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In bumblebees, dominance behaviour contributes to the regulation of the reproductive division of labour between queens and workers. Towards the end of the colony cycle, at the onset of the competition phase, reproductive workers will establish a dominance hierarchy and challenge the reproductive monopoly of the queen by laying unfertilized, male-destined eggs. However, it has been suggested that the dominance and reproductive hierarchies in bumblebee workers are not completely aligned. By performing manipulative experiments and observing both aggressive behaviour and ovarian activation in Bombus terrestris workers, we aimed to elucidate how these two hierarchies interact and are modulated by the presence of the queen and other reproductive workers. We found that the reintroduction of a queen in a queenless colony not only caused worker ovary regression, but also decreased aggressive interactions between workers, thereby restoring the harmony in the colony. Furthermore, transplanting dominant reproductive workers from queenless colonies into queenright colonies induced the resident workers to activate their ovaries and aggressively compete over reproduction, thereby implying that positive feedback drives the onset of the competition phase. However, we did not see this result when subordinate reproductive workers from queenless colonies were added to queenright colonies, suggesting that ovary activation is mainly initiated in reaction to displays of dominance. Additionally, we observed that workers were attacked irrespective of their reproductive state, questioning the importance of signals that advertise either fertility or sterility in bumblebees. Finally, larger workers were significantly more aggressive and significantly more likely to be attacked, even though smaller workers were equally likely to have activated ovaries. This suggests that large workers resort to aggression to increase their chances of successfully reproducing due to their inherent fighting advantage, whereas small cheater workers could possibly reproduce by staying under the radar to evade nestmate aggression.

To locate mating partners and essential resources such as food, oviposition sites and shelter, insects rely to a large extent on chemical cues. While most research has focused on cues derived from plants and insects, there is mounting evidence that indicates that micro‐organisms emit volatile compounds that may play an important role in insect behaviour. In this study, we assessed how volatile compounds emitted by phylogenetically diverse bacteria affected the olfactory response of the primary parasitoid Aphidius colemani and one of its secondary parasitoids, Dendrocerus aphidum. Olfactory responses were evaluated for volatile blends emitted by bacteria isolated from diverse sources from the parasitoid's habitat, including aphids, aphid mummies and honeydew, and from the parasitoids themselves. Results revealed that A. colemani showed a wide variation in response to bacterial volatiles, ranging from significant attraction over no response to significant repellence. Our results further showed that the olfactory response of A. colemani to bacterial volatile emissions was different from that of D. aphidum. Gas chromatography‐mass spectrometry analysis of the volatile blends revealed that bacterial strains repellent to A. colemani produced significantly higher amounts of esters, organic acids, aromatics and cycloalkanes than attractive strains. Strains repellent to D. aphidum produced significantly higher amounts of alcohols and ketones, whereas the strains attractive to D. aphidum produced higher amounts of the monoterpenes limonene, linalool and geraniol. Overall, our results indicate that bacterial volatiles can have an important impact on insect olfactory responses, and should therefore be considered as an additional, so far often overlooked factor in studying multitrophic interactions between plants and insects. A free Plain Language Summary can be found within the Supporting Information of this article. ispartof: FUNCTIONAL ECOLOGY vol:34 issue:2 pages:507-520 status: published

Animal gut microbiota affect host physiology and behaviour. In social insects, where colony level integrity is preserved via a nestmate discrimination system based on cuticular hydrocarbon mixtures, microorganismal effects may therefore influence social dynamics. Although nestmate recognition has undergone a thorough exploration during the last four decades, few studies have investigated the putative role of gut microbes. Here, we integrated 16S rRNA-based microbial community profiling, chemical and behavioural approaches to test whether gut microbes affect nestmate recognition in Acromyrmex echinatior leaf-cutting ants. Treating workers with a sterile diet or with antibiotics resulted in a substantial alteration of their gut microbial communities. In pairwise social interactions, untreated versus antibiotic-treated nestmates behaved more aggressively than other nestmate and non-nestmate pairs, suggesting that bacterial suppression may alter chemical social cues and trigger aggressive behaviour. Chemical analyses of treated individuals revealed a decrease in the abundance of two metapleural gland antifungal compounds, and confirmed the correspondence between aggression levels and chemical profile differences. Feeding microbiota-remodelled ants with conspecific faecal droplets partially restored the original bacterial communities. Ants fed with faecal droplets from different colonies were unusually aggressive compared to pairs fed with faecal droplets from the same colony. We cannot exclude confounding effects resulting from the potentially harmful action of antibiotics on ant hosts. However, our results suggest a correlation between chemical profiles and the presence of certain microbial species in the gut, which may affect nestmate recognition and division of labour. This opens novel questions about the role of symbiotic microorganisms in the evolution of social insect behaviour. Accepted version

In the highly eusocial wasp, Vespula vulgaris, queens produce honest signals to alert their subordinate workers of their fertility status, and therefore they are reproductively suppressed and help in the colony. The honesty of the queen signals is likely maintained due to hormonal regulation, which affects fertility and fertility cue expression. Here, we tested if hormonal pleiotropy could support the hypothesis that juvenile hormone controls fertility and fertility signaling in workers. In addition, we aimed to check oocyte size as a proxy of fertility. To do that, we treated V. vulgaris workers with synthetic versions of juvenile hormone (JH) analogue and a JH inhibitor, methoprene and precocene, respectively. We dissected the treated females to check ovary activation and analyzed their chemical profile. Our results showed that juvenile hormone has an influence on the abundance of fertility linked compounds produced by workers, and it also showed to increase oocyte size in workers. Our results corroborate the hypothesis that juvenile hormone controls fertility and fertility signaling in workers, whereby workers are unable to reproduce without alerting other colony members of their fertility. This provides supports the hypothesis that hormonal pleiotropy contributes to keeping the queen fertility signals honest.

Chemical cues are among the most important information-sharing mechanisms in insect societies, in which cuticular hydrocarbons play a central role, e.g., from nestmate recognition to queen signaling. The nestmate recognition mechanism usually prevents intruders from taking advantage of the resources stored in the nest. However, nestmate recognition is not unconditionally effective, and foreign individuals can sometimes infiltrate unrelated nests and take advantage of the colony resources. In this study, we investigated the role of overall colony odor profiles on the ability of conspecific workers to drift into unrelated colonies. We hypothesized that drifters would have higher chances of success by infiltrating colonies with the odor profiles most similar to their own nest, avoiding being detected as non-nestmates. By performing a drifting bioassay, we found that workers of the ant Formica fusca infiltrated unrelated conspecific colonies at a rate of 2.4%, significantly infiltrating colonies displaying CHC profiles most similar to their natal nests. Notably, methyl branched hydrocarbons seem to play a role as recognition cues in this species. In addition, we show that environmental rather than genetic factors are responsible for most contributions on the CHC phenotype, presenting ca. of 50% and 27.5% of explained variation respectively, and playing a major role in how worker ants detect and prevent the infiltration of non-nestmates in the colony. Hence, relying on cuticular hydrocarbons similarities could be a profitably evolutionary strategy by which workers can identify conspecific colonies, evade detection by guards, and avoid competition with genetic relatives.

Sexual pheromones are chemical molecules responsible for mediating sex recognition and mating events. Long- and close-range sexual pheromones act differently. The first type is released to attract potential partners, whereas the second coordinates the interactions after potential mating partners encounter each other. Cuticular hydrocarbons (CHCs) have been suggested to be important cues in the mating systems of several Hymenoptera species, although empirical data are still lacking for many species. Here, we evaluated whether males of the model species Polistes dominula can differentiate the sex of individuals based on their CHC composition. In August 2019, several post-worker emergent nests (n = 19) were collected in the vicinity of Leuven (Belgium) and taken to the lab (KU Leuven), where newly emerged females and males were sampled, marked individually, and kept in plastic boxes for at least a week before being used in the mating trials. Focal males were paired with females and males from different nests and subjected to five different conditions: (I) alive, (II) dead, (III) CHCs washed, (IV) CHCs partially returned, and (V) CHCs from the opposite sex. We videotaped the interactions for 10 min and analysed the duration and different behavioural interactions of the focal male. Our results indicate that CHCs may be used by males as cues to recognise a potential mating partner in P. dominula, since the focal males displayed specific courtship behaviours exclusively toward females. Although we cannot exclude that visual cues could also be used in combination with the chemical ones, we empirically demonstrate that CHCs may be important to convey sexual information at close range in mating systems, allowing fast decisions toward potential sexual partners or rivals.

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 their eggs were more queen-like, thereby causing fewer of their eggs to be policed compared to in the control. Overall, our results identify JH as a key regulator of both reproduction and the production of egg marking pheromones that mediate policing behaviour in eusocial wasps. ispartof: SCIENTIFIC REPORTS vol:10 issue:1 ispartof: location:England status: published

Indirect interactions occur when a species affects another species by altering the density (density-mediated interactions) or influencing traits (trait-mediated interactions) of a third species. We studied variation in these two types of indirect interactions in a network of red wood ants and symbiotic arthropods living in their nests. We tested whether the ant workers indirectly affected survival of a symbiotic prey species (Cyphoderus albinus) by changing the density and/or traits of three symbiotic predators, i.e., Mastigusa arietina, Thyreosthenius biovatus and Stenus aterrimus, provoking, respectively, low, medium and high ant aggression. An ant nest is highly heterogeneous in ant worker density and the number of aggressive interactions towards symbionts increases with worker density. We, therefore, hypothesized that varying ant density could indirectly impact prey-predator interactions of the associated symbiont community. Ants caused trait-mediated indirect effects in all three prey-predator interactions, by affecting the prey capture rate of the symbiotic predators at different worker densities. Prey capture rate of the highly and moderately aggressed spider predators M. arietina and T. biovatus decreased with ant density, whereas the prey capture rate of the weakly aggressed beetle predator S. aterrimus increased. Ants also induced density-mediated indirect interactions as high worker densities decreased the survival rate of the two predatory spider species. These results demonstrate for the first time that a host can indirectly mediate the trophic interactions between associated symbionts. In addition, we show that a single host can induce opposing indirect effects depending on its degree of aggression towards the symbionts. ispartof: OECOLOGIA vol:188 issue:4 pages:1145-1153 ispartof: location:Germany status: published

Social insect colonies provide a valuable resource that attracts and offers shelter to a large community of arthropods. Previous research has suggested that many specialist parasites of social insects chemically mimic their host in order to evade aggression. In the present study, we carry out a systematic study to test how common such chemical deception is across a group of 22 arthropods that are associated with red wood ants (Formica rufa group). In contrast to the examples of chemical mimicry documented in some highly specialized parasites in previous studies, we find that most of the rather unspecialized red wood ant associates surveyed did not use mimicry of the cuticular hydrocarbon recognition cues to evade host detection. Instead, we found that myrmecophiles with lower cuticular hydrocarbon concentrations provoked less host aggression. Therefore, some myrmecophiles with low hydrocarbon concentrations appear to evade host detection via a strategy known as chemical insignificance. Others showed no chemical disguise at all and, instead, relied on behavioral adaptations such as particular defense or evasion tactics, in order to evade host aggression. Overall, this study indicates that unspecialized myrmecophiles do not require the matching of host recognition cues and advanced strategies of chemical mimicry, but can integrate in a hostile ant nest via either chemical insignificance or specific behavioral adaptations. ispartof: Journal of Chemical Ecology vol:43 issue:7 pages:644-661 ispartof: location:United States status: published

In several highly eusocial insect species with morphologically distinct castes, queen-characteristic cuticular hydrocarbons (CHCs) have been shown to act as queen signals that suppress the reproduction of nestmate workers. However, it is not known whether such queen pheromones might also play a role in regulating reproductive division of labour in primitively eusocial insects that lack morphologically defined castes. Here, we experimentally tested whether a blend of CHCs which occurred in higher concentrations in the dominant breeding female act as a queen pheromone, and inhibit reproduction by subordinate females in the primitively eusocial paper wasp Polistes satan. In contrast to earlier findings with highly eusocial species, our results show that although specific compounds were enhanced in dominant, reproductively active females, a blend of five of these compounds did not inhibit development of the ovaries of female nestmates. Instead, the dominant female had to be physically present to prevent subordinate females from reproducing. Our results are in line with earlier evidence suggesting that fertility-linked compounds in primitively eusocial wasps act only as cues and help to regulate reproduction when used in conjunction with aggressive dominance behaviour, meaning the physical presence of the dominant female. Alternatively, our results support the hypothesis that queen pheromones in highly eusocial insects were co-opted from fertility cues that were already present in primitively eusocial ancestors, even when initially, such compounds were merely produced as by-products of ovarian activation, without actually serving to signal reproductive status.

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.

The division of labour between reproductive queens and mostly sterile workers is among the defining characteristics of social insects. Queen-produced chemical signals advertising her presence and fertility status, i.e. queen pheromones, are normally used to assert the queen's reproductive dominance in the colony. Most queen pheromones identified to date are chemicals that stop the daughter workers from reproducing. Nevertheless, it has long been suggested that queen pheromones could also regulate reproduction in different ways. In some multiple-queen ants with obligately sterile workers, for example—such as fire ants and pharaoh ants—queen pheromones are thought to regulate reproduction by inhibiting the rearing of new sexuals. Here, we identify the first such queen pheromone in the pharaoh ant Monomorium pharaonis and demonstrate its mode of action via bioassays with the pure biosynthesized compound. In particular, we show that the monocyclic diterpene neocembrene, which in different Monomorium species is produced solely by fertile, egg-laying queens, strongly inhibits the rearing of new sexuals (queens and males) and also exerts a weakly attractive ‘queen retinue’ effect on the workers. This is the first time that a queen pheromone with such a dual function has been identified in a social insect species with obligately sterile workers.

© 2018 The Author(s). Many parasites display complex strategies to evade host detection. The principal view is that the parasites of social insects deceive their host by means of advanced chemical adaptations such as mimicking the cuticular host recognition cues, being chemically odorless, or emitting manipulative volatiles. Apart from these chemical adaptations, parasites of social insects may also use simpler behavioral strategies to evade host detection. As yet, such a behavior has rarely been studied. Here we tested which chemical and behavioral strategies the unspecialized parasitic rove beetle Thiasophila angulata uses to avoid detection by its aggressive Formica rufa red wood ant host. Chemical comparisons of the beetle's and the host ants' cuticular hydrocarbons showed that the beetle carried an idiosyncratic cuticular profile that was clearly different from that of its host. Beetles that were isolated from their host or were placed in the nests of another Formica species perfectly retained their original cuticular profiles and provoked equal levels of aggression. These results suggest that the beetles do not avoid host detection through chemical deception. In contrast, the beetle adapted its behavior to avoid aggression by the ants. In the presence of ants, the beetle behaved much more prudently by hiding more frequently and engaging in less risky runs. Overall, these results highlight that for relatively unspecialized parasites, general strategies such as prudent behavior can be equally effective as more specialized deception strategies to evade host detection. ispartof: BEHAVIORAL ECOLOGY vol:29 issue:6 pages:1225-1233 status: published

The aphid Aphis fabae (Scopoli) is facultatively tended by Lasius niger (Linnaeus) ants. Previously, we found that A. fabae colonies can be made up of several clones, and that clones display significant differences in the composition of their honeydew sugars, especially in the amount of the ant attractant sugar melezitose that they produce. 2. These clonal differences could greatly impact the strength of the mutualistic interaction with ants as well as the aphids' fitness. 3. Hence, the aim of this study was to compare the fitness of different A. fabae clones that differed in their melezitose secretion, and whether or not they were tended by ants. 4. Individual fitness indices, colony growth, and alate production of single-clone aphid colonies were analysed. 5. The results demonstrate that the fitness consequences of ant attendance critically depend on an interaction between levels of melezitose production. In particular, we show that high-melezitose secreting clones produce fewer alates and hence might have a lower dispersal ability in the presence of ants. 6. Furthermore, these data confirm previous evidence that ant attendance is costly and results in the production of fewer apterae.

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.

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

As in most Hymenoptera, the eusocial stingless bees (Meliponini) have a complementary sex determination (CSD) system. When a queen makes a "matched mating" with a male that shares a CSD allele with her, half of their diploid offspring are diploid males rather than females. Matched mating imposes a cost, since diploid male production reduces the colony workforce. Hence, adaptations preventing the occurrence or attenuating its effects are likely to arise. Here we provide clear evidence that in the stingless bee Scaptotrigona depilis, the emergence of diploid males induces queen death, and this usually occurs within 10-20 days of the emergence of diploid male offspring from their pupae. Queens that have not made a matched mating die when introduced into a colony in which diploid males are emerging. This shows that the adult diploid males, and not the queen that has made a matched mating herself, are the proximate cause of queen death. Analysis of the cuticular hydrocarbon profiles of adult haploid and diploid males shows six compounds with significant differences. Moreover, the diploid and haploid males only acquire distinct cuticular hydrocarbon profiles 10 days after emergence. Our data shows that the timing of queen death occurs when the cuticular hydrocarbons of haploid and diploid males differ significantly, suggesting that these chemical differences could be used as cues or signals to trigger queen death. ispartof: JOURNAL OF CHEMICAL ECOLOGY vol:43 issue:4 pages:403-410 ispartof: location:United States status: published

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 of 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-egglaying 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. ispartof: Scientific Reports vol:7 issue:1 ispartof: location:England status: published

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.

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 QMP compounds 9-ODA and 9-HDA tested individually were as effective as the blend of all four major QMP compounds, suggesting considerable signal redundancy. Possible adaptive reasons for the observed complexity of the honeybee queen signal mix are discussed. ispartof: Proceedings Of The Royal Society B-Biological Sciences vol:286 issue:1905 ispartof: location:England status: published

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.

In a recent article we showed that human extra-pair paternity (EPP) rates did not substantially decline in contemporary relative to historical Western societies over the past few hundred years [1]. In both cases, ∼1–2% of all children appeared to be the product of cuckoldry. This came as a great surprise, given the known steady increase in the adoption rate and reliability of contraception over the past century [2]. We proposed several hypotheses to explain this paradox. One, which Harris [3] focused on, was that women may have become more sexually liberated, and now engage in relatively more extramarital affairs.

Background A host infected with multiple parasitic species provides a unique system to test evolutionary and ecological hypotheses. Different parasitic species associated with a single host are expected to occupy different niches. This niche specialization can evolve from intraguild competition among parasites. However, niche specialization can also be structured directly by the host when its defence strategy depends on the parasite’s potential impact. Then it can be expected that species with low or no tendency to prey on host brood will elicit less aggression than severe brood parasitic species and will be able to integrate better in the host system. We examined this hypothesis in a large community of symbionts associated with European red wood ants (Formica rufa group) by testing the association between 1) level of symbiont integration (i.e. presence in dense brood chambers vs. less populated chambers without brood) 2) level of ant aggression towards the symbiont 3) brood predation tendency of the symbiont. Results Symbionts differed vastly in integration level and we demonstrated for the first time that relatively unspecialized ant symbionts or myrmecophiles occur preferentially in brood chambers. Based on their integration level, we categorize the tested myrmecophiles into three categories: 1) species attracted to the dense brood chambers 2) species rarely or never present in the brood chambers 3) species randomly distributed throughout the nest. The associates varied greatly in brood predation tendency and in aggression elicited. However, we did not find a correlation for the whole myrmecophile community between a) brood predation tendency and host’s aggression b) integration level and host’s aggression c) integration level and brood predation tendency. Conclusions Our results indicate that red wood ants did not act more hostile towards species that have a high tendency to prey on brood compared to species that are less likely or do not prey on brood. We show that potentially harmful parasites can penetrate into the deepest parts of a social insect fortress. We discuss these seemingly paradoxical findings in relation to models on coevolution and evolutionary arms races and list factors which can make the presence of potentially harmful parasites within the brood chambers evolutionary stable. Electronic supplementary material The online version of this article (doi:10.1186/s12862-016-0583-6) contains supplementary material, which is available to authorized users.

International audience; Dynamism was originally defined as the proportion of online versus offline orders in the literature on dynamic logistics. Such a definition however, loses meaning when considering purely dynamic problems where all customer requests arrive dynamically. Existing measures of dynamism are limited to either (1) measuring the proportion of online versus offline orders or (2) measuring urgency, a concept that is orthogonal to dynamism, instead. The present paper defines separate and independent formal definitions of dynamism and urgency applicable to purely dynamic problems. Using these formal definitions, instances of a dynamic logistic problem with varying levels of dynamism and urgency were constructed and several route scheduling algorithms were executed on these problem instances. Contrary to previous findings, the results indicate that dynamism is positively correlated with route quality; urgency, however, is negatively correlated with route quality. The paper contributes the theory that dynamism and urgency are two distinct concepts that deserve to be treated separately.

In most ants, bees, and wasps, the workers are capable of challenging the reproductive monopoly of the queen by laying unfertilized, male eggs. An important mechanism that can resolve this conflict is policing, whereby the queen or workers prevent successful worker reproduction by selectively eating worker-laid eggs or by attacking egg-laying workers. Egg policing by workers has been shown to occur in several social wasp species, but the information used by worker wasps to discriminate between queen-laid and worker-laid eggs has never been investigated. Our aim, therefore, was to investigate if hydrocarbons might be used in egg policing by workers in the common wasp, Vespula vulgaris, where worker policing previously has been shown to be effective. Our results show that 51 different hydrocarbons are present on the surface of newly-laid eggs, and that there are pronounced quantitative differences in the hydrocarbon profiles of queen-laid and worker-laid eggs, with longer-chained alkenes and methylated alkanes (C28–C31) in particular being more abundant on the surface of queen-laid eggs. We further show that the hydrocarbon profiles on the surface of queen-laid and worker-laid eggs resemble those found on the mother queen’s and workers’ cuticles. Interestingly, longer-chained methylated alkanes also were more abundant on the cuticle of both mother queens and reproductive workers, suggesting that these compounds are linked to fertility, as has also been found to be the case in several ant species. ispartof: Journal of Chemical Ecology vol:38 issue:1 pages:42-51 ispartof: location:United States status: published

Aphids are a worldwide pest and an important model in ecology and evolution. Little is known, however, about the genetic structure of their colonies at a microgeographic level. For example, it remains largely unknown whether most species form monoclonal or polyclonal colonies. Here, we present the first detailed study on levels of clonal mixing in a nonsocial facultative ant mutualist, the black bean aphid Aphis fabae. In contrast to the earlier suggestion that colonies of this species are generally monoclonal, we found that across two subspecies of the black bean aphid, A. fabae cirsiiacanthoidis and A. fabae fabae, 32% and 67% of the aphid colonies were in fact polyclonal, consisting of a mix of up to four different clones, which resulted in an overall average relatedness within colonies of 0.90 and 0.79 in the two subspecies. Data further show that the average relatedness in A. f. cirsiiacanthoidis remained relatively constant throughout the season, which means that clonal erosion due to clonal selection more or less balanced with the influx of new clones from elsewhere. Nevertheless, relatedness tended to decrease over the lifetime of a given colony, implying that clonal mixing primarily resulted from the joining of pre-existing colonies as opposed to via simultaneous host colonisation by several foundresses. Widespread clonal mixing is argued to affect the ecology and evolution of the aphids in various important ways, for example with respect to the costs and benefits of group living, the evolution of dispersal and the interaction with predators as well as with the ant mutualists.

In some ants, bees, and wasps, workers kill or "police" male eggs laid by other workers in order to maintain the reproductive primacy of the queen. Kin selection theory predicts that multiple mating by the queen is one factor that can selectively favor worker policing. This is because when the queen is mated to multiple males, workers are more closely related to the queen’s sons than to the sons of other workers. Earlier work has suggested that reproductive patterns in the German wasp Vespula germanica may contradict this theory, because in some colonies a large fraction of the adult males were inferred to be the workers’ sons, despite the effective queen mating frequency being greater than 2 (2.4). In the present study, we reexamine the V. germanica case and show that it does support the theory. First, genetic analysis confirms that the effective queen mating frequency is high, 2.9, resulting in workers being more related to the queen’s sons than to other workers’ sons. Second, behavioral assays show that worker-laid eggs are effectively killed by other workers, despite worker-laid eggs having the same intrinsic viability as queen-laid ones. Finally, we estimate that approximately 58.4% of the male eggs but only 0.44% of the adult males are worker derived in queenright colonies, consistent with worker reproduction being effectively policed. ispartof: Behavioral Ecology vol:19 issue:2 pages:272-278 status: published

Queen pheromones are essential for regulation of the reproductive division of labor in eusocial insect species. Although only the queen is able to lay fertilized eggs and produce females, in some cases workers may develop their ovaries and lay male-destined eggs, thus reducing the overall colony efficiency. As long as the queen is healthy, it is usually in the workers’ collective interest to work for the colony and remain sterile. Queens signal their fertility via pheromones, which may have a primer effect, affecting the physiology of workers, or a releaser effect, influencing worker behavior. The queen pheromone of the ant Lasius niger was among the first queen pheromones of social insects to be identified. Its major component is 3-methylhentriacontane (3-MeC31), which is present in relatively large amounts on the queen’s cuticle and on her eggs. 3-MeC31 regulates worker reproduction by inhibiting ovarian development. Most monomethyl-branched hydrocarbons can exist in two stereoisomeric forms. The correct stereochemistry is fundamental to the activity of most bioactive molecules, but this has rarely been investigated for methyl-branched hydrocarbons. Here, we tested the bioactivity of the (S)- and (R)-enantiomers of 3-MeC31, and found that whereas both enantiomers were effective in suppressing worker ovarian development,(S)-3-MeC31 appeared to be more effective at suppressing aggressive behavior by workers. This suggests that the natural pheromone may be a mixture of the two enantiomers. The enantiomeric ratio produced by queens remains unknown because of the small amounts of the compound available from each queen. ispartof: The Journal of Experimental Biology vol:219 issue:11 pages:1632-1638 ispartof: location:England status: published

Lehmann & Keller (2006) convincingly argue that cooperation or altruism can evolve only when at least one of the following conditions are met: (i) cooperation has direct personal benefits, (ii) individuals are genetically related, (iii) individuals have information on the likely behaviour of others or (iv) individuals recognize other cooperators through a phenotypic label (green beard recognition). The first condition is quite obvious. The three others are also intuitive, given that they provide various conditions under which interacting individuals are positively related, meaning more likely than chance to interact with fellow cooperators (Frank, 1998; Pepper & Smuts, 2002; Foster & Wenseleers, 2006; Foster et al., 2006). By focusing on costs and benefits and relatedness, Lehmann and Keller (2006) are adopting an inclusive fitness or Hamilton’s rule-based approach to classify social evolution models (Hamilton, 1964). Personally, I believe a Hamiltonian perspective is indeed a very intuitive one, and should be adopted more widely. This is true particularly in the area of game theory, where currently little effort is made to interpret results this way, and models are frequently simulation-based, making general, intuitive interpretation of results difficult. In fact, in my own work, Hamilton’s rule has always taken a central place in the derivation and interpretation of model results (e.g. Wenseleers et al., 2003, 2004a, b; Ratnieks et al., 2006). At the same time, however, one may also wonder whether it is possible to translate every single social evolution model into the form of Hamilton’s rule. Here, I am skeptical, the reason being that Hamilton’s rule has well-known limitations. In particular, Hamilton’s rule only works correctly under weak selection and additive gene action (Cavalli-Sforza & Feldman, 1978; Michod, 1982; Grafen, 1985; Bulmer, 1994; Hamilton, 1964, 1995; Frank, 1997; Roze & Rousset, 2003; Rousset, 2004). In addition, evolution is normally assumed to be close to equilibrium, with most of the population fixed for a single type (Frank, 1998). Finally, with Hamilton’s rule being a deterministic equation, it entirely neglects stochasticity, and thus ignores the possibility for deleterious altruistic genotypes to go to fixation as a result of drift (Frank, 1997), which models have shown to be quite possible in small populations (Eshel, 1972; Rousset, 2004). In the section below I will give two worked-out examples where some of these limitations come into play and where, due to violations of assumptions, Hamilton’s rule does not correctly predict evolutionary change. The implication is that partitioning selection into direct and indirect fitness components is not always as straightforward as Lehmann and Keller make out. In many cases, the conditions under which a cooperative genotype would spread relative to a noncooperative one simply cannot be written in the form of Hamilton’s rule. In such situations, the inclusive fitness framework of Lehmann and Keller cannot be used to accurately classify models.

Microbial populations often contain a fraction of slow-growing persister cells that withstand antibiotics and other stress factors. Current theoretical models predict that persistence levels should reflect a stable state in which the survival advantage of persisters under adverse conditions is balanced with the direct growth cost impaired under favourable growth conditions, caused by the nonreplication of persister cells. Based on this direct growth cost alone, however, it remains challenging to explain the observed low levels of persistence (<

Inclusive fitness theory, put forward by English biologist William Hamilton in 1964, is considered by many as the most important addition to the theory of natural selection since Darwin. One prediction of the theory is that animals should often show a tendency to nepotistically favour close relatives. Goodisman et al. (2007) test this theory for the first time using molecular methods in a vespine wasp, the eastern yellowjacket, Vespula maculifrons. Somewhat surprisingly, nepotism was found to be absent. This begs the question why nepotism is predicted by theory, yet in a growing list of species is shown to be absent. Is inclusive fitness theory in trouble? As we show, it is not: costs and constraints explain the general absence of queen rearing nepotism, and nepotism in insect societies in fact is well supported in the context of male rearing and manipulation of colony sex ratios.

Eusocial insect societies display a remarkable reproductive division of labor between a single fertile queen and thousands of largely sterile workers. In most species, however, the workers retain the capacity to reproduce, particularly in queenless colonies where typically many workers lay eggs. As yet, the molecular determinants that initiate this shift in worker fertility are still poorly documented. By using RNA interference we here demonstrate that the knockdown of epidermal growth factor receptor, a gene which was previously shown to be involved in queen-worker caste differentiation, also induces reproduction in worker honeybees (Apis mellifera). These data show that worker fertility and queen-worker caste determination partly rely on the same gene regulatory networks, thereby providing a major breakthrough in our understanding of the molecular determinants of the social insects’ spectacular reproductive division of labor.

Insect societies are well known for their high degree of cooperation, but their colonies can potentially be exploited by reproductive workers who lay unfertilized, male eggs, rather than work for the good of the colony. Recently, it has also been discovered that workers in bumblebees and Asian honeybees can succeed in entering and parasitizing unrelated colonies to produce their own male offspring. The aim of this study was to investigate whether such intraspecific worker parasitism might also occur in stingless bees, another group of highly social bees. Based on a large-scale genetic study of the species Melipona scutellaris, and the genotyping of nearly 600 males from 45 colonies, we show that ca. 20% of all males are workers’ sons, but that around 80% of these had genotypes that were incompatible with them being the sons of workers of the resident queen. By tracking colonies over multiple generations, we show that these males were not produced by drifted workers, but rather by workers that were the offspring of a previous, superseded queen. This means that uniquely, workers reproductively parasitize the next-generation workforce. Our results are surprising given that most colonies were sampled many months after the previous queen had died and that workers normally only have a life expectancy of ca. 30 days. It also implies that reproductive workers greatly outlive all other workers. We explain our results in the context of kin selection theory, and the fact that it pays workers more from exploiting the colony if costs are carried by less related individuals. ispartof: Molecular Ecology vol:18 issue:19 pages:4102-4111 ispartof: location:England status: published

The evolution of mutualisms presents a puzzle. Why does selection favour cooperation among species rather than cheaters that accept benefits but provide nothing in return? Here we present a general model that predicts three key factors will be important in mutualism evolution: (i) high benefit to cost ratio, (ii) high within-species relatedness and (iii) high between-species fidelity. These factors operate by moderating three types of feedback benefit from mutualism: cooperator association, partner-fidelity feedback and partner choice. In defining the relationship between these processes, our model also allows an assessment of their relative importance. Importantly, the model suggests that phenotypic feedbacks (partner-fidelity feedback, partner choice) are a more important explanation for between-species cooperation than the development of genetic correlations among species (cooperator association). We explain the relationship of our model to existing theories and discuss the empirical evidence for our predictions. ispartof: Journal of evolutionary biology vol:19 issue:4 pages:1283-93 ispartof: location:Switzerland status: published

In insect societies, eggs laid by workers are frequently killed by other workers – a behaviour known as ”worker policing”. The traditional explanation of worker policing is that it is a mechanism to resolve intracolony conflict, and maintain the reproductive monopoly of the queen. Recently, Pirk et al. (2004) proposed that worker policing instead is aimed at removing unviable worker-laid eggs and is ultimately just another example of hygienic behaviour. Here we test this hypothesis for the common wasp Vespula vulgaris, a species with highly effective worker policing.We show that worker-laid eggs from queenless colonies have a lower hatch rate (68%) than queen-laid eggs (82%). Analysis of egg laying rates of queens and workers, however, shows that the difference is not big enough to explain the apparent absence of adult worker-derived males in this species. ispartof: Insectes sociaux vol:53 issue:4 pages:399-402 status: published

Evolution Policing is a feature not only of human society but also of social insect societies, being prevalent among certain species of bee, wasp, and ant. In their Perspective, Ratnieks and Wenseleers take an in-depth look at policing in insect societies and discuss whether insect policing could perhaps shed light on better ways to police human societies.

In social groups composed of kin, inclusive fitness benefits can favor greater cooperation. Alternatively, cooperation can be enforced through the policing of less cooperative individuals. Here, we show that the effect of policing can be twofold: not only can it directly suppress individual selfishness, it can also entirely remove the incentive for individuals to act selfishly in the first place. We term such individual restraint in response to socially imposed policing "acquiescence" and illustrate the concept using examples drawn from the social Hymenoptera (the ants, bees, and wasps). Inclusive fitness models confirm that when a policing system is in place, individuals should be less tempted to act selfishly. This is shown to have important consequences for the resolution of conflict within their societies. For example, it can explain why in many species very few workers attempt to reproduce and why immature females usually do not attempt to develop as queens rather than workers. Although our analyses are primarily focused on the social insects, our conclusions are likely to be general and to apply to other societies as well. ispartof: The American naturalist vol:164 issue:6 pages:154-167 ispartof: location:United States status: published

SummaryEusocial insects exhibit a remarkable reproductive division of labor between queens and largely sterile workers [1, 2]. Recently, it was shown that queens of diverse groups of social insects employ specific, evolutionarily conserved cuticular hydrocarbons to signal their presence and inhibit worker reproduction [3]. Workers also recognize and discriminate between eggs laid by the queen and those laid by workers, with the latter being destroyed by workers in a process known as “policing” [4, 5]. Worker policing represents a classic example of a conflict-reducing mechanism, in which the reproductive monopoly of the queen is maintained through the selective destruction of worker-laid eggs [5, 6]. However, the exact signals used in worker policing have thus far remained elusive [5, 7]. Here, we show that in the common wasp, Vespula vulgaris, the pheromone that signals egg maternity and enables the workers to selectively destroy worker-laid eggs is in fact the same as one of the sterility-inducing queen signals that we identified earlier [3]. These results imply that queen pheromones regulate insect sociality in two distinct and complementary ways, i.e., by signaling the queen’s presence and inhibiting worker reproduction, and by facilitating the recognition and policing of worker-laid eggs.

For more than 20 years, sex allocation in hymenopteran societies has been a major topic in insect sociobiology. A recurring idea was that relatedness asymmetries arising from their haplodiploid sex determination system would lead to various parent-offspring conflicts over optimal reproduction. A possible weakness of existing theory is that only interests of nuclear genes are properly accounted for. Yet, a diversity of maternally transmitted elements manipulate the reproduction of their host in many solitary arthropod groups. The bacterium Wolbachia is a striking example of such a selfish cytoplasmic element, with effects ranging from reproductive incompatibility between host strains, induction of parthenogenesis and feminization of males. This paper reports on a first PCR-based Wolbachia screening in ants. Out of 50 Indo-Australian species, 50% screened positive for an A-group strain. One of these species also harboured a B-group strain in a double infection. Various factors that might explain the unusually high incidence of Wolbachia in ants are discussed. In general, Wolbachia may represent a widespread and previously unrecognized party active in the conflicts of interest within social insect colonies. ispartof: Proceedings of the Royal Society B: Biological Sciences vol:265 issue:1404 pages:1447-1452 ispartof: location:England status: published

In ca. 150 species of queenless ants, a specialized queen caste is rare or absent, and mated workers take over the role of the queen in some or all of the colonies. Previously, it has been shown that reproduction in queenless ants is regulated by a combination of dominance behavior and chemical fertility signaling. It is unknown, however, whether chemical signals alone can sufficiently regulate reproduction. To investigate this possibility, we studied reproductive regulation in the facultatively queenless ant Gnamptogenys striatula, a species where dominance behavior is rare or absent. Active egg layers and infertile workers showed qualitative and quantitative differences in their cuticular hydrocarbon profile. Five long-chain methyl alkanes, 3,13- and 3,15-dimethyl pentriacontane, 3,13- and 3,15-dimethyl heptentriacontane, and 3,11,15-trimethyl heptentriacontane occurred only on the cuticles of virgin and mated egg layers. Pronounced quantitative differences were found in a further 27 alkenes; alkanes; and mono-, di-, and trimethyl alkanes. Workers that had recently stopped laying eggs had profiles similar to infertile workers, and mating status did not affect this chemical pattern. We conclude that the cuticular hydrocarbon profiles of G. striatula workers provide reliable information about their current fertility. In the interest of colony productivity, this allows reproduction to be regulated without the use of aggression. ispartof: Journal of chemical ecology vol:32 issue:9 pages:2023-2034 ispartof: location:United States status: published

Background The Member States of European Union are encouraged to improve the general conditions for the production and marketing of apicultural products. In Belgium, programmes on the restocking of honey bee hives have run for many years. Overall, the success ratio of this queen breeding programme has been only around 50%. To tackle this low efficacy, we organized sanitary controls of the breeding queens in 2012 and 2014. Results We found a high quantity of viruses, with more than 75% of the egg samples being infected with at least one virus. The most abundant viruses were Deformed Wing Virus and Sacbrood Virus (≥40%), although Lake Sinai Virus and Acute Bee Paralysis Virus were also occasionally detected (between 10-30%). In addition, Aphid Lethal Paralysis Virus strain Brookings, Black Queen Cell Virus, Chronic Bee Paralysis Virus and Varroa destructor Macula-like Virus occurred at very low prevalences (≤5%). Remarkably, we found Apis mellifera carnica bees to be less infected with Deformed Wing Virus than Buckfast bees (p