Environmental decomposition of olefinic cuticular hydrocarbons of Periplaneta americana generates a volatile pheromone that guides social behaviour

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 vapour 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 behavioural assays, nymphs strongly avoided aggregating in shelters exposed to the breakdown VOCs from cuticular alkenes. The three treatments (air, water vapour, 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 2-nonanone, 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 faeces 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 behaviour. Our results demonstrate that common environmental agents degrade CHCs into behaviourally active volatile compounds that potentially may serve as necromones or epideictic pheromones, mediating group dissolution.

Attractiveness and Sexual Competitiveness of Anastrepha obliqua Males (Diptera: Tephritidae) Fed on a Diet Enriched With Providencia rettgeri

“…The analysis of chemical signals depends on understanding the relationship between social and/or environmental context and the expression of different chemical combinations ( Gershman et al, 2014 ). Although CHCs are not volatile, they can be broken into volatile fragments by reacting with environmental agents ( Hatano et al, 2020 ), which could be used to produce a wide range of compounds as by-products of physiological processes and its regulation during the communication ( Gershman et al, 2014 ).…”

Experimental disruption of social structure reveals totipotency in the orchid bee, Euglossa dilemma

“…In addition, NMDS analysis of CHC profiles revealed mostly the same clustering pattern as seen in brain DEGs, with subordinates clustering separately from the other sampled behaviors, which are all non-foraging. This pattern may be explained by differential light exposure among individuals, along with behavioral and physiological variation, which can have a strong impact on CHC profiles due to UV exposure and degradation, possibly influencing these clustering patterns (Hatano et al, 2020).…”

Aldehyde-specific responses of olfactory sensory neurons in the praying mantis

“…Thus, mantises might also detect aldehydes to locate prey habitat. Aldehydes might also be used to discriminate live prey from dead prey because the degeneration of unsaturated cuticular hydrocarbons on insect integument generates long-chain aldehydes such as tetradecanal 28 .…”

“…Thus, mantises might also detect aldehydes to locate prey habitat. Aldehydes might also be used to discriminate live prey from dead prey because the degeneration of unsaturated cuticular hydrocarbons on insect integument generates longchain aldehydes such as tetradecanal 28 . However, the perception of aldehyde odours might also facilitate the evasion of vertebrate predators, such as lizards and birds 10 .…”