Field-realistic exposure to neonicotinoid and sulfoximine insecticides impairs visual and olfactory learning and memory in Polistes paper wasps.

Exposure to insecticides may contribute to global insect declines due to sublethal insecticide effects on non-target species. Thus far, much research on non-target insecticide effects has focused on neonicotinoids in a few bee species. Much less is known about effects on other insect taxa or newer insecticides, such as sulfoxaflor. Here, we studied the effects of an acute insecticide exposure on both olfactory and visual learning in free-moving Polistes fuscatus paper wasps. Wasps were exposed to a single, field-realistic oral dose of low-dose imidacloprid, high-dose imidacloprid or sulfoxaflor. Then, visual and olfactory learning and short-term memory were assessed. We found that acute insecticide exposure influenced performance, as sulfoxaflor- and high-dose imidacloprid-exposed wasps made fewer correct choices than control wasps. Notably, both visual and olfactory performance were similarly impaired. Wasps treated with high-dose imidacloprid were also less likely to complete the learning assay than wasps from the other treatment groups. Instead, wasps remained stationary and unmoving in the testing area, consistent with imidacloprid interfering with motor control. Finally, wasps treated with sulfoxaflor were more likely to die in the week after treatment than wasps in the other treatment groups. Our findings demonstrate that sublethal, field-realistic dosages of both neonicotinoid- and sulfoximine-based insecticides impair wasp learning and short-term memory, which may have additional effects on survival and motor functioning. Insecticides have broadly detrimental effects on diverse non-target insects that may influence foraging effectiveness, pollination services and ecosystem function.

Social experience drives the development of holistic face processing in paper wasps.

Most recognition is based on identifying features, but specialization for face recognition in some taxa 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. Although previous work suggests that extensive experience may be required for the development of holistic processing, we lack experiments that test how age and experience interact to influence holistic processing. Here, we test how age and experience influence the development of holistic face processing in Polistes fuscatus paper wasps. Previous work has shown that P. fuscatus use facial patterns to individually identify conspecifics and wasps use holistic processing to discriminate between conspecific faces. We tested face processing in three groups of P. fuscatus: young (1-week-old), older, experienced (2-weeks-old, normal experience), and older, inexperienced (2-weeks-old, 1 week normal social experience and 1 week social isolation). Older, experienced wasps used holistic processing to discriminate between conspecific faces. In contrast, older inexperienced wasps used featural rather than holistic mechanisms to discriminate between faces. Young wasps show some evidence of holistic face processing, but this ability was less refined than older, experienced wasps. Notably, wasps only required 2 weeks of normal experience to develop holistic processing, while previous work suggests that humans may require years of experience. Overall, P. fuscatus wasps rapidly develop holistic processing for conspecific faces. Experience rather than age facilitates the transition between featural and holistic face processing mechanisms.

Paper wasps form abstract concept of 'same and different'.

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.

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.

The challenge hypothesis in insects.

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.

Transitive inference in Polistes paper wasps.

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 (A0B-, B0C-, C0D-, D0E-), 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.

Socially selected ornaments influence hormone titers of signalers and receivers.

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.

Intraspecific Variation in Learning: Worker Wasps Are Less Able to Learn and Remember Individual Conspecific Faces than Queen Wasps.

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.

Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation.

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 in Polistes dominula paper wasps. Polistes dominula queens 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 mediates Polistes fertility. 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.

WASPnest: a worldwide assessment of social Polistine nesting behavior.

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.

Cognitive specialization for learning faces is associated with shifts in the brain transcriptome of a social wasp.

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.

Different axes of environmental variation explain the presence vs. extent of cooperative nest founding associations in Polistes paper wasps.

Ecological constraints on independent breeding are recognised as major drivers of cooperative breeding across diverse lineages. How the prevalence and degree of cooperative breeding relates to ecological variation remains unresolved. Using a large data set of cooperative nesting in Polistes wasps we demonstrate that different aspects of cooperative breeding are likely to be driven by different aspects of climate. Whether or not a species forms cooperative groups is associated with greater short-term temperature fluctuations. In contrast, the number of cooperative foundresses increases in more benign environments with warmer, wetter conditions. The same data set reveals that intraspecific responses to climate variation do not mirror genus-wide trends and instead are highly heterogeneous among species. Collectively these data suggest that the ecological drivers that lead to the origin or loss of cooperation are different from those that influence the extent of its expression within populations.

Coevolution of visual signals and eye morphology in Polistes paper wasps.

To be effective, signals must propagate through the environment and be detected by receivers. As a result, signal form evolves in response to both the constraints imposed by the transmission environment and receiver perceptual abilities. Little work has examined the extent to which signals may act as selective forces on receiver sensory systems to improve the efficacy of communication. If receivers benefit from accurate signal assessment, selection could favour sensory organs that improve discrimination of established signals. Here, we provide evidence that visual resolution coevolves with visual signals in Polistes wasps. Multiple Polistes species have variable facial patterns that function as social signals, whereas other species lack visual signals. Analysis of 19 Polistes species shows that maximum eye facet size is positively associated with both eye size and presence of visual signals. Relatively larger facets within the eye's acute zone improve resolution of small images, such as wasp facial signals. Therefore, sensory systems may evolve to optimize signal assessment. Sensory adaptations to facilitate signal detection may represent an overlooked area of the evolution of animal communication.

The Evolution of Simplifying Heuristics in Visual Cognition: Categorization, Specialization, and Visual Illusions.

Animals live in visually complex environments. As a result, visual systems have evolved mechanisms that simplify visual processing and allow animals to focus on the information that is most relevant to adaptive decision making. This review explores two key mechanisms that animals use to efficiently process visual information: categorization and specialization. Categorization occurs when an animal's perceptual system sorts continuously varying stimuli into a set of discrete categories. Specialization occurs when particular classes of stimuli are processed using distinct cognitive operations that are not used for other classes of stimuli. We also describe a nonadaptive consequence of simplifying heuristics: visual illusions, where visual perception consistently misleads the viewer about the state of the external world or objects within it. We take an explicitly comparative approach by exploring similarities and differences in visual cognition across human and nonhuman taxa. Considering areas of convergence and divergence across taxa provides insight into the evolution and function of visual systems and associated perceptual strategies.

Habitat quality influences pollinator pathogen prevalence through both habitat-disease and biodiversity-disease pathways.

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.

Honeybee visitation to shared flowers increases Vairimorpha ceranae prevalence in bumblebees.

Vairimorpha (=Nosema) ceranae is a widespread pollinator parasite that commonly infects honeybees and wild pollinators, including bumblebees. Honeybees are highly competent V. ceranae hosts and previous work in experimental flight cages suggests V. ceranae can be transmitted during visitation to shared flowers. However, the relationship between floral visitation in the natural environment and the prevalence of V. ceranae among multiple bee species has not been explored. Here, we analyzed the number and duration of pollinator visits to particular components of squash flowers-including the petals, stamen, and nectary-at six farms in southeastern Michigan, USA. We also determined the prevalence of V. ceranae in honeybees and bumblebees at each site. Our results showed that more honeybee flower contacts and longer duration of contacts with pollen and nectar were linked with greater V. ceranae prevalence in bumblebees. Honeybee visitation patterns appear to have a disproportionately large impact on V. ceranae prevalence in bumblebees even though honeybees are not the most frequent flower visitors. Floral visitation by squash bees or other pollinators was not linked with V. ceranae prevalence in bumblebees. Further, V. ceranae prevalence in honeybees was unaffected by floral visitation behaviors by any pollinator species. These results suggest that honeybee visitation behaviors on shared floral resources may be an important contributor to increased V. ceranae spillover to bumblebees in the field. Understanding how V. ceranae prevalence is influenced by pollinator behavior in the shared floral landscape is critical for reducing parasite spillover into declining wild bee populations.

The effect of juvenile hormone on Polistes wasp fertility varies with cooperative behavior.

Social insects provide good models for studying how and why the mechanisms that underlie reproduction vary, as there is dramatic reproductive plasticity within and between species. Here, we test how the effect of juvenile hormone (JH) on fertility covaries with cooperative behavior in workers and nest-founding queens in the primitively eusocial wasp Polistes metricus. P. metricus foundresses and workers appear morphologically similar and both are capable of reproduction, though there is variation in the extent of social cooperation and the probability of reproduction across castes. Do the endocrine mechanisms that mediate reproduction co-vary with cooperative behavior? We found dramatic differences in the effect of JH on fertility across castes. In non-cooperative nest-founding queens, all individuals responded to JH by increasing their fertility. However, in cooperative workers, the effect of JH on fertility varies with body weight; large workers increase their fertility in response to JH while small workers do not. The variation in JH response may be an adaptation to facilitate resource allocation based on the probability of independent reproduction. This work contrasts with previous studies in closely related Polistes dominulus paper wasps, in which both foundresses and workers form cooperative associations and both castes show similar, condition-dependent JH response. The variation in JH responsiveness within and between species suggests that endocrine responsiveness and the factors influencing caste differentiation are surprisingly evolutionarily labile.

The establishment and maintenance of dominance hierarchies.

Animal groups are often organized hierarchically, with dominant individuals gaining priority access to resources and reproduction over subordinate individuals. Initial dominance hierarchy formation may be influenced by multiple interacting factors, including an animal's individual attributes, conventions and self-organizing social dynamics. After establishment, hierarchies are typically maintained over the long-term because individuals save time, energy and reduce the risk of injury by recognizing and abiding by established dominance relationships. A separate set of behaviours are used to maintain dominance relationships within groups, including behaviours that stabilize ranks (punishment, threats, behavioural asymmetry), as well as signals that provide information about dominance rank (individual identity signals, signals of dominance). In this review, we describe the behaviours used to establish and maintain dominance hierarchies across different taxa and types of societies. We also review opportunities for future research including: testing how self-organizing behavioural dynamics interact with other factors to mediate dominance hierarchy formation, measuring the long-term stability of social hierarchies and the factors that disrupt hierarchy stability, incorporating phenotypic plasticity into our understanding of the behavioural dynamics of hierarchies and considering how cognition coevolves with the behaviours used to establish and maintain hierarchies. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Pollinator community species richness dilutes prevalence of multiple viruses within multiple host species.

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 condition dependence and heritability of signaling and nonsignaling color traits in paper wasps.

Research on quality signal development typically focuses on signals with production costs; less is known about signals that lack production costs (conventional signals). Here, I test the condition dependence and heritability of the facial patterns that function as a conventional signal of quality in Polistes dominulus wasps. Two aspects of facial patterns are compared: (1) amount of black pigment (no signal value) and (2) disruption in the black pigment's distribution (quality signal). When colonies received the same diet, they produced offspring with similar facial patterns and both traits were heritable. However, experimental diet manipulation substantially influenced quality signal development. Wasps fed unlimited caterpillars developed more disrupted facial patterns than wasps fed a restricted diet. Further, signal heritability was obscured following the diet treatment. In contrast, the nonsignaling trait was not influenced by the diet treatment and remained heritable. Overall, the quality signal in P. dominulus is condition dependent and heritable, but its heritability may be obscured by environmental variance. The nonsignaling aspect of wasp facial patterns is not condition dependent and is more consistently heritable across environments. Therefore, the information a signal conveys may be influenced by its developmental properties rather than its honesty-ensuring cost or the pigments that constitute it.