Functional genomic and phenotypic responses to desiccation in natural populations of a desert drosophilid

Abstract

We used whole-transcriptome microarrays to assess changes in gene expression and monitored mortality rates and epicuticular hydrocarbons (CHCs) in response to desiccation stress in four natural populations of Drosophila mojavensis from Baja California and mainland Mexico. Desiccation had the greatest effect on gene expression, followed by biogeographical variation at regional and population levels. Genes involved in environmental sensing and cuticular structure were up-regulated in dry conditions, while genes involved in transcription itself were down-regulated. Flies from Baja California had higher expression of reproductive and mitochondrial genes, suggesting that these populations have greater fecundity and higher metabolic rates. Host plant differences had a surprisingly minor effect on the transcriptome. In most cases, desiccation-caused mortality was greater in flies reared on fermenting cactus tissues than that on laboratory media. Water content of adult females and males was significantly different and was lower in Baja California males. Different groups of CHCs simultaneously increased and decreased in amounts due to desiccation exposure of 9 and 18 h and were population-specific and dependent on larval rearing substrates. Overall, we observed that changes in gene expression involved a coordinated response of behavioural, cuticular and metabolic genes. Together with differential expression of cuticular hydrocarbons, this study revealed some of the mechanisms that have allowed D. mojavensis to exploit its harsh desert conditions. Certainly, for D. mojavensis that uses different host plants, population-level understanding of responses to stressors associated with future climate change in desert regions must be evaluated across geographical and local ecological scales.

Figure 1

Age at death of adult male D. mojavensis reared on cactus or lab food from four populations that were of different ages when placed in control (ambient humidity) or zero humidity conditions to start the experiment. Ages were not graphed to emphasize rearing substrate and population differences. Females were not included in this analysis because they were used for microarray analysis. Letters above the error bars indicate posthoc groupings from Duncan's Multiple Range test (P < 0.05) – least square means were unavailable for some treatment combinations due to unequal sample sizes.

Figure 2

Differences in wet and dry mass of male and female D. mojavensis from the four populations in this study that were reared on agria and organ pipe cactus. Adult body water content, delta mass, is the difference between wet and dry mass after drying adults overnight at 50° C. Different letters above the error bars indicate significant least square mean differences between groups (P < 0.05).

Figure 3

Canonical Discriminant Function biplot showing shifts in cuticular hydrocarbon profiles of female D. mojavensis from the four populations in this study exposed to zero humidity. 0, 9, and 18 hr mean centroids for CV 1 and 2 are shown, and P values refer to significantly different Euclidean distances between means. Cactus differences were not included. OPNM = Organ Pipe National Monument, Arizona; PO = Punta Onah, Sonora; PP = Punta Prieta, Baja California; SQ = San Quintin, Baja California.

Figure 4

Gene expression network generated using Cytoscape. All genes whose expression differed by at least 50% in at least one pairwise comparison of experimental treatments (Table 8) were included in the analysis. Dashed lines separate samples from the mainland and Baja California after 9 and 18 hr of desiccation.

Figure 5

Relative expression of genes associated with reproduction in flies from the mainland and Baja California. These genes were identified by DAVID from a list of genes with at least a 50% difference in expression between these geographic regions.

Figure 6

Relative expression of genes associated with oxidative phosphorylation (GO:0006119) in flies from the mainland and Baja California.