The Many Dimensions of Diet Breadth: Phytochemical, Genetic, Behavioral, and Physiological Perspectives on the Interaction between a Native Herbivore and an Exotic Host

Abstract

From the perspective of an herbivorous insect, conspecific host plants are not identical, and intraspecific variation in host nutritional quality or defensive capacity might mediate spatially variable outcomes in plant-insect interactions. Here we explore this possibility in the context of an ongoing host breadth expansion of a native butterfly (the Melissa blue, Lycaeides melissa) onto an exotic host plant (alfalfa, Medicago sativa). We examine variation among seven alfalfa populations that differed in terms of colonization by L. melissa; specifically, we examined variation in phytochemistry, foliar protein, and plant population genetic structure, as well as responses of caterpillars and adult butterflies to foliage from the same populations. Regional patterns of alfalfa colonization by L. melissa were well predicted by phytochemical variation, and colonized patches of alfalfa showed a similar level of inter-individual phytochemical diversity. However, phytochemical variation was a poor predictor of larval performance, despite the fact that survival and weight gain differed dramatically among caterpillars reared on plants from different alfalfa populations. Moreover, we observed a mismatch between alfalfa supporting the best larval performance and alfalfa favored by ovipositing females. Thus, the axes of plant variation that mediate interactions with L. melissa depend upon herbivore life history stage, which raises important issues for our understanding of adaptation to novel resources by an organism with a complex life history.

Deconstruction of a plant‐arthropod community reveals influential plant traits with nonlinear effects on arthropod assemblages

“…We were not able to link variation in plant traits or arthropod assemblages to variation in fungal richness or diversity using the random forest algorithm (Figure S10), which suggests we have much to learn regarding how plant‐associated microbial communities assemble (Andrews & Harris, ; Harrison, Forister, Parchman, & Koch, ). It is possible that the fungal community was partly homogenized during air drying and storage, thus leading to the poor performance of our models.…”

“…Accordingly, for each sample, we calculated the numbers equivalent of Shannon's diversity index individually for saponins, phenolics and unidentified compounds. were aligned (231,973,765 reads) to a previously generated draft genome of M. sativa (Harrison, Gompert et al 2016) using bwa (Li & Durbin, 2009). Variable positions within aligned contigs and genotype likelihoods at those positions were determined using the Unified Genotyper in GATK (DePristo et al, 2011).…”

“…Alfalfa is a rich resource for arthropods in part because it associates with rhizosphere bacteria, which fix nitrogen that is subsequently incorporated into plant tissues. However, alfalfa is phytochemically diverse and well-defended by a variety of triterpene saponins, phenolics, flavanoids and other compounds that can affect insect herbivores (Dyer, Richards, Short, & Dodson, 2013;Harrison, Gompert et al, 2016;Oleszek, 1996;Sen, Makkar, & Becker, 1998). Alfalfa is also more genetically diverse than most crops as it is an obligate outcrosser and cultivars are multiparental in origin (Julier, Huyghe, & Ecalle, 2000), which results in more phenotypic variation within alfalfa fields than is typical for monocultures.…”

Caterpillars on a phytochemical landscape: the case of alfalfa and the Melissa blue butterfly

“…The finding that our specialist herbivore is affected by a wide range of metabolites, primary and secondary, that vary greatly even within a single host population has implications for our understanding of heterogeneity in the system and for the course of local adaptation of the herbivore to the novel host. Lycaeides melissa typically colonizes weedy or feral patches of M. sativa on roadsides or integrated into natural communities, and previous work has documented dramatic variation among individual alfalfa locations (often in close proximity) in the extent to which they can support caterpillar development (Harrison et al , 2016). Previous phytochemical data with a lower resolution was less successful in explaining that variation (Harrison et al , 2016), and the results reported here suggest that among patch variation could be explained by future studies using metabolomic data as used here.…”

“…Lycaeides melissa typically colonizes weedy or feral patches of M. sativa on roadsides or integrated into natural communities, and previous work has documented dramatic variation among individual alfalfa locations (often in close proximity) in the extent to which they can support caterpillar development (Harrison et al , 2016). Previous phytochemical data with a lower resolution was less successful in explaining that variation (Harrison et al , 2016), and the results reported here suggest that among patch variation could be explained by future studies using metabolomic data as used here. The within-population complexity described in the current study combined with previous evidence for dramatic among-population variation in M. sativa suitability for the focal herbivore also raises the possibility that the novel host presents a multi-faceted and potentially ever-shifting target from the perspective of evolving butterfly populations.…”