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.     

Three new host species of the social wasp parasite, Polistes atrimandibularis (Hymenoptera, Vespidae)

Summary. We report that the social parasite Polistes atrimandibularis (Zimmermann) can exploit at least three more host species than previously described. One of these, P. associus, has never been reported as host of a social parasite. Our data show no constraints in host choice, indicating P. atrimandibularis is a generalist social parasite.     

Comparative morphology of Van der Vecht's organ in Polistes social parasites: host ecology and adaptation of the parasite

Camouflage strategies are common in insect social parasites. Being accepted into an alien colony as a dominant nestmate favours behavioural and morphological adaptations to mimic a specific odour. In Polistes social parasites, abdominal tegumental glands are involved in this camouflage strategy. These glands secreting cuticular hydrocarbons are connected with a modified cuticular area of the last gastral sternite of female wasps, named Van der Vecht's organ, whose secretion is involved in rank and dominance recognition. The size of this exocrine area has been demonstrated to be under selective pressure in Polistes, as a response to an efficient dominance recognition. Because chemical and behavioural integration differs between parasitic species, we carried out a comparison of Van der Vecht's organ size between the three Polistes social parasites and their respective hosts. The parasites Polistes sulcifer and Polistes semenowi, capable of a rapid chemical mimicry and specialized to exploit a lowland host, also show an enlarged Van der Vecht's organ. Conversely, the parasite Polistes atrimandibularis, specialized on a mountain species and showing a slow chemical integration, has a smaller organ. The time available for the parasite to tune up its chemical mimicry, before the emergence of workers to be accepted as a dominant nestmate, appears to be the most important selective pressure acting on the size of this abdominal organ. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013 , 109 , 313–319.     

Being a parasitoid of parasites: host finding in the tick wasp Ixodiphagus hookeri by odours from mammals

The parasitic wasp Ixodiphagus hookeri Howard (Hymenoptera: Encyrtidae) parasitizes larvae and nymphs of a number of tick species worldwide. Ticks themselves are parasitic on vertebrate hosts. To study the specificity and reliability of vertebrate odours used by I. hookeri for host location, we conducted bioassays in a four‐chamber olfactometer. Wasps were arrested by carbon dioxide and by odours from roe deer faeces and odours from hair of roe deer and wild boar. Odours from faeces of cattle, rabbit, and field mouse as well as odours from hair of cattle and field mouse had no effect. Odours from faeces of the host tick species Ixodes ricinus L. (Acari: Ixodidae) were attractive only up to a distance of 1 cm. Thus, I. hookeri reacts to general (carbon dioxide) and specific vertebrate odours from wild boar and deer. Examination of freshly shot specimens demonstrates that deer and wild boars are infested with a sufficient number of tick nymphs to tap the full reproductive potential of an I. hookeri female, which makes cues from these mammal species reliable. These results indicate that I. hookeri locates its hosts using specific and reliable mammal odours and that ticks are parasitized on their vertebrate hosts. The implications of this host‐finding strategy and its benefits for the parasitoid are discussed.     

Age and social experience induced plasticity across brain regions of the paper wasp Polistes fuscatus

Developmental studies of brain volumes can reveal which portions of neural circuits are sensitive to environmental inputs. In social insects, differences in relative investment across brain regions emerge as behavioural repertoires change during ontogeny or as a result of experience. Here, we test the effects of maturation and social experience on morphological brain development in Polistes fuscatus paper wasps, focusing on brain regions involved in visual and olfactory processing. We find that mature wasps regardless of social experience have relatively larger brains than newly emerged wasps and this difference is driven by changes to mushroom body calyx and visual regions but not olfactory processing neuropils. Notably, social wasps invest more in the anterior optic tubercle (AOT), a visual glomerulus involved in colour and object processing in other taxa, relative to other visual integration centres the mushroom body calyces compared with aged socially naive wasps. Differences in developmental plasticity between visual and olfactory neuropil volumes are discussed in light of behavioural maturation in paper wasps, especially as it relates to social recognition. Previous research has shown that P. fuscatus need social experience to develop specialized visual processing of faces, which is used to individually recognize conspecifics. The present study suggests that the AOT is a candidate brain region that could mediate facial processing in this species.     

Not only cuticular lipids: first evidence of differences between foundresses and their daughters in polar substances in the paper wasp Polistes dominulus

Several studies have shown that differences in the relative abundance of cuticular hydrocarbons occur between reproductives and non-reproductives in many social insects. These differences also exist between Polistes dominulus foundresses and their first emerged daughters (usually indicated as workers), but they gradually disappear when workers from orphaned colonies develop their ovaries and assume a reproductive role in the colony. However, hydrocarbons are not the exclusive components of cuticular layer of wasps. Mass-spectrometry analysis of cuticular methanol extracts from Polistes paper wasps showed a complex pattern of polar substances, partly or totally proteinaceous in nature. We found that these compounds, ranging from 918 to 2679 Da, showed a clear caste differentiation between foundresses and their first emerged daughters (usually indicated as "workers"), both in queen-right and in orphaned colonies. Conversely to hydrocarbons, workers from orphaned colonies maintain a significant difference from foundresses in the pattern of the medium molecular weight (MW) polar compounds obtained by MALDI-TOF. On the basis of such results we hypothesize that a reliable cue to identify foundresses from daughters, and not only their reproductive status, may exist in Polistes wasps. Although the great majority of previous work on social insect communication has focused on cuticular hydrocarbons, our findings suggest that the medium MW component of cuticular substances may be involved in recognition.     

Intra‐specific body size variation in Polistes paper wasps as a response to social parasite pressure

1. Like avian brood parasites, obligate insect social parasites exploit the parental care of a host species to rear their brood, causing an evident loss of host reproductive success. This fitness cost imposes selective pressure on the host to reduce the parasite effect. A possible outcome of an evolutionary arms race is the selection of host morphological counter‐adaptations to resist parasite attacks. 2. We studied host–parasite pairs of Polistes wasps in which the fighting equipment of the parasite's body allows it to enter the host colony. 3. We searched for host morphological traits related to fighting ability that could be considered counter‐adaptations. As a host–parasite co‐evolutionary arms race can only occur where the two lineages co‐exist, we compared morphological traits of hosts belonging to populations with or without parasite pressure. We report that host foundresses belonging to populations under strong parasite pressure have a larger body size than those belonging to populations without parasite pressure. 4. Behavioural experiments carried out to test if an increase in host body size is useful to oppose parasite usurpation show that large body size foundresses exhibit a greater ability of nest defence.     

Colony membership is reflected by variations in cuticular hydrocarbon profile in a Neotropical paper wasp, Polistes satan (Hymenoptera, Vespidae)

Nestmate recognition is one the most important features in social insect colonies. Although epicuticular lipids or cuticular hydrocarbons have both structural and defensive functions in insects, they also seem to be involved in several aspects of communication in wasps, bees and ants. We analyzed and described for the first time the cuticular hydrocarbons of a Neotropical paper wasp, Polistes satan, and found that variation in hydrocarbon profile was sufficiently strong to discriminate individuals according to their colony membership. Therefore, it seems that small differences in the proportion of these compounds can be detected and used as a chemical-based cue by nestmates to detect invaders and avoid usurpation.     

Reproductivity of early males of the temperate paper wasp Polistes rothneyi iwatai

In Polistes paper wasps, haploid early males can mate with early emerging females and leave viable offspring. In contrast, diploid early males are eventually sterile because they contribute triploid offspring via diploid sperm. Clarifying the ploidy of early males is important for determining whether early male production is a reproductive strategy for the species. We examined the mating behavior and the ploidy of early males in the Japanese paper wasp, Polistes rothneyi iwatai van der Vecht. Thirteen early males from four colonies were all diploid. Two of the nine early males (22.2%) attempted to mate with females, but only one individual (11.1%) was successful (the female's spermatheca contained spermatozoa). These results suggest that although most early males of P. rothneyi iwatai do not produce offspring, their mating may be linked to the occasional production of triploid females.     

Reproductive plasticity in Polistes paper wasp workers and the evolutionary origins of sociality

Regulatory pathways in solitary species provide the raw materials for the evolution of sociality. Therefore, comparing the mechanisms that mediate reproductive plasticity in social species and their solitary ancestors can provide insight into the evolutionary origin of sociality. In many solitary insects, the effect of juvenile hormone (JH) on fertility is mediated through the fat body; individuals in good physical condition show a stronger fertility response to JH than individuals in poor physical condition. Here, we test whether a similar, condition-dependent JH response mediates fertility in workers of the primitively eusocial Polistes dominulus wasps. We test how body weight, JH, and adult nutrition influence worker ovarian development. Both JH-treatment and adult nutrition dramatically increased ovarian development. Body weight also influenced ovarian development, as large workers developed more eggs than smaller workers. Body weight and fat are strongly linked in P. dominulus workers, so these results suggest that the fat-dependent JH responsiveness common in solitary insects is conserved in social wasps. The simple, ancestral relationship between reproductive investment and physical condition may facilitate cooperation by allowing workers to adaptively allocate energy into reproduction based on their probability of successfully becoming a queen.     

Phylogeny and historical biogeography of the paper wasp genus Polistes (Hymenoptera: Vespidae): implications for the overwintering hypothesis of social evolution

The phylogeny of the paper wasp genus Polistes is investigated using morphological and behavioural characters, as well as molecular data from six genes (COI, 12S, 16S, 28S, H3, and EF1‐α). The results are used to investigate the following evolutionary hypotheses about the genus: (i) that Polistes first evolved in Southeast Asia, (ii) that dispersal to the New World occurred only once, and (iii) that long‐term monogyny evolved as an adaptation to overwintering in a temperate climate. Optimization of distribution records on the recovered tree does not allow unambiguous reconstruction of the ancestral area of Polistes. While the results indicate that Polistes dispersed into the New World from Asia, South America is recovered as the ancestral area for all New World Polistes: Nearctic species groups evolved multiple times from this South American stock. The final tree topology suggests strongly that the genus first arose in a tropical environment, refuting the idea of monogyny as an overwintering adaptation.     

Division of labour in colony defence against vertebrate predators by the social wasp Polistes fuscatus

In this study I examined how the paper wasp, Polistes fuscatus, defends a colony when faced with a vertebrate attack. I looked for a division of labour in defensive behaviour within a colony and examined whether this behaviour changes over the colony cycle. The colonies were presented with a model of an adult red-winged blackbird, Agelaius phoeniceus, and a speaker that vibrated the comb. There was a pronounced division of labour in the defence against vertebrate predators within a colony. The queen was consistently the most aggressive individual in the colony. The subordinate foundresses and workers both became more aggressive towards a vertebrate predator as they aged. Gynes and males did not participate in colony defence. The level of aggression in colony members of P. fuscatus appears to be related to the reproductive investment of the colony. Copyright 2000 The Association for the Study of Animal Behaviour.     

Social wasps without workers: geographic variation of caste expression in the paper wasp Polistes biglumis

In primitively eusocial insects, caste expression is flexible. Even though Polistes species are well known to show social trait variation (e.g., worker vs. gyne) depending on ecological context, loss of worker caste in some populations of a eusocial, worker-containing species has never been documented. We report first data on geographic variation in caste expression in Polistes biglumis. We compared physiological and behavioural traits of the first female offspring from four populations that experience different climatic conditions and social parasite prevalence. We demonstrated that the first female offspring to emerge in cold areas with high parasite prevalence had more abundant, gyne-like fat bodies and exhibited lower foraging effort, in comparison to the first female offspring produced in warm areas with low parasite prevalence. Thus, the populations under severe environmental conditions produced a totipotent female offspring and suppressed worker production, whereas the population living in less extreme environmental conditions produced worker-like females as first female offspring and gyne-like females as offspring that emerged later. The existence of mixed social strategies among populations of primitively eusocial species could have important consequences for the study of social evolution, shedding light on the sequence of steps by which populations evolve between the extremes of solitary state and eusocial state.