Environmental decomposition of cuticular hydrocarbons generates a volatile pheromone that guides insect social behavior

Abstract

Once emitted, semiochemicals are exposed to reactive environmental factors that may alter them, thus disrupting chemical communication. Some species, however, might have adapted to detect environmentally mediated breakdown products of their natural chemicals as semiochemicals. We demonstrate that air, water vapor, and ultraviolet (UV) radiation break down unsaturated cuticular hydrocarbons (CHCs) of Periplaneta americana (American cockroach), resulting in the emission of volatile organic compounds (VOCs). In behavioral assays, nymphs strongly avoided aggregating in shelters exposed to the breakdown VOCs from cuticular alkenes. The three treatments (air, water vapor, UV) produced the same VOCs, but at different time-courses and ratios. Fourteen VOCs from UV-exposed CHCs elicited electrophysiological responses in nymph antennae; 10 were identified as 1-pentanol, 1-octanol, 1-nonanol, tetradecanal, acetic acid, propanoic acid, butanoic acid, pentanoic acid and hexanoic acid. When short-chain fatty acids were tested as a mix and a blend of the alcohols and aldehyde was tested as a second mix, nymphs exhibited no preference for control or treated shelters. However, nymphs avoided shelters that were exposed to VOCs from the complete 10-compound mix. Conditioned shelters (occupied by cockroaches with feces and CHCs deposited on the shelters), which are normally highly attractive to nymphs, were also avoided after UV-exposure, confirming that breakdown products from deposited metabolites, including CHCs, mediate this behavior. Our results demonstrate that common environmental and anthropogenic agents degrade CHCs into volatile semiochemicals that may serve as necromones or epideictic pheromones, mediating group formation and dissolution.\n\nSignificance StatementCuticular hydrocarbons (CHCs) cover the outer surface of insects, where they prevent water loss and serve as sex pheromones and in nest-mate recognition in social insects. Although CHCs are not volatile, they can be broken into volatile fragments by reacting with environmental agents. We demonstrate that volatile breakdown products of CHCs affect the social behavior of the American cockroach. A synthetic mix of volatiles dispersed cockroaches away from shelters, signaling an unsuitable shelter. These results highlight that some insect species have evolved communication strategies that exploit environmental and anthropogenic agents to produce bioactive compounds that mediate ecological interactions.