Formic acid modulates latency and accuracy of nestmate recognition in carpenter ants

Decision-making processes face the dilemma of being accurate or faster, a phenomenon that has been described as speed-accuracy trade-off in numerous studies on animal behaviour. In social insects, discriminating between colony members and aliens is subjected to this trade-off as rapid and accurate rejection of enemies is of primary importance for the maintenance and ecological success of insect societies. Recognition cues distinguishing aliens from nestmates are embedded in the cuticular hydrocarbon (CHC) layer and vary among colonies. In walking carpenter ants, exposure to formic acid (FA), an alarm pheromone, improves accuracy of nestmate recognition by decreasing both alien acceptance and nestmate rejection. Here we studied the effect of FA exposure on the spontaneous aggressive mandible opening response of harnessed Camponotus aethiops ants presented with either nestmate or alien CHCs. FA modulated both MOR accuracy and the latency to respond to odours of conspecifics. In particular, FA decreased MOR towards nestmates but increased it towards aliens. Furthermore, FA decreased MOR latency towards aliens but not towards nestmates. As response latency can be used as a proxy of response speed, we conclude that contrary to the prediction of the speed-accuracy trade-off theory, ants did not trade off speed against accuracy in the process of nestmate recognition.

Social complexity, life-history and lineage influence the molecular basis of caste in a major transition in evolution

Major evolutionary transitions describe how biological complexity arises; e.g. in the evolution of complex multicellular bodies, and superorganismal insect societies. Such transitions involve the evolution of division of labour, e.g. as queen and worker castes in insect societies. A key mechanistic hypothesis for the evolution of division of labour is that a shared set of genes co-opted from a common solitary ancestral ground plan - a so-called genetic toolkit for sociality - regulate insect castes across different levels of social complexity. The vespid wasps represent an excellent system in which to test this. Here, using conventional and machine learning analyses of brain transcriptome data from nine species of vespid wasps, we find evidence of a shared genetic toolkit across species representing different levels of social complexity, with a large suite of genes classifying castes correctly across species. However, we also found evidence of additional fine-scale differences in predictive gene sets, functional enrichment and rates of gene evolution that were related to level of social complexity, but also life-history traits (e.g. mode of colony founding). Thus, there appear to be shifts in the gene networks regulating social behaviour and rates of gene evolution that are influenced by innovations in both social complexity and life-history. These results suggest that the concept of a shared genetic toolkit for sociality may be too simplistic to fully describe the process of the major transition to sociality, even within a single lineage. Diversity in lineage, social complexity and life-history traits must be taken into account in the quest to uncover the molecular bases of the major transition to sociality.

Strength surpasses relatedness–queen larva selection in honeybees

Nepotism was initially theoretically predicted and sometimes found to trigger the selection of specific larvae to be reared as queens in the honeybee Apis mellifera. Although the importance of selecting the next queen for a colony indicates that it should not occur at random, nepotism is increasingly considered unlikely in eusocial insect societies. Different prenatal maternal supplies of embryos have been found to impact fitness in many other species and therefore could be a possible trigger underlying the likelihood of being raised as a queen. We offered related or unrelated larvae from six colonies originating from eggs of different weights for emergency queen rearing in queenless units with worker bees from these six colonies. We showed that nurses did not significantly prefer related larvae during queen rearing, which confirms the theory that different relatedness-driven kin preferences within a colony cannot be converted into a colony-level decision. However, we found that larvae originating from heavier eggs were significantly preferred for queen breeding. Studies on other species have shown that superior maternal supply is important for later reproductive success. However, we did observe tendencies in the expected direction (e.g., queens that hatched from heavier eggs had both more ovarioles and a shorter preoviposition period). Nevertheless, our data do not allow for a significant conclusion that the selection of larvae from heavy eggs truly offers fitness advantages.

The role of epigenetics, particularly DNA methylation, in the evolution of caste in insect societies

Eusocial insects can be defined as those that live in colonies and have distinct queens and workers. For most species, queens and workers arise from a common genome, and so caste-specific developmental trajectories must arise from epigenetic processes. In this review, we examine the epigenetic mechanisms that may be involved in the regulation of caste dimorphism. Early work on honeybees suggested that DNA methylation plays a causal role in the divergent development of queen and worker castes. This view has now been challenged by studies that did not find consistent associations between methylation and caste in honeybees and other species. Evidence for the involvement of methylation in modulating behaviour of adult workers is also inconsistent. Thus, the functional significance of DNA methylation in social insects remains equivocal. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

Honeybee Queen mandibular pheromone induces starvation in Drosophila melanogaster, implying a role for nutrition signalling in the evolution of eusociality.

Eusocial insect societies are defined by the reproductive division of labour, a social structure that is generally enforced by the reproductive dominant or queen. Reproductive dominance is maintained through behavioural dominance in some species as well as production of queen pheromones in others, or a mixture of both. Queen mandibular pheromone (QMP) is produced by honeybee (Apis mellifera) queens and has been characterised chemically. How QMP acts to repress worker reproduction, and how it has evolved this activity, remains less well understood. Surprisingly, QMP is capable of repressing reproduction in non-target arthropods which have not co-evolved with QMP, are never exposed to QMP in nature, and are up to 530 million years diverged from the honeybee. Here we show that, in Drosophila melanogaster, QMP treatment mimics nutrient limiting conditions, leading to disrupted reproduction. Exposure to QMP induces an increase in food consumption, consistent with that observed in D. melanogaster in response to starvation conditions. This response induces the activation of two checkpoints within the ovary that inhibit oogenesis. The first is the 2a/b ovarian checkpoint in the germarium, which reduces the flow of presumptive oocytes. A stage 9 ovarian checkpoint is also activated, causing degradation of oocytes. The magnitude of activation of both checkpoints is indistinguishable between QMP treated and starved individuals. As QMP seems to trigger a starvation response in an insect highly diverged from honeybees, we propose that QMP originally evolved by co-opting nutrition signalling pathways to regulate reproduction, a key step in the evolution of eusociality.

Ants modulate stridulatory signals depending on the behavioural context

Insect societies require an effective communication system to coordinate members’ activities. Although eusocial species primarily use chemical communication to convey information to conspecifics, there is increasing evidence suggesting that vibroacoustic communication plays a significant role in the behavioural contexts of colony life. In this study, we sought to determine whether stridulation can convey information in ant societies. We tested three main hypotheses using the Mediterranean ant Crematogaster scutellaris: (i) stridulation informs about the emitter’caste; (ii) workers can modulate stridulation based on specific needs, such as communicating the profitability of a food resource, or (iii) behavioural contexts. We recorded the stridulations of individuals from the three castes, restrained on a substrate, and the signals emitted by foragers workers feeding on honey drops of various sizes. Signals emitted by workers and sexuates were quantitatively and qualitatively distinct as was stridulation emitted by workers on different honey drops. Comparing across the experimental setups, we demonstrated that signals emitted in different contexts (restraining vs feeding) differed in emission patterns as well as certain parameters (dominant frequency, amplitude, duration of chirp). Our findings suggest that vibrational signaling represents a flexible communication channel paralleling the well-known chemical communication system.

Body Size and Behavioural Plasticity Interact to Influence the Performance of Free-Foraging Bumble Bee Colonies

Specialisation and plasticity are important for many forms of collective behaviour, but the interplay between these factors is little understood. In insect societies, workers are often developmentally primed to specialise in different tasks, sometimes with morphological or physiological adaptations, facilitating a division of labour. Workers may also plastically switch between tasks or vary their effort. The degree to which developmentally primed specialisation limits plasticity is not clear and has not been systematically tested in ecologically relevant contexts. We addressed this question in 20 free-foraging bumble bee (Bombus terrestris) colonies by continually manipulating colonies to contain either a typically diverse, or a reduced (“homogeneous”), worker body size distribution while keeping the same mean body size, over two trials. Pooling both trials, diverse colonies produced a larger comb mass, an index of colony performance. The link between body size and task was further corroborated by the finding that foragers were larger than nurses even in homogeneous colonies with a very narrow body size range. However, the overall effect of size diversity stemmed mostly from one trial. In the other trial, homogeneous and diverse colonies showed comparable performance. By comparing behavioural profiles based on several thousand observations of individuals, we found evidence that workers in homogeneous colonies in this trial rescued colony performance by plastically increasing behavioural specialisation and/or individual effort, compared to same-sized individuals in diverse colonies. Our results are consistent with a benefit to colonies of large and small specialists under certain conditions, but also suggest that plasticity or effort can compensate for reduced (size-related) specialisation. Thus, we suggest that an intricate interplay between specialisation and plasticity is functionally adaptive in bumble bee colonies.

Dufour’s gland analysis reveals caste and physiology specific signals in Bombus impatiens

Reproductive division of labor in insect societies is regulated through multiple concurrent mechanisms, primarily chemical and behavioral. Here, we examined if the Dufour’s gland secretion in the primitively eusocial bumble bee Bombus impatiens signals information about caste, social condition, and reproductive status. We chemically analyzed Dufour’s gland contents across castes, age groups, social and reproductive conditions, and examined worker behavioral and antennal responses to gland extracts. We found that workers and queens each possess caste-specific compounds in their Dufour’s glands. Queens and gynes differed from workers based on the presence of diterpene compounds which were absent in workers, whereas four esters were exclusive to workers. These esters, as well as the total amounts of hydrocarbons in the gland, provided a separation between castes and also between fertile and sterile workers. Olfactometer bioassays demonstrated attraction of workers to Dufour’s gland extracts that did not represent a reproductive conflict, while electroantennogram recordings showed higher overall antennal sensitivity in queenless workers. Our results demonstrate that compounds in the Dufour’s gland act as caste- and physiology-specific signals and are used by workers to discriminate between workers of different social and reproductive status.

Genetic toolkit for sociality predicts castes across the spectrum of social complexity in wasps

Major evolutionary transitions describe how biological complexity arises; e.g. in evolution of complex multicellular bodies, and superorganismal insect societies. Such transitions involve the evolution of division of labour, e.g. as queen and worker castes in insect societies. Castes across different evolutionary lineages are thought to be regulated by a conserved genetic toolkit. However, this hypothesis has not been tested thoroughly across the complexity spectrum of the major transition. Here we reveal, using machine learning analyses of brain transcription, evidence of a shared genetic toolkit across the spectrum of social complexity in Vespid wasps. Whilst molecular processes underpinning the simpler societies (which likely represent the origins of social living) are conserved throughout the major transition, additional processes appear to come into play in more complex societies. Such fundamental shifts in regulatory processes with complexity may typify other major evolutionary transitions, such as the evolution of multicellularity.

Reproductive inhibition among nestmate queens in the invasive Argentine ant

In social species, the presence of several reproductive individuals can generate conflict. In social insects, as queen number increases, individual oviposition rate may decrease because of direct and indirect behavioural and/or chemical interactions. Understanding the factors that mediate differences in queen fecundity should provide insight into the regulation and maintenance of highly polygynous insect societies, such as those of the invasive Argentine ant (Linepithema humile). In this study, we investigated (1) whether differences in the oviposition rates of Argentine ant queens exposed to polygynous conditions could result from interactions among them; (2) whether such differences in fecundity stemmed from differences in worker attention; and (3) whether polygynous conditions affected the cuticular hydrocarbon profiles of queens (CHCs). We found that differences in queen fecundity and CHC profiles observed under polygynous conditions disappeared when queens were exposed to monogynous conditions, suggesting some form of reproductive inhibition may exist when queens cohabit. These differences did not seem to arise from variation in worker attention because more fecund queens were not more attractive to workers. Levels of some CHCs were higher in more fecund queens. These CHCs are associated with greater queen productivity and survival. Our findings indicate that such compounds could be multifunctional queen pheromones.