Endogenous rhythm variation and adaptation to the tidal environment in the freshwater snail, Semisulcospira reiniana

Abstract

Organisms have endogenous timekeeping system(s) to coordinate their biological processes with environmental cycles, allowing adaptation to external rhythmic changes in their environment. The change in endogenous rhythms could contribute to range expansion in a novel rhythmic environment. We hypothesized that populations of the freshwater snail near estuaries show a circatidal rhythm to synchronize with the tidal cycle. We compared the behavioral and gene expression rhythms between non-tidal and tidal populations of the freshwater snail, Semisulcospira reiniana. Individuals inhabiting tidal areas exhibited a rhythmic activity pattern coordinated with the tidal cycle under both field and laboratory conditions, but individuals inhabiting upstream non-tidal areas showed a circadian activity pattern. The proportion of circadian oscillating genes was greater in non-tidal than in tidal individuals, while that of circatidal oscillating genes was greater in tidal than in non-tidal individuals. Additionally, transcriptome-wide population genetic analyses revealed that these two adjacent populations can be clearly distinguished genetically, though the genetic distance was very small. Our results provide evidence of the shift in an endogenous rhythm via range expansion to a novel rhythmic environment. The changes in a small number of genes and/or phenotypic plasticity may contribute to the difference in the endogenous rhythms between non-tidal and tidal populations.

Plasticity of circadian and circatidal rhythms in activity and transcriptomic dynamics in a freshwater snail

“…The plasticity of the endogenous rhythm and subsequent phenotypic differentiation by genetic changes likely played a role in the adaptation of S. reiniana to tidal areas in rivers. We have previously revealed minimal genetic differentiation between the two populations (Yokomizo and Takahashi 2022 ), supporting the contribution of plasticity and the evolution of a small number of genes to range expansion. By investigating other rivers where S. reiniana is limited to nontidal areas, we can further explore the relationship between the plasticity of the endogenous rhythm and the establishment in tidal areas.…”

“…The freshwater snail S . reiniana , found in tidal areas, exhibits the circatidal rhythm, which is believed to be an adaptation to the tidal environment (Yokomizo and Takahashi 2022 ). In the present study, we investigated whether the differential rhythmicity in S. reiniana between tidal and nontidal populations is a result of evolutionary differentiation or plastic expression of rhythms depending on dominant environmental cycles.…”

“…To investigate variations in endogenous rhythm across habitats with distinct environmental cycles, we focused on the freshwater snail Semisulcospira reiniana , which inhabits both nontidal and tidal areas of a river. Our previous study revealed that snails in nontidal areas exhibit circadian rhythms, whereas those in tidal areas exhibit both circadian and circatidal rhythms (Yokomizo and Takahashi 2022 ). However, it remains unclear whether the differential rhythmicity arises from evolutionary differentiation or plasticity in response to environmental cycles.…”

Plasticity of circadian and circatidal rhythms in activity and transcriptomic dynamics in a freshwater snail

“…Marine and intertidal habitats, characterized by the tidal cycle, experience complex and drastic environmental variations, unlike terrestrial and inland water habitats. The freshwater snail S. reiniana, found in tidal areas, exhibits the circatidal rhythm, which is believed to be an adaptation to the tidal environment [26]. In the present study, we investigated whether the differential rhythmicity in S. reiniana between tidal and nontidal populations is a result of evolutionary differentiation or plastic expression of rhythms depending on dominant environmental cycles.…”

“…To investigate variations in endogenous rhythm across habitats with distinct environmental cycles, we focused on the freshwater snail Semisulcospira reiniana, which inhabits both nontidal and tidal areas of rivers. Our previous study revealed that snails in nontidal areas exhibit circadian rhythms, whereas those in tidal areas exhibit both circadian and circatidal rhythms [26]. However, it remains unclear whether the differential rhythmicity arises from evolutionary differentiation or plasticity in response to environmental cycles.…”