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The origin of novel communication systems has long been an evolutionary puzzle because communication requires interdependent signals and responses. Either component is not useful in isolation. Previous work has shown that novel communication systems may arise when pre-existing traits are co-opted for a novel function. However, research on developmental plasticity suggests we may benefit from considering how plasticity facilitates the origin and diversification of communication systems. In particular, plasticity can stabilize novel traits that are the first step towards signals or receiver responses (precursors) because plasticity allows individuals to rapidly adjust their phenotype based on their partner's phenotype, termed ‘reciprocal plasticity’. For example, exposure to a new sender precursor (e.g. new song) can produce a rapid, reciprocal change in receiver responses (e.g. preference for the new song). Reciprocal plasticity may facilitate the origin of new communication systems because precursors that influence conspecifics are more likely to become established signalling systems than precursors that are ignored by conspecifics. We review evidence that plasticity is important in the development and expression of a range of signals and preferences, the implications for divergence in signalling systems and its potential impacts on speciation and diversification. We outline areas of exciting future research, from incorporating more developmental realism into evolutionary models of signalling systems to using experimental evolution and novel anthropogenic environments to study genetic assimilation of plastic signals and preferences.

The dilution effect hypothesis posits that increasing biodiversity reduces infectious disease transmission. Here, we propose that habitat quality might modulate this negative biodiversity-disease relationship. Habitat may influence pathogen prevalence directly by affecting host traits like nutrition and immune response (we coined the term "habitat-disease relationship" to describe this phenomenon) or indirectly by changing host biodiversity (biodiversity-disease relationship). We used a path model to test the relative strength of links between habitat, biodiversity, and pathogen prevalence in a pollinator-virus system. High-quality habitat metrics were directly associated with viral prevalence, providing evidence for a habitat-disease relationship. However, the strength and direction of specific habitat effects on viral prevalence varied based on the characteristics of the habitat, host, and pathogen. In general, more natural area and richness of land-cover types were directly associated with increased viral prevalence, whereas greater floral density was associated with reduced viral prevalence. More natural habitat was also indirectly associated with reduced prevalence of two key viruses (black queen cell virus and deformed wing virus) via increased pollinator species richness, providing evidence for a habitat-mediated dilution effect on viral prevalence. Biodiversity-disease relationships varied across viruses, with the prevalence of sacbrood virus not being associated with any habitat quality or pollinator community metrics. Across all viruses and hosts, habitat-disease and biodiversity-disease paths had effects of similar magnitude on viral prevalence. Therefore, habitat quality is a key driver of variation in pathogen prevalence among communities via both direct habitat-disease and indirect biodiversity-disease pathways, though the specific patterns varied among different viruses and host species. Critically, habitat-disease relationships could either contribute to or obscure dilution effects in natural systems depending on the relative strength and direction of the habitat-disease and biodiversity-disease pathways in that host-pathogen system. Therefore, habitat may be an important driver in the complex interactions between hosts and pathogens.

Geographical variation in animal phenotypes is common, yet we know surprisingly little about how recognition varies across populations. Instead, much recognition research focuses on one or a few populations and assumes recognition behaviour is consistent across a species' range. Here, we show that individual identity signals and individual recognition vary across the geographical range of Polistes fuscatus wasps. Polistes fuscatus in Michigan and New York, U.S.A., have variable facial patterns that signal individual identity and are used by receivers for individual recognition. However, P. fuscatus from Rothrock, Pennsylvania, U.S.A., lack individual identity signals, as they have less variable facial patterns than P. fuscatus from Michigan. Furthermore, P. fuscatus from Pennsylvania are not capable of individual recognition. Pennsylvania P. fuscatus do not learn and remember individual conspecifics during social interactions or during training. The Michigan and Pennsylvania populations are genetically differentiated, but the differentiation is driven by geographical distance, not adaptive differentiation based on recognition differences. Overall, both signals and receiver responses vary across populations of P. fuscatus. Our results suggest that recognition systems may rapidly evolve to produce variation in signals and receiver responses across a species’ geographical range.

Concept formation requires animals to learn and use abstract rules that transcend the characteristics of specific stimuli. Abstract concepts are often associated with high levels of cognitive sophistication, so there has been much interest in which species can form and use concepts. A key abstract concept is that of sameness and difference, where stimuli are classified as either the same as or different than an original stimulus. Here, we used a simultaneous two-item same-different task to test whether paper wasps ( Polistes fuscatus) can learn and apply a same-different concept. We trained wasps by simultaneously presenting pairs of same or different stimuli (e.g. colours). Then, we tested whether wasps could apply the concept to new stimuli of the same type (e.g. new colours) and to new stimulus types (e.g. odours). We show that wasps learned a general concept of sameness or difference and applied it to new samples and types of stimuli. Notably, wasps were able to transfer the learned rules to new stimuli in a different sensory modality. Therefore, P. fuscatus can classify stimuli based on their relationships and apply abstract concepts to novel stimulus types. These results indicate that abstract concept learning may be more widespread than previously thought.

Theory suggests honest status signals mediate agonistic interactions between unfamiliar individuals, but may be less important during interactions between familiar individuals. Few studies have tested receiver responses to status signals in multiple contexts. Polistes dominula have facial spots that signal agonistic ability by communicating fighting abilities to unknown rivals. We test receiver response to experimentally altered facial spots during on-nest interactions in two experiments (1) between nest-founding queens prior to worker emergence and (2) between workers on queenright nests. We found no difference in aggression towards experimental and control wasps, indicating that P. dominula do not use facial markings during interactions with familiar wasps on nests. Instead, facial patterns are primarily during agonistic interactions with unfamiliar rivals. Therefore, social context plays a key role in signal response.

Many aspects of behaviour depend on recognition, but accurate recognition is difficult because the traits used for recognition often overlap. For example, brood parasitic birds mimic host eggs, so it is challenging for hosts to discriminate between their own eggs and parasitic eggs. Complex signals that occur in multiple sensory modalities or involve multiple signal components are thought to facilitate accurate recognition. However, we lack models that explore the effect of complex signals on the evolution of recognition systems. Here, we use individual-based models with a genetic algorithm to test how complex signals influence recognition thresholds, signaller phenotypes and receiver responses. The model has three main results. First, complex signals lead to more accurate recognition than simple signals. Second, when two signals provide different amounts of information, receivers will rely on the more informative signal to make recognition decisions and may ignore the less informative signal. As a result, the particular traits used for recognition change over evolutionary time as sender and receiver phenotypes evolve. Third, complex signals are more likely to evolve when recognition errors are high cost than when errors are low cost. Overall, redundant, complex signals are an evolutionarily stable mechanism to reduce recognition errors. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

Nest parasites attempt to shift the cost of rearing young from themselves to others. Despite strong selection to avoid this exploitation, there is considerable variation among-individuals in susceptibility to nest parasites. We evaluated the effects of individual variation in boldness, aggressiveness, and olfactory responsiveness on egg discrimination in wasps: Polistes metricus, which founds nests as singleton individuals, and P. dominula, which founds nests in small coalitions. Aggressiveness and boldness were evaluated using individuals’ response to mechanical disturbance, and olfactory responsiveness was evaluated using individuals’ tendency to respond to a novel rewarding stimulus. Egg discrimination was evaluated by presenting each queen with a variety of foreign eggs: 1) unaltered eggs laid by the resident (negative control group), 2) eggs produced by the resident female that were removed and replaced (procedural control), 3) eggs of foreign conspecifics (conspecific egg), and 4) eggs of a heterospecific congener (heterospecific egg). Females of both species never rejected untampered eggs and rejected procedural controls in only 35% of cases. Both species were twice as likely (70% rejection rate) to reject eggs of foreign conspecifics or heterospecifics. In P. dominula, bolder individuals and those with low olfactory responsiveness were more likely to reject foreign eggs. In P. metricus, boldness was not associated with egg rejection, but individuals with heightened olfactory responsiveness were more likely to reject foreign eggs. Thus, there are contrasting associations between behavioral phenotypes and egg rejection across species. These results are discussed in light of differences in the colony founding behavior of these species.

Much work has shown that social isolation has lasting negative effects on adult social interactions, but less is known about precisely how and why isolation alters social behaviour. One way isolation may alter social behaviour is by interfering with the development of effective communication. Here, we test how social isolation influences individual recognition, a key aspect of social communication in Polistes fuscatus paper wasps. Polistes fuscatus reared in a typical social environment learn and remember the unique faces of conspecifics during social interactions. Typical P. fuscatus use individual face recognition to minimize conflict and stabilize social interactions. As wasps are adept face learners, they also readily learn to discriminate between wasp face images during training. Here, we show that social isolation had dramatic effects on recognition. We isolated wasps for 6 days after eclosion from pupation, then tested them for face recognition in social and nonsocial contexts. Isolated wasps did not learn and remember other individuals during social interactions. Furthermore, isolated wasps did not learn to discriminate between wasp face images during training. Therefore, social experience with conspecifics is essential for the development of individual recognition and face learning in paper wasps. Many aspects of wasp behaviour develop rapidly with little experience required. However, complex social interactions like individual recognition require social experience with conspecifics.

Some animals are thought to exhibit cognitive specialization, as they have specialized cognitive modules that solve specific social or ecological problems instead of one general-purpose mechanism that addresses diverse problems. Although there are many examples of specialized cognition, little is known about whether specialization develops through experience or is produced by innate, species-specific differences. Previous work has shown that Polistes fuscatus wasps use face recognition to individually identify other wasps and that P. fuscatus are specialized for learning conspecific faces. Here, we test how experimentally altering face experience in three Polistes species influences the development of face specialization. We show face learning is influenced by both experience and innate, species-specific differences. In P. fuscatus, experience with conspecific faces is not required for the development of face specialization. In two related Polistes species that naturally lack individual face recognition, Polistes metricus and Polistes dominula, experience has different effects on specialization. Polistes metricus, a close relative of P. fuscatus, develops face specialization with experience. However, P. dominula, a more distant relative, uses general pattern recognition to learn faces regardless of experience. Therefore, some species have innate mechanistic architecture that facilitates the development of face specialization, while other species do not. These results suggest that selection shapes animal minds in a modular manner. The capacity for specialized cognitive skills evolves in response to specific ecological or social demands, such as social benefits associated with accurate individual face recognition.

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.

Most pathogens are embedded in complex communities composed of multiple interacting hosts, but we are still learning how community-level factors, such as host diversity, abundance, and composition, contribute to pathogen spread for many host-pathogen systems. Evaluating relationships among multiple pathogens and hosts may clarify whether particular host or pathogen traits consistently drive links between community factors and pathogen prevalence. Pollinators are a good system to test how community composition influences pathogen spread because pollinator communities are extremely variable and contain several multi-host pathogens transmitted on shared floral resources. We conducted a field survey of four pollinator species to test the prevalence of three RNA viruses (deformed wing virus, black queen cell virus, and sacbrood virus) among pollinator communities with variable species richness, abundance, and composition. All three viruses showed a similar pattern of prevalence among hosts. Apis mellifera and Bombus impatiens had significantly higher viral prevalence than Lasioglossum spp. and Eucera pruinosa. In each species, lower virus prevalence was most strongly linked with greater pollinator community species richness. In contrast, pollinator abundance, species-specific pollinator abundance, and community composition were not associated with virus prevalence. Our results support a consistent dilution effect for multiple viruses and host species. Pollinators in species-rich communities had lower viral prevalence than pollinators from species-poor communities, when accounting for differences in pollinator abundance. Species-rich communities likely had lower viral prevalence because species-rich communities contained more native bee species likely to be poor viral hosts than species-poor communities, and all communities contained the highly competent hosts A. mellifera and B. impatiens. Interestingly, the strength of the dilution effect was not consistent among hosts. Instead, host species with low viral prevalence exhibited weaker dilution effects compared to hosts with high viral prevalence. Therefore, host species susceptibility and competence for each virus may contribute to variation in the strength of dilution effects. This study expands biodiversity-disease studies to the pollinator-virus system, finding consistent evidence of the dilution effect among multiple similar pathogens that infect "replicate" host communities.

The 'challenge hypothesis' provides a predictive framework for how the social environment influences within-species variation in hormone titers. High testosterone levels are beneficial during reproduction and competition, but they also impose costs because they may suppress traits like parental care and immunity. As a result, the challenge hypothesis predicts that individuals will change their testosterone levels to match the current social environment. Although the vast majority of work on the challenge hypothesis has focused on androgens in vertebrates, there is growing evidence that insect hormones, especially juvenile hormone (JH), may respond to social stimuli in ways that parallel androgens in vertebrates. Many insects rapidly upregulate JH titers during social competition with rivals. Some insects also modulate JH titers based on contest outcomes, with winners upregulating JH and losers downregulating JH. This review will integrate work on social modulation of hormone titers in vertebrates and insects. First, we provide background on insect hormones and describe the functional parallels between androgens and JH. Second, we review evidence that insects rapidly change JH titers in response to social competition. Finally, we highlight opportunities for future work on social modulation of hormones in insects. Overall, the challenge hypothesis provides a useful conceptual framework for hypothesis-driven research in insect endocrinology. Comparing vertebrates and insects provides insight into how selection has shaped patterns of hormone responsiveness as well as the generality of hypotheses originally developed for vertebrates.

Summary Many animals minimize the costs of conflict by using social eavesdropping to learn about the fighting ability of potential rivals before they interact. Learning about individual conspecifics via social eavesdropping allows individuals to assess potential opponents without personal risk. However, keeping track of a network of individually differentiated social relationships is thought to be cognitively challenging. Here, we test how Polistes fuscatus nest-founding queens use social eavesdropping to assess individual rivals. Bystanders watched conspecifics fight through a clear partition. Then, bystanders were allowed to interact with fighters. Bystander behavior toward fighters was strongly influenced by the observed fight; bystanders were less aggressive toward fighters that were seen to initiate more and receive less aggression. Control trials allow us to reject alternative explanations for the link between observed aggression and bystander behavior, including priming or winner/loser effects. Therefore, P. fuscatus wasps observe and remember a complex network of social interactions between individual conspecifics rather than only paying attention to individuals they interact with directly. Wasps have an impressive capacity to learn, remember, and make social deductions about individuals. These results indicate that insects can have surprisingly complex social lives involving a network of individually differentiated social relationships.

When males and females have distinct behaviour, learning may vary between the sexes. Polistes fuscatus wasps provide an interesting model to study sex differences in learning because males and females have different social behaviour. Female wasps have highly variable facial patterns used for individual face recognition, live in cooperative groups where interactions depend on individual face recognition and excel at learning female faces. In contrast, male wasps lack the type of variable facial patterns necessary for individual face recognition and do not participate in the type of social interactions known to favour individual recognition in females. Instead, males leave the nest soon after adulthood and devote their energy to mating. Given the behavioural differences between males and females, females may be more adept at learning wasp faces than males. Here, we train male and female P. fuscatus to discriminate between pairs of female P. fuscatus face images and pairs of colours. Females learned to discriminate between pairs of face images more accurately than males. However, males and females were equally adept at colour learning, indicating that there are no generalized sex differences in learning. The sex differences in face, but not colour, learning are consistent with the adaptive specialization hypothesis, which posits that cognitive abilities are selected to solve particular social or ecological problems. Overall, general learning capacity is similar across male and female wasps, but face learning is shaped by sex-specific recognition behaviour.

Research on individual recognition often focuses on species-typical recognition abilities rather than assessing intraspecific variation in recognition. As individual recognition is cognitively costly, the capacity for recognition may vary within species. We test how individual face recognition differs between nest-founding queens (foundresses) and workers in Polistes fuscatus paper wasps. Individual recognition mediates dominance interactions among foundresses. Three previously published experiments have shown that foundresses (1) benefit by advertising their identity with distinctive facial patterns that facilitate recognition, (2) have robust memories of individuals, and (3) rapidly learn to distinguish between face images. Like foundresses, workers have variable facial patterns and are capable of individual recognition. However, worker dominance interactions are muted. Therefore, individual recognition may be less important for workers than for foundresses. We find that (1) workers with unique faces receive amounts of aggression similar to those of workers with common faces, indicating that wasps do not benefit from advertising their individual identity with a unique appearance; (2) workers lack robust memories for individuals, as they cannot remember unique conspecifics after a 6-day separation; and (3) workers learn to distinguish between facial images more slowly than foundresses during training. The recognition differences between foundresses and workers are notable because Polistes lack discrete castes; foundresses and workers are morphologically similar, and workers can take over as queens. Overall, social benefits and receiver capacity for individual recognition are surprisingly plastic.

The specialized ability to learn and recall individuals based on distinct facial features is known in only a few, large-brained social taxa. Social paper wasps in the genus Polistes are the only insects known to possess this form of cognitive specialization. We analyzed genome-wide brain gene expression during facial and pattern training for two species of paper wasps (P. fuscatus, which has face recognition, and P. metricus, which does not) using RNA sequencing. We identified 237 transcripts associated with face specialization in P. fuscatus, including some transcripts involved in neuronal signaling (serotonin receptor and tachykinin). Polistes metricus that learned faces (without specialized learning) and P. fuscatus in social interactions with familiar partners (from a previous study) showed distinct sets of brain differentially expressed transcripts. These data suggest face specialization in P. fuscatus is related to shifts in the brain transcriptome associated with genes distinct from those related to general visual learning and social interactions.

Consistent differences in behavior between individuals, otherwise known as animal personalities, have become a staple in behavioral ecology due to their ability to explain a wide range of phenomena. Social organisms are especially serviceable to animal personality techniques because they can be used to explore behavioral variation at both the individual and group level. Despite the success of personality research in social organisms generally, and social Hymenoptera in particular, social wasps (Vespidae) have received little to no attention in the personality literature. In the present study, we test Polistes metricus (Vespidae; Polistinae) paper wasp queens for the presence of repeatable variation in, and correlations (“behavioral syndromes”) between, several commonly used personality metrics: boldness, aggressiveness, exploration, and activity. Our results indicate that P. metricus queens exhibit personalities for all measured traits and correlations between different behavioral measures. Given that paper wasps have served as a model organism for a wide range of phenomena such as kin selection, dominance hierarchies, mate choice, facial recognition, social parasitism, and chemical recognition, we hope that our results will motivate researchers to explore whether, or to what degree, queen personality is important in their research programs.

The founding individuals of a new group or lineage are uniquely poised to have long-lasting effects on their descendants. Here we explore how the behavioural traits of new foundresses influence their task allocation strategies and the downstream collective behaviour of their colonies. We collected individual paper wasp (Polistes metricus) queens from the wild and measured their boldness, aggressiveness, exploration, activity and time budgets in the laboratory. We then provided queens with food and nest materials and waited for their workers to eclose. We subsequently tested for links between queen behavioural traits (e.g. boldness, aggressiveness) and the collective aggressiveness of their colonies, as estimated by the number of workers that responded to and stung a model predator. We found that bolder queens (i.e. queens that were less likely to leave their nests after repeated exposure to an agonistic stimulus) spent more time nest guarding, reared more workers and produced groups that were less responsive to a model predator. Thus, there appears to be parent–offspring, or queen–worker, resemblance in the degree to which individuals remain on their nests in different social contexts (solitary queen versus queen + her worker group). To our knowledge this represents the first study to explicitly test for links between individual variation in foundress behaviour, worker production and intercolony collective behaviour; the results highlight the possibility that cross-contextual and transgenerational behavioural links could be a reasonably common and potentially important phenomenon in complex societies.

The founders of a social group or colony have the potential to greatly influence the success or failure of the societies that they initiate. Whether through their genetic contribution, or through behavioral maternal effects related to temperament, resource acquisition, or brood care, the traits of founders deserve special consideration. The queens of many social insects are ideally suited to address questions relating to the importance of founder traits due to her solitary involvement in performing a multitude of tasks necessary to produce a functioning colony. While it has been suggested that a queen’s behavioral phenotype might contribute to differences in colony success, no study has yet demonstrated these links in situ. Here, we use the singly founding (haplometrotic) paper wasp Polistes metricus to examine whether queen personality, measured shortly after colony founding (pre-emergent phase), and morphology, can predict colony size (a proxy for queen fitness) and parasite load in the wild. We found that larger and bolder queens gave rise to larger colonies than smaller and shyer queens, and there was no relationship between queen personality and parasite load. Differences in queen traits therefore appear to be a major determinant of colony success under field conditions. In social species, the personality composition of groups has been shown to be a large determinant of group behavior, which in turn can determine group performance and survival. In this study, we explore the degree to which the behavioral tendencies of key group members—wasp queens—influence the performance of their descendant societies. We tested the behavioral tendencies and morphology of Polistes metricus paper wasp queens in the early spring, placed them back in the field in nest boxes, and recorded each nest’s cell count at the end of the season—a reliable proxy for queen fitness. We found that larger and bolder queens gave rise to larger descendant colonies on average than their smaller, shyer counterparts. Individual variation in queen traits therefore appears to be a determinant of colony success under field conditions.

Transitive inference (TI) is a form of logical reasoning that involves using known relationships to infer unknown relationships (A > B; B > C; then A > C). TI has been found in a wide range of vertebrates but not in insects. Here, we test whether Polistes dominula and Polistes metricus paper wasps can solve a TI problem. Wasps were trained to discriminate between five elements in series (A 0 B−, B 0 C−, C 0 D−, D 0 E−), then tested on novel, untrained pairs (B versus D). Consistent with TI, wasps chose B more frequently than D. Wasps organized the trained stimuli into an implicit hierarchy and used TI to choose between untrained pairs. Species that form social hierarchies like Polistes may be predisposed to spontaneously organize information along a common underlying dimension. This work contributes to a growing body of evidence that the miniature nervous system of insects does not limit sophisticated behaviours.

Colonies of social insects exhibit a spectacular variety of life histories. Here we documented the degree of variation in colony life-history traits, mostly related to productivity, in two species of wild paper wasps. We then tested for associations between colony life-history traits to look for trade-offs or positively associated syndromes, and examined whether individual differences in the behavioral tendencies of foundresses (Polistes metricus) or the number of cofoundresses (P. fuscatus) influenced colony life-history. The majority of our measures of colony life-history were positively related, indicating no obvious resource allocation trade-offs. Instead, the positive association of traits into a productivity syndrome appears to be driven by differences in queen or microhabitat quality. Syndrome structure differed only marginally between species. Queen boldness and body size were not associated with colony life-history in P. metricus. Colonies initiated by multiple P. fuscatus foundresses were generally more productive, and this advantage was approximately proportional to the number of cofoundresses. These findings demonstrate that colony life-history traits can be associated together much like individual life-history traits, and the associations seen here convey that differences in overall productivity drive between-colony differences in life-history.

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.

Although developmental plasticity facilitates the evolutionary origin of many traits, the role of plasticity in the origin of novel communication systems has received little attention. If plasticity mediates the origin of new communication systems, exposure to a novel environment will induce new traits that could function as signals or receiver responses. Here, we test whether plasticity facilitates the origin of individual recognition. We reared a species of paper wasp that naturally lacks individual recognition (Polistes metricus) with a relative that has facial patterns that signal individual identity (Polistes fuscatus). We found P. metricus reared with individual identity signals learned unique wasp faces significantly more accurately than P. metricus reared without individual identity signals. However, exposure to individual identity signals was not sufficient to induce individual recognition in social contexts. These results suggest that if variable facial patterns arose in P. metricus, wasps would immediately improve their ability learn variable facial patterns, thereby facilitating the origin of individual face recognition. Improved learning is an initial step toward individual recognition that would need to be refined by selection to produce an established signaling system. Developmental plasticity may be an underappreciated factor facilitating the evolutionary origin of novel recognition systems.

Cooperative breeding decreases the direct reproductive output of subordinate individuals, but cooperation can be evolutionarily favored when there are challenges or constraints to breeding independently. Environmental factors, including temperature, precipitation, latitude, high seasonality, and environmental harshness have been hypothesized to correlate with the presence of cooperative breeding. However, to test the relationship between cooperation and ecological constraints requires comparative data on the frequency and variation of cooperative breeding across differing environments, ideally replicated across multiple species. Paper wasps are primitively social species, forming colonies composed of reproductively active dominants and foraging subordinates. Adult female wasps, referred to as foundresses, initiate new colonies. Nests can be formed by a single solitary foundress (noncooperative) or by multiple foundress associations (cooperative). Cooperative behavior varies within and among species, making paper wasps species well suited to disentangling ecological correlates of variation in cooperative behavior. This data set reports the frequency and extent of cooperative nest founding for 87 paper wasp species. Data were assembled from more than 170 published sources, previously unpublished field observations, and photographs contributed by citizen scientists to online natural history repositories. The data set includes 25,872 nest observations and reports the cooperative behavioral decisions for 45,297 foundresses. Species names were updated to reflect modern taxonomic revisions. The type of substrate on which the nest was built is also included, when available. A smaller population-level version of this data set found that the presence or absence of cooperative nesting in paper wasps was correlated with temperature stability and environmental harshness, but these variables did not predict the extent of cooperation within species. This expanded data set contains details about individual nests and further increases the power to address the relationship between the environment and the presence and extent of cooperative breeding. Beyond the ecological drivers of cooperation, these high-resolution data will be useful for future studies examining the evolutionary consequences of variation in social behavior. This data set may be used for research or educational purposes provided that this data paper is cited.

Many animals have ornaments that mediate choice and competition in social and sexual contexts. Individuals with elaborate sexual ornaments typically have higher fitness than those with less elaborate ornaments, but less is known about whether socially selected ornaments are associated with fitness. Here, we test the relationship between fitness and facial patterns that are a socially selected signal of fighting ability in Polistes dominula wasps. We found wasps that signal higher fighting ability have larger nests, are more likely to survive harsh winters, and obtain higher dominance rank than wasps that signal lower fighting ability. In comparison, body weight was not associated with fitness. Larger wasps were dominant over smaller wasps, but showed no difference in nest size or survival. Overall, the positive relationship between wasp facial patterns and fitness indicates that receivers can obtain diverse information about a signaler's phenotypic quality by paying attention to socially selected ornaments. Therefore, there are surprisingly strong parallels between the information conveyed by socially and sexually selected signals. Similar fitness relationships in social and sexually selected signals may be one reason it can be difficult to distinguish the role of social versus sexual selection in ornament evolution.

Animals frequently compete over limited resources such as food, territories or mating opportunities. Contest behaviour varies based on factors such as the value of the contested resources and the agonistic ability of rivals. Much work on animal contests has examined aggression, but vigilance, or a state of heightened alertness directed towards specific stimuli, may also be an important component of competition in many species. In this study, we measure the relationships among social vigilance, aggression, agonistic ability and resource value during staged contests over nest ownership in Polistes dominula nest-founding wasps. Our results show that both social vigilance and aggression are involved in mediating social risk during contests. Nest owner vigilance towards a rival increased with the time of season, a measure of nest value. Owner vigilance was also positively associated with aggression such that more aggressive owners were more vigilant. During contests, aggression of owners and rivals was influenced by different factors. Owner aggression was positively associated with nest size, another measure of nest value, while rival aggression was unrelated to nest size. Instead, rival aggression was associated with facial patterns that function as signals of agonistic ability; rivals were less aggressive to owners that signalled high agonistic ability than they were to owners that signalled low agonistic ability. The distinct predictors of contest behaviour between owners and rivals indicate that competitive role has a surprisingly strong influence on cues used to inform contest behaviour. Differences may occur because owners and rivals have different information and/or motivation. These results also suggest that social vigilance and aggression may be complementary behaviours that animals use to mitigate social threat.

Sexually selected signals are theoretically expected to exhibit heightened condition dependence compared to non-signaling traits. This link to condition enables sexual signals to provide information regarding individual quality and also provides a mechanism that allows animals to develop signals that accurately reflect their abilities. Most previous work on sexual signal condition dependence has focused on signals that have clear developmental costs, while less is known about the development of other types of quality signals. Male Polistes dominulus paper wasps have yellow-on-black abdominal spots that are important signals during female choice and male–male competition. These signals lack obvious production costs, as males are covered in yellow and black patterns composed of the same pigments. Here, we assess signal condition dependence by testing whether larval diet has a stronger influence on the development of male spots than on the development of control traits composed of the same pigments. Males reared on ad libitum diets developed elliptical spots similar to those seen on dominant, attractive males, while males reared on restricted diets developed irregularly shaped spots similar to those seen on subordinate, unattractive males. Remarkably, the development of a control trait composed of the same yellow and black pigments was not influenced by larval diet. Therefore, sexually selected signals can be developmentally decoupled from traits comprised of the same pigments. Condition dependence of sexually selected signals is likely to be a widespread solution to the challenge of developing sexually selected signals that accurately convey information about individual quality.

In many cooperatively breeding animals, subordinate group members have lower reproductive capacity than dominant group members. Theory suggests subordinates may downregulate their reproductive capacity because dominants punish subordinates who maintain high fertility. However, there is little direct experimental evidence that dominants cause physiological suppression in subordinates. Here, we experimentally test how social interactions influence subordinate reproductive hormones inPolistes dominulapaper wasps.Polistes dominulaqueens commonly found nests in cooperative groups where the dominant queen is more fertile than the subordinate queen. In this study, we randomly assigned wasps to cooperative groups, assessed dominance behaviour during group formation, then measured levels of juvenile hormone (JH), a hormone that mediatesPolistesfertility. Within three hours, lowest ranking subordinates had less JH than dominants or solitary controls, indicating that group formation caused rapid JH reduction in low-ranking subordinates. In a second experiment, we measured the behavioural consequences of experimentally increasing subordinate JH. Subordinates with high JH-titres received significantly more aggression than control subordinates or subordinates from groups where the dominant's JH was increased. These results suggest that dominants aggressively punished subordinates who attempted to maintain high fertility. Low-ranked subordinates may rapidly downregulate reproductive capacity to reduce costly social interactions with dominants. Rapid modulation of subordinate reproductive physiology may be an important adaptation to facilitate the formation of stable, cooperative groups.

In living color Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between individual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and diversification. Science , this issue p. eaan0221

Some primates and one species of paper wasp recognize faces using specific processing strategies to extract individual identity information from conspecific faces. Explanations for the evolution of face specialization typically focus on the complexity associated with individual recognition because all currently identified species with face specialization use faces for individual recognition. In the present study, we show an independent evolution of face specialization in a paper wasp species with facial patterns that signal quality rather than individual identity. Quality signals are simpler to process than individual identity signals because quality signals do not require simultaneous integration across multiple stimuli or learning and memory. Therefore, the results of the present study suggest that the complexity of processing may not be the key factor favouring the evolution of specialization. Instead, the predictable location of socially important signals relative to other anatomical features may allow easy categorization of features, thereby favouring specialized visual processing. Given that visual quality signals are found in many taxa, specific-processing mechanisms for social signals may be widespread. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 992–997.

Much research on animal communication has addressed how costs such as social costs or physiological costs favor the accuracy of signals. Previous work has largely considered these costs separately, but we may be missing essential connections by studying costs in isolation. After all, social interactions produce rapid changes in hormone titers which can then affect individual behavior and physiology. As a result, social costs are likely to have widespread physiological consequences. Here, I present a new perspective on the factors that maintain honest signals by describing how the interplay between social costs and physiological costs may maintain an accurate link between an animal's abilities and ornament elaboration. I outline three specific mechanisms by which the interaction between social behavior and hormones could favor honest signals and present specific predictions for each of the three models. Then, I review how ornaments alter agonistic behavior, agonistic behavior influences hormones, and how these hormonal effects influence fitness. I also describe the few previous studies that have directly tested how ornaments influence hormones. Finally, opportunities for future work are discussed. Considering the interaction between social behavior and physiology may address some challenges associated with both social and physiological models of costs. Understanding the dynamic feedbacks between physiology and social costs has potential to transform our understanding of the stability of animals' communication systems.

Many animals adapt to rapidly changing social environments by using social information to modulate their hormone titres. Modulation of hormone titres, as proposed by the challenge hypothesis, provides a mechanism by which individuals can match their behaviour to their current social environment and thereby avoid costs associated with prolonged high hormone titres. Thus far, most work on social responsiveness of hormone titres has focused on androgens in vertebrates. However, there is mounting evidence that insect hormones, especially juvenile hormone, may respond to social stimuli in ways that parallel androgens in vertebrates. This review will integrate work on social modulation of hormone titres in vertebrates and insects. First we review how the hormone-mediated trade-off between fecundity and life span may be a key selective force favouring socially responsive hormone titres in both systems. Then we review theoretical and empirical work in vertebrates and insects that address how factors such as social instability, dominance rank and mating system influence hormone titre responsiveness. These studies illustrate that (1) juvenile hormone (JH) is responsive to social stimuli in a range of insect taxa and (2) JH responses match key predictions of the challenge hypothesis. We conclude that there are strong similarities in endocrine responsiveness across vertebrate and insect taxa. The challenge hypothesis provides a useful conceptual framework for hypothesis-driven research in insect endocrinology. In addition, exploring areas of convergence and divergence across vertebrates and insects may help clarify how selection has shaped patterns of endocrine responsiveness.

In many signalling systems, intraspecific variation in recognition abilities is based on developmental stage, experience or caste. However, the occurrence of intraspecific variation in recognition has not been thoroughly examined in species with individual recognition. For example, previous work has shown that individual recognition is an important aspect of the social life of Polistes fuscatus (paper wasp) nest-founding queens, as individual recognition stabilizes dominance interactions and reduces aggression. To date, the potential for individual recognition among P. fuscatus workers has been largely ignored. Here, we explore whether there is intraspecific variation in individual recognition by testing P. fuscatus worker recognition abilities in a series of staged contests. The results indicate that P. fuscatus workers are capable of individual recognition: focal workers paired with previously encountered partners experienced significantly less aggression and more nonaggressive bodily contact than focal workers paired with unknown social partners. We propose two potential explanations for individual recognition among workers: (1) worker individual recognition may be favoured because it provides social benefits to workers, or (2) worker individual recognition may be a byproduct of selection for individual recognition in foundresses. Individual recognition is often considered a cognitively challenging form of recognition, so future studies that compare the sophistication of recognition across castes will be useful to assess whether there are more subtle differences in cognitive abilities or recognition behaviour between P. fuscatus nest-founding queens and workers.

Polistes are an ideal system to study ultimate and proximate questions of dominance, and to test theoretical predictions about social evolution. The behaviors typically associated with dominance in Polistes are similar to those observed in many vertebrate societies. Here, we review recent ethological, mechanistic, and evolutionary studies on how social dominance hierarchies are established and maintained in Polistes spp. From the ultimate perspective, we address individual and group benefits of hierarchy formation, as well as issues such as reproductive skew, queen-worker conflict, and costs of challenging the dominant. From the proximate perspective, we review social, physical, and physiological factors influencing hierarchy formation, including co-foundress interactions, age structure, body size, endocrine system, and chemical and visual signals. We also discuss the extensive inter- and intra-specific variation of Polistes in the formation and maintenance of hierarchies, as well as levels of within-colony aggression. We conclude the review by highlighting the utility of this variation for comparative studies and the immense potential of the genus Polistes to address fundamental and unanswered questions about the evolution and maintenance of dominance behavior in animals.

A wide range of complex social behaviors are facilitated by the recognition of individual conspecifics. Individual recognition requires sufficient phenotypic variation to provide identity information as well as receivers that process and respond to identity information. Understanding how a complex trait such as individual recognition evolves requires that we consider how each component has evolved. Previous comparative studies have examined phenotypic variability in senders and receiver learning abilities, although little work has compared receiver responses to identity information among related species with and without individual recognition. Here, we compare responses to identity information in two Polistes paper wasps: P. fuscatus, which visually recognizes individuals, and P. metricus, which does not normally show evidence of individual recognition. Although the species differ in individual recognition, the results of this study show that receiver responses to experimentally manipulated identity information are surprisingly similar in both species. Receivers direct less aggression toward identifiable individuals than unidentifiable individuals. Therefore, the responses necessary for individual recognition may pre-date its evolution in the P. fuscatus lineage. Additionally, our data demonstrate the apparent binary differences in a complex behavior between the two species, such as individual recognition, likely involve incremental differences along a number of axes.

The article reports that scientists have discovered that paper wasps have the ability to recognize and memorize each other's unique facial features as of December 2013. The authors say the discoveries have revealed that humans with their large mammalian brain are not the only animals with this capability. Results of the studies show small-brained insects use a face-processing mechanism that is similar to the ones humans use to distinguish faces.

Animals can influence their social environment by preferentially associating with certain conspecifics. Such preferential association has gained increasing theoretical attention, as it may influence social evolution and population dynamics. However, relatively little empirical work has examined the occurrence of preferential association and its effects on cooperative group formation. Here, we test the factors associated with cooperative group formation in Polistes dominulus nest-founding queen wasps. P. dominulus are a good system to study preferential association, as foundresses can nest alone or in groups and group membership is flexible. We found that both social and environmental factors were associated with partner choice. First, facial patterns were associated with cooperation. Wasps with more similar facial patterns were more likely to cooperate than wasps with less similar facial patterns. This preferential phenotypic association fits the theoretical criteria for the evolution of tag-based cooperation. Season was also associated with cooperation; wasps on early-season nests were more likely to cooperate than wasps on late-season nests. High levels of aggression by nest owners during initial interactions were also correlated with lower probabilities of subsequent cooperation, suggesting that nest owners have some control over group membership. Other factors including body weight, weight similarity and nest productivity were not linked with cooperation. Overall, multiple factors influence cooperation in paper wasps, including facial pattern similarity. The occurrence of preferential phenotypic association in paper wasps is quite interesting and may influence the evolution of cooperation and population divergence in this group.

The reproductive ground plan hypothesis (RGPH) proposes that the ovarian cycle in solitary insects provides the basis for social evolution, so similar mechanisms are predicted to influence reproductive plasticity in social and solitary species. Specifically, reproductive plasticity in social species originated via modification of nutrition-dependent fertility response to juvenile hormone (JH) in solitary insects. Testing this prediction requires information about the factors that influence fertility in non-social relatives of the eusocial hymenoptera. However, no previous studies have examined how JH or nutritional condition influence fertility in Eumenines, the non-social group most closely related to social wasps. Here, we find support for the RGPH, as JH increases Euodynerus foraminatus fertility. Fertility is also condition-dependent, as heavy E. foraminatus are more fertile than light E. foraminatus. In addition, we measure the factors associated with mating success in E. foraminatus, finding that multiple factors influence mating success, including male weight, male mating experience, and female age. There is also higher variance in male than female reproductive success, suggesting that males may experience substantial sexual selection in this species. Overall, the relationships between JH, body weight, and fertility in E. foraminatus support the RGPH for the origin of sociality by demonstrating that there are strong parallels in the mechanisms that mediate fertility of social and non-social wasps.

Decades of behavioral endocrinology research have shown that hormones and behavior have a bidirectional relationship; hormones both influence and respond to social behavior. In contrast, hormones are often thought to have a unidirectional relationship with ornaments. Hormones influence ornament development, but little empirical work has tested how ornaments influence hormones throughout life. Here, we experimentally alter a visual signal of fighting ability in Polistes dominulus paper wasps and measure the behavioral and hormonal consequences of signal alteration in signalers and receivers. We find wasps that signal inaccurately high fighting ability receive more aggression than controls and receiving aggression reduces juvenile hormone (JH) titers. As a result, immediately after contests, inaccurate signalers have lower JH titers than controls. Ornaments also directly influence rival JH titers. Three hours after contests, wasps who interacted with rivals signaling high fighting ability have higher JH titers than wasps who interacted with rivals signaling low fighting ability. Therefore, ornaments influence hormone titers of both signalers and receivers. We demonstrate that relationships between hormones and ornaments are flexible and bidirectional rather than static and unidirectional. Dynamic relationships among ornaments, behavior, and physiology may be an important, but overlooked factor in the evolution of honest communication.

Although sexually selected ornaments are common across diverse taxa, little is known about mate choice and sexually selected ornamentation in social insects. Polistes dominulus paper wasps are a good system to study sexual selection, as males have a lek-based mating system as well as sexually dimorphic abdominal spots. Here, we demonstrate that the abdominal spots of male P. dominulus paper wasps function as signals in both inter- and intrasexual selection. Males with smaller, elliptically shaped spots were more dominant over male rivals and were more preferred by females than males with larger, irregularly shaped spots. Furthermore, experimental manipulation of male spots demonstrates that spot morphology acts as a signal. Males with experimentally reduced abdominal spots won a greater proportion of fights and were preferred by females as mates over control males. These results demonstrate that male ornaments are an important mediator of mating dynamics in P. dominulus paper wasps. They also highlight the importance of additional research examining sexually selected ornamentation in social insects.

Some animals minimize the high costs of aggressive conflict by using conventional signals of agonistic ability to assess rivals prior to interacting. Conventional signals are more controversial than other signals of agonistic ability because they lack an inherent physical or physiological link with their bearer’s agonistic ability. Here, we test whether the variable brown facial stripes in Polistes exclamans paper wasps function as a conventional signal. Polistes exclamans were given the option of challenging or avoiding a rival with an experimentally altered facial pattern. Our results show that rival assessment is based on the facial patterns of rivals, as well as an individual’s own size, facial patterns, and nesting strategy. Individuals with larger body size and larger brown facial stripes were more likely to challenge rivals than individuals with smaller body size and smaller brown facial stripes. In addition, large individuals were more likely to challenge rivals with large brown facial stripes than small individuals, while an individual’s own body size did not influence whether or not they challenged rivals with small brown stripes. Individuals who previously nested in multiple queen groups approached rivals more rapidly than individuals who previously nested alone, suggesting that social experience also plays a role in rival assessment. Finally, rivals with small facial stripes were challenged more rapidly than those with large facial stripes. These results demonstrate that P. exclamans facial patterns function as a signal used to minimize the cost of conflict. However, individuals do not make simple decisions based on their rival’s signal alone, as an individual’s own social experience and agonistic abilities also influence rival assessment decisions.

Developmental stability is the ability of organisms to buffer development against perturbations. Different classes of traits typically have different levels of fluctuating asymmetry (FA), a measure of developmental instability. In particular, elevated FA in sexually selected quality signals has attracted a great deal of attention. There are 3 main hypotheses to explain elevated developmental instability in quality signals. Developmental instability may be related to the cost of trait production, a trait’s condition dependence, or the levels of interindividual trait variation. Here we test these 3 hypotheses by comparing FA in structural traits, nonsignaling color traits, and 2 signaling color traits: a condition-dependent quality signal in Polistes dominulus wasps and noncondition-dependent identity signals in P. fuscatus wasps. Overall, color traits have higher FA than structural traits, though FA differs among the 3 classes of color traits. The clypeal identity signal in P. fuscatus has the highest interindividual trait variation, yet shows relatively low FA, indicating that interindividual trait variation does not explain heightened FA. The quality signal in P. dominulus has the highest FA, though it is not costly to produce. Therefore, the elevated FA in quality signals cannot be attributed to costs of signal production. The quality signal in P. dominulus is condition dependent, however, so our results indicate that increased developmental instability in quality signaling traits can be attributed to their condition-dependent development. A link between developmental stability and condition dependence provides a mechanism through which quality signals may integrate information about overall condition in the absence of costly trait development. Key words: badge of status, condition dependence, fluctuating asymmetry, identity signal, Polistes, quality signal, sexual selection. [Behav Ecol]