Serotonin Mediates Maternal Effects and Directs Developmental and Behavioral Changes in the Progeny of Snails

•Snail uterus shows variation of serotonin levels according to changing seasons•Serotonin-based signal modulates developmental dynamics and behavior of juveniles•Balance of intra- and extracellular serotonin is a key for relay of maternal signal•Serotonylation of proteins is necessary for transmission of maternal effects

SummaryMany organisms survive in constantly changing environments, including cycling seasons. Developing embryos show remarkable instant adaptations to the variable environmental challenges they encounter during their adult life, despite having no direct contact with the changing environment until after birth or hatching. The mechanisms by which such non-genetic information is transferred to the developing embryos are largely unknown. Here, we address this question by using a freshwater pond snail (Lymnaea stagnalis) as a model system. This snail normally lives in a seasonal climate, and the seasons define its locomotion, feeding, and reproductive behavior. We discovered that the serotonergic system plays a crucial role in transmitting a non-genetic instructive signal from mother to progeny. This maternal serotonin-based signal functions in embryos during a short time window at exclusively early pre-neural developmental stages and modulates the dynamics of embryonic and juvenile growth, feeding behavior, and locomotion.

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