Ricardo Caliari Oliveira

Conserved class of queen pheromones stops social insect workers from reproducing

Long Live the Queen Eusociality is often considered to have arisen, at least in part, due to the inclusive fitness that workers gain through helping their queen sister to raise her offspring. Van Oystaeyen et al. (p. 287; see the Perspective by Chapuisat) characterized the sterility-inducing queen pheromone across three distantly related eusocial hymenopterans (a wasp, a bumblebee, and a desert ant) and synthesized data across 69 other species. Queen pheromones appear to be remarkably conserved, which suggests that reproductive manipulation has ancient roots. Social insect queens use an ancient, evolutionarily conserved class of pheromones to prevent worker reproduction. [Also see Perspective by Chapuisat] 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.

The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems

Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to remain sterile, are considered to play a key role in regulating the reproductive division of labor of insect societies. Although queen pheromones were long thought to be highly taxon-specific, recent studies have shown that structurally related long-chain hydrocarbons act as conserved queen signals across several independently evolved lineages of social insects. These results imply that social insect queen pheromones are very ancient and likely derived from an ancestral signalling system that was already present in their common solitary ancestors. Based on these new insights, we here review the literature and speculate on what signal precursors social insect queen pheromones may have evolved from. Furthermore, we provide compelling evidence that these pheromones should best be seen as honest signals of fertility as opposed to suppressive agents that chemically sterilize the workers against their own best interests.

The origin and evolution of queen and fertility signals in Corbiculate bees.

BackgroundIn social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle have been shown to act as fertility signals. In addition, specific queen-characteristic hydrocarbons have been implicated as sterility-inducing queen signals in ants, wasps and bumblebees. In Corbiculate bees, however, the chemical nature of queen-characteristic and fertility-linked compounds appears to be more diverse than in ants and wasps. Moreover, it remains unknown how queen signals evolved across this group and how they might have been co-opted from fertility signals in solitary ancestors.ResultsHere, we perform a phylogenetic analysis of fertility-linked compounds across 16 species of solitary and eusocial bee species, comprising both literature data as well as new primary data from a key solitary outgroup species, the oil-collecting bee Centris analis, and the highly eusocial stingless bee Scaptotrigona depilis. Our results demonstrate the presence of fertility-linked compounds belonging to 12 different chemical classes. In addition, we find that some classes of compounds (linear and branched alkanes, alkenes, esters and fatty acids) were already present as fertility-linked signals in the solitary ancestors of Corbiculate bees, while others appear to be specific to certain species.ConclusionOverall, our results suggest that queen signals in Corbiculate bees are likely derived from ancestral fertility-linked compounds present in solitary bees that lacked reproductive castes. These original fertility-linked cues or signals could have been produced either as a by-product of ovarian activation or could have served other communicative purposes, such as in mate recognition or the regulation of egg-laying.

Sneaky queens in Melipona bees selectively detect and infiltrate queenless colonies

Insect societies are characterized by advanced cooperation, but at the same time the complexity of their colonies renders them susceptible to reproductive parasitism. Recently, a genetic study on the Brazilian stingless bee Melipona scutellaris showed that unrelated queens frequently invade and take over colonies in which the mother queen had died. In the present study, we investigated this phenomenon using radio frequency identification (RFID) tags. We confirmed that alien queen take-overs are common within this species, and demonstrated that mated queens actively seek out colonies without a queen to reproduce in. Furthermore, we found that queens only penetrate their target colonies in the evening, when guarding efficiency is significantly reduced. We hypothesize that this strategy reduces the chance of the queens being attacked by entrance guards, thus maximizing their chance of successful infiltration.

Intraspecific worker parasitism in the common wasp, Vespula vulgaris

Insect societies display a remarkable level of cooperation, but their colonies also represent a valuable resource that can be taken advantage of by genetically unrelated individuals. Indeed, several recent studies have documented cases of intraspecific reproductive parasitism, whereby workers penetrate and lay eggs in unrelated colonies in order to have their brood raised by the host workers. Previously, it has been predicted that queenless colonies should be a prime target of such intraspecific worker parasitism, as in such colonies the parasite workers would be able to reproduce without interference from either the queen or other workers. So far, this prediction has been supported with data from the honeybee, but evidence from other social insect groups is currently lacking. Here we present the first such test in the common wasp, Vespula vulgaris. In particular, workers from queenright colonies left the natal nest at a higher rate than those from queenless colonies. However, contrary to our predictions, drifter workers targeted queenless and queenright colonies equally. Chemical data suggest that this lack of discrimination may be linked to recognition constraints and the lack of volatile signals that reliably indicate the presence or absence of the queen. In addition, in queenright colonies, drifters activated their ovaries at a rate that was ca. five times higher than the natal workers. Overall, our results suggest that also in wasps, workers can gain inclusive fitness by drifting to unrelated nests, even if the chances of successfully reproducing there may be very slim.

Conserved queen pheromones in bumblebees: a reply to Amsalem et al.

In a recent study, Amsalem, Orlova & Grozinger (2015) performed experiments with Bombus impatiens bumblebees to test the hypothesis that saturated cuticular hydrocarbons are evolutionarily conserved signals used to regulate reproductive division of labor in many Hymenopteran social insects. They concluded that the cuticular hydrocarbon pentacosane (C25), previously identified as a queen pheromone in a congeneric bumblebee, does not affect worker reproduction in B. impatiens. Here we discuss some shortcomings of Amsalem et al.’s study that make its conclusions unreliable. In particular, several confounding effects may have affected the results of both experimental manipulations in the study. Additionally, the study’s low sample sizes (mean n per treatment = 13.6, range: 4–23) give it low power, not 96–99% power as claimed, such that its conclusions may be false negatives. Inappropriate statistical tests were also used, and our reanalysis found that C25 substantially reduced and delayed worker egg laying in B. impatiens. We review the evidence that cuticular hydrocarbons act as queen pheromones, and offer some recommendations for future queen pheromone experiments.

Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp

In insect societies, both queens and workers produce chemicals that reliably signal caste membership and reproductive status. The mechanisms that help to maintain the honesty of such queen and fertility signals, however, remain poorly studied. Here we test if queen signal honesty could be based on the shared endocrine control of queen fertility and the production of specific signals. In support of this “hormonal pleiotropy” hypothesis, we find that in the common wasp, application of methoprene (a juveline hormone analogue) caused workers to acquire a queen-like cuticular hydrocarbon profile, resulting in the overproduction of known queen pheromones as well as some compounds typically linked to worker fertility. By contrast, administration of precocene-I (a JH inhibitor) had a tendency to have the opposite effect. Furthermore, a clear gonadotropic effect of JH in queens was suggested by the fact that circulating levels of JH were ca. 2 orders of magnitude higher in queens than those in workers and virgin, non-egg-laying queens, even if methoprene or precocene treatment did not affect the ovary development of workers. Overall, these results suggest that queen signal honesty in this system is maintained by queen fertility and queen signal production being under shared endocrine control.