Patrizia d’Ettorre

Disentangling environmental and heritable nestmate recognition cues in a carpenter ant.

Discriminating between group members and strangers is a key feature of social life. Nestmate recognition is very effective in social insects and is manifested by aggression and rejection of alien individuals, which are prohibited to enter the nest. Nestmate recognition is based on the quantitative variation in cuticular hydrocarbons, which can include heritable cues from the workers, as well as acquired cues from the environment or queen-derived cues. We tracked the profile of six colonies of the ant Camponotus aethiops for a year under homogeneous laboratory conditions. We performed chemical and behavioral analyses. We show that nestmate recognition was not impaired by constant environment, even though cuticular hydrocarbon profiles changed over time and were slightly converging among colonies. Linear hydrocarbons increased over time, especially in queenless colonies, but appeared to have weak diagnostic power between colonies. The presence of a queen had little influence on nestmate discrimination abilities. Our results suggest that heritable cues of workers are the dominant factor influencing nestmate discrimination in these carpenter ants and highlight the importance of colony kin structure for the evolution of eusociality.

Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism.

The evolution of sociality is facilitated by the recognition of close kin, but if kin recognition is too accurate, nepotistic behaviour within societies can dissolve social cohesion. In social insects, cuticular hydrocarbons act as nestmate recognition cues and are usually mixed among colony members to create a Gestalt odour. Although earlier studies have established that hydrocarbon profiles are influenced by heritable factors, transfer among nestmates and additional environmental factors, no studies have quantified these relative contributions for separate compounds. Here, we use the ant Formica rufibarbis in a cross‐fostering design to test the degree to which hydrocarbons are heritably synthesized by young workers and transferred by their foster workers. Bioassays show that nestmate recognition has a significant heritable component. Multivariate quantitative analyses based on 38 hydrocarbons reveal that a subset of branched alkanes are heritably synthesized, but that these are also extensively transferred among nestmates. In contrast, especially linear alkanes are less heritable and little transferred; these are therefore unlikely to act as cues that allow within‐colony nepotistic discrimination or as nestmate recognition cues. These results indicate that heritable compounds are suitable for establishing a genetic Gestalt for efficient nestmate recognition, but that recognition cues within colonies are insufficiently distinct to allow nepotistic kin discrimination.

Sick ants become unsociable.

Parasites represent a severe threat to social insects, which form high‐density colonies of related individuals, and selection should favour host traits that reduce infection risk. Here, using a carpenter ant (Camponotus aethiops) and a generalist insect pathogenic fungus (Metarhizium brunneum), we show that infected ants radically change their behaviour over time to reduce the risk of colony infection. Infected individuals (i) performed less social interactions than their uninfected counterparts, (ii) did not interact with brood anymore and (iii) spent most of their time outside the nest from day 3 post‐infection until death. Furthermore, infected ants displayed an increased aggressiveness towards non‐nestmates. Finally, infected ants did not alter their cuticular chemical profile, suggesting that infected individuals do not signal their physiological status to nestmates. Our results provide evidence for the evolution of unsociability following pathogen infection in a social animal and suggest an important role of inclusive fitness in driving such evolution.

Fertility signaling—the proximate mechanism of worker policing in a clonal ant

In eusocial insects, the ability to regulate reproduction relies on cues that signal the presence of fertile individuals. We investigated the variation of cuticular hydrocarbons (CHCs) with reproductive status in Platythyrea punctata, an ant, in which all workers are capable of producing daughters from unfertilized eggs (thelytoky). Who reproduces is determined through dominance and worker policing. New reproductives, which developed their ovaries after separation from an old reproductive for a short period of time, were attacked by nonreproductives upon reintroduction into their colony. In contrast, aggression against new reproductives with fully developed ovaries, which had been separated over a longer period, was initiated by fights between old and new reproductives. CHC profiles varied with ovarian development. New reproductives were only attacked when they expressed a CHC profile similar to old reproductives, but not when it was similar to that of nonreproductives. CHCs appear to signal the fertility of individuals and induce policing behavior towards surplus reproductive workers.

Learning and perceptual similarity among cuticular hydrocarbons in ants

Nestmate recognition in ants is based on perceived differences in a multi-component blend of hydrocarbons that are present on the insect cuticle. Although supplementation experiments have shown that some classes of hydrocarbons, such as methyl branched alkanes and alkenes, have a salient role in nestmate recognition, there was basically no information available on how ants detect and perceive these molecules. We used a new conditioning procedure to investigate whether individual carpenter ants could associate a given hydrocarbon (linear or methyl-branched alkane) to sugar reward. We then studied perceptual similarity between a hydrocarbon previously associated with sugar and a novel hydrocarbon. Ants learnt all hydrocarbon-reward associations rapidly and with the same efficiency, regardless of the structure of the molecules. Ants could discriminate among a large number of pairs of hydrocarbons, but also generalised. Generalisation depended both on the structure of the molecule and the animals experience. For linear alkanes, generalisation was observed when the novel molecule was smaller than the conditioned one. Generalisation between pairs of methyl-alkanes was high, while generalisation between hydrocarbons that differed in the presence or absence of a methyl group was low, suggesting that chain length and functional group might be coded independently by the ant olfactory system. Understanding variations in perception of recognition cues in ants is necessary for the general understanding of the mechanisms involved in social recognition processes based on chemical cues.

Significance of chemical recognition cues is context dependent in ants.

Recognition of group members is of fundamental importance in social animals, allowing individuals to protect resources against intruders and parasites, as well as ensuring social cohesion within the group. In ants and other social insects, social recognition relies on multicomponent chemical signatures, composed primarily of long-chain cuticular hydrocarbons. These signatures are colony specific and allow discrimination between nestmates and non-nestmates. Nevertheless, the mechanisms underlying detection, perception and information processing of chemical signatures are poorly understood. It has been suggested that associative learning might play a role in nestmate recognition. We investigated whether Camponotus aethiops ants can associate a complete cuticular hydrocarbon profile, consisting of about 40 compounds, with a food reward and whether the new association, developed in an appetitive context, affects aggression against non-nestmates carrying the hydrocarbon profile associated with food. Individual ant workers were able to associate the non-nestmate chemical profile with food. However, conditioned ants were still aggressive when encountering a non-nestmate carrying the odour profile used as training odour in our experiments. This suggests that ants, like some, but not all other insects, show interactions between different modalities (i.e. olfactory and visual), and can treat complex chemical cues differently, according to the context in which they are perceived. This plasticity ensures that learning in an appetitive context does not interfere with the crucial task of colony defence.

Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp

Inclusive fitness theory predicts that in colonies of social Hymenoptera headed by a multiple‐mated queen, workers should benefit from policing eggs laid by other workers. Foster & Ratnieks provided evidence that in the vespine wasp Dolichovespula saxonica, workers police other workers’ eggs only in colonies headed by a multiple‐mated queen, but not in those headed by a single‐mated one. This conclusion, however, was based on a relatively small sample size, and the original study did not control for possible confounding variables such as the seasonal colony progression of the nests. Our aim, therefore, was to reinvestigate whether or not facultative worker policing occurs in D. saxonica. Remarkably, our data show that in the studied Danish population, there was no correlation between worker–worker relatedness and the percentage of worker‐derived males. In addition, we show that variability in cuticular hydrocarbon profiles among the workers did not significantly correlate with relatedness and that workers therefore probably did not have sufficient information on queen mating frequency from the workers’ cuticular hydrocarbon profiles. Hence, there was no evidence that workers facultatively policed other workers’ eggs in response to queen mating frequency. Nevertheless, our data do show that the seasonal progression of the nest and the location in which the males were reared both explain the patterns of worker reproduction found. Overall, our results suggest that the earlier evidence for facultative worker policing in D. saxonica may have been caused by accidental correlations with certain confounding variables, or, alternatively, that there are large interpopulation differences in the expression of worker policing.

Crozier’s paradox revisited: maintenance of genetic recognition systems by disassortative mating

BackgroundOrganisms are predicted to behave more favourably towards relatives, and kin-biased cooperation has been found in all domains of life from bacteria to vertebrates. Cooperation based on genetic recognition cues is paradoxical because it disproportionately benefits individuals with common phenotypes, which should erode the required cue polymorphism. Theoretical models suggest that many recognition loci likely have some secondary function that is subject to diversifying selection, keeping them variable.ResultsHere, we use individual-based simulations to investigate the hypothesis that the dual use of recognition cues to facilitate social behaviour and disassortative mating (e.g. for inbreeding avoidance) can maintain cue diversity over evolutionary time. Our model shows that when organisms mate disassortatively with respect to their recognition cues, cooperation and recognition locus diversity can persist at high values, especially when outcrossed matings produce more surviving offspring. Mating system affects cue diversity via at least four distinct mechanisms, and its effects interact with other parameters such as population structure. Also, the attrition of cue diversity is less rapid when cooperation does not require an exact cue match. Using a literature review, we show that there is abundant empirical evidence that heritable recognition cues are simultaneously used in social and sexual behaviour.ConclusionsOur models show that mate choice is one possible resolution of the paradox of genetic kin recognition, and the literature review suggests that genetic recognition cues simultaneously inform assortative cooperation and disassortative mating in a large range of taxa. However, direct evidence is scant and there is substantial scope for future work.

Social context predicts recognition systems in ant queens.

Recognition of group‐members is a key feature of sociality. Ants use chemical communication to discriminate nestmates from intruders, enhancing kin cooperation and preventing parasitism. The recognition code is embedded in their cuticular chemical profile, which typically varies between colonies. We predicted that ants might be capable of accurate recognition in unusual situations when few individuals interact repeatedly, as new colonies started by two to three queens. Individual recognition would be favoured by selection when queens establish dominance hierarchies, because repeated fights for dominance are costly; but it would not evolve in absence of hierarchies. We previously showed that Pachycondyla co‐founding queens, which form dominance hierarchies, have accurate individual recognition based on chemical cues. Here, we used the ant Lasius niger to test the null hypothesis that individual recognition does not occur when co‐founding queens do not establish dominance hierarchies. Indeed, L. niger queens show a similar level of aggression towards both co‐foundresses and intruders, indicating that they are unable of individual recognition, contrary to Pachycondyla. Additionally, the variation in chemical profiles of Lasius and Pachycondyla queens is comparable, thus informational constraints are unlikely to apply. We conclude that selection pressure from the social context is of crucial significance for the sophistication of recognition systems.

Knowing your enemies: seasonal dynamics of host–social parasite recognition

Despite its evolutionary significance, behavioural flexibility of social response has rarely been investigated in insects. We studied a host–social parasite system: the slave-making ant Polyergus rufescens and its host Formica rufibarbis. Free-living host workers from parasitized and from unparasitized areas were compared in their level of aggression against the parasite and alien conspecifics. We expected that a seasonal change would occur in the acceptance threshold of F. rufibarbis workers from a parasitized area towards the parasite, whereas F. rufibarbis workers from an unparasitized area would not show substantial changes connected with the parasite’s peak in activity (raiding and colony-founding season). The results showed a significant adaptive behavioural flexibility of host species workers and are consistent with the acceptance threshold model’s (Reeve 1989) prediction that recognition systems are not fixed but context-dependent. In particular, host workers from the unparasitized area were highly aggressive towards the parasite regardless of the season, whereas host workers from the parasitized area significantly increased their aggression towards the parasite during its raiding and colony-founding season. Being able to detect and possibly kill a Polyergus scout searching for host nests can be an effective strategy for a Formica colony to avoid being raided or usurped by a parasite queen.