Parental energy-sensing pathways control intergenerational offspring sex determination in the nematode Auanema freiburgensis.

BACKGROUND: Environmental stimuli experienced by the parental generation influence the phenotype of subsequent generations (Demoinet et al., Proc Natl Acad Sci U S A 114:E2689-E2698, 2017; Burton et al., Nat Cell Biol 19:252-257, 2017; Agrawal et al., Nature 401:60-63, 1999). The effects of these stimuli on the parental generation may be passed through the germline, but the mechanisms at the basis of this non-Mendelian type of inheritance, their level of conservation, how they lead to adaptive vs non-adaptive, and intergenerational vs transgenerational inheritance are poorly understood. Here we show that modulation of nutrient-sensing pathways in the parental generation of the nematode Auanema freiburgensis regulates phenotypic plasticity of its offspring. RESULTS: In response to con-specific pheromones indicative of stress, AMP-activated protein kinase (AMPK), mechanistic target of rapamycin complex 1 (mTORC1), and insulin signaling regulate stress resistance and sex determination across one generation, and these effects can be mimicked by pathway modulators. The effectors of these pathways are closely associated with the chromatin, and their regulation affects the chromatin acetylation status in the germline. CONCLUSION: These results suggest that highly conserved metabolic sensors regulate phenotypic plasticity through regulation of subcellular localization of their effectors, leading to changes in chromatin acetylation and epigenetic status of the germline.

Mating dynamics in a nematode with three sexes and its evolutionary implications.

Nematodes have diverse reproductive strategies, which make them ideal subjects for comparative studies to address how mating systems evolve. Here we present the sex ratios and mating dynamics of the free-living nematode Rhabditis sp. SB347, in which males, females and hermaphrodites co-exist. The three sexes are produced by both selfing and outcrossing, and females tend to appear early in a mother's progeny. Males prefer mating with females over hermaphrodites, which our results suggest is related to the female-specific production of the sex pheromones ascr#1 and ascr#9. We discuss the parallels between this system and that of parasitic nematodes that exhibit alternation between uniparental and biparental reproduction.

Regulation of sexual plasticity in a nematode that produces males, females, and hermaphrodites.

The mechanisms by which new modes of reproduction evolve remain important unsolved puzzles in evolutionary biology. Nematode worms are ideal for studying the evolution of mating systems because the phylum includes both a large range of reproductive modes and large numbers of evolutionarily independent switches [1, 2]. Rhabditis sp. SB347, a nematode with sexual polymorphism, produces males, females, and hermaphrodites [3]. To understand how the transition between mating systems occurs, we characterized the mechanisms that regulate female versus hermaphrodite fate in Rhabditis sp. SB347. Hermaphrodites develop through an obligatory nonfeeding juvenile stage, the dauer larva. Here we show that by suppressing dauer formation, Rhabditis sp. SB347 develops into females. Conversely, larvae that under optimal growth conditions develop into females can be respecified toward hermaphroditic development if submitted to dauer-inducing conditions. These results are of significance to understanding the evolution of complex mating systems present in parasitic nematodes.