Endogenous rhythm shift and adaptation to the tidal environment in the freshwater snail

Organisms have an endogenous timekeeping system to coordinate their biological processes with environmental cycles, allowing adaptation to external rhythmic changes in their environment. Modification of biological clocks could contribute to range expansion in a novel rhythmic environment. We hypothesized that populations of freshwater species near estuaries have acquired a circatidal rhythm to synchronize with the tidal cycle. Here, we compared the locomotion activity and gene expression rhythms of the freshwater snail Semisulcospira reiniana between individuals inhabiting freshwater and brackish-water areas. Individuals inhabiting brackish-water areas exhibited a rhythmic activity pattern coordinated with the tidal cycle under both field and laboratory conditions. Individuals inhabiting upstream freshwater areas showed a nocturnal activity pattern. The proportion of circadian oscillating genes was greater in freshwater than in brackish-water individuals, while that of circatidal oscillating genes was greater in brackish-water than in freshwater individuals. Interestingly, expression of 16 genes exhibited circadian and circatidal rhythms in freshwater and brackish-water individuals, respectively. Additionally, transcriptome-wide population genetic analyses supported our assumption that these two populations are genetically almost identical. These findings suggest that the slight divergence contributed to the shift in the timekeeping system, and that endogenous rhythms could differ in their periods between freshwater and brackish-water populations. Our results provide evidence of the evolution of endogenous rhythm via range expansion to novel rhythmic environment in a single species.

生物体拥有内源性计时系统，可将自身生物过程与环境周期相匹配，从而适应外界环境的节律性变化。对生物节律的重塑，或可助力物种在新型节律环境中实现分布范围的扩张。我们提出假说：河口周边的淡水物种种群，或许已演化出潮汐节律（circatidal rhythm）以适配潮汐周期。本研究对比了栖息于淡水与咸淡水区域的淡水螺川蜷（Semisulcospira reiniana）的运动活性与基因表达节律。栖息于咸淡水区域的个体，在野外与实验室环境下均表现出与潮汐周期同步的节律性活动模式；而栖息于上游淡水区域的个体则呈现出夜行性活动模式。淡水个体中呈现昼夜振荡（circadian oscillating）的基因比例显著高于咸淡水个体，反之，咸淡水个体中潮汐振荡（circatidal oscillating）的基因比例更高。有趣的是，分别有16个基因在淡水个体与咸淡水个体中呈现昼夜节律与潮汐节律。此外，全转录组群体遗传分析（transcriptome-wide population genetic analyses）证实，这两个种群在遗传层面几乎完全一致。上述发现表明，微小的遗传分化已促成计时系统的转变，且淡水与咸淡水种群的内源性节律周期存在差异。本研究结果证实，单一物种在向新型节律环境扩张分布范围的过程中，其内源节律可发生适应性演化。