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. 2024 May;132(5):267-274.
doi: 10.1038/s41437-024-00680-7. Epub 2024 Mar 27.

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

Takumi Yokomizo  1 , Yuma Takahashi  2
Affiliations

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

Takumi Yokomizo et al. Heredity (Edinb). 2024 May.

Abstract

Organisms have diverse biological clocks synchronised with environmental cycles depending on their habitats. Anticipation of tidal changes has driven the evolution of circatidal rhythms in some marine species. In the freshwater snail, Semisulcospira reiniana, individuals in nontidal areas exhibit circadian rhythms, whereas those in tidal areas exhibit both circadian and circatidal rhythms. We investigated whether the circatidal rhythms are genetically determined or induced by environmental cycles. The exposure to a simulated tidal cycle did not change the intensity of circatidal rhythm in individuals in the nontidal population. However, snails in the tidal population showed different activity rhythms depending on the presence or absence of the exposure. Transcriptome analysis revealed that genes with circatidal oscillation increased due to entrainment to the tidal cycle in both populations and dominant rhythmicity was consistent with the environmental cycle. These results suggest plasticity in the endogenous rhythm in the gene expression in both populations. Note that circatidal oscillating genes were more abundant in the tidal population than in the nontidal population, suggesting that a greater number of genes are associated with circatidal clocks in the tidal population compared to the nontidal population. This increase of circatidal clock-controlled genes in the tidal population could be caused by genetic changes in the biological clock or the experience of tidal cycle in the early life stage. Our findings suggest that the plasticity of biological rhythms may have contributed to the adaptation to the tidal environment in S. reiniana.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1
Fig. 1. Activity patterns of individuals in the nontidal and tidal populations of the control group under laboratory DD conditions.
a Mean locomotor distance of individuals in the control (left panels) and the treatment (right panels) of the nontidal (upper panels) and tidal (lower panels) populations. Error bars represent the standard error of the mean (SEM). Subjective day and night are indicated by grey and black bars above the patterns, respectively. The expected tide level in the laboratory is shown as a grey dotted line. b Mean power of Lomb–Scargle periodogram analysis for each individual. Error bars represent the SEM.
Fig. 2
Fig. 2. Gene expression patterns and rhythms of individuals in the nontidal and tidal populations under laboratory DD conditions.
Control samples were kept under LD conditions without the tidal cycle. Treatment samples were exposed to the simulated tidal cycle for four weeks. a Probabilistic PCA of the expression of all genes after filtering in the nontidal and tidal populations. b Heatmaps of standardised expression patterns of rhythmic transcripts with circatidal periods in the nontidal and tidal individuals under DD conditions detected via RAIN. The dotted wavy lines above the heatmaps of treatment samples represent the simulated tide level. c Venn diagrams detailing the number of circatidal and circadian oscillating genes detected in the nontidal and tidal populations. d The dominant rhythmicity of the transcriptome in the control and treatment groups of the nontidal and tidal populations evaluated by log-scaled ratio of the P value of circadian periodicity to that of circatidal periodicity in the transcriptome. The positive value of log-scaled ratio represents that the circatidal rhythm is dominant in the transcriptome and the negative value represents that the circadian rhythm is dominant. The dashed line represents the same P values for circadian and circatidal periodicity. Error bars represent the SEM.
Fig. 3
Fig. 3. KEGG pathway analysis of the tidal population.
a KEGG pathway over-representation analysis of the tidal population. Gene ratio refers to the ratio of the number of differentially expressed genes (DEGs) to the total number of genes in a specific pathway. The size of the circles represents the count of DEGs. Circles are coloured based on the adjusted P value. b KEGG-GSEA of the tidal population. Gene ratio refers to the ratio of the number of core enriched genes to the total number of genes in a specific pathway. The size of the circles represents the count of the core enriched genes. No pathways involved in decreased circatidal rhythmicity were detected.
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