Chemical and transcriptomic diversity do not correlate with ascending levels of social complexity in the insect order Blattodea.

Eusocial insects, such as ants and termites, are characterized by high levels of coordinated social organization. This is contrasted by solitary insects that display more limited forms of collective behavior. It has been hypothesized that this gradient in sociobehavioral sophistication is positively correlated with chemical profile complexity, due to a potentially increased demand for diversity in chemical communication mechanisms in insects with higher levels of social complexity. However, this claim has rarely been assessed empirically. Here, we compare different levels of chemical and transcriptomic complexity in selected species of the order Blattodea that represent different levels of social organization, from solitary to eusocial. We primarily focus on cuticular hydrocarbon (CHC) complexity, since it has repeatedly been demonstrated that CHCs are key signaling molecules conveying a wide variety of chemical information in solitary as well as eusocial insects. We assessed CHC complexity and divergence between our studied taxa of different social complexity levels as well as the differentiation of their respective repertoires of CHC biosynthesis gene transcripts. Surprisingly, we did not find any consistent pattern of chemical complexity correlating with social complexity, nor did the overall chemical divergence or transcriptomic repertoire of CHC biosynthesis genes reflect on the levels of social organization. Our results challenge the assumption that increasing social complexity is generally reflected in more complex chemical profiles and point toward the need for a more cautious and differentiated view on correlating complexity on a chemical, genetic, and social level.

Defensive behavior is linked to altered surface chemistry following infection in a termite society.

The care-kill response determines whether a sick individual will be treated or eliminated from an insect society, but little is known about the physiological underpinnings of this process. We exploited the stepwise infection dynamics of an entomopathogenic fungus in a termite to explore how care-kill transitions occur, and identify the chemical cues behind these shifts. We found collective responses towards pathogen-injected individuals to vary according to severity and timing of pathogen challenge, with elimination, via cannibalism, occurring sooner in response to a severe active infection. However, injection with inactivated fungal blastospores also resulted in increased albeit delayed cannibalism, even though it did not universally cause host death. This indicates that the decision to eliminate an individual is triggered before pathogen viability or terminal disease status has been established. We then compared the surface chemistry of differently challenged individuals, finding increased amounts of long-chained methyl-branched alkanes with similar branching patterns in individuals injected with both dead and viable fungal blastospores, with the latter showing the largest increase. This coincided with the highest amounts of observed cannibalism as well as signs of severe moribundity. Our study provides new mechanistic insight into the emergent collective behaviors involved in the disease defense of a termite society.

Neglected Very Long-Chain Hydrocarbons and the Incorporation of Body Surface Area Metrics Reveal Novel Perspectives for Cuticular Profile Analysis in Insects.

Most of our knowledge on insect cuticular hydrocarbons (CHCs) stems from analytical techniques based on gas-chromatography coupled with mass spectrometry (GC-MS). However, this method has its limits under standard conditions, particularly in detecting compounds beyond a chain length of around C40. Here, we compare the CHC chain length range detectable by GC-MS with the range assessed by silver-assisted laser desorption/ionization mass spectrometry (Ag-LDI-MS), a novel and rarely applied technique on insect CHCs, in seven species of the order Blattodea. For all tested species, we unveiled a considerable range of very long-chain CHCs up to C58, which are not detectable by standard GC-MS technology. This indicates that general studies on insect CHCs may frequently miss compounds in this range, and we encourage future studies to implement analytical techniques extending the conventionally accessed chain length range. Furthermore, we incorporate 3D scanned insect body surface areas as an additional factor for the comparative quantification of extracted CHC amounts between our study species. CHC quantity distributions differed considerably when adjusted for body surface areas as opposed to directly assessing extracted CHC amounts, suggesting that a more accurate evaluation of relative CHC quantities can be achieved by taking body surface areas into account.