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

Itai Antoine Toker*, Itamar Lev*, Yael Mor*, Yael Gurevich, Doron Fisher, Leah Houri-Zeevi, Olga Antonova, Hila Doron, Sarit Anava, Hila Gingold, Lilach Hadany, Shai Shaham, Oded Rechavi*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Pages (from-to)298-309.e9
JournalDevelopmental Cell
Volume57
Issue number3
DOIs
StatePublished - 7 Feb 2022

Funding

FundersFunder number
N.I.H.P40 OD010440
National Institutes of HealthR35NS105094
NIH Office of the DirectorP40OD010440
Achelis Foundation0604916191
Rockefeller University
European Research Council819151, 0140001000, 335624
Minerva Foundation713740
Deutsche ForschungsgemeinschaftSCHU 2494/10-1
Israel Science Foundation2064/18

    Keywords

    • C. elegans
    • epigenetics
    • evolution
    • genetic variation
    • germ granules
    • germline
    • non-Mendelian inheritance
    • sex pheromones
    • sexual attractiveness
    • small RNA inheritance
    • transgenerational inheritance

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