RRC ID 76075
Author Toker IA, Lev I, Mor Y, Gurevich Y, Fisher D, Houri-Zeevi L, Antonova O, Doron H, Anava S, Gingold H, Hadany L, Shaham S, Rechavi O.
Title Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans.
Journal Dev Cell
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.
Volume 57(3)
Pages 298-309.e9
Published 2022-2-7
DOI 10.1016/j.devcel.2022.01.005
PII S1534-5807(22)00005-3
PMID 35134343
PMC PMC8826646
MeSH Animals Biological Evolution* Caenorhabditis elegans / genetics* Caenorhabditis elegans Proteins / metabolism Environment Female Gene Expression Regulation Inheritance Patterns / genetics* Male RNA / metabolism* Sex Characteristics* Spermatozoa / metabolism Stress, Physiological / genetics
Resource
C.elegans tm4259 tm1163 tm1200 tm1155 tm1163