Patrizia d'Ettorre

Nestmate recognition in social insects and the role of hydrocarbons

One of the conditions favoring the evolution and maintenance of sociality is the ability to discriminate between kin and non-kin, because it allows altruistic acts to be directed to recipients of high relatedness (Hamilton, 1987). Nestmate recognition is the process whereby social insects recognize individuals belonging to their own colony or an alien colony, and accordingly allow or prohibit entry to their nest. Nestmate recognition often results in the discrimination of kin from non-kin, but in social insects there is a distinction to be made between nestmate and kin recognition. Where kin recognition is the assessment of the degree of relatedness towards another individual, nestmate recognition is the binary recognition of group membership (Arnold et al. , 1996; Lenoir et al. , 1999). In ants, wasps and termites, the blend of hydrocarbons present on the cuticle appears to comprise the essential compounds that serve as nestmate recognition cues (Howard and Blomquist, 2005), although in honeybees fatty acids and esters may also play an important role (Breed, 1998a; but see Dani et al. , 2005; Ch?ine et al. , 2005). At the end of the 1990s, the notion that cuticular hydrocarbons act as recognition cues was supported mainly by correlative evidence (Singer, 1998; Vander Meer and Morel, 1998; Lenoir et al. , 1999), but significant progress has been made over the last decade.

Conserved class of queen pheromones stops social insect workers from reproducing

Long Live the Queen Eusociality is often considered to have arisen, at least in part, due to the inclusive fitness that workers gain through helping their queen sister to raise her offspring. Van Oystaeyen et al. (p. 287; see the Perspective by Chapuisat) characterized the sterility-inducing queen pheromone across three distantly related eusocial hymenopterans (a wasp, a bumblebee, and a desert ant) and synthesized data across 69 other species. Queen pheromones appear to be remarkably conserved, which suggests that reproductive manipulation has ancient roots. Social insect queens use an ancient, evolutionarily conserved class of pheromones to prevent worker reproduction. [Also see Perspective by Chapuisat] A major evolutionary transition to eusociality with reproductive division of labor between queens and workers has arisen independently at least 10 times in the ants, bees, and wasps. Pheromones produced by queens are thought to play a key role in regulating this complex social system, but their evolutionary history remains unknown. Here, we identify the first sterility-inducing queen pheromones in a wasp, bumblebee, and desert ant and synthesize existing data on compounds that characterize female fecundity in 64 species of social insects. Our results show that queen pheromones are strikingly conserved across at least three independent origins of eusociality, with wasps, ants, and some bees all appearing to use nonvolatile, saturated hydrocarbons to advertise fecundity and/or suppress worker reproduction. These results suggest that queen pheromones evolved from conserved signals of solitary ancestors.

Ants recognize foes and not friends

Discriminating among individuals and rejecting non-group members is essential for the evolution and stability of animal societies. Ants are good models for studying recognition mechanisms, because they are typically very efficient in discriminating ‘friends’ (nest-mates) from ‘foes’ (non-nest-mates). Recognition in ants involves multicomponent cues encoded in cuticular hydrocarbon profiles. Here, we tested whether workers of the carpenter ant Camponotus herculeanus use the presence and/or absence of cuticular hydrocarbons to discriminate between nest-mates and non-nest-mates. We supplemented the cuticular profile with synthetic hydrocarbons mixed to liquid food and then assessed behavioural responses using two different bioassays. Our results show that (i) the presence, but not the absence, of an additional hydrocarbon elicited aggression and that (ii) among the three classes of hydrocarbons tested (unbranched, mono-methylated and dimethylated alkanes; for mono-methylated alkanes, we present a new synthetic pathway), only the dimethylated alkane was effective in eliciting aggression. Our results suggest that carpenter ants use a fundamentally different mechanism for nest-mate recognition than previously thought. They do not specifically recognize nest-mates, but rather recognize and reject non-nest-mates bearing odour cues that are novel to their own colony cuticular hydrocarbon profile. This begs for a reappraisal of the mechanisms underlying recognition systems in social insects.

Identification of an ant queen pheromone regulating worker sterility

The selective forces that shape and maintain eusocial societies are an enduring puzzle in evolutionary biology. Ordinarily sterile workers can usually reproduce given the right conditions, so the factors regulating reproductive division of labour may provide insight into why eusociality has persisted over evolutionary time. Queen-produced pheromones that affect worker reproduction have been implicated in diverse taxa, including ants, termites, wasps and possibly mole rats, but to date have only been definitively identified in the honeybee. Using the black garden ant Lasius niger, we isolate the first sterility-regulating ant queen pheromone. The pheromone is a cuticular hydrocarbon that comprises the majority of the chemical profile of queens and their eggs, and also affects worker behaviour, by reducing aggression towards objects bearing the pheromone. We further show that the pheromone elicits a strong response in worker antennae and that its production by queens is selectively reduced following an immune challenge. These results suggest that the pheromone has a central role in colony organization and support the hypothesis that worker sterility represents altruistic self-restraint in response to an honest quality signal.

Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa

SUMMARY Primitive ant societies, with their relatively simple social structure, provide an opportunity to explore the evolution of chemical communication, in particular of mechanisms underlying within-colony discrimination. In the same colony, slight differences in individual odours can be the basis for discrimination between different castes, classes of age and social status. There is some evidence from correlative studies that such inter-individual variation is associated with differences in reproductive status, but direct proof that certain chemical compounds are detected and recognized by ants is still lacking. In the ponerine ant Pachycondyla inversa, fertile queens and, in orphaned colonies, dominant egg-laying workers are characterized by the predominance of a branched hydrocarbon, 3,11-dimethylheptacosane (3,11-diMeC27) on the cuticle. Using electroanntennography and gas chromatography with electroantennographic detection, we show that the antennae of P. inversa workers react to this key compound. 3,11-diMeC27 is correlated with ovarian activity and, because it is detected, is likely to assume the role of a fertility signal reflecting the quality of the sender.

Individual Recognition in Ant Queens

Personal relationships are the cornerstone of vertebrate societies, but insect societies are either too large for individual recognition, or their members were assumed to lack the necessary cognitive abilities . This paradigm has been challenged by the recent discovery that paper wasps recognize each others unique facial color patterns . Individual recognition is advantageous when dominance hierarchies control the partitioning of work and reproduction . Here, we show that unrelated founding queens of the ant Pachycondyla villosa use chemical cues to recognize each other individually. Aggression was significantly lower in pairs of queens that had previously interacted than in pairs with similar social history but no experience with one another. Moreover, subordinates discriminated familiar and unfamiliar dominants in choice experiments in which physical contact, but not odor perception, was prevented and in tests with anaesthetized queens. The cuticular chemical profiles of queens were neither associated with dominance nor fertility and, therefore, do not represent status badges , and nestmate queens did not share a common odor. Personal recognition facilitates the maintenance of stable dominance hierarchies in these small societies. This suggests that the ability to discriminate between individual traits is selected for when it incurs net benefits for the resolution of conflict.

Worker policing by egg eating in the ponerine ant Pachycondyla inversa

We investigated worker policing by egg eating in the ponerine ant Pachycondyla inversa, a species with morphologically distinct queens and workers. Colonies were split into one half with the queen and one half without. Workers in queenless colony fragments started laying unfertilized male eggs after three weeks. Worker–laid eggs and queen–laid eggs were introduced into five other queenright colonies with a single queen and three colonies with multiple queens, and their fate was observed for 30 min. Significantly more worker–laid eggs (range of 35–62%, mean of 46%) than queen–laid eggs (range of 5–31%, mean of 15%) were eaten by workers in single–queen colonies, and the same trend was seen in multiple–queen colonies. This seems to be the first well–documented study of ants with a distinct caste polymorphism to show that workers kill worker–laid eggs in preference to queen–laid eggs. Chemical analyses showed that the surfaces of queen–laid and worker–laid eggs have different chemical profiles as a result of different relative proportions of several hydrocarbons. Such differences might provide the information necessary for differential treatment of eggs. One particular alkane, 3,11–dimeC27, was significantly more abundant on the surfaces of queen–laid eggs. This substance is also the most abundant compound on the cuticles of egg layers.

The Evolution of Invasiveness in Garden Ants

It is unclear why some species become successful invaders whilst others fail, and whether invasive success depends on pre-adaptations already present in the native range or on characters evolving de-novo after introduction. Ants are among the worst invasive pests, with Lasius neglectus and its rapid spread through Europe and Asia as the most recent example of a pest ant that may become a global problem. Here, we present the first integrated study on behavior, morphology, population genetics, chemical recognition and parasite load of L. neglectus and its non-invasive sister species L. turcicus. We find that L. neglectus expresses the same supercolonial syndrome as other invasive ants, a social system that is characterized by mating without dispersal and large networks of cooperating nests rather than smaller mutually hostile colonies. We conclude that the invasive success of L. neglectus relies on a combination of parasite-release following introduction and pre-adaptations in mating system, body-size, queen number and recognition efficiency that evolved long before introduction. Our results challenge the notion that supercolonial organization is an inevitable consequence of low genetic variation for chemical recognition cues in small invasive founder populations. We infer that low variation and limited volatility in cuticular hydrocarbon profiles already existed in the native range in combination with low dispersal and a highly viscous population structure. Human transport to relatively disturbed urban areas thus became the decisive factor to induce parasite release, a well established general promoter of invasiveness in non-social animals and plants, but understudied in invasive social insects.

Honest and dishonest communication in social Hymenoptera

SUMMARY Communication in social insects usually serves the good of the whole society and thus increases the inclusive fitness of all individuals. Hence, cheating and dishonesty are not expected when nestmates are to be alarmed or recruited to food sources. However, kin selection predicts a conflict of interest among individuals about the partitioning of reproduction. Dishonest communication may then be advantageous. Workers usually do not lay eggs in the presence of a fertile queen, but in many species they do so when the queen is removed. This effect has been explained by manipulative, i.e. dishonest, queen control or honest fertility signalling. Numerous studies have documented qualitative and quantitative differences in the pheromone blends of reproductives and non-reproductives. We examine these data for signs of honest signalling, conflict and manipulation.

Wax combs mediate nestmate recognition by guard honeybees

Research has shown that the wax combs are important in the acquisition of colony odour in the honeybee, Apis mellifera. However, many of these studies were conducted in the laboratory or under artificial conditions. We investigated the role of the wax combs in nestmate recognition in the natural context of bees at colony entrances. Wax combs constructed by each experimental colony were swapped between hives and the acceptance of nestmate and non-nestmate forager workers was recorded before and after the swap, and in relation to a control hive not involved in the swap. We conducted the experiment twice, in consecutive years with three different colonies each time. Colonies that exchanged combs became more accepting of each others workers than of workers from the third colony. The overall acceptance of comb swap non-nestmates increased significantly from 3% before the swap to 23% after the swap in the first year, and from 8 to 47% in the second year. This effect wore off within 3 weeks. Chemical analyses showed that the cuticular profile of non-nestmates involved in the experimental comb swap became more similar to each other after the swap, and that acceptance by guards of bees from different hives was negatively correlated with chemical distance between the hydrocarbon profiles of the workers from different hives.