Autumnal Helpers of Polistes dominulus Represent a Distinct Behavioural Phenotype
Abstract and Figures
Cini, A. & Dapporto, L. 2009: Autumnal helpers of Polistes dominulus represent a distinct behav-ioural phenotype. — Ann. Zool. Fennici 46: 423–430. Division of labour is a major feature of insect societies. Behavioural differences can be present also during non-colonial stages of the life cycle, when it is difficult to discrimi-nate between distinct behavioural phenotypes and by-products of differences in overall activity levels. We used the social wasp Polistes dominulus to address this issue. In pre-hibernating aggregations some individuals (helpers) perform external tasks by col-lecting food and providing it to cluster mates. Such helpers have been so far identified using only a descriptive approach, and their behaviour was not disentangled from a possible higher level of overall activity. Here we provide an operational definition of the helper's trait and we then compare behavioural patterns of helpers and non helpers, verifying that helpers actually represent a peculiar behavioural phenotype. Our result expands knowledge on the caste differentiation issue in Polistes wasps and on the assessment of behavioural phenotypes in a non-colonial context.
Figures - uploaded by Alessandro Cini
Author content
All figure content in this area was uploaded by Alessandro Cini
Content may be subject to copyright.
... All Ritualized Dominance Interactions (hereafter RDI) that occurred between any two individuals were recorded, noting the identities of the actor (i.e. the wasp that started the interaction) and the recipient. RDI includes domination acts, in which one wasp (the dominant individual) climbs on and antennates another wasp (the subordinate), and trophallaxis, i.e. liquid food exchange by mouth-to-mouth contact (Cini and Dapporto 2009;Pardi 1948) (Fig. 1b). Both interactions are directional, with dominant individuals (the actor) performing and not receiving RDI, and subordinate individuals receiving and not performing RDI. ...
... During trophallaxis the liquid is regurgitated by the subordinate individual toward the dominant one. To maintain the directionality of dominance, for trophallaxis the actor was considered the individual which received the liquid (i.e. the dominant individual) and the recipient the individual who gave the liquid (the subordinate one) [as in (Cini and Dapporto 2009)]. ...
The strong coevolutionary arms race between social parasites and their hosts has dramatically shaped the life-history traits of both parties. One of the main strategies exhibited by hosts in response to parasitism is reproduction by host workers. We lack a mechanistic understanding of how these defence strategies unfold and, specifically, whether hosts exhibit more subtle strategies to reduce the costs of parasitism from the outset. Here we test the hypothesis that there are both behavioural and neurogenomic signatures of worker responses to parasitism, prior to overt expression in the form of egg-laying; we test this using the social parasite—social host system of the paper wasps Polistes sulcifer-Polistes dominula. We characterized individual workers’ position within the social interaction network of queenright and host colonies immediately after parasite usurpation, weeks before the workers’ reproductive rebellion is evident. Parasitism influenced network centrality measures, with workers in parasitized colonies showing increased connectedness and centrality compared to those in unparasitized ones. Next, we quantified brain gene expression levels for five genes related to physiological and behavioural phenotypes in Polistes wasps. The gene Imaginal disc growth factor (Idgf4), thought to be responsive to changes in the social environment, was significantly down-regulated in workers from parasitized colonies; this may be an indication that parasitized workers are anticipating a shift toward a less worker-like phenotype in preparation for their reproductive rebellion. Our results provide the first evidence of early behavioural and neurogenomic responses of host workers toward the presence of an inquiline social parasite in a social insect.
... Reproductive individuals, males and gynes, emerge only later in the season, from the end of July (reproductive phase) (Reeve, 1991). Mating occurs outside of the colony at the end of summer (Beani, 1996); mated females overwinter in large groups and then start new colonies in the following spring (Dapporto and Palagi, 2006;Cini and Dapporto, 2009). ...
Nestmate recognition, i.e., the ability to discriminate nestmates from foreign individuals, is a crucial feature of insect societies, and it has been traditionally considered to be predominantly based on chemical cues. Recent empirical evidence, however, suggests a relevant plasticity in the use of different communication channels according to cue availability and reliability in different contexts. In particular, visual cues have been shown to influence various types of social recognition in several social insects, but their role in nestmate recognition is still under-investigated. We tested the hypothesis of plasticity in the use of visual and chemical recognition cues in the primitively eusocial wasp Polistes dominula, in which the availability and reliability of recognition cues vary across the colony cycle. Indeed, before the emergence of workers, P. dominula colonies are rather small (one to few individuals), and the variability in the facial pattern might allow resident wasps to use visual cues for nestmate recognition. After workers' emergence, the increase in the number of colony members reduces the reliability of visual cues, thus leaving chemical cues as the most reliable nestmate recognition cues. We thus predict a differential use of chemical and visual cues along colony life. We experimentally separated visual and chemical cues of nestmates and non-nestmates and presented them alone or in combination (with coherent or mismatched cues) to resident wasps to test which communication channel was used in the two stages and, in case, how visual and chemical cues interacted. Our results show, for the first time in a social insect, the differential use of visual and chemical cues for nestmate recognition in two different phases of colony, which supports the hypothesis of a plastic, reliability-based use of recognition cues in this species according to the different colonial contexts.
... The aim of this long-term study was to assess the influence of X. vesparum on the phenotype of P. dominulus females. We focused on wasp overwintering aggregations (Dapporto et al. 2006a;Cini & Dapporto 2009), comprising both infected and uninfected P. dominulus females, during 7 years. First, we hypothesized that parasites subtly exploit the gregarious behaviour of the host, here, the clustering tendency of wasps outside the colony, to survive until spring: we expected that stylopized wasps should initiate aggregations when colonies fall down, in August, and that they lengthen this gregarious phase of host inactivity until spring. ...
The macroparasite Xenos vesparum affects both the behaviour and the physical traits of its host, the social wasp Polistes dominulus. Female wasps, if parasitized, do not perform any social tasks and desert the colony to gather at specific sites, where the parasite mates; at the end of summer they form prehibernating clusters joined by healthy future queens to overwinter. Parasitized wasps become highly gregarious. In April, healthy wasps leave the aggregations to found new colonies, while parasitized wasps remain in overwintering groups and release parasites to infect wasp larvae only later in the season. We studied the prolonged gregarious behaviour of parasitized wasps and analysed the morphology of parasitized and healthy wasps in aggregations collected over a 7-year period to determine whether the parasite affects host size, wing symmetry, ovarian development and lipid stores. All parasitized wasps were smaller and had undeveloped ovaries and more wing fluctuating asymmetry than unparasitized wasps, irrespective of time of year, parasite load and parasite sex. If infected only by one or two X. vesparum females, the wasps had large fat bodies, which could facilitate their overwintering. In contrast, wasps infected by at least one male parasite had little lipid and died at the end of the summer. Thus, X. vesparum, may play a role in the fate of its host, by exploiting wasps' tendency to form aggregations outside the colony and by altering its caste system, nutrient allocation, diapause timing and life span to achieve its own reproduction and dispersal.
... Polistes' worker/queen caste determination occurs in the adult stage [12] and may be determined by constraints on breeding [13] such as physiological costs of work undertaken by workers [14] and/or behavioral dominance of workers by queens [15]. Worker caste determination is not random, however, as Polistes colonies are characterized by a temporal pattern in which workers precede non-workers of the same generation [9,16,17], although both early non-workers [18] and late workers [19,20] may occur at low frequencies [9,21]. Hunt and Amdam [21] recognized that any adult female Polistes can become either a worker or queen and that worker/queen castes are determined among adults, but they proposed a specific hypothesis for a process whereby larval developmental divergence yields females reared early in the colony cycle that are biased to become workers and females reared later in the colony cycle that are biased to become gynes. ...
Polistes paper wasps are models for understanding conditions that may have characterized the origin of worker and queen castes and, therefore, the origin of paper wasp sociality. Polistes is "primitively eusocial" by virtue of having context-dependent caste determination and no morphological differences between castes. Even so, Polistes colonies have a temporal pattern in which most female larvae reared by the foundress become workers, and most reared by workers become future-reproductive gynes. This pattern is hypothesized to reflect development onto two pathways, which may utilize mechanisms that regulate diapause in other insects. Using expressed sequence tags (ESTs) for Polistes metricus we selected candidate genes differentially expressed in other insects in three categories: 1) diapause vs. non-diapause phenotypes and/or worker vs. queen differentiation, 2) behavioral subcastes of worker honey bees, and 3) no a priori expectation of a role in worker/gyne development. We also used a non-targeted proteomics screen to test for peptide/protein abundance differences that could reflect larval developmental divergence. We found that foundress-reared larvae (putative worker-destined) and worker-reared larvae (putative gyne-destined) differed in quantitative expression of sixteen genes, twelve of which were associated with caste and/or diapause in other insects, and they also differed in abundance of nine peptides/proteins. Some differentially-expressed genes are involved in diapause regulation in other insects, and other differentially-expressed genes and proteins are involved in the insulin signaling pathway, nutrient metabolism, and caste determination in highly social bees. Differential expression of a gene and a peptide encoding hexameric storage proteins is especially noteworthy. Although not conclusive, our results support hypotheses of 1) larval developmental pathway divergence that can lead to caste bias in adults and 2) nutritional differences as the foundation of the pathway divergence. Finally, the differential expression in Polistes larvae of genes and proteins also differentially expressed during queen vs. worker caste development in honey bees may indicate that regulatory mechanisms of caste outcomes share similarities between primitively eusocial and advanced eusocial Hymenoptera.
Contrasting phenotypes arise from similar genomes through a combination of losses, gains, co-option and modifications of inherited genomic material. Understanding the molecular basis of this phenotypic diversity is a fundamental challenge in modern evolutionary biology. Comparisons of the genes and their expression patterns underlying traits in closely related species offer an unrivaled opportunity to evaluate the extent to which genomic material is reorganized to produce novel traits. Advances in molecular methods now allow us to dissect the molecular machinery underlying phenotypic diversity in almost any organism, from single-celled entities to the most complex vertebrates. Here we discuss how comparisons of social parasites and their free-living hosts may provide unique insights into the molecular basis of phenotypic evolution. Social parasites evolve from a eusocial ancestor and are specialized to exploit the socially acquired resources of their closely-related eusocial host. Molecular comparisons of such species pairs can reveal how genomic material is re-organized in the loss of ancestral traits (i.e., of free-living traits in the parasites) and the gain of new ones (i.e., specialist traits required for a parasitic lifestyle). We define hypotheses on the molecular basis of phenotypes in the evolution of social parasitism and discuss their wider application in our understanding of the molecular basis of phenotypic diversity within the theoretical framework of phenotypic plasticity and shifting reaction norms. Currently there are no data available to test these hypotheses, and so we also provide some proof of concept data using the paper wasp social parasite/host system (Polistes sulcifer—Polistes dominula). This conceptual framework and first empirical data provide a spring-board for directing future genomic analyses on exploiting social parasites as a route to understanding the evolution of phenotypic specialization.
After mating and leaving the maternal nest, gynes of several paper wasp species living in temperate climates aggregate in sheltered places. Some authors state that the social stage of paper wasps ends at the beginning of autumn. Here, we show that the death of workers and the abandonment of the nest do not imply the end of the social phase in Polistes dominulus, and that many social interactions also occur in pre-hibernating clusters. In particular, a few individuals performed external tasks, i.e. foraging and providing food via trophallaxis to other wasps. These "helpers" died early in winter, as workers generally do, but they were fertilised like gynes.
We present a simple, general model of how the optimal level of intragroup aggression should vary in different social contexts. A key component of this model is the Value of the recipient of aggression to a potential aggressor (i.e., the ratio of expected long-term group productivity with the recipient present to the expected group productivity with the recipient absent). The recipient's Value measures its contribution to group reproductive success. We demonstrate theoretically that if aggression increases the aggressor's share of the group's expected total reproductive output, but at the same time decreases the magnitude of this overall reproductive output, then the optimal level of aggression toward a recipient will decrease with increasing recipient's value. This proof establishes a rigorous theoretical connection between the level of aggression within a group and the benefits of belonging to such a group and can be tested by experimentally manipulating the values of group members to each other. We test, and thus illustrate the utility of, this model by examining aggression within experimentally-manipulated foundress associations of social wasps. We show that the value of co-foundresses to each other in the social wasp Polistes fuscatus lies in their ability to provide insurance against colony failure caused by the loss of all tending foundresses. Removals of worker-destined eggs and pupae, which increase the value of co-foundresses, both lead to significant reductions in aggression by the dominant foundress, despite the fact that the immediate, selfish benefits of competitive aggression should increase when empty brood cells are present. Removal of reproductive-destined eggs, which does not affect co-foundress value, but increases the benefits of selfish aggression, causes a significant increase in aggression by beta foundresses. Finally, wing reduction of subordinate co-foundresses significantly increases aggression by dominant foundresses, as expected since the subordinate's value is reduced. Our results indicate that foundress aggression is sensitive to the value of future cooperation, as predicted by the optimal aggression model. The model may apply widely to both invertebrate and vertebrate societies.
The asymptotic theory of the distribution of the latent roots and vector of principal components analysis (PCA) of samples has hitherto been tied t multivariate normal (MVN) distributions. However, much real behavior dat are not normal. The results of the present study show, using arguments base on Monte Carlo methods, that if there is enough meaningful structure in th population, then PCA of samples of data with multivariate non-normal (NN distribution may provide answers relative to the "true" population principal components (PC) of comparable reliability to PCA of samples of MVAT data.