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

Authors
  • Toker, Itai Antoine1
  • Lev, Itamar2
  • Mor, Yael3
  • Gurevich, Yael4
  • Fisher, Doron5
  • Houri-Zeevi, Leah5
  • Antonova, Olga5
  • Doron, Hila5
  • Anava, Sarit5
  • Gingold, Hila5
  • Hadany, Lilach4
  • Shaham, Shai6
  • Rechavi, Oded7
  • 1 Department of Neurobiology, Faculty of Life Sciences & Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel. Electronic address: [email protected] , (Israel)
  • 2 Department of Neurobiology, Faculty of Life Sciences & Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel. Electronic address: [email protected] , (Israel)
  • 3 Department of Neurobiology, Faculty of Life Sciences & Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel. Electronic address: [email protected] , (Israel)
  • 4 School of Plant Sciences and Food Security, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel. , (Israel)
  • 5 Department of Neurobiology, Faculty of Life Sciences & Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel. , (Israel)
  • 6 Laboratory of Developmental Genetics, The Rockefeller University, New York, NY, USA.
  • 7 Department of Neurobiology, Faculty of Life Sciences & Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel. Electronic address: [email protected] , (Israel)
Type
Published Article
Journal
Developmental cell
Publication Date
Feb 07, 2022
Volume
57
Issue
3
Identifiers
DOI: 10.1016/j.devcel.2022.01.005
PMID: 35134343
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

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. Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

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