Abstract
To cope with seasonal changes in the environment, organisms adapt their physiology and behavior. Although color perception varies among seasons, the underlying molecular basis and its physiological significance remain unclear. Here we show that dynamic plasticity in phototransduction regulates seasonal changes in color perception in medaka fish. Medaka are active and exhibit clear phototaxis in conditions simulating summer, but remain at the bottom of the tank and fail to exhibit phototaxis in conditions simulating winter. Mate preference tests using virtual fish created with computer graphics demonstrate that medaka are more attracted to orange-red-colored model fish in summer than in winter. Transcriptome analysis of the eye reveals dynamic seasonal changes in the expression of genes encoding photopigments and their downstream pathways. Behavioral analysis of photopigment-null fish shows significant differences from wild type, suggesting that plasticity in color perception is crucial for the emergence of seasonally regulated behaviors.
Highlights
To cope with seasonal changes in the environment, organisms adapt their physiology and behavior
There is evidence in non-human animals that opsin expression varies in response to environmental changes including seasons, for example, (i) SWS1 opsin expression in damsel fish changes in winter compared with those in summer[5]; (ii) LWS opsin in stickleback[6] and OPN4-related genes in zebrafish[7] vary in response to photoperiod; (iii) LWS and RH2 opsins are differentially expressed according to water depth in damsel fish[5]; (iv) SWS2B opsin changes in wildcaught and lab-reared cichlids[8]; and (v) coexpression of LWS and RH2A is influenced by environmental background spectra in cichlid[9]
We addressed the functional significance of seasonal changes in opsin expression directly using Japanese medaka (Oryzias latipes), an excellent model for studying seasonal adaptation[10]
Summary
To cope with seasonal changes in the environment, organisms adapt their physiology and behavior. There is evidence in non-human animals that opsin expression varies in response to environmental changes including seasons, for example, (i) SWS1 (short-wavelength sensitive; ultraviolet sensitive) opsin expression in damsel fish changes in winter compared with those in summer[5]; (ii) LWS (long-wavelength sensitive; red sensitive) opsin in stickleback[6] and OPN4 (opsin[4]; melanopsin)-related genes in zebrafish[7] vary in response to photoperiod; (iii) LWS and RH2 (rhodopsin 2; green sensitive) opsins are differentially expressed according to water depth in damsel fish[5]; (iv) SWS2B (blue/violet) opsin changes in wildcaught and lab-reared cichlids[8]; and (v) coexpression of LWS and RH2A is influenced by environmental background spectra in cichlid[9] These gene expression changes appear to cause alterations in the spectral sensitivity of vision, their physiological and ecological significance remains unclear. We demonstrated the functional significance of seasonally regulated plasticity in opsin gene expression on seasonally regulated behaviors, using fish harboring null mutations in the LWS opsins, and found that seasonal changes in color sensitivity underlie seasonal behavioral changes
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