Transcriptional response in larvae of the generalist fruit fly Anastrepha obliqua feeding on three different tropical host plants

Abstract

Understanding the molecular mechanisms used by phytophagous insects to survive and feed on new hosts is key to explaining their mechanisms of range expansion and diversification. However, only a few Neotropical biological models have been used to understand these mechanisms. In this study, we investigated the differences in gene expression of the Neotropical phytophagous insect Anastrepha obliqua Macquart (Diptera: Tephritidae), the West Indian Fruit Fly, when feeding on three different host plant species under sympatric and synchronous conditions. Third-instar larvae of A. obliqua infesting red mombin (Spondias purpurea L.), mango (Mangifera indica L.), and carambola (Averrhoa carambola L.) were collected in two localities in southwestern Colombia. After assembling a de novo transcriptome, differences in gene expression between larvae infesting the three host species were established using a batch effect design, controlling the variability introduced by location. Sixty-four differentially expressed unigenes were identified among flies infesting the different hosts, with the greatest number of genes differentially expressed between red mombin and carambola. Digestive genes, such as alpha-amylases and serine proteases, were upregulated in larvae from red mombin compared with mango (six genes) and carambola (four genes), suggesting the response of A. obliqua to the nutritional composition in red mombin. Also, two genes related to immune system responses, glutactin and acidic phospholipase A2, were upregulated in mango compared to carambola. Notably, genes annotated as transposable elements (TEs) were consistently upregulated in larvae infesting carambola and mango compared to larvae infesting red mombin. This may suggest the activation of these TEs in acclimation or adaptation to new hosts. Based on our results, the main categories of differentially expressed genes in A. obliqua were serine proteases, detoxification proteins, and proteins associated with the regulation of gene expression. These results support the potential of A. obliqua to adapt to host plants and its qualification as a generalist species.