Dual Effect of Wasp Queen Pheromone in Regulating Insect Sociality (original) (raw)
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BioEssays : news and reviews in molecular, cellular and developmental biology, 2015
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 ...
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.
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.
Reproduction and signals regulating worker policing under identical hormonal control in social wasps
Scientific Reports
In social Hymenoptera, fertility and fertility signalling are often under identical hormonal control, and it has been suggested that such hormonal pleiotropies can help to maintain signal honesty. In the common wasp Vespula vulgaris, for example, fertile queens have much higher juvenile hormone (JH) titers than workers, and JH also controls the production of chemical fertility cues present on the females’ cuticle. To regulate reproductive division of labour, queens use these fertility cues in two distinct ways: as queen pheromones that directly suppress the workers’ reproduction as well as to mark queen eggs and enable the workers to recognize and police eggs laid by other workers. Here, we investigated the hormonal pleiotropy hypothesis by testing if experimental treatment with the JH analogue methoprene could enable the workers to lay eggs that evade policing. In support of this hypothesis, we find that methoprene-treated workers laid more eggs, and that the chemical profiles of 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.
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
Workers of a Polistes Paper Wasp Detect the Presence of Their Queen by Chemical Cues
Chemical Senses, 2007
Differences in long-chain hydrocarbon mixtures among reproductive and nonreproductive individuals have been often revealed in social insects. However, very few papers demonstrated that these signatures actually act as contact pheromones used by nonreproductive to recognize the presence of a related queen in the colony. Cuticular and glandular hydrocarbons of Polistes paper wasps have been extensively studied, but, until now, the perception and recognition of such cues was not demonstrated. In this paper, we show, for the first time in Vespidae, that Polistes gallicus workers distinguish nestmates from alien individuals and queens from workers by the hydrocarbon mixtures of the Van der Vecht organ secretion (VVS). We also demonstrated that stroking behavior (a peculiar behavior of Polistes by which queens probably lay VVS on the nest) acts as an inhibitor of ovarian development in workers.
Chemical Communication and Reproduction Partitioning in Social Wasps
Journal of Chemical Ecology, 2018
Social wasps encompass species displaying diverse social organization regarding colony cycle, nest foundation, caste differences (from none to significant dimorphism) and number of reproductive queens. Current phylogenetic data suggests that sociality occured independently in the subfamily Stenogastrinae and in the Polistinae+Vespinae clade. In most species, including those with the simplest social organization, colony reproduction is monopolised by a single or few females. Since their nest mates can also develop ovaries and lay eggs, dominant females must somehow inhibit them from reproducing. Physical interactions in the form of open aggression or, usually, ritualised dominance by the fertile females contribute to fertility inhibition in several species, but it is unlikely to function in large colonies. In the latter case, reproduction within the colony is likely to be regulated through pheromones. Relatively little is known about these semiochemicals. Studies on all the three social wasp subfamilies, revealed that cuticular hydrocarbon components differ in abundance between egg-laying and not egg-laying females and that their composition depends on fertility status. In several species, females have been reported to manifestly react towards females with activated ovaries, but there is little evidence to support the hypothesis that fertile individuals are either recognized through their CHC composition, or that over-represented CHC constituents can inhibit fertility. Moreover, very little information exists on the possibility that exocrine glands release fertility signals or chemicals inhibiting fertility. Keywords Reproduction partitioning. Queen pheromone. Oophagy. Cuticular hydrocarbons. Dufour gland. Social parasites Social wasps comprise a broad group of genera and species with very diverse social organizations, colony size and colony cycle. Since the first comprehensive review on pheromones and chemical communication in social wasps (Downing 1991), only a limited number of studies have investigated volatiles from exocrine glands and their role in communication (Bruschini et al. 2010). On the contrary, several researches have considered the role of cuticular hydrocarbons (CHCs) as recognition pheromones in different social contexts (Dani 2006; Kather and Martin 2015; Lorenzi 2006). The literature on CHCs in the context of dominance hierarchies in females of Polistes species has recently been reviewed (Jandt et al. 2014). Here we analyze the current knowledge on chemical communication in reproductive partitioning in social wasps and discuss the limits of the current state of art, addressing possible directions for future research.
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...