Insect cuticular hydrocarbons (CHCs) prevent desiccation and serve as chemical signals that mediate social interactions. Drosophila melanogaster CHCs have been studied extensively, but the genetic basis for individual variation in CHC composition is largely unknown. We quantified variation in CHC profiles in the D. melanogaster Genetic Reference Panel (DGRP) and identified novel CHCs. We used principal component (PC) analysis to extract PCs that explain the majority of CHC variation and identified polymorphisms in or near 305 and 173 genes in females and males, respectively, associated with variation in these PCs. In addition, 17 DGRP lines contain the functional Desat2 allele characteristic of African and Caribbean D. melanogaster females (more 5,9-C27:2 and less 7,11-C27:2, female sex pheromone isomers). Disruption of expression of 24 candidate genes affected CHC composition in at least one sex. These genes are associated with fatty acid metabolism and represent mechanistic targets for individual variation in CHC composition.DOI: http://dx.doi.org/10.7554/eLife.09861.001

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For highly specialized insect herbivores, plant chemical defenses are often co-opted as cues for oviposition and sequestration. In such interactions, can plants evolve novel defenses, pushing herbivores to trade off benefits of specialization with costs of coping with toxins? We tested how variation in milkweed toxins (cardenolides) impacted monarch butterfly (Danaus plexippus) growth, sequestration, and oviposition when consuming tropical milkweed (Asclepias curassavica), one of two critical host plants worldwide. The most abundant leaf toxin, highly apolar and thiazolidine ring–containing voruscharin, accounted for 40% of leaf cardenolides, negatively predicted caterpillar growth, and was not sequestered. Using whole plants and purified voruscharin, we show that monarch caterpillars convert voruscharin to calotropin and calactin in vivo, imposing a burden on growth. As shown by in vitro experiments, this conversion is facilitated by temperature and alkaline pH. We next employed toxin-target site experiments with isolated cardenolides and the monarch’s neural Na+/K+-ATPase, revealing that voruscharin is highly inhibitory compared with several standards and sequestered cardenolides. The monarch’s typical >50-fold enhanced resistance to cardenolides compared with sensitive animals was absent for voruscharin, suggesting highly specific plant defense. Finally, oviposition was greatest on intermediate cardenolide plants, supporting the notion of a trade-off between benefits and costs of sequestration for this highly specialized herbivore. There is apparently ample opportunity for continued coevolution between monarchs and milkweeds, although the diffuse nature of the interaction, due to migration and interaction with multiple milkweeds, may limit the ability of monarchs to counteradapt.

Honey bees provide critical pollination services for many agricultural crops. While the contribution of pesticides to current hive loss rates is debated, remarkably little is known regarding the magnitude of risk to bees and mechanisms of exposure during pollination. Here, we show that pesticide risk in recently accumulated beebread was above regulatory agency levels of concern for acute or chronic exposure at 5 and 22 of the 30 apple orchards, respectively, where we placed 120 experimental hives. Landscape context strongly predicted focal crop pollen foraging and total pesticide residues, which were dominated by fungicides. Yet focal crop pollen foraging was a poor predictor of pesticide risk, which was driven primarily by insecticides. Instead, risk was positively related to diversity of non-focal crop pollen sources. Furthermore, over 60% of pesticide risk was attributed to pesticides that were not sprayed during the apple bloom period. These results suggest the majority of pesticide risk to honey bees providing pollination services came from residues in non-focal crop pollen, likely contaminated wildflowers or other sources. We suggest a greater understanding of the specific mechanisms of non-focal crop pesticide exposure is essential for minimizing risk to bees and improving the sustainability of grower pest management programs.

SignificanceUnderstanding the mechanisms that social insects use to communicate their individual status within the colony is vital to understanding the evolution of sociality. This study accomplishes this goal by identifying a royal-recognition pheromone in termites, as well as a king pheromone. Our behavioral assay defines royal-specific responses for one species of termites, which will foster future studies of termite behavior. This study also dates cuticular hydrocarbons as royal pheromones to the rise of termites ∼150 million years ago, suggesting that termites and social Hymenoptera convergently evolved the use of these ubiquitous compounds for communication. In conclusion, we have expanded our understanding of chemically mediated royal recognition in termites and helped to understand the evolution of insect societies.