Transcriptional variation associated with cactus host plant adaptation in Drosophila mettleri populations

Abstract

Although the importance of host plant chemistry in plant-insect interactions is widely accepted, the genetic basis of adaptation to host plants is not well understood. Here, we investigate transcriptional changes associated with a host plant shift in Drosophila mettleri. While D. mettleri is distributed mainly throughout the Sonoran Desert where it specializes on columnar cacti (Carnegiea gigantea and Pachycereus pringleii), a population on Santa Catalina Island has shifted to chemically divergent coastal prickly pear cactus (Opuntia littoralis). We compared gene expression of larvae from the Sonoran Desert and Santa Catalina Island when reared on saguaro (C. gigantea), coastal prickly pear and laboratory food. Consistent with expectations based on the complexity and toxicity of cactus relative to laboratory food, within-population comparisons between larvae reared on these food sources revealed transcriptional differences in detoxification and other metabolic pathways. The majority of transcriptional differences between populations on the cactus hosts were independent of the rearing environment and included a disproportionate number of genes involved in processes relevant to host plant adaptation (e.g. detoxification, central metabolism and chemosensory pathways). Comparisons of transcriptional reaction norms between the two populations revealed extensive shared plasticity that likely allowed colonization of coastal prickly pear on Santa Catalina Island. We also found that while plasticity may have facilitated subsequent adaptive divergence in gene expression between populations, the majority of genes that differed in expression on the novel host were not transcriptionally plastic in the presumed ancestral state.

Gene expression plasticity across hosts of an invasive scale insect species

“…Pervasive host-insensitivity in the expression of detoxification genes appears to be the rule across plant-eating insects [18, 45]. However, we did find that ABC transporters were more differentially expressed across hosts than expected by chance.…”

“…Most of the significant host-induced changes in gene expression do not appear to be related to detoxification. For example, researchers have found consistent host-dependent expression of many genes involved in primary metabolism [8, 18]. Furthermore, some studies have recovered evidence of a trade-off between expression of genes for detoxification and primary metabolism [7, 18]; for some plant-eating insects, increased investment in the expression of detoxification genes may come at the cost of reduced investment in growth and reproduction.…”

A Genomic Perspective on the Generation and Maintenance of Genetic Diversity in Herbivorous Insects

“…Differences in gene expression paralleled phenotypic differences between populations: inter-population differences in expression of some genes involved in metabolism and larval development also depended on the host species on which flies were reared (Etges et al 2015). A similar study found a diverse suite of genes – enriched for functions in detoxification, metabolism, and sensory perception – that exhibited host-dependent expression level differences between populations of D. mettleri specializing on different host cacti (Hoang et al 2015). While these transcriptomic studies revealed insights into the likely physiological basis of local adaptation in cactophilic Drosophila , population genomic scans coupled with genome-wide measurements of allele frequency change during exposure to local and non-local hosts could definitively identify the targets of selection and genomic architecture of local adaptation.…”

The transcriptome response of Heliconius melpomene larvae to a novel host plant

“…) and Drosophila mettleri (Hoang et al . ). These studies mainly focused on polyphagous insects (or generalists) feeding on different hosts and detected the expression patterns of differentially expressed genes.…”