Abstract
C. elegans nematodes transmit responses to environmental cues transgenerationally, however it is unknown whether this non-DNA-based inheritance impacts the genome and consequently the process of evolution. Here we show that inherited small RNAs regulate the crucial decision of whether to self-fertilize or outcross, and thus indirectly control genetic variation. Under standard growth conditions, hermaphrodites secrete a male-attracting pheromone only when they are old and their supply of self-produced sperm is depleted. Since heat compromises sperm functions, from worms to humans, we examined young hermaphrodites that were cultivated at a mildly stressful temperature (25°C), and discovered that they become more attractive due to the premature secretion of the pheromone. Moreover, we discovered that the enhanced attractiveness transmits transgenerationally to unstressed progeny via heritable small RNAs and the Argonaute protein Heritable RNAi Deficient-1 (HRDE-1). We identified a specific endogenous small interfering RNA (endo-siRNA) pathway, enriched in endosiRNAs which target sperm genes, that can transgenerationally regulate sexual attraction, prevalence of males, and the rate of successful mating. Mathematical simulations and multigenerational competition experiments 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” which, via small RNA inheritance, can enhance outcrossing in challenging environments, when increasing genetic variation is advantageous.
Competing Interest Statement
The authors have declared no competing interest.
