Urban environment has been considered to be detrimental to species composition and richness, leading to a decline in population abundance or even local extinction. However, populations of two cicadas
Cryptotympana atrata and
Hyalessa fuscata (Hemiptera: Cicadoidea) flourish in Metropolitan Seoul. These annual species usually emerge in summer and their noisy calling songs are nuisance to city dwellers. Enumeration survey of cicada exuviae depicts more prevailing population densities in urban and suburban habitats than in countryside one. The increased number of cicadas in urban areas compared with countryside counterparts has been attributed to several reasons, such as the availability of host plant species, the difference in predator avoidance strategies and habitat fragmentation, or the elevation in soil hardness along an urban-rural gradient and difference in soil burrowing capacity. As temperature is one of the most influential environmental variables on insects, here we examine the response of cicadas to temperature in the context of an urban heat island (UHI) effect, which is the phenomenon occurs when temperatures of urban cores become hotter than the surrounding areas. We hypothesize that UHI is responsible for the population prevalence of
C. atrata and
H. fuscata in Metropolitan Seoul. First, we examined the potential association between UHI intensity and cicada population densities by testing the critical environmental factors to the prevalence of cicada species in urban habitat. Among factors related to urbanization, only temperature was significantly positively correlated to resource-weighted densities of both species. Second, as thermal responses are frequently employed as a measure of thermal adaptation of cicadas to habitat conditions, we investigated the dependence of thermal responses of
C. atrata and
H. fuscata on thermal regimes of their habitats. Again, individuals inhabiting warmer urban areas exhibited significantly higher heat tolerance than those in cooler areas. Besides, 1 oC increase in ambient temperature incurred more profound magnitude of changes in heat torpor temperature in
H. fuscata compared to C.
atrata. Third, whole genome
de novo transcriptome analysis was conducted to explore the role of gene expression underlying thermal adaptation of
H. fuscata to the elevation of UHI intensity. Under exposure to heat stress, individuals occupying high UHI area expressed more significantly up- and down-regulated genes than those in low UHI or surrounding areas. Heat shock proteins, antioxidants and genes related to energy metabolisms are more up-regulated in high UHI occupants compared to low UHI or surrounding counterparts, which facilitates urban-adapted
H. fuscata to deal with potential heat stress in their habitat. In non-stressful conditions, gene expression profiles were analogous across cicada populations. Overall, these results indicate that UHI phenomenon has promoted the abundance of two cicada species by enhancing cicada thermal tolerance and aiding in upregulation of genes in response to heat stress.
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