Polistes Sulcifer Research Articles

Social parasitism and the molecular basis of phenotypic evolution.

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.

Facial markings in the social cuckoo wasp Polistes sulcifer: No support for the visual deception and the assessment hypotheses

Insect social parasites have to conquer a host colony by overcoming its defensive barriers. In addition to increased fighting abilities, many social parasites evolved sophisticated sensory deception mechanisms to elude host colonies defenses by exploiting host communication channels. Recently, it has been shown that the conspicuous facial markings of a paper wasp social parasite, Polistes sulcifer, decrease the aggressiveness of host foundresses. Two main hypotheses stand as explanations of this phenomenon: visual sensory deception (i.e. the black patterning reduces host aggression by exploiting the host visual communication system) and visual quality assessment (i.e. facial markings reduce aggressiveness as they signal the increased fighting ability of parasites). Through behavioral assays and morphological measurements we tested three predictions resulting from these hypotheses and found no support either for the visual sensory deception or for the quality assessment to explain the reduction in host aggressiveness towards the parasite. Our results suggest that other discrimination processes may explain the observed phenomenon.

Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp

Insect social parasites, like other parasites, may benefit from inhibiting their host from reproducing (complete or partial parasitic castration) because they can then exploit more of the host’s resources for their own reproduction. In particular, social parasites that kill or expel the host queen need to prevent host workers from reproducing; this is a common worker response to the absence of their queen. Indeed, host workers would benefit from detecting the presence of the parasite and investing in direct and indirect fitness. Studying whether and how social parasites control host worker reproduction can provide information about the degree of integration of the parasite in the host colony and help identify factors regulating workers’ reproductive decisions in social insects. We investigated whether the paper wasp social parasite, Polistes sulcifer, suppresses Polistes dominula (host) worker reproduction as efficiently as the dominant host female does in queen-right colonies by comparing worker reproductive efforts in parasitized and non-parasitized (control) colonies. Our results show that 6 weeks after usurpation of their colony by the social parasite, parasitized workers (1) had more developed ovaries than control workers and (2) laid more eggs as soon as the opportunity arose. This reproductive readiness of parasitized workers was not apparent 2 weeks after colony usurpation. This suggests that P. dominula workers have evolved means to react to social parasitism, as occurs in some ants, and that the parasite has only limited control over host reproduction.

Venom volatiles of the paper wasp social parasite Polistes sulcifer elicit intra-colonial aggression on the nest of the host species Polistes dominulus

Insect social parasites rely on host workers to rear and protect their own brood. To conquer a host colony, a parasite must overcome the defensive mechanisms of the host, often by exploiting its chemical communication system. A widespread strategy involves the production of specific allomones (the so-called “propaganda pheromones”) to facilitate the usurpation process by manipulating the defensive behavior of the host. Polistes sulcifer is the obligate and permanent social parasite of the congeneric paper wasp Polistes dominulus. In this study, we investigated if the venom volatiles, well known to be alarm pheromones in the host species, could be used by the parasite to manipulate the host defense. We thus performed laboratory bioassays, to evaluate the possible effect of the venom volatile compounds of the parasite on the host. Our results show that host colony members reacted to the venom volatiles extract of the parasite with an increase in intra-colonial aggression compared to the reaction induced by the venom volatiles extract of the host foundress. Besides, a re-analysis of previously published chemical data showed that the parasite venom volatiles profile differs from that of the host: the spiroacetals are absent, whilst the amides are very abundant in the parasite venom when compared with that of the host. Similar to other insect social parasites, Polistes wasp parasites might be able to increase their invasion success by using venom volatile pheromones to distract the host defenders.

Recognition of a paper wasp social parasite by its host: evidence for a visual signal reducing host aggressiveness

Obligate social parasite insects are specialized in exploiting the parental service of the workers of another social species by invading their colonies. As social insects are usually aggressive towards intruders, social parasites have to circumvent the host’s nestmate recognition system to enter the host colony successfully. Many studies on paper wasps have shown that, after host nest invasion, Polistes social parasites change their chemical profile to match the host’s odour, thus allowing their acceptance into its colony. However, a social parasite’s usurpation strategy may benefit from signals that reduce or eliminate the aggression of the host. We used lure presentation experiments to investigate whether Polistes sulcifer , a social parasite of the paper wasp P. dominulus , is able to reduce the aggressive reaction of its host. We found that the parasite lure elicited lower host aggressiveness than the conspecific lure, suggesting that parasite species have evolved cues able to inhibit host aggressiveness. We investigated separately the effects of chemical and visual patterns on host aggressiveness. The lower host reaction to the parasite lure was not due to chemical cues, but was elicited by the visual facial pattern of the parasite. Experimental manipulation of this visual pattern demonstrated that the black lower part of the clypeus of the parasite is the trait able to reduce host aggression. This pattern can be considered an honest signal since it visually amplifies the mandibular width, giving information about the parasite’s dangerousness.

Spring Usurpation Restlessness: A Wasp Social Parasite Adapts its Seasonal Activity to the Host Cycle

AbstractIn animals, restlessness is a strategy to fulfil a goal within a narrow seasonal window when ecological and physiological constraints require the performance of certain fundamental events. Although restlessness can be expected in parasitic species that have their biological cycle similar to that of the host, no ‘urge to parasitize’ has thus far been demonstrated in any host‐parasite pair. The paper wasp, Polistes sulcifer, is a social parasite that has lost the nest‐building ability and marked by the absence of the worker caste; it depends on a congeneric host species to reproduce. Host colony usurpation is successful when it occurs in a well‐defined seasonal window. The short time available for host‐nest usurpation might lead to parasite restlessness that overlaps this period. Under controlled laboratory conditions, we demonstrated that the parasite females exhibit ‘usurpation restlessness’ during the period in which field usurpations occur. Additional experiments showed that both this period and laboratory temperature influence the parasite’s ‘urge to usurp’.

Rank integration in dominance hierarchies of host colonies by the paper wasp social parasite Polistes sulcifer (Hymenoptera, Vespidae)

In multiple-foundress nests of the wasp Polistes dominulus, dominance hierarchies are established among foundresses, and only the dominant (=alpha) individual lays eggs. The alpha female can be distinguished from subordinate females and workers on the basis of the proportions of some hydrocarbons present on the cuticle, suggesting that chemical signaling of her reproductive status could occur. P. dominulus is also the host species of the obligate social parasite Polistes sulcifer. After aggressively usurping host colonies and behaviorally replacing the host alpha female, parasites are characterized by a change in the proportions of their cuticular hydrocarbons to match that of the host cuticular profile at both species and colony levels. In the current study, we demonstrate that P. sulcifer queens also modify their cuticular hydrocarbon proportions after usurpation to match that of the host alpha female. Parasite females, therefore, acquire the dominant rank in host colonies both reproductively and chemically by mimicking the typical alpha profile of the host. Parasite females were not able to fully inhibit ovary development in host foundresses, and 10 days after usurpation, parasites, alpha and beta foundresses show similar chemical profiles and ovarian development.

Recognition of social parasites as nest-mates: adoption of colony-specific host cuticular odours by the paper wasp parasite Polistes sulcifer.

Colonies of the polistine wasp Polistes dominulus are parasitized by the permanent worker-less social parasite Polistes sulcifer. After usurpation of the host colony, parasite females are characterized by a change in the relative proportions of their cuticular hydrocarbons to match those of the host species. In this paper we present evidence from field data and laboratory experiments that P. sulcifer females adopt a colony-specific host odour that facilitates their acceptance by host females of the usurped colony. Presentation experiments demonstrate that parasite females are recognized as foreign individuals by workers of other parasitized nests. We show that the modification of parasite cuticular compounds is sufficient for this recognition. This provides evidence that, after invasion, P. sulcifer queens do not require appeasement or propaganda substances for their acceptance by host colonies. Furthermore, multivariate discriminant analysis of the cuticular hydrocarbon proportions of the parasites after usurpation assigns the parasites together with P. dominulus females of their own host colony. To the authors' knowledge, this is the first confirmation that social parasites adopt colony-specific host odours.

Olfactory cues in host nest detection by the social parasite Polistes sulcifer (Hymenoptera, Vespidae)

Sometimes the nests of the paper wasp Polistes dominulus are parasitized by the obligate social parasite Polistes sulcifer. It is not known how, in the spring, this parasite searches for established nests of its host species. This study investigates the capacity to detect the host nest by olfactory cues alone. In laboratory experiments P. sulcifer females were allowed to choose different options hidden from view: host nest and dummy, various portions of the host nest (larvae, pupae and material), nests or immature brood pertaining to different sympatric species ( P. dominulus, P. nimpha and P. gallicus). The parasites proved to be capable of perceiving nest odour and of discriminating between different species of Polistes. The odour of the immature host brood, rather than the nest material, elicits the greatest response in the parasites.

Host nest preference and nest choice in the cuckoo paper wasppolistes sulcifer (Hymenoptera: Vespidae)

Polistes sulcifer is a cuckoo paper wasps, an obligate social parasite which must usurp a colony of another species in order to reproduce. Field data show thatP. sulcifer females usurp exclusively nests belonging to one species only (P. dominulus). Moreover, they are more frequently found on large and puparich nests. A series of laboratory trials, in which parasite females were offered a binary choice of nests with different characteristics, confirm both the species specificity betweenP. sulcifer andP. dominulus and the parasite's preference to usurp larger nests containing pupae. The data support the hypothesis thatP. sulcifer females choose between available nests. The biological meaning of these findings is discussed.