Synchronous seasonal plasticity in coloration, behaviour and visual gene expression in a wild butterfly population

Abstract Phenotypic plasticity allows many animals to quickly respond to seasonal changes in their environment. Seasonal changes to physiological systems, such as sensory systems, may explain other more obvious changes in behaviour, often working synergistically with changes in morphology. Here we investigate if there are covarying seasonal changes to morphology, behaviour and the visual system in the seasonally plastic butterfly Junonia coenia . To describe when seasonal wing patterns occur at our field sites in the central United States and for analysis of gene expression in eye tissue, we collected animals throughout the summer and fall in 2018, 2019, 2020 and 2021. For the first 3 years, we also visited field sites to observe behaviour during focal watches and point counts throughout the flight period. We found that more J. coenia exhibit seasonal dark wing patterns in September and October compared to butterflies collected in previous months, independent of sex. This change in wing pattern correlates with an increase in basking behaviour. Eye tissues of dark fall animals and lighter summer animals exhibit different patterns of gene expression, including visual system development genes, pigmentation genes and clock genes. Subsequent analysis of monthly variation in opsin gene expression in eye tissues confirmed that opsin genes are not differentially expressed throughout the year, though females have higher expression of blue sensitive opsin genes than males. Subsequent analysis also confirmed that eye tissue from fall caught animals has higher expression levels of the clock gene period , a gene implicated in seasonal physiology and circadian activity in other species. This concurrent seasonal shift in coloration, behaviour and underlying visual physiology indicates that J. coenia undergoes a complex shift in phenotype that encompasses more than traits directly related to thermoregulation. Sensory systems in this species show clear interactions between sex and season; future studies could further explore if this interaction extends to observed behaviour. Read the free Plain Language Summary for this article on the Journal blog.