Jelle van Zweden

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.

Queen signaling in social wasps.

Social Hymenoptera are characterized by a reproductive division of labor, whereby queens perform most of the reproduction and workers help to raise her offspring. A long‐lasting debate is whether queens maintain this reproductive dominance by manipulating their daughter workers into remaining sterile (queen control), or if instead queens honestly signal their fertility and workers reproduce according to their own evolutionary incentives (queen signaling). Here, we test these competing hypotheses using data from Vespine wasps. We show that in natural colonies of the Saxon wasp, Dolichovespula saxonica, queens emit reliable chemical cues of their true fertility and that these putative queen signals decrease as the colony develops and worker reproduction increases. Moreover, these putative pheromones of D. saxonica show significant conservation with those of Vespula vulgaris and other Vespinae, thereby arguing against fast evolution of signals as a result of a queen–worker arms race ensuing from queen control. Lastly, levels of worker reproduction in these species correspond well with their average colony kin structures, as predicted by the queen signaling hypothesis but not the queen control hypothesis. Altogether, this correlative yet comprehensive analysis provides compelling evidence that honest signaling explains levels of reproductive division of labor in social wasps.

Crozier’s paradox revisited: maintenance of genetic recognition systems by disassortative mating

BackgroundOrganisms are predicted to behave more favourably towards relatives, and kin-biased cooperation has been found in all domains of life from bacteria to vertebrates. Cooperation based on genetic recognition cues is paradoxical because it disproportionately benefits individuals with common phenotypes, which should erode the required cue polymorphism. Theoretical models suggest that many recognition loci likely have some secondary function that is subject to diversifying selection, keeping them variable.ResultsHere, we use individual-based simulations to investigate the hypothesis that the dual use of recognition cues to facilitate social behaviour and disassortative mating (e.g. for inbreeding avoidance) can maintain cue diversity over evolutionary time. Our model shows that when organisms mate disassortatively with respect to their recognition cues, cooperation and recognition locus diversity can persist at high values, especially when outcrossed matings produce more surviving offspring. Mating system affects cue diversity via at least four distinct mechanisms, and its effects interact with other parameters such as population structure. Also, the attrition of cue diversity is less rapid when cooperation does not require an exact cue match. Using a literature review, we show that there is abundant empirical evidence that heritable recognition cues are simultaneously used in social and sexual behaviour.ConclusionsOur models show that mate choice is one possible resolution of the paradox of genetic kin recognition, and the literature review suggests that genetic recognition cues simultaneously inform assortative cooperation and disassortative mating in a large range of taxa. However, direct evidence is scant and there is substantial scope for future work.

Conservation of Queen Pheromones Across Two Species of Vespine Wasps.

Social insects are known for their reproductive division of labor between queens and workers, whereby queens lay the majority of the colony’s eggs, and workers engage mostly in non-reproductive tasks. Queens produce pheromones that signal their presence and fertility to workers, which in turn generally remain sterile. Recently, it has been discovered that specific queen-characteristic cuticular hydrocarbons (CHCs) function as queen pheromones across multiple lineages of social insects. In the common wasp, Vespula vulgaris, several long-chain linear alkanes and 3-methylalkanes were shown to act as queen signals. Here, we describe similar bioassays with a related species of highly eusocial vespine wasp, the Saxon wasp, Dolichovespula saxonica. We show that a blend of queen-characteristic hydrocarbons that are structurally related to those of the common wasp inhibit worker reproduction, suggesting conservation of queen pheromones across social wasps. Overall, our results highlight the central importance of CHCs in chemical communication among social insects in general, and as conserved queen pheromones in these social wasps in particular.

A statistical approach to identify candidate cues for nestmate recognition

The ability of social insects to discriminate nestmates from non-nestmates is mainly achieved through chemical communication. To ultimately understand this recognition and its decision rules, identification of the recognition cues is essential. Although recognition cues are most likely cuticular hydrocarbons, identifying the exact cues for specific species has remained a daunting task, partly due to the sheer number of odor compounds. Perhaps unsurprisingly, one of the few species where the recognition cues have been identified, Formica exsecta, has only around ten major hydrocarbons on its cuticle. In this study we use previous results of this species to search for nestmate recognition cues in two other species of ants, Camponotus aethiops and Monomorium pharaonis. Employing chemical distances and observed aggression between colonies, we first ask which type of data normalization, centroid, and distance calculation is most diagnostic to discriminate between nestmate recognition cues and other compounds. We find that using a “global centroid” instead of a “colony centroid” significantly improves the analysis. One reason may be that this new approach, unlike previous ones, provides a biologically meaningful way to quantify the chemical distances between nestmates, allowing for within-colony variation in recognition cues. Next, we ask which subset of hydrocarbons most likely represents the cues that the ants use for nestmate recognition, which shows less clear results for C. aethiops and M. pharaonis than for F. exsecta, possibly due to less than ideal datasets. Nonetheless, some compound sets performed better than others, showing that this approach can be used to identify candidate compounds to be tested in bio-assays, and eventually crack the sophisticated code that governs nestmate recognition.

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.

Social evolution: when promiscuity breeds cooperation.

In social evolution theory, it has become common wisdom that close family ties should promote cooperative behaviour. Yet, in social insects, evidence is accumulating that queen promiscuity and low relatedness sometimes work better.

Sensory and cognitive adaptations to social living in insect societies

A key question in evolutionary biology is to explain the causes and consequences of the so-called “major transitions in evolution,” which resulted in the progressive evolution of cells, organisms, and animal societies (1⇓–3). Several studies, for example, have now aimed to determine which suite of adaptive changes occurred following the evolution of sociality in insects (4). In this context, a long-standing hypothesis is that the evolution of the spectacular sociality seen in insects, such as ants, bees, or wasps, should have gone hand in hand with the evolution of more complex chemical communication systems, to allow them to coordinate their complex social behavior (5). Indeed, whereas solitary insects are known to use pheromone signals mainly in the context of mate attraction and species-recognition, social insects use chemical signals in a wide variety of contexts: to communicate their caste or reproductive status, recognize nestmates from invaders, mark the way to food sources, or alarm nestmates about imminent danger (5). Well-controlled studies of the change in investment in chemical communication systems in highly eusocial insects, such as ants, termites, or Corbiculate bees, however, have proven hard to conduct, because eusociality in these taxa evolved long ago in the Cretaceous (6) and closely related solitary species are no longer around (Fig. 1). In PNAS, Wittwer et al. (7) now provide an elegant solution to this problem. By studying Halictinae sweat bees—a group of primitively eusocial insects that evolved sociality more recently and on several occasions reverted back to a solitary lifestyle (8) (Fig. 1)—they succeed in making an accurate comparison of the investment in chemosensory systems made by social and derived, closely related, nonsocial species. Fig. 1. Cladogram showing the independent origins and secondary losses of sociality in the Hymenoptera (after refs. 6 and 20⇓⇓⇓–24). For clarity, … [↵][1]1To whom correspondence should be addressed. Email: tom.wenseleers{at}kuleuven.be. [1]: #xref-corresp-1-1