The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems (original) (raw)
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Cooperation, Conflict, and the Evolution of Queen Pheromones
Journal of chemical ecology, 2011
While chemical communication regulates individual behavior in a wide variety of species, these communication systems are most elaborated in insect societies. In these complex systems, pheromones produced by the reproductive individuals (queens) are critical in establishing and maintaining dominant reproductive status over hundreds to thousands of workers. The proximate and ultimate mechanisms by which these intricate pheromone communication systems evolved are largely unknown, though there has been much debate over whether queen pheromones function as a control mechanism or as an honest signal facilitating cooperation. Here, we summarize results from recent studies in honey bees, bumble bees, wasps, ants and termites. We further discuss evolutionary mechanisms by which queen pheromone communication systems may have evolved. Overall, these studies suggest that queen-worker pheromone communication is a multicomponent, labile dialog between the castes, rather than a simple, fixed signal-response system. We also discuss future approaches that can shed light on the proximate and ultimate mechanisms that underlie these complex systems by focusing on the development of increasingly sophisticated genomic tools and their potential applications to examine the molecular mechanisms that regulate pheromone production and perception.
Honeybees possess a structurally diverse and functionally redundant set of queen pheromones
Proceedings of the Royal Society B: Biological Sciences, 2019
Queen pheromones, which signal the presence of a fertile queen and induce workers to remain sterile, play a key role in regulating reproductive division of labour in insect societies. In the honeybee, volatiles produced by the queen's mandibular glands have been argued to act as the primary sterility-inducing pheromones. This contrasts with evidence from other groups of social insects, where specific queen-characteristic hydrocarbons present on the cuticle act as conserved queen signals. This led us to hypothesize that honeybee queens might also employ cuticular pheromones to stop workers from reproducing. Here, we support this hypothesis with the results of bioassays with synthetic blends of queen-characteristic alkenes, esters and carboxylic acids. We show that all these compound classes suppress worker ovary development, and that one of the blends of esters that we used was as effective as the queen mandibular pheromone (QMP) mix. Furthermore, we demonstrate that the two main...
A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees ( Bombus impatiens )
Proceedings of the Royal Society B: Biological Sciences, 2015
The regulation of reproductive division of labour is a key component in the evolution of social insects. Chemical signals are important mechanisms to regulate worker reproduction, either as queen-produced pheromones that coercively inhibit worker reproduction or as queen signals that honestly advertise her fecundity. A recent study suggested that a conserved class of hydrocarbons serve as queen pheromones across three independent origins of eusociality. In bumblebees ( Bombus terrestris ), pentacosane ( C 25) was suggested to serve as a queen pheromone. Here, we repeat these studies using a different species of bumblebee ( Bombus impatiens ) with a more controlled experimental design. Instead of dequeened colonies, we used same-aged, three-worker queenless groups comprising either experienced or naive workers (with/without adult exposure to queen pheromone). We quantified three hydrocarbons ( C 23, C 25 and C 27) on the cuticular surfaces of females and tested their effects on the t...
Conserved queen pheromones in bumblebees: a reply to Amsalem et al
PeerJ, 2017
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 a...
Primer Pheromones in Social Hymenoptera
Annual Review of Entomology, 2008
Social insect are profoundly influenced by primer pheromones (PPhs), which are efficient means for maintaining social harmony in the colony. PPhs act by affecting the physiology of the recipients with a subsequent shift in their behavior, and many PPhs have a releaser effect (i.e., changing the probability of performing a certain behavior upon perception). In this review we try to clarify the interplay between such dual pheromonal effects. Only a few PPhs have been identified, and we provide evidence for their existence in multiple species of social Hymenoptera, which is the most extensively studied of the social insects. We focus on the regulation of reproduction, social policing, and task allocation. Considering PPhs in a broad sense, we also discuss fertility signals and the role of cuticular hydrocarbons as putative PPhs. Identification of the underlying chemistry of PPhs offers insights into insect physiology and the evolution of social behavior. PPhs of the honey bee are used to demonstrate the complexity of pheromonal communication in social insects. Primer pheromone (PPh): a pheromone that upon perception affects long-term physiological or endocrine processes in the recipient followed by delayed changes in behavioral response Mode of Action of Queen PPhs: Queen Control or Queen Signal? A major question pertaining to PPhs in social Hymenoptera is their mode of action 524 Conte • Hefetz
Queen Pheromone and Monopoly of Reproduction by the Queen in the Social Wasp Ropalidia marginata
Ropalidia marginata is a primitively eusocial (truly social) wasp found in peninsular India. It is different from the typical primitively eusocial species in having docile queens that cannot use aggression to maintain reproductive monopoly. Recent studies using chemical analysis and bioassays indicate that Dufour’s gland is a source of the queen pheromone in this species. Queens appear to signal their presence to workers through their Dufour’s gland compounds, possibly by applying them on the nest surface, and this results in suppression of reproduction by workers, resulting in reproductive monopoly by the queen. The Dufour’s gland was found to contain saturated long chain hydrocarbons, which have recently been suggested to be the ancestral state of fertility signals in Hymenoptera. The Dufour’s gland composition differed significantly between queens and workers, and was also correlated with the state of ovarian development, varying continuously as a function of ovarian development, thereby advocating the honesty of the queen pheromone. This elucidates the mechanism of maintenance of eusociality through pheromonal queen signalling by the Dufour’s gland compounds.
Chemical communication is fundamental to success in social insect colonies. Species-, colony-, and caste-specific blends of cuticular hydrocarbons (CHCs) and other chemicals have been well documented as pheromones, mediating important behavioral and physiological aspects of social insects. More specifically, royal pheromones used by queens (and kings in termites) enable workers to recognize and care for these vital individuals and maintain the reproductive division of labor. In termites, however, no royal-recognition pheromones have been identified to date. In the current study, solvent extracts of the subterranean termite Reticulitermes flavipes were analyzed to assess differences in cuticular compounds among castes. We identified a royal-specific hydrocarbon—heneicosane—and several previously un-reported and highly royal enriched long-chain alkanes. When applied to glass dummies, heneicosane elicited worker behavioral responses identical to those elicited by live termite queens, including increased vibratory shaking and antennation. Further, the behavioral effects of heneicosane were amplified when presented with nestmate termite workers' cuticular extracts, underscoring the importance of chemical context in termite royal recognition. Thus, heneicosane is a royal-recognition pheromone that is active in both queens and kings of R. flavipes. The use of heneicosane as a queen and king recognition pheromone by termites suggests that CHCs evolved as royal phero-mones ∼150 million years ago, ∼50 million years before their first use as queen-recognition pheromones in social Hymenoptera. We therefore infer that termites and social Hymenoptera convergently evolved the use of these ubiquitous compounds in royal recognition.
Behavioral Ecology, 2019
The evolutionary origin of queen pheromones (QPs), 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 QPs—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 preexisting 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 t...
Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp
Scientific Reports, 2017
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.