The impact of quality-adjusted life years on evaluating COVID-19 mitigation strategies: lessons from age-specific vaccination roll-out and variants of concern in Belgium (2020-2022).

BACKGROUND: When formulating and evaluating COVID-19 vaccination strategies, an emphasis has been placed on preventing severe disease that overburdens healthcare systems and leads to mortality. However, more conventional outcomes such as quality-adjusted life years (QALYs) and inequality indicators are warranted as additional information for policymakers. METHODS: We adopted a mathematical transmission model to describe the infectious disease dynamics of SARS-COV-2, including disease mortality and morbidity, and to evaluate (non)pharmaceutical interventions. Therefore, we considered temporal immunity levels, together with the distinct transmissibility of variants of concern (VOCs) and their corresponding vaccine effectiveness. We included both general and age-specific characteristics related to SARS-CoV-2 vaccination. Our scenario study is informed by data from Belgium, focusing on the period from August 2021 until February 2022, when vaccination for children aged 5-11 years was initially not yet licensed and first booster doses were administered to adults. More specifically, we investigated the potential impact of an earlier vaccination programme for children and increased or reduced historical adult booster dose uptake. RESULTS: Through simulations, we demonstrate that increasing vaccine uptake in children aged 5-11 years in August-September 2021 could have led to reduced disease incidence and ICU occupancy, which was an essential indicator for implementing non-pharmaceutical interventions and maintaining healthcare system functionality. However, an enhanced booster dose regimen for adults from November 2021 onward could have resulted in more substantial cumulative QALY gains, particularly through the prevention of elevated levels of infection and disease incidence associated with the emergence of Omicron VOC. In both scenarios, the need for non-pharmaceutical interventions could have decreased, potentially boosting economic activity and mental well-being. CONCLUSIONS: When calculating the impact of measures to mitigate disease spread in terms of life years lost due to COVID-19 mortality, we highlight the impact of COVID-19 on the health-related quality of life of survivors. Our study underscores that disease-related morbidity could constitute a significant part of the overall health burden. Our quantitative findings depend on the specific setup of the interventions under review, which is open to debate or should be contextualised within future situations.

Chemical signatures of egg maternity and Dufour's gland in Vespine wasps.

Cuticular hydrocarbons (CHCs) are often used in the chemical communication among social insects. CHCs can be used in nestmate recognition and as queen pheromones, the latter allows the regulation of the reproductive division of labor. In the common wasp Vespula vulgaris, CHCs and egg-marking hydrocarbons are caste-specific, being hydrocarbon queen pheromones and egg maternity signals. Whether these compounds are conserved among other Vespinae wasps remains unknown. Queens, virgin queens, reproductive workers, and workers belonging to four different wasp species, Dolichovespula media, Dolichovespula saxonica, Vespa crabro, and Vespula germanica, were collected and studied. The cuticular hydrocarbons, egg surface, and Dufour's gland composition were characterized and it was found that chemical compounds are caste-specific in the four species. Quantitative and qualitative differences were detected in the cuticle, eggs, and Dufour's gland. Some specific hydrocarbons that were shown to be overproduced in the cuticle of queens were also present in higher quantities in queen-laid eggs and in their Dufour's gland. These hydrocarbons can be indicated as putative fertility signals that regulate the division of reproductive labor in these Vespine societies. Our results are in line with the literature for V. vulgaris and D. saxonica, in which hydrocarbons were shown to be conserved queen signals. This work presents correlative evidence that queen chemical compounds are found not only over the body surface of females but also in other sources, such as the Dufour's gland and eggs.

Population Bottlenecks Strongly Affect the Evolutionary Dynamics of Antibiotic Persistence.

Bacterial persistence is a potential cause of antibiotic therapy failure. Antibiotic-tolerant persisters originate from phenotypic differentiation within a susceptible population, occurring with a frequency that can be altered by mutations. Recent studies have proven that persistence is a highly evolvable trait and, consequently, an important evolutionary strategy of bacterial populations to adapt to high-dose antibiotic therapy. Yet, the factors that govern the evolutionary dynamics of persistence are currently poorly understood. Theoretical studies predict far-reaching effects of bottlenecking on the evolutionary adaption of bacterial populations, but these effects have never been investigated in the context of persistence. Bottlenecking events are frequently encountered by infecting pathogens during host-to-host transmission and antibiotic treatment. In this study, we used a combination of experimental evolution and barcoded knockout libraries to examine how population bottlenecking affects the evolutionary dynamics of persistence. In accordance with existing hypotheses, small bottlenecks were found to restrict the adaptive potential of populations and result in more heterogeneous evolutionary outcomes. Evolutionary trajectories followed in small-bottlenecking regimes additionally suggest that the fitness landscape associated with persistence has a rugged topography, with distinct trajectories toward increased persistence that are accessible to evolving populations. Furthermore, sequencing data of evolved populations and knockout libraries after selection reveal various genes that are potentially involved in persistence, including previously known as well as novel targets. Together, our results do not only provide experimental evidence for evolutionary theories, but also contribute to a better understanding of the environmental and genetic factors that guide bacterial adaptation to antibiotic treatment.

Tragedy of the commons in Melipona bees revisited.

Melipona stingless bees display a paradoxical overproduction of queens, which are later eliminated by nest-mate workers. Mechanistically, it was suggested that the monoterpenoid geraniol deposited into newly provisioned cells by adult bees would cause larvae to develop into queens in Melipona beecheii. This system could be evolutionarily stable if many of these new queens were to leave the nest and parasitize other genetically unrelated colonies nearby, as was shown to occur in a congeneric species. Here, we use microsatellite markers to test whether queen overproduction could be a strategy by which adult workers control the caste fate of the developing larvae to export copies of their own genes to the rest of the population via queen parasitism in M. beecheii. In addition, we re-examined whether artificially increasing the levels of geraniol indeed caused larvae to develop as queens rather than workers. Contrary to our prediction, we found no evidence for queen parasitism in M. beecheii and observed no effect of geraniol on the rearing of new queens. Together, these results support the original 'tragedy of the commons' hypothesis for queen overproduction in Melipona bees, where individual larvae selfishly bias their development towards the queen pathway according to their best evolutionary interests.

Similarities in Recognition Cues Lead to the Infiltration of Non-Nestmates in an Ant Species.

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.

Close-range cues used by males of Polistes dominula in sex discrimination.

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.

Identification of a queen pheromone mediating the rearing of adult sexuals in the pharaoh ant Monomorium pharaonis.

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.

Honeybees possess a structurally diverse and functionally redundant set of queen pheromones.

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.

The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp.

Despite the mitochondrion's long-recognized role in energy production, mitochondrial DNA (mtDNA) variation commonly found in natural populations was assumed to be effectively neutral. However, variation in mtDNA has now been increasingly linked to phenotypic variation in life history traits and fitness. We examined whether the relative fitness in native and invasive common wasp (Vespula vulgaris) populations in Belgium and New Zealand (NZ), respectively, can be linked to mtDNA variation. Social wasp colonies in NZ were smaller with comparatively fewer queen cells, indicating a reduced relative fitness in the invaded range. Interestingly, queen cells in this population were significantly larger leading to larger queen offspring. By sequencing 1,872 bp of the mitochondrial genome, we determined mitochondrial haplotypes and detected reduced genetic diversity in NZ. Three common haplotypes in NZ frequently produced many queens, whereas the four rare haplotypes produced significantly fewer or no queens. The entire mitochondrial genome for each of these haplotypes was sequenced to identify polymorphisms associated with fitness reduction. We found 16 variable sites; however, no nonsynonymous mutation that was clearly causing impaired mitochondrial function was detected. We discuss how detected variants may alter secondary structures, gene expression or mito-nuclear interactions, or could be associated with nuclear-encoded variation. Whatever the ultimate mechanism, we show reduced fitness and mtDNA variation in an invasive wasp population as well as specific mtDNA variants associated with fitness variation within this population. Ours is one of only a few studies that confirm fitness impacts of mtDNA variation in wild nonmodel populations.

Fifteen shades of green: The evolution of Bufotes toads revisited.

The radiation of Palearctic green toads (Bufotes) holds great potential to evaluate the role of hybridization in phylogeography at multiple stages along the speciation continuum. With fifteen species representing three ploidy levels, this model system is particularly attractive to examine the causes and consequences of allopolyploidization, a prevalent yet enigmatic pathway towards hybrid speciation. Despite substantial efforts, the evolutionary history of this species complex remains largely blurred by the lack of consistency among the corresponding literature. To get a fresh, comprehensive view on Bufotes phylogeography, here we combined genome-wide multilocus analyses (RAD-seq) with an extensive compilation of mitochondrial, genome size, niche modelling, distribution and phenotypic (bioacoustics, morphometrics, toxin composition) datasets, representing hundreds of populations throughout Eurasia. We provide a fully resolved nuclear phylogeny for Bufotes and highlight exceptional cyto-nuclear discordances characteristic of complete mtDNA replacement (in 20% of species), mitochondrial surfing during post-glacial expansions, and the formation of homoploid hybrid populations. Moreover, we traced the origin of several allopolyploids down to species level, showing that all were exclusively fathered by the West Himalayan B. latastii but mothered by several diploid forms inhabiting Central Asian lowlands, an asymmetry consistent with hypotheses on mate choice and Dobzhansky-Muller incompatibilities. Their intermediate call phenotypes potentially allowed for rapid reproductive isolation, while toxin compositions converged towards the ecologically-closest parent. Across the radiation, we pinpoint a stepwise progression of reproductive isolation through time, with a threshold below which hybridizability is irrespective of divergence (<6My), above which species barely admix and eventually evolve different mating calls (6-10My), or can successfully cross-breed through allopolyploidization (>15My). Finally, we clarified the taxonomy of Bufotes (including genetic analyses of type series) and formally described two new species, B. cypriensis sp. nov. (endemic to Cyprus) and B. perrini sp. nov. (endemic to Central Asia). Embracing the genomic age, our framework marks the advent of a new exciting era for evolutionary research in these iconic amphibians.

Analysis of Cuticular Lipids of the Pharaoh Ant (Monomorium pharaonis) and Their Selective Adsorption on Insecticidal Zeolite Powders.

The pharaoh ant is a notorious and hard to eradicate pest, which poses a threat in hospitals, spreading pathogens and contaminating sterile equipment. When applied on ants, zeolites adsorb part of their epicuticular wax layer. The ants are then vulnerable to desiccation, since this layer regulates water exchange. We analyzed the chemical composition of this wax layer using GC-MS (Gas Chromatography-Mass Spectrometry). A hexane wash of M. pharaonis foragers resulted in the identification of 53 components, four of which were not previously defined in Monomorium species. Selective adsorption of specific compounds on zeolites assisted in the identification of compounds which could not be separated on the GC column and allowed for the identification of three additional compounds. Zeolites show different affinities for the wax compounds depending on pore structure and chemical composition. Selective adsorption of alkanes on zeolites is also investigated in the fields of refinery processes and catalysis. Pore mouth and key lock adsorption mechanisms and selectivity according to molecular weight and branching, investigated in these fields, are also involved in adsorption processes of epicuticular waxes. The insecticidal activity of a zeolite is related to adsorption selectivity rather than capacity. One of the best adsorbing zeolites showed limited insecticidal activity and can be considered as a non-lethal alternative for epicuticular wax sampling.

Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival.

Several studies have suggested that covert stressors can contribute to bee colony declines. Here we provide a novel case study and show using radiofrequency identification tracking technology that covert deformed wing virus (DWV) infections in adult honeybee workers seriously impact long-term foraging and survival under natural foraging conditions. In particular, our experiments show that adult workers injected with low doses of DWV experienced increased mortality rates, that DWV caused workers to start foraging at a premature age, and that the virus reduced the workers' total activity span as foragers. Altogether, these results demonstrate that covert DWV infections have strongly deleterious effects on honeybee foraging and survival. These results are consistent with previous studies that suggested DWV to be an important contributor to the ongoing bee declines in Europe and the USA. Overall, our study underlines the strong impact that covert pathogen infections can have on individual and group-level performance in bees.

Arthropods Associate with their Red Wood ant Host without Matching Nestmate Recognition Cues.

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.

Diploid Male Production Results in Queen Death in the Stingless Bee Scaptotrigona depilis.

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.

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.

Genetic-genealogy approach reveals low rate of extrapair paternity in historical Dutch populations.

OBJECTIVE: Evolutionary theory has shown that seeking out extrapair paternity (EPP) can be a viable reproductive strategy for both sexes in pair-bonded species, also in humans. As yet, estimates of the contemporary or historical EPP rate in human population are still rare. In the present study, we estimated the historical EPP rate in the Dutch population over the last 400 years and compared the rate with those obtained for other human populations to determine the evolutionary, cultural, and socio-demographic factors that influence human cuckoldry behavior. METHODS: We estimated the historical EPP rate for the Dutch population via the "genealogical pair method", in which the EPP rate is derived from Y-chromosome mismatches between pairs of individuals that, based on genealogical evidence, share a common paternal ancestor. RESULTS: Based on the analysis of 68 representative genealogical pairs, separated by a total of 1013 fertilization events, we estimated that the historical EPP rate for the Dutch population over the last 400 years was 0.96% per generation (95% confidence interval 0.46%-1.76%). CONCLUSION: The Dutch EPP rate fits perfectly within the range reported for other contemporary and historical populations in Western Europe and was highly congruent with that estimated for neighboring Flanders, despite the socio-economic and religious differences between both populations. The estimated low EPP rate challenges the "dual mating strategy hypothesis" that states that women could obtain fitness benefits by securing investment from one man while cuckolding him to obtain good genes from an affair partner.

Fast and Reliable Quantitative Peptidomics with labelpepmatch.

The use of stable isotope tags in quantitative peptidomics offers many advantages, but the laborious identification of matching sets of labeled peptide peaks is still a major bottleneck. Here we present labelpepmatch, an R-package for fast and straightforward analysis of LC-MS spectra of labeled peptides. This open-source tool offers fast and accurate identification of peak pairs alongside an appropriate framework for statistical inference on quantitative peptidomics data, based on techniques from other -omics disciplines. A relevant case study on the desert locust Schistocerca gregaria proves our pipeline to be a reliable tool for quick but thorough explorative analyses.

Do well-integrated species of an inquiline community have a lower brood predation tendency? A test using red wood ant myrmecophiles.

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.

Biological activity of the enantiomers of 3-methylhentriacontane, a queen pheromone of the ant Lasius niger.

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.

Evolution of Self-Organized Task Specialization in Robot Swarms.

Division of labor is ubiquitous in biological systems, as evidenced by various forms of complex task specialization observed in both animal societies and multicellular organisms. Although clearly adaptive, the way in which division of labor first evolved remains enigmatic, as it requires the simultaneous co-occurrence of several complex traits to achieve the required degree of coordination. Recently, evolutionary swarm robotics has emerged as an excellent test bed to study the evolution of coordinated group-level behavior. Here we use this framework for the first time to study the evolutionary origin of behavioral task specialization among groups of identical robots. The scenario we study involves an advanced form of division of labor, common in insect societies and known as "task partitioning", whereby two sets of tasks have to be carried out in sequence by different individuals. Our results show that task partitioning is favored whenever the environment has features that, when exploited, reduce switching costs and increase the net efficiency of the group, and that an optimal mix of task specialists is achieved most readily when the behavioral repertoires aimed at carrying out the different subtasks are available as pre-adapted building blocks. Nevertheless, we also show for the first time that self-organized task specialization could be evolved entirely from scratch, starting only from basic, low-level behavioral primitives, using a nature-inspired evolutionary method known as Grammatical Evolution. Remarkably, division of labor was achieved merely by selecting on overall group performance, and without providing any prior information on how the global object retrieval task was best divided into smaller subtasks. We discuss the potential of our method for engineering adaptively behaving robot swarms and interpret our results in relation to the likely path that nature took to evolve complex sociality and task specialization.