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.

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.

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.

Toward greater realism in inclusive fitness models: the case of caste fate conflict in insect societies.

In the field of social evolution, inclusive fitness theory has been successful in making a wide range of qualitative predictions on expected patterns of cooperation and conflict. Nevertheless, outside of sex ratio theory, inclusive fitness models that make accurate quantitative predictions remain relatively rare. Past models dealing with caste fate conflict in insect societies, for example, successfully predicted that if female larvae can control their own caste fate, an excess should opt to selfishly develop as queens. Available models, however, were unable to accurately predict levels of queen production observed in Melipona bees-a genus of stingless bees where caste is self-determined-as empirically observed levels of queen production are approximately two times lower than the theoretically predicted ones. Here, we show that this discrepancy can be resolved by explicitly deriving the colony-level cost of queen overproduction from a dynamic model of colony growth, requiring the incorporation of parameters of colony growth and demography, such as the per-capita rate at which new brood cells are built and provisioned, the percentage of the queen's eggs that are female, costs linked with worker reproduction and worker mortality. Our revised model predicts queen overproduction to more severely impact colony productivity, resulting in an evolutionarily stable strategy that is approximately half that of the original model, and is shown to accurately predict actual levels of queen overproduction observed in different Melipona species. Altogether, this shows how inclusive fitness models can provide accurate quantitative predictions, provided that costs and benefits are modeled in sufficient detail and are measured precisely.

The inheritance of alternative nest architectural traditions in stingless bees.

The transmission of complex behavior and culture in humans has long been attributed to advanced forms of social learning,1,2 which play a crucial role in our technological advancement.3 While similar phenomena of behavioral traditions and cultural inheritance have been observed in animals,1,2,4,5,6 including in primates,7 whales,8 birds,9 and even insects,10 the underlying mechanisms enabling the persistence of such animal traditions, particularly in insects, are less well understood. This study introduces pioneering evidence of enduring architectural traditions in the stingless bee Scaptotrigona depilis, which are maintained without any evidence for social learning. We demonstrate that S. depilis exhibits two distinct nest architectures, comprising either helicoidal or flat, stacked horizontal combs, which are transmitted across generations through stigmergy11,12,13,14,15,16,17-an environmental feedback mechanism whereby the presence of the existing comb structures guides subsequent construction behaviors-thereby leading to a form of environmental inheritance.18,19,20 Cross-fostering experiments further show that genetic factors or prior experience does not drive the observed variation in nest architecture. Moreover, the experimental introduction of corkscrew dislocations within the combs prompted helicoidal building, confirming the use of stigmergic building rules. At a theoretical level, we establish that the long-term equilibrium of building in the helicoidal pattern fits with the expectations of a two-state Markov chain model. Overall, our findings provide compelling evidence for the persistence of behavioral traditions in an insect, based on a simple mechanism of environmental inheritance and stigmergic interactions, without requiring any sophisticated learning mechanism, thereby expanding our understanding of how traditions can be maintained in non-human species.

Evolution of self-organised division of labour driven by stigmergy in leaf-cutter ants.

Social insects owe their widespread success to their ability to efficiently coordinate behaviour to carry out complex tasks. Several leaf-cutter ant species employ an advanced type of division of labour known as task partitioning, where the task of retrieving leaves is distributed between workers that cut and drop and those that collect the fallen leaves. It is not entirely clear how such highly coordinated behaviour can evolve, as it would seem to require the simultaneous mutations of multiple traits during the same generation. Here, we use an agent-based simulation model to show how task partitioning in leaf-cutter ants can gradually evolve by exploiting stigmergy (indirect coordination through the environment) through gravity (leaves falling from the treetop on the ground forming a cache). Our simple model allows independent variation in two core behavioural dimensions: the tendency to drop leaves and the tendency to pick up dropped leaves. Task partitioning readily evolves even under these minimal assumptions through adaptation to an arboreal environment where traveling up and down the tree is costly. Additionally, we analyse ant movement dynamics to demonstrate how the ants achieve efficient task allocation through task switching and negative feedback control.

Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp.

In insect societies, both queens and workers produce chemicals that reliably signal caste membership and reproductive status. The mechanisms that help to maintain the honesty of such queen and fertility signals, however, remain poorly studied. Here we test if queen signal honesty could be based on the shared endocrine control of queen fertility and the production of specific signals. In support of this "hormonal pleiotropy" hypothesis, we find that in the common wasp, application of methoprene (a juveline hormone analogue) caused workers to acquire a queen-like cuticular hydrocarbon profile, resulting in the overproduction of known queen pheromones as well as some compounds typically linked to worker fertility. By contrast, administration of precocene-I (a JH inhibitor) had a tendency to have the opposite effect. Furthermore, a clear gonadotropic effect of JH in queens was suggested by the fact that circulating levels of JH were ca. 2 orders of magnitude higher in queens than those in workers and virgin, non-egg-laying queens, even if methoprene or precocene treatment did not affect the ovary development of workers. Overall, these results suggest that queen signal honesty in this system is maintained by queen fertility and queen signal production being under shared endocrine control.

Conserved class of queen pheromones stops social insect workers from reproducing.

A major evolutionary transition to eusociality with reproductive division of labor between queens and workers has arisen independently at least 10 times in the ants, bees, and wasps. Pheromones produced by queens are thought to play a key role in regulating this complex social system, but their evolutionary history remains unknown. Here, we identify the first sterility-inducing queen pheromones in a wasp, bumblebee, and desert ant and synthesize existing data on compounds that characterize female fecundity in 64 species of social insects. Our results show that queen pheromones are strikingly conserved across at least three independent origins of eusociality, with wasps, ants, and some bees all appearing to use nonvolatile, saturated hydrocarbons to advertise fecundity and/or suppress worker reproduction. These results suggest that queen pheromones evolved from conserved signals of solitary ancestors.