Physiological and transcriptional changes associated with obligate aestivation in the cabbage stem flea beetle (Psylliodes chrysocephala)

Abstract

Aestivation is a form of seasonal dormancy observed in various insect species, usually coinciding with the summer season. The cabbage stem flea beetle, Psylliodes chrysocephala (Coleoptera: Chrysomelidae), is a key pest of oilseed rape that obligatorily aestivates as adult in late summer. Since the physiological and transcriptional processes linked to aestivation in P. chrysocephala are still little understood, we analyzed relevant physiological parameters and performed RNA-seq analyses on laboratory-reared beetles in their pre-aestivation, aestivation, and post-aestivation stages. We found that the beetles reached aestivation at 15 days post-eclosion, showing strongly reduced metabolic activity, with less than 50% CO2 production, compared to pre-aestivating individuals. Under constant laboratory conditions, the beetles aestivated for about 25 days. Female beetles reached reproductive maturity at a median of 52 days post-eclosion. Furthermore, aestivating beetles had significantly reduced carbohydrate reserves and increased lipid reserves compared with pre-aestivating beetles, indicating that aestivation is associated with drastic changes in energy metabolism. Aestivating beetles contained 30% less water and their survival rates under high-temperature conditions (30 °C) were 40% higher compared to pre-aestivating beetles. RNA-seq studies showed that, in particular, gene ontology terms related to carbohydrate and lipid metabolism, digestion, and mitochondrial activity were enriched, with clear differences in transcript abundance between beetles in aestivation compared to pre- or post-aestivation. Specifically, mitochondrial transcripts, such as respiratory chain I subunits, and digestion-related transcripts, such as trypsin, were less abundant during aestivation, which supports the idea that aestivation is associated with decreased metabolic activity. This study represents the first exploration of the transcriptomic and physiological processes linked to aestivation in P. chrysocephala.