Evolved and Plastic Gene Expression in Adaptation of a Specialist Fly to a Novel Niche

Abstract

How gene expression evolves to enable divergent ecological adaptation and how changes in gene expression relate to genomic architecture are pressing questions for understanding the mechanisms enabling adaptation and ecological speciation. Furthermore, how plasticity in gene expression can both contribute to and be affected by the process of ecological adaptation is crucial to understanding gene expression evolution, colonisation of novel niches and response to rapid environmental change. Here, we investigate the role of constitutive and plastic gene expression differences between host races, or host-specific ecotypes, of the peacock fly Tephritis conura, a thistle bud specialist. By cross-fostering larvae to new buds of their natal host plant or the alternative, novel host plant, we uncover extensive constitutive differences in gene expression between the host races, especially genes associated with processing of host plant chemicals. However, evidence for expression plasticity was minimal and limited to the ancestral host race. Genes with host race-specific expression are found more often than expected within a large inversion in the T. conura genome, adding to evidence that inversions are important for enabling diversification in the face of gene flow and underscores that altered gene expression may be key to understanding the evolutionary consequences of inversions.