The evolutionary origin of queen pheromones, which regulate reproductive division of labor in insect societies, has been explained by two evolutionary scenarios: the sender-precursor hypothesis and the sensory exploitation hypothesis. These scenarios differ in terms of whether the signaling system was built on preadaptations on the part of either the sender queens or the receiver workers. While some social insect queen pheromones – such as cuticular hydrocarbons – were likely derived from ancestral fertility cues and evolved according to the former theory, the honeybee’s queen mandibular pheromone (QMP) has been suggested to act directly on pre-existing gene-regulatory networks linked with reproduction. This is evidenced by the fact that QMP has been shown to also inhibit ovary activation in fruit flies, thereby implying exploitation of conserved physiological pathways. To verify whether QMP has similar effects on more closely related eusocial species, we here tested for QMP cross-activity in the bumblebee Bombus terrestris. Interestingly, we found that the non-native QMP blend significantly inhibited egg-laying in both worker and queen bumblebees and caused accompanying shifts in ovary activation. The native bumblebee queen pheromone pentacosane, by contrast, only inhibited the reproduction of the workers. Overall, these findings support the hypothesis that honeybee QMP likely evolved via a route of sensory exploitation. We argue that such exploitation could allow social insect queens to produce compounds that manipulate the workers to remain sterile, but that a major hurdle would be that the queens themselves would have to be immune to such compounds.

Kin recognition mediates altruistic behavior and inbreeding avoidance in many animal societies. So far, evidence for accurate kin recognition, when individuals distinguish fine scale differences in genetic relatedness, in social insects is mixed. Although this ability should be counter selected to reduce risks of nepotism in eusocial colonies, accurate kin recognition may be beneficial in less integrated societies where genetic conflicts are reduced. Here we show that gregarious cockroaches Blattella germanica discriminate multiple levels of relatedness and identify inherited cuticular odors as potential kin recognition cues. When given a choice between aggregation sites containing either full siblings or less related conspecifics, cockroaches showed an increasing preference for resting with full siblings with increasing genetic distance between stimuli groups, from 50% of choices in the presence of half siblings or cousins, to 60.7% with less related cockroaches from the same strain, and 72.9% with cockroaches from a different strain. Examination of the cuticular hydrocarbon profiles of 288 nymphs and their 54 parents revealed that the chemical distance between cockroaches was negatively correlated to their relatedness. Using a Bayesian animal model approach for quantitative genetic analyses, we identified several highly heritable methyl-branched alkanes as good candidates for kin recognition cues. Our results suggest that kin recognition is based on genetically inherited odors in this gregarious insect and highlight mechanistic similarities with nestmate recognition in eusocial species.

Fungus-farming ant colonies vary four to five orders of magnitude in size. They employ compounds from actinomycete bacteria and exocrine glands as antimicrobial agents. Atta colonies have millions of ants and are particularly relevant for understanding hygienic strategies as they have abandoned their ancestors' prime dependence on antibiotic-based biological control in favour of using metapleural gland (MG) chemical secretions. Atta MGs are unique in synthesizing large quantities of phenylacetic acid (PAA), a known but little investigated antimicrobial agent. We show that particularly the smallest workers greatly reduce germination rates of Escovopsis and Metarhizium spores after actively applying PAA to experimental infection targets in garden fragments and transferring the spores to the ants' infrabuccal cavities. In vitro assays further indicated that Escovopsis strains isolated from evolutionarily derived leaf-cutting ants are less sensitive to PAA than strains from phylogenetically more basal fungus-farming ants, consistent with the dynamics of an evolutionary arms race between virulence and control for Escovopsis, but not Metarhizium. Atta ants form larger colonies with more extreme caste differentiation relative to other attines, in societies characterized by an almost complete absence of reproductive conflicts. We hypothesize that these changes are associated with unique evolutionary innovations in chemical pest management that appear robust against selection pressure for resistance by specialized mycopathogens.

A major evolutionary transition to eusociality with reproductive division of labor between queens and workers has arisen independently at least 10 times in the ants, bees, and wasps. Pheromones produced by queens are thought to play a key role in regulating this complex social system, but their evolutionary history remains unknown. Here, we identify the first sterility-inducing queen pheromones in a wasp, bumblebee, and desert ant and synthesize existing data on compounds that characterize female fecundity in 64 species of social insects. Our results show that queen pheromones are strikingly conserved across at least three independent origins of eusociality, with wasps, ants, and some bees all appearing to use nonvolatile, saturated hydrocarbons to advertise fecundity and/or suppress worker reproduction. These results suggest that queen pheromones evolved from conserved signals of solitary ancestors.