A Non-Gradual Development Process of Cicada Eyes at the End of the Fifth-Instar Nymphal Stage to Obtain Visual Ability

SIMPLE SUMMARY: Visual systems of insects reflect high adaptation to their habitats. Cicadas undergo a significant niche change during ontogenetic development, which results in an obvious difference in color and ultrastructure of the compound eyes between nymphal and adult stages. However, little is known about when and how cicadas obtain their visual ability to deal with the new habitat. Here we use transcriptome analyses to clarify the timing and potential molecular mechanisms underlying the structural and functional transformation of the eyes of the cicada Meimuna mongolica. These results improve understanding of developmental and adaptive changes in compound eyes in insects which undergo a drastic ontogenic shift in habitat. ABSTRACT: Insects’ visual system is directly related to ecology and critical for their survival. Some cicadas present obvious differences in color and ultrastructure of compound eyes between nymphal and adult stages, but little is known about when cicadas obtain their visual ability to deal with the novel above-ground habitat. We use transcriptome analyses and reveal that cicada Meimuna mongolica has a trichromatic color vision system and that the eyes undergo a non-gradual development process at the end of the 5th-instar nymphal stage. The white-eye 5th-instar nymphs (i.e., younger 5th-instar nymphs) have no visual ability because critical components of the visual system are deficient. The transformation of eyes toward possessing visual function takes place after a tipping point in the transition phase from the white-eye period to the subsequent red-eye period, which is related to a decrease of Juvenile Hormone. The period shortly after adult emergence is also critical for eye development. Key differentially-expressed genes related to phototransduction and chromophore synthesis play positive roles for cicadas to adapt to above-ground habitat. The accumulation of ommochromes corresponds to the color change of eyes from white to red and dark brown during the end of the 5th-instar nymphal period. Cuticle tanning leads to eye color changing from dark-brown to light-brown during the early adult stage. We hypothesize that the accumulation of ommochromes occurring at the end of 5th-instar nymphal stage and the early adult stage is not only for cicadas to obtain visual ability, but also is a secure strategy to cope with potential photodamage after emergence.