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.     

Individual recognition is associated with holistic face processing in Polistes paper wasps in a species-specific way

Most recognition is based on identifying features, but specialization for face recognition in primates relies on a different mechanism, termed ‘holistic processing’ where facial features are bound together into a gestalt which is more than the sum of its parts. Here, we test whether individual face recognition in paper wasps also involved holistic processing using a modification of the classic part-whole test in two related paper wasp species: Polistes fuscatus, which use facial patterns to individually identify conspecifics, and Polistes dominula, which lacks individual recognition. We show that P. fuscatus use holistic processing to discriminate between P. fuscatus face images but not P. dominula face images. By contrast, P. dominula do not rely on holistic processing to discriminate between conspecific or heterospecific face images. Therefore, P. fuscatus wasps have evolved holistic face processing, but this ability is highly specific and shaped by species-specific and stimulus-specific selective pressures. Convergence towards holistic face processing in distant taxa (primates, wasps) as well as divergence among closely related taxa with different recognition behaviour (P. dominula, P. fuscatus) suggests that holistic processing may be a universal adaptive strategy to facilitate expertise in face recognition.     

Nestmate recognition and identification of cuticular hydrocarbons composition in the swarm founding paper wasp Ropalidia opifex

Eusocial polistine wasps comprise species in which new colonies are founded by single wasps or groups of foundresses (independent founding species) or by swarms of queens and workers (swarm founding species). The first ones have relatively small societies generally comprising only one egg-laying queen, while the second ones have larger colonies where several egg-laying queens are usually present. These differences in social organisation are expected to influence the acceptance threshold of conspecifics in the colony and the intra-colony communication modalities. In this paper, we showed by field experiments that Ropalidia opifex (a swarm founding species) presents a good discrimination between alien and nestmate conspecifics. Moreover by GC/MS, we identified 19 cuticular hydrocarbons in this species, and we demonstrated that cuticular signature in this species depends mainly on colony membership, not showing any correlation with fertility.     

Social learning of predators in the dark: understanding the role of visual,chemical and mechanical information

The ability of prey to observe and learn to recognize potential predators from the behaviour of nearby individuals can dramatically increase survival and, not surprisingly, is widespread across animal taxa. A range of sensory modalities are available for this learning, with visual and chemical cues being well-established modes of transmission in aquatic systems. The use of other sensory cues in mediating social learning in fishes, including mechano-sensory cues, remains unexplored. Here, we examine the role of different sensory cues in social learning of predator recognition, using juvenile damselfish (Amphiprion percula). Specifically, we show that a predator-naive observer can socially learn to recognize a novel predator when paired with a predator-experienced conspecific in total darkness. Furthermore, this study demonstrates that when threatened, individuals release chemical cues (known as disturbance cues) into the water. These cues induce an anti-predator response in nearby individuals; however, they do not facilitate learnt recognition of the predator. As such, another sensory modality, probably mechano-sensory in origin, is responsible for information transfer in the dark. This study highlights the diversity of sensory cues used by coral reef fishes in a social learning context.     

The Rules of Aggression: How Genetic,Chemical and Spatial Factors Affect Intercolony Fights in a Dominant Species,the Mediterranean Acrobat Ant Crematogaster scutellaris

Nest-mate recognition plays a key role in the biology of ants. Although individuals coming from a foreign nest are, in most cases, promptly rejected, the degree of aggressiveness towards non nest-mates may be highly variable among species and relies on genetic, chemical and environmental factors. We analyzed intraspecific relationships among neighboring colonies of the dominant Mediterranean acrobat ant Crematogaster scutellaris integrating genetic, chemical and behavioral analyses. Colony structure, parental relationships between nests, cuticular hydrocarbons profiles (CHCs) and aggressive behavior against non nest-mates were studied in 34 nests located in olive tree trunks. Bayesian clustering analysis of allelic variation at nine species-specific microsatellite DNA markers pooled nests into 14 distinct clusters, each representing a single colony, confirming a polydomous arrangement of nests in this species. A marked genetic separation among colonies was also detected, probably due to long distance dispersion of queens and males during nuptial flights. CHCs profiles varied significantly among colonies and between nests of the same colony. No relationship between CHCs profiles and genetic distances was detected. The level of aggressiveness between colonies was inversely related to chemical and spatial distance, suggesting a ‘nasty neighbor’ effect. Our findings also suggest that CHCs profiles in C. scutellaris may be linked to external environmental factors rather than genetic relationships.     

Mate recognition systems in a species flock of Mexican pupfish

The pupfishes of Lake Chichancanab (Mexico) provide a unique opportunity to study the evolution of premating reproductive barriers. This group of endemic species is of recent origin and the lineages differ in morphological traits indicating trophic specialization, but show very little genetic change. We studied the function of visual and chemical cues in the mate recognition system of three morphospecies, Cyprinodon beltrani, C. labiosus and C. maya. Only in C. maya, which is genetically the most distinct member of the group, do females show the ability to identify males of their own type, both visually and chemically. C. labiosus females discriminated between their own and C. beltrani males based on chemical but not visual cues. C. beltrani, which is morphologically the least differentiated member of the group, showed no interspecific mate recognition. Females responded more strongly to the visual and chemical cues of their own males than to their own females, but they did not discriminate between their own males and those of the other two morphospecies based upon either type of cue. These results suggest that different levels of behavioural isolation have been established: most isolated is C. maya, and the least is C. beltrani. C. labiosus has an intermediate position. The results also suggest that species recognition cues based on different sensory modalities do not necessarily evolve together, and may evolve at different rates.     

Pupal experience and nestmate recognition in <Emphasis Type="Italic">Polistes dominula</Emphasis> wasps

Social insects can discriminate between nestmates and aliens by comparing the chemical phenotype of an individual with the neural representation of their own colony odor (template). For social paper wasps of the genus Polistes, a general recognition model has been proposed and tested on few North American species: wasps learn colonial recognition cues from the nest paper during the first hours after emergence as adults. However, a recent study revealed that workers of Polistes dominula do not necessarily use the nest paper for early post-emergence cue-learning, suggesting that cues used for the formation of the referent template in this species could be learned at different life stages. Pre-natal learning is a widespread phenomenon in animals and it can shape various behaviors in adults. Here, we investigated whether pre-imaginal learning affects later nestmate recognition in P. dominula wasps. We reared worker pupae in artificial conditions to test whether the absence of nest material, or the exposure to nest material taken from a foreign conspecific colony, during pupal development would alter the nestmate recognition ability in adult life. Our results show that wasps maintain their correct recognition ability regardless of the treatment, suggesting that wasps do not form their referent template during the pupal stage from the nest paper. Alternative hypotheses for template formation timing and source of recognition cues are discussed. Moreover, we investigated whether young wasps already possess, on their own body, reliable chemical cues to form a recognition template by self-referent phenotype matching.     

Nestmate recognition in Parischnogaster striatula (Hymenoptera Stenogastrinae), visual and olfactory recognition cues

The recognition of nestmates from alien individuals is a well known phenomenon in social insects. In the stenogastrine wasp Parischnogaster striatula, we investigated the ability of females to recognize nestmates and the cues on which such recognition is based. Recognition of nestmates was observed in naturally occurring interactions between wasps approaching a nest and the resident females on that nest. This recognition was confirmed in experiments in which nestmates or alien conspecifics were presented to resident females. In naturally occurring interactions, nestmates generally approach their nest with a direct flight, while aliens usually hover in front of the nest before landing. In experiments in which the presented wasps were placed close to the nest in a direct manner, antennation of the presented wasp generally occurred, indicating that chemical cues are involved. Experiments in which dead alien individuals, previously washed in hexane, and then reapplied with extracts were recognized by colonies giving further evidence that chemical cues mediate nestmate recognition. Epicuticular lipids, known to be nestmate recognition cues in social insects, were chemically analysed by GC-MS for 44 P. striatula females from two different populations (13 different colonies). Discriminant analysis was performed on the data for the lipid mixture composition. The discriminant model showed that, in the samples from these two populations, 68.2% and 81.9% of the specimens could be correctly assigned to their colony.     

The Role of Passive Defense (Selfish Herd and Dilution Effect) in the Gregarious Nesting of Liostenogaster Wasps (Vespidae, Hymenoptera, Stenogastrinae)

The advantages of the selfish herd and encounter-dilution effects were studied in two congeneric gregarious-nesting species of Stenogastrine wasps, Liostenogaster vechti Turillazzi and L. flavolineata (Cameron), in Malaysia. Results show that nesting in clusters affords these wasps some degree of protection against their main invertebrate predators, parasites and parasitoids. This advantage is reflected in the geometry of the aggregation as well as in the behavior of the individuals. The costs and benefits of group living and the implications of the selection of this nesting strategy in the evolution of sociality in these wasps are discussed.     

Larval memory affects adult nest-mate recognition in the ant Aphaenogaster senilis

Prenatal olfactory learning has been demonstrated in a wide variety of animals, where it affects development and behaviour. Young ants learn the chemical signature of their colony. This cue-learning process allows the formation of a template used for nest-mate recognition in order to distinguish alien individuals from nest-mates, thus ensuring that cooperation is directed towards group members and aliens are kept outside the colony. To date, no study has investigated the possible effect of cue learning during early developmental stages on adult nest-mate recognition. Here, we show that odour familiarization during preimaginal life affects recognition abilities of adult Aphaenogaster senilis ants, particularly when the familiarization process occurs during the first larval stages. Ants eclosed from larvae exposed to the odour of an adoptive colony showed reduced aggression towards familiar, adoptive individuals belonging to this colony compared with alien individuals (true unfamiliar), but they remained non-aggressive towards adult individuals of their natal colony. Moreover, we found that the chemical similarity between the colony of origin and the adoptive colony does not influence the degree of aggression, meaning that the observed effect is likely to be due only to preimaginal learning experience. These results help understanding the developmental processes underlying efficient recognition systems.     

A Unique Nest-Protection Strategy in a New Species of Spider Wasp

Hymenoptera show a great variation in reproductive potential and nesting behavior, from thousands of eggs in sawflies to just a dozen in nest-provisioning wasps. Reduction in reproductive potential in evolutionary derived Hymenoptera is often facilitated by advanced behavioral mechanisms and nesting strategies. Here we describe a surprising nesting behavior that was previously unknown in the entire animal kingdom: the use of a vestibular cell filled with dead ants in a new spider wasp (Hymenoptera: Pompilidae) species collected with trap nests in South-East China. We scientifically describe the ‘Bone-house Wasp’ as Deuteragenia ossarium sp. nov., named after graveyard bone-houses or ossuaries. We show that D. ossarium nests are less vulnerable to natural enemies than nests of other sympatric trap-nesting wasps, suggesting an effective nest protection strategy, most likely by utilizing chemical cues emanating from the dead ants.     

Odour cues from suitors’ nests determine mating success in a fish

Animals use a range of sensory cues for finding food, avoiding predators and choosing mates. In this regard, the aquatic environment is particularly suitable for the use of olfactory and other chemical cues. Nevertheless, mate choice research, even on aquatic organisms, has focused on visual signals, while chemical cues relevant in sexual selection have been assumed to be ‘intrinsic’ excretions of mate candidates. Here, using the sand goby Pomatoschistus minutus, a small fish with paternal egg care, we investigated the possibility that ‘extrinsic’ chemical cues in the males’ nests could also have a significant contribution to mating success. We found that females strongly avoided laying eggs into nests subject to the odour of Saprolegnia water moulds (an egg infection) and that this effect was independent of the females’ initial, visually based preference for males. To the best of our knowledge, this is the first study to show that chemical cues related to parental failure can play a large role in sexual selection.     

Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens

In 1959, P. Karlson and M. Lüscher introduced the term ‘pheromone’, broadly used nowadays for various chemicals involved in intraspecific communication. To demonstrate the term, they depicted the situation in termite societies, where king and queen inhibit the reproduction of nest-mates by an unknown chemical substance. Paradoxically, half a century later, neither the source nor the chemical identity of this ‘royal’ pheromone is known. In this study, we report for the first time the secretion of polar compounds of proteinaceous origin by functional reproductives in three termite species, Prorhinotermes simplex, Reticulitermes santonensis and Kalotermes flavicollis. Aqueous washes of functional reproductives contained sex-specific proteinaceous compounds, virtually absent in non-reproducing stages. Moreover, the presence of these compounds was clearly correlated with the age of reproductives and their reproductive status. We discuss the putative function of these substances in termite caste recognition and regulation.     

Double Deception: Ant-Mimicking Spiders Elude Both Visually- and Chemically-Oriented Predators

Biological mimicry is often multimodal, in that a mimic reinforces its resemblance to another organism via different kinds of signals that can be perceived by a specific target audience. In this paper we describe a novel scenario, in which a mimic deceives at least two distinct audiences, each of which relies primarily on a different sensory modality for decision-making. We have previously shown that Peckhamia picata, a myrmecomorphic spider that morphologically and behaviorally resembles the ant Camponotus nearcticus, experiences reduced predation by visually-oriented jumping spiders. Here we report that Peckhamia also faces reduced aggression from spider-hunting sphecid wasps as well as from its model ant, both of which use chemical cues to identify prey. We also report that Peckhamia does not chemically resemble its model ants, and that its total cuticular hydrocarbons are significantly lower than those of the ants and non-mimic spiders. Although further studies are needed to clarify the basis of Peckhamia''s chemically-mediated protection, to our knowledge, such ‘double deception,’ in which a single organism sends misleading visual cues to one set of predators while chemically misleading another set, has not been reported; however, it is likely to be common among what have until now been considered purely visual mimics.     

Cuticular hydrocarbons rather than peptides are responsible for nestmate recognition in Polistes dominulus

A colony of social insects is like a fortress where access is allowed only to colony members. The epicuticular mixture of hydrocarbons has been widely reported to be involved in nestmate recognition in insects. However, recent studies have shown that polar compounds (mainly peptides) are also present, mixed with hydrocarbons, on the cuticle of various insects, including the paper wasps of the genus Polistes. As these polar compounds are variable among Polistes species and are perceived by the wasps, this cuticular fraction could also be involved in nestmate recognition. Through MALDI-TOF (Matrix-Assisted Laser Desorption Ionization Time of Flight) mass spectrometry analysis, we assessed, for the first time, the intercolonial variability of the cuticular polar fraction of Polistes dominulus in order to evaluate its reliability as source of nestmate recognition cues. We then tested through behavioral assays the importance of the 2 isolated fractions (apolar and polar) in nestmate recognition by presenting them separately to colonies of P. dominulus. Our results showed that the cuticular polar compounds are not colony specific and they are not used by paper wasps to discriminate nestmates from non-colony members. On the contrary, we confirmed that the isolated cuticular hydrocarbons are the chemical mediators prompting nestmate recognition in paper wasps.     

Discrimination of conspecific-built chimneys from human-built ones by the burrowing crayfish, Fallicambarus fodiens (Decapoda, Cambaridae)

Abstract. The vast majority of tested juvenile crayfish of Fallicambarus fodiens consistently preferred conspecific-built mud chimneys over similar-looking human-built chimneys. When the chimneys were surrounded by transparent acetate sheets, the crayfish no longer discriminated between conspecific-built and human-built chimneys. This suggests that visual cues were not important in allowing the crayfish to discriminate between the two chimney types. In the absence of chimneys, significantly more crayfish showed an initial preference for mud saturated with water that had contained conspecifics, over similar mud saturated with distilled water. This indicates that chemical cues play a role in allowing these crayfish to discriminate between the conspecific-conditioned mud and the control wet mud. The preference of F. fodiens individuals for conspecific-built chimneys appears to be based, at least in part, on chemical cues, possibly in addition to tactile cues.     

A common perceptual temporal limit of binding synchronous inputs across different sensory attributes and modalities

The human brain processes different aspects of the surrounding environment through multiple sensory modalities, and each modality can be subdivided into multiple attribute-specific channels. When the brain rebinds sensory content information (‘what’) across different channels, temporal coincidence (‘when’) along with spatial coincidence (‘where’) provides a critical clue. It however remains unknown whether neural mechanisms for binding synchronous attributes are specific to each attribute combination, or universal and central. In human psychophysical experiments, we examined how combinations of visual, auditory and tactile attributes affect the temporal frequency limit of synchrony-based binding. The results indicated that the upper limits of cross-attribute binding were lower than those of within-attribute binding, and surprisingly similar for any combination of visual, auditory and tactile attributes (2–3 Hz). They are unlikely to be the limits for judging synchrony, since the temporal limit of a cross-attribute synchrony judgement was higher and varied with the modality combination (4–9 Hz). These findings suggest that cross-attribute temporal binding is mediated by a slow central process that combines separately processed ‘what’ and ‘when’ properties of a single event. While the synchrony performance reflects temporal bottlenecks existing in ‘when’ processing, the binding performance reflects the central temporal limit of integrating ‘when’ and ‘what’ properties.     

Blinded by Beauty: Attractiveness Bias and Accurate Perceptions of Academic Performance

Despite the old adage not to ‘judge a book by its cover’, facial cues often guide first impressions and these first impressions guide our decisions. Literature suggests there are valid facial cues that assist us in assessing someone’s health or intelligence, but such cues are overshadowed by an ‘attractiveness halo’ whereby desirable attributions are preferentially ascribed to attractive people. The impact of the attractiveness halo effect on perceptions of academic performance in the classroom is concerning as this has shown to influence students’ future performance. We investigated the limiting effects of the attractiveness halo on perceptions of actual academic performance in faces of 100 university students. Given the ambiguity and various perspectives on the definition of intelligence and the growing consensus on the importance of conscientiousness over intelligence in predicting actual academic performance, we also investigated whether perceived conscientiousness was a more accurate predictor of academic performance than perceived intelligence. Perceived conscientiousness was found to be a better predictor of actual academic performance when compared to perceived intelligence and perceived academic performance, and accuracy was improved when controlling for the influence of attractiveness on judgments. These findings emphasize the misleading effect of attractiveness on the accuracy of first impressions of competence, which can have serious consequences in areas such as education and hiring. The findings also have implications for future research investigating impression accuracy based on facial stimuli.     

Human ability to detect kinship in strangers' faces: effects of the degree of relatedness

The resemblance between human faces has been shown to be a possible cue in recognizing the relatedness between parents and children, and more recently, between siblings. However, the general inclusive fitness theory proposes that kin-selective behaviours are also relevant to more distant relatives, which requires the detection of larger kinship bonds. We conducted an experiment to explore the use of facial clues by ‘strangers’, i.e. evaluators from a different family, to associate humans of varying degrees of relatedness. We hypothesized that the visual capacity to detect relatedness should be weaker with lower degrees of relatedness. We showed that human adults are capable of (although not very efficient at) assessing the relatedness of unrelated individuals from photographs and that visible facial cues vary according to the degree of relatedness. This sensitivity exists even for kin pair members that are more than a generation apart and have never lived together. Collectively, our findings are in agreement with emerging knowledge on the role played by facial resemblance as a kinship cue. But we have progressed further to show how the capacity to distinguish between related and non-related pairs applies to situations relevant to indirect fitness.     

Abnormal Brain Functional Connectivity of the Hypothalamus in Cluster Headaches

The aim of this study was to detect the abnormality of the brain functional connectivity of the hypothalamus during acute spontaneous cluster headache (CH) attacks (‘in attack’) and headache-free intervals (‘out of attack’) using resting-state functional magnetic resonance imaging (RS-fMRI) technique. The RS-fMRI data from twelve male CH patients during ‘in attack’ and ‘out of attack’ periods and twelve age- and sex-matched normal controls were analyzed by the region-of-interest -based functional connectivity method using SPM5 software. Abnormal brain functional connectivity of the hypothalamus is present in CH, which is located mainly in the pain system during the spontaneous CH attacks. It extends beyond the pain system during CH attack intervals.