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

Abstract

The maternal effects that increase the adaptability of offspring are often caused by stressful conditions that persist in the environment. However, it is not clear where the threshold lies at which maternal effects cease to be adaptive for offspring and lead to developmental instability. One of the known environmental stressors is the unpredictable changes in environmental conditions. We aimed to test whether instability of the maternal environment lead to a decrease in developmental robustness in the offspring 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. The unstable conditions alone did not affect the frequency of developmental anomalies in the offspring. Since serotonin is thought to play the role of the signaling molecule mediating the maternal effect in L. stagnalis, we exposed the 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 for the offspring of mothers living in unstable conditions. We also demonstrated rich serotoninergic innervation of the hermaphroditic gland (ovotestis) and accumulation of serotonin in the cytoplasm of the forming oocytes, supporting the role of serotonin in the maternal signaling. Our experiments suggest that, accumulation of serotonin in the oocyte/zygote may exceed the adaptive level and increase the risk of malformations during embryonic development.