Stress-specific regulation of germline development in Caenorhabditis elegans

Stress during a critical period early in development has been shown to induce reproductive plasticity in animals. However, the mechanisms by which early-life environmental stress affects adult fecundity are still unclear. Caenorhabditis elegans is an excellent model system to study how stress induces phenotypic plasticity since its developmental trajectory is dependent upon environmental cues. Nematodes that experience environmental stress (starvation, high pheromone, or high temperature) during early larval development will enter an alternative, stress-resistant stage named dauer. The animal will exit dauer and proceed to adulthood once conditions improve (postdauers, PD). Recent work from our lab has found that postdauers that entered dauer due to high pheromone conditions (PDphe) have distinct changes in gene expression profiles and an increased brood size compared to postdauers that entered dauer due to starvation (PDstv). Given that the brood size of selfing hermaphrodites is sperm limited, we hypothesize that PD spermatogenesis is modulated differently by distinct early life stresses. Here, we investigate germline proliferation, the mitotic/meiotic switch, and the timing of germline development during the third larval stage. We hypothesize that altering any of these processes could affect spermatogenesis and result in the observable fecundity phenotype. In developmentally age-matched animals, we examined the number of germ cell rows in the mitotic stem cell niche and that have entered meiosis, expression of the translational repressor GLD-1, and the gonad area in continuously growing worms (CON), PDphe, and PDstv larva. Our results indicate that, while the number of mitotic cell rows is similar in these populations, the number of meiotic cell rows, as well as gonad area, is significantly different in CON, PDphe, and PDstv larva. We suggest that the timing of germline proliferation is modulated by developmental history. However, the change in meiotic cell rows is not reflected by a concomitant change in GLD-1 level in PDstv individuals. To explore signaling mechanisms that may modulate the timing of germline proliferation during larval development, we examined worm lines carrying mutations in genes with functions in systemic RNAi, steroid signaling, reproductive longevity, and lipid metabolism pathways. We find that steroid signaling, and reproductive longevity pathways are required in the starvation condition. In contrast, lipid metabolism and systemic RNAi pathways are required in the pheromone condition to regulate the onset of germline proliferation. Together, our results suggest a model where germ cell proliferation is modulated by early environmental and developmental experience, resulting in reproductive plasticity in adult animals.