activation of the K+ channel, leading to reduced vulval muscle excitability, and thus reduced expulsion of embryos, irrespective of environment. Using reciprocal allelic replacements, we show that this amino acid change is sufficient to induce constitutive matricidal hatching whilst re-establishing the ancestral protein abolishes matricidal hatching and restores egg-laying, thereby doubling lifetime reproductive fitness under benign conditions. While highly deleterious in the laboratory, experimental evolution showed that KNCL-1(V530L) is maintained under fluctuating resource availability. Selection on a single point mutation can therefore underlie the genetic assimilation of an ancestrally plastic trait with drastic life-history consequences.

Competing Interest Statement

The authors have declared no competing interest.

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Posted June 29, 2020.
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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, Christian Frøkjær-Jensen, Thomas Boulin, Henrique Teotónio, Christian Braendle
bioRxiv 2020.06.29.176990; doi: https://doi.org/10.1101/2020.06.29.176990
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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, Christian Frøkjær-Jensen, Thomas Boulin, Henrique Teotónio, Christian Braendle
bioRxiv 2020.06.29.176990; doi: https://doi.org/10.1101/2020.06.29.176990

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