Patterns of genetic variation and local adaptation of a native herbivore to a lethal invasive plant.

Understanding the evolutionary processes that influence fitness is critical to predicting species' responses to selection. Interactions among evolutionary processes including gene flow, drift and the strength of selection can lead to either local adaptation or maladaptation, especially in heterogenous landscapes. Populations experiencing novel environments or resources are ideal for understanding the mechanisms underlying adaptation or maladaptation, specifically in locally co-evolved interactions. We used the interaction between a native herbivore that oviposits on a patchily distributed introduced plant that in turn causes significant mortality to the larvae to test for signatures of local adaptation in areas where the two co-occurred. We used whole-genome sequencing to explore population structure, patterns of gene flow and signatures of local adaptation. We found signatures of local adaptation in response to the introduced plant in the absence of strong population structure with no genetic differentiation and low genetic variation. Additionally, we found localized allele frequency differences within a single population between habitats with and without the lethal plant, highlighting the effects of strong selection. Finally, we identified that selection was acting on larval ability to feed on the plant rather than on females' ability to avoid oviposition, thus uncovering the specific ontogenetic target of selection. Our work highlights the potential for adaptation to occur in a fine-grained landscape in the presence of gene flow and low genetic variation.

Predictability in the evolution of Orthopteran cardenolide insensitivity.

The repeated evolutionary specialization of distantly related insects to cardenolide-containing host plants provides a stunning example of parallel adaptation. Hundreds of herbivorous insect species have independently evolved insensitivity to cardenolides, which are potent inhibitors of the alpha-subunit of Na+,K+-ATPase (ATPα). Previous studies investigating ATPα-mediated cardenolide insensitivity in five insect orders have revealed remarkably high levels of parallelism in the evolution of this trait, including the frequent occurrence of parallel amino acid substitutions at two sites and recurrent episodes of duplication followed by neo-functionalization. Here we add data for a sixth insect order, Orthoptera, which includes an ancient group of highly aposematic cardenolide-sequestering grasshoppers in the family Pyrgomorphidae. We find that Orthopterans exhibit largely predictable patterns of evolution of insensitivity established by sampling other insect orders. Taken together the data lend further support to the proposal that negative pleiotropic constraints are a key determinant in the evolution of cardenolide insensitivity in insects. Furthermore, analysis of our expanded taxonomic survey implicates positive selection acting on site 111 of cardenolide-sequestering species with a single-copy of ATPα, and sites 115, 118 and 122 in lineages with neo-functionalized duplicate copies, all of which are sites of frequent parallel amino acid substitution. This article is part of the theme issue 'Convergent evolution in the genomics era: new insights and directions'.