Age-associated morphology and transcriptome analyses reveal functional transformation of Malpighian tubules of cicadas in response to development and niche shift.

Abstract

Malpighian tubules (MTs) of insects are integral to osmoregulation, detoxification, immunity and stress responses. Cicadas experience an ecological transition from subterranean to aboveground during ontogeny. However, little is known about the morphological/functional differences related to MTs between their nymphal and adult stages and potential molecular mechanisms underlying the transition. We described morphological changes of MTs from nymph to adult, including more elongated and densified microvilli and drastically dissolved secretory vacuoles. These alterations indicate MTs functionally transitioned from multifunctional secretory organs in nymphs to primarily excretory organs in adults. Transcriptomic analyses revealed differentially expressed genes were related to osmoregulation, energy metabolism, detoxification, immunity and protein synthesis, etc., across developmental stages. The upregulation of genes involved in ion transport and energy metabolism in adults suggests that enhanced capabilities for rapid waste excretion and energy acquisition are essential for aboveground adults. Increased expression of detoxification and immune-related genes indicates evolutionary adaptations of MTs to manage dietary toxicity and bolster defence mechanisms in adults. These adaptations facilitate the transition from subterranean nymphs to aboveground adults and enhance cicadas' ability to thrive in diverse ecological niches. Our findings infer the role of hormonal regulation in facilitating functional modifications of MTs to adult emergence during cicadas' growth and development. Results of this study have important implications for the evolution of life-history strategy of insects responding to diet/habitat changes during ontogeny. These findings enhance our understanding of how insects adapt to dietary/habitat shift and emphasise the importance of MTs in physiological responses to environmental challenges.