Comparative transcriptomic analysis reveals sex-specific molecular strategies during diapause in the Colorado potato beetle

To cope with harsh environmental conditions, many overwintering insects enter diapause. Many of the phenotypic changes that occur during diapause are well understood, but less is known about their underlying physiological mechanisms and how these mechanisms might differ between sexes. Using RNA-seq, we characterized sex-specific transcriptomic profiles of diapausing and non-diapausing adult Colorado potato beetles (Leptinotarsa decemlineata) to study the mechanistic basis of this complex phenotype. We identified 2,366 transcripts exhibiting concordant differential expression during diapause between sexes, 228 transcripts displaying significant sex-by-diapause interactions, and thousands of transcripts differentially expressed in a sex-specific manner. The shared transcriptional profiles suggest that both sexes employ a systematic suppression of aerobic metabolism, most dramatically through electron transport chain shutdown (cytochrome b: -28-fold) coupled with coordinated downregulation of central carbon metabolism pathways including TCA cycle, glycolysis, and pentose phosphate pathway enzymes. We also observed significant increases in abundance of transcripts encoding proteins involved in stress response, including extreme upregulation of protein stabilization machinery (protein lethal(2)essential for life: +26-37-fold) and hypoxia-inducible factor-1α (+20-29-fold).

Sex-specific profiles suggest that males may maintain enhanced metabolic transport and DNA repair systems while females employ a variety of alternative regulatory strategies during diapause. Taken together, these findings demonstrate that diapause involves the differential regulation of a core set of sex-independent processes as well as robust, sex-specific regulation.