De Novo Transcriptome Analysis Reveals Potential Thermal Adaptation Mechanisms in the Cicada Hyalessa fuscata

SIMPLE SUMMARY: In metropolitan Seoul and its vicinity, cicadas of the species Hyalessa fuscata living in warmer areas could tolerate the heat better than those living in cooler areas, but genetic mechanisms involved in better heat tolerance remained unclear. In this study, we examined differences in gene expression of cicadas living in a warm urban area, a cool urban area and a suburban area in three experimental treatments: no heating, 10 min heating and heating until the cicadas lost their mobility. Cicadas from the warm urban area changed their gene expressions the most. Activated genes were mostly related to heat shock, energy metabolism, and detoxification. These results suggested that under heat stress, cicadas inhabiting warm areas could differentially express genes to increase their thermal tolerance. ABSTRACT: In metropolitan Seoul, populations of the cicada Hyalessa fuscata in hotter urban heat islands (“high UHIs”) exhibit higher thermal tolerance than those in cooler UHIs (“low UHIs”). We hypothesized that heat stress may activate the expression of genes that facilitate greater thermal tolerance in high-UHI cicadas than in those from cooler areas. Differences in the transcriptomes of adult female cicadas from high-UHI, low-UHI, and suburban areas were analyzed at the unheated level, after acute heat stress, and after heat torpor. No noticeable differences in unheated gene expression patterns were observed. After 10 min of acute heat stress, however, low-UHI and suburban cicadas expressed more heat shock protein genes than high-UHI counterparts. More specifically, remarkable changes in the gene expression of cicadas across areas were observed after heat torpor stimulus, as represented by a large number of up- and downregulated genes in the heat torpor groups compared with the 10 min acute heat stress and control groups. High-UHI cicadas expressed the most differentially expressed genes, followed by the low-UHI and suburban cicadas. There was a notable increase in the expression of heat shock, metabolism, and detoxification genes; meanwhile, immune-related, signal transduction, and protein turnover genes were downregulated in high-UHI cicadas versus the other cicada groups. These results suggested that under heat stress, cicadas inhabiting high-UHIs could rapidly express genes related to heat shock, energy metabolism, and detoxification to protect cells from stress-induced damage and to increase their thermal tolerance toward heat stress. The downregulation of apoptosis mechanisms in high-UHI cicadas suggested that there was less cellular damage, which likely contributed to their high tolerance of heat stress.