Effects of temperature on transcriptome and cuticular hydrocarbon expression in ecologically differentiated populations of desert Drosophila

Abstract

We assessed the effects of temperature differences on gene expression using whole‐transcriptome microarrays and cuticular hydrocarbon variation in populations of cactophilic Drosophila mojavensis. Four populations from Baja California and mainland Mexico and Arizona were each reared on two different host cacti, reared to sexual maturity on laboratory media, and adults were exposed for 12 hr to 15, 25, or 35°C. Temperature differences influenced the expression of 3,294 genes, while population differences and host plants affected >2,400 each in adult flies. Enriched, functionally related groups of genes whose expression changed at high temperatures included heat response genes, as well as genes affecting chromatin structure. Gene expression differences between mainland and peninsular populations included genes involved in metabolism of secondary compounds, mitochondrial activity, and tRNA synthases. Flies reared on the ancestral host plant, pitaya agria cactus, showed upregulation of genes involved in metabolism, while flies reared on organ pipe cactus had higher expression of DNA repair and chromatin remodeling genes. Population × environment (G × E) interactions had widespread effects on the transcriptome where population × temperature interactions affected the expression of >5,000 orthologs, and there were >4,000 orthologs that showed temperature × host plant interactions. Adults exposed to 35°C had lower amounts of most cuticular hydrocarbons than those exposed to 15 or 25°C, including abundant unsaturated alkadienes. For insects adapted to different host plants and climatic regimes, our results suggest that temperature shifts associated with climate change have large and significant effects on transcriptomes of genetically differentiated natural populations.

Post‐eclosion temperature effects on insect cuticular hydrocarbon profiles

“…In addition to potential function in the stress response, CHCs are also involved in pheromonal and other chemical communications (Bagneres et al, 1996;Berson et al, 2019;Blomquist & Bagneres, 2010;Chung & Carroll, 2015;Fan et al, 2013;Kuo et al, 2012;Le Conte & Hefetz, 2008;Oystaeyen et al, 2014). Geographical variation in these compounds has also been reported in many Drosophila species from Australia and North America (Etges et al, 2017;Francesca & Chenoweth, 2010;Matzkin et al, 2007;Rajpurohit et al, , 2017.…”

“…Water loss is temperature sensitive (Gibbs & Rajpurohit, 2010), so temperature immediately after eclosion can have significant effects on water balance and survival. Numerous studies have examined the effects of temperature on CHC and water loss of drosophilids (Etges et al., 2017; Toolson, 1982, Gibbs et al., 1998; Rajpurohit et al., 2017; Krupp et al., 2019) and other terrestrial arthropods (Hadley, 1978; Toolson & Hadley, 1979; Rourke, 2000). In all cases, however, experimental animals were fully mature adults.…”

Prolonged Heat Stress during Winter Diapause Alters the Expression of Stress-Response Genes in Ostrinia nubilalis (Hbn.)

“…There are countless examples of the upregulation of HSP genes and proteins under heat stress in insects. In the fruit fly Drosophila mojavensis , one third of its entire transcriptome was affected after 12 h of exposure to temperatures of 15 °C, 25 °C and 35 °C, including significant upregulation of six genes encoding HSPs [ 64 ]. Similarly, in the whitefly Bemisia tabaci , the entire set of stress-related genes was thermally induced at 40 °C—among them those encoding three heat shock proteins—HSP90, HSP70 and HSP40 [ 65 ].…”

Transcriptional profiling of populations in the clamRuditapes decussatussuggests genetically determined differentiation in gene-expression along parallel temperature gradients and between races of the Atlantic Ocean and West Mediterranean sea

“…One of the clear results that have emerged from studies of population transcriptomics in relation to temperature is that individuals native to different localities often show differences in the patterns of gene expression when they are exposed to a common thermal environment in the laboratory or in the field [7,13,14]. This is expected, because organisms usually show genetic differences among populations.…”