Instability of the Mother’s Environment Leads to Reduced Developmental Robustness in <i>Lymnaea stagnalis</i> (Mollusca: Gastropoda)

Abstract

Adaptive maternal effects that increase the adaptability of offspring are often caused by stressful conditions that persist in the environment for an extended period of time. The question arises, what is the threshold at which maternal effects cease to be adaptive for offspring and lead to developmental disorders? One of the stressors is considered to be unpredictable changes in environmental conditions. We aimed to test whether a mother’s inhabitation of unstable environment could lead to a decrease of developmental robustness in the embryos of the gastropod mollusk Lymnaea stagnalis. The laboratory population of snails was split into two groups. For the first group, conditions were maintained as stable as possible, with constant water exchange and excessive feeding. The second group was kept under unstable (stressful) conditions, with episodic feeding and water exchange. It turned out that unstable conditions alone did not affect the frequency of developmental anomalies in the offspring. Since serotonin is presumably plays the role of the signaling molecule mediating the maternal effect in L. stagnalis, we subjected embryos of both groups to the biochemical precursor of serotonin (5-HTP). After incubation in 5-HTP, the proportion of embryos with developmental anomalies was significantly higher among the offspring of mothers living in unstable conditions. We confirmed the important role of serotonin as a factor mediating communication between the organisms of mother and offspring by revealing serotoninergic innervation of the hermaphroditic gland (ovotestis) and accumulation of serotonin in the cytoplasm of forming oocytes. Our experiments suggest that under the stressful environmental conditions, serotonin accumulation by the oocyte/zygote may increase to a maladaptive level and lead to a decrease in the robustness of embryonic development.