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Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans

It is unknown whether transient transgenerational epigenetic responses to environmental challenges affect the process of evolution, which typically unfolds over many generations. Here, we show that in C. elegans, inherited small RNAs control genetic variation by regulating the crucial decision of wh...

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Autores principales: Toker, Itai Antoine, Lev, Itamar, Mor, Yael, Gurevich, Yael, Fisher, Doron, Houri-Zeevi, Leah, Antonova, Olga, Doron, Hila, Anava, Sarit, Gingold, Hila, Hadany, Lilach, Shaham, Shai, Rechavi, Oded
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8826646/
https://www.ncbi.nlm.nih.gov/pubmed/35134343
http://dx.doi.org/10.1016/j.devcel.2022.01.005
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author Toker, Itai Antoine
Lev, Itamar
Mor, Yael
Gurevich, Yael
Fisher, Doron
Houri-Zeevi, Leah
Antonova, Olga
Doron, Hila
Anava, Sarit
Gingold, Hila
Hadany, Lilach
Shaham, Shai
Rechavi, Oded
author_facet Toker, Itai Antoine
Lev, Itamar
Mor, Yael
Gurevich, Yael
Fisher, Doron
Houri-Zeevi, Leah
Antonova, Olga
Doron, Hila
Anava, Sarit
Gingold, Hila
Hadany, Lilach
Shaham, Shai
Rechavi, Oded
author_sort Toker, Itai Antoine
collection PubMed
description It is unknown whether transient transgenerational epigenetic responses to environmental challenges affect the process of evolution, which typically unfolds over many generations. Here, we show that in C. elegans, inherited small RNAs control genetic variation by regulating the crucial decision of whether to self-fertilize or outcross. We found that under stressful temperatures, younger hermaphrodites secrete a male-attracting pheromone. Attractiveness transmits transgenerationally to unstressed progeny via heritable small RNAs and the Argonaute Heritable RNAi Deficient-1 (HRDE-1). We identified an endogenous small interfering RNA pathway, enriched in endo-siRNAs that target sperm genes, that transgenerationally regulates sexual attraction, male prevalence, and outcrossing rates. Multigenerational mating competition experiments and mathematical simulations revealed that over generations, animals that inherit attractiveness mate more and their alleles spread in the population. We propose that the sperm serves as a “stress-sensor” that, via small RNA inheritance, promotes outcrossing in challenging environments when increasing genetic variation is advantageous.
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spelling pubmed-88266462022-02-14 Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans Toker, Itai Antoine Lev, Itamar Mor, Yael Gurevich, Yael Fisher, Doron Houri-Zeevi, Leah Antonova, Olga Doron, Hila Anava, Sarit Gingold, Hila Hadany, Lilach Shaham, Shai Rechavi, Oded Dev Cell Article It is unknown whether transient transgenerational epigenetic responses to environmental challenges affect the process of evolution, which typically unfolds over many generations. Here, we show that in C. elegans, inherited small RNAs control genetic variation by regulating the crucial decision of whether to self-fertilize or outcross. We found that under stressful temperatures, younger hermaphrodites secrete a male-attracting pheromone. Attractiveness transmits transgenerationally to unstressed progeny via heritable small RNAs and the Argonaute Heritable RNAi Deficient-1 (HRDE-1). We identified an endogenous small interfering RNA pathway, enriched in endo-siRNAs that target sperm genes, that transgenerationally regulates sexual attraction, male prevalence, and outcrossing rates. Multigenerational mating competition experiments and mathematical simulations revealed that over generations, animals that inherit attractiveness mate more and their alleles spread in the population. We propose that the sperm serves as a “stress-sensor” that, via small RNA inheritance, promotes outcrossing in challenging environments when increasing genetic variation is advantageous. Cell Press 2022-02-07 /pmc/articles/PMC8826646/ /pubmed/35134343 http://dx.doi.org/10.1016/j.devcel.2022.01.005 Text en © 2022 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Toker, Itai Antoine
Lev, Itamar
Mor, Yael
Gurevich, Yael
Fisher, Doron
Houri-Zeevi, Leah
Antonova, Olga
Doron, Hila
Anava, Sarit
Gingold, Hila
Hadany, Lilach
Shaham, Shai
Rechavi, Oded
Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans
title Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans
title_full Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans
title_fullStr Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans
title_full_unstemmed Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans
title_short Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans
title_sort transgenerational inheritance of sexual attractiveness via small rnas enhances evolvability in c. elegans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8826646/
https://www.ncbi.nlm.nih.gov/pubmed/35134343
http://dx.doi.org/10.1016/j.devcel.2022.01.005
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