Lack of conflict during queen production in the social wasp Vespula maculifrons

Social insects display extreme cooperative and helping behaviours. However, social insect colonies are also arenas of intense competitive interactions. One particularly important matter over which colony members may compete centres on the development of sexual offspring. Specifically, colony members may engage in selfish behaviours leading to reproductive competition, whereby individuals either strive to develop as sexuals or assist kin so that close relatives emerge as new reproductives. We investigated whether reproductive competition occurred in the polyandrous social wasp Vespula maculifrons. We genotyped V. maculifrons workers and new queens at eight polymorphic microsatellite loci to determine if larvae of particular genotypes were reared as gynes more frequently than expected by chance. However, we found no significant evidence of reproductive competition in this species. The proportional contributions of males to workers and new queens did not vary within colonies. Moreover, male reproductive skew did not differ between workers and new queens. Finally, novel statistical techniques uncovered no evidence of patriline reversal, the phenomenon whereby males that contribute little to worker production contribute substantially to new queen production. Consequently, we conclude that individual level selection operating to increase the frequency of selfish behaviours that would lead to reproductive competition has been nullified by colony-level selection acting to maintain colony efficiency and cooperation.     

Detecting selection on morphological traits in social insect castes: the case of the social wasp Vespula maculifrons

Highly social insects dominate terrestrial ecosystems because society members belong to discrete castes that undertake distinct tasks. The distinct functional roles of members of different castes may lead to divergent selective regimes, which may ultimately lead to morphological specialization and differentiation of the castes. This study used morphological and genetic analyses to identify traits that experienced caste‐specific selection in the social wasp Vespula maculifrons (Buysson, 1905). Traits putatively under selection were identified based on their degree of caste dimorphism, levels of variability, strength of correlations with other traits, and patterns of allometric scaling. Analyses of trait characteristics suggested that queen thorax length, thorax width, and possibly mass, have experienced queen‐specific selection. Additionally, trait dimorphism and intercaste phenotypic correlation values were negatively correlated, as expected if some morphological traits were subject to selection, leading to alternate phenotypic optima in the two castes. Overall, our analyses demonstrate how techniques used to identify selection between dimorphic groups can be applied to social species with distinct castes. In addition, our analyses suggest the operation of selection may be stronger in reproductive than in non‐reproductive castes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 93–102.     

The spread of the social wasp,Vespula germanica,in Australia

Abstract

Between 1977 and 1989 the social wasp Vespula germanicacolonised mainland Australia and became established in New South Wales, Victoria, and South Australia. Accidental transport between towns is the main mechanism of spread. In many towns wasp nests have not been detected until they became widespread; therefore, eradication is difficult Successful eradication has, however, been achieved in many other towns.

Nesting places vary considerably among localities but relatively little among years at anyone locality. Peak wasp abundance occurs between January and April. Control of V. germanica nests costs Australia an estimated $600,000 (Aust. $) annually.     

Application of microsatellite primers for the social wasp Polistes to another social wasp genus, Parapolybia, to estimate genetic relationships among nestmates

We tested 14 pairs of microsatellite primers that had been developed for the genus Polistes to assess their applicability for determining genetic structure in a colony of the genus Parapolybia. At least one of the 14 Polistes primer sets was useful for Parapolybia indica, and the locus identified by this primer set was highly polymorphic. Using this primer set, we estimated the average relatedness among female nestmates of Parapolybia indica to be 0.82 ± 0.05 (mean ± SE), indicating that in this species single mating is normal, although some cases of multiple mating was found.     

Mating frequency and mating system of the polygynous ant, Leptothorax acervorum

Multiple mating by queens (polyandry) and the occurrence of multiple queens in the same colony (polygyny) alter patterns of relatedness within societies of eusocial insects. This is predicted to influence kin-selected conflicts over reproduction. We investigated the mating system of a facultatively polygynous UK population of the ant Leptothorax acervorum using up to six microsatellite loci. We estimated mating frequency by genotyping 79 dealate (colony) queens and the contents of their sperm receptacles and by detailed genetic analysis of 11 monogynous (single-queen) and nine polygynous colonies. Results indicated that 95% of queens were singly mated and 5% of queens were doubly mated. The corrected population mean mating frequency was 1.06. Parentage analysis of adults and brood in 17 colonies (10 monogynous, 7 polygynous) showed that female offspring attributable to each of 31 queens were full sisters, confirming that queens typically mate once. Inbreeding coefficients, queen-mate relatedness of zero and the low incidence of diploid males provided evidence that L. acervorum sexuals mate entirely or almost entirely at random. Males mated to queens in the same polygynous colony were not related to one another. Our data also confirmed that polygynous colonies contain queens that are related on average and that their workers had a mixed maternity. We conclude that the mating system of L. acervorum involves queens that mate near nests with unrelated males and then seek readoption by those nests, and queens that mate in mating aggregations away from nests, also with unrelated males.     

Body temperature and thermoregulation in two species of yellowjackets,Vespula germanica and V. maculifrons

In spite of the abundance and broad distribution of social wasps, little information exists concerning thermoregulation by individuals. We measured body temperatures of the yellowjackets Vespula germanica and V. maculifrons and examined their thermoregulatory mechanisms. V. germanica demonstrated thermoregulation via a decreasing gradient between thorax temperature and ambient temperature as ambient temperature increased. V. maculifrons exhibited a constant gradient at lower ambient temperatures but thorax temperature was constant at high ambient temperatures. Head temperature exhibited similar patterns in both species. In spite of low thermal conductances, a simple heat budget model predicts substantial heat loads in warm conditions in the absence of thermoregulation. Both species regurgitated when heated on the head. A smaller volume of regurgitant was produced at lower head temperatures and a larger volume at higher head temperatures. Small regurgitations resulted in stabilization of head temperature, while large ones resulted in 4°C decreases in head temperature. Regurgitation was rare when wasps were heated upon the thorax. Abdomen temperature was 3–4°C above ambient temperature, and approached ambient temperature under the hottest conditions. No evidence was found for shunting of hot hemolymph from thorax to abdomen as a cooling mechanism. The frequency of regurgitation in workers returning to the nest increased with ambient temperature. Regurgitation may be an important thermoregulatory strategy during heat stress, but is probably not the only mechanism used in yellowjackets.Abbreviations M _b body mass - M _th thorax mass - T _a ambient temperature - T _ab abdomen temperature - T _b body temperature - T _h head temperature - T _th thorax temperature - C _t thermal conductance     

Distribution,dispersal and spread of the invasive social wasp (Vespula germanica) in Argentina

We studied the distribution and spread of the invasive social wasp Vespula germanica in Argentina, focusing on the contribution of queen dispersal to territorial expansion. Vespula germanica is native to Eurasia and has invaded several regions of the world, including Southern Argentina. Flight potential of field‐collected queens was measured using flight mills. Also, by means of an extensive survey we estimated the rate of spread by analysing the relationship between years since arrival and distance from the introduction locality. The mean distance flown by wasp queens in flight mills was 404.7 ± 140.8 m (mean ± SE, n = 59), while the rate of spread of V. germanica was estimated at 37.2 ± 2.1 km year^?1 (mean ± SE, n = 67), although faster towards the south. The observed spread rate of V. germanica wasps in Argentina confirms the invasive potential shown by several Hymenoptera species worldwide. Still, a stratified geographical expansion pattern does not match observed queen dispersal abilities, suggesting that human‐aided transport of hibernating queens is the central driver of the current distribution of these wasps. We suggest that despite several life‐history traits known for social insects that contribute to successful invasion, wasp spread must still rely strongly on human mediated pathways. This observation sheds light on those factors that are crucial for managing invasions of this and related pestiferous wasps.     

Resource allocation in a social wasp: effects of breeding system and life cycle on reproductive decisions

Organisms must make important decisions on how to allocate resources to reproduction. We investigated allocation decisions in the social wasp Vespula maculifrons to understand how social insects make reproductive choices. We first determined how annual colonies apportioned resources to growth and reproduction by analysing developing brood. In contrast to expectations, colonies invested in both growth (workers) and reproduction (males) simultaneously. In addition, colonies showed evidence of producing males in pulses and reversing their reproductive choices by decreasing investment in males late in the season. This reversal is consistent with theory suggesting that colonies decrease production in males if fitness of late emerging males is low. To further investigate reproductive decisions within colonies, we determined if the male mates of multiply-mated queens varied in their reproductive success over time. Sperm use by queens did vary over time suggesting that male success may depend on sperm clumping within the female reproductive tract. Finally, we tested if colony sex ratio conformed to expectations under kin selection theory that nestmate relatedness would positively correlate with investment in new queens if workers controlled sex allocation. Surprisingly, the proportion of queens produced by colonies was negatively correlated with nestmate relatedness, suggesting that allocation may be shaped by advantages arising from increased genetic diversity resulting from multiple mating by queens. Overall, our study suggests that the reproductive decisions of colonies are flexible and may depend both on environmental cues arising from energetic needs of the colony and genetic cues arising from mating behaviours of queens.     

Queen–worker conflict over male production and the sex ratio in a facultatively polyandrous bumblebee, Bombus hypnorum: the consequences of nest usurpation

Evolutionary conflicts among social hymenopteran nestmates are theoretically likely to arise over the production of males and the sex ratio. Analysis of these conflicts has become an important focus of research into the role of kin selection in shaping social traits of hymenopteran colonies. We employ microsatellite analysis of nestmates of one social hymenopteran, the primitively eusocial and monogynous bumblebee Bombus hypnorum, to evaluate these conflicts. In our 14 study colonies, B. hypnorum queens mated between one and six times (arithmetic mean 2.5). One male generally predominated, fathering most of the offspring, thus the effective number of matings was substantially lower (1-3.13; harmonic mean 1.26). In addition, microsatellite analysis allowed the detection of alien workers, those who could not have been the offspring of the queen, in approximately half the colonies. Alien workers within the same colony were probably sisters. Polyandry and alien workers resulted in high variation among colonies in their sociogenetic organization. Genetic data were consistent with the view that all males (n = 233 examined) were produced by a colony's queen. Male parentage was therefore independent of the sociogenetic organization of the colony, suggesting that the queen, and not the workers, was in control of the laying of male-destined eggs. The population-wide sex ratio (fresh weight investment ratio) was weakly female biased. No evidence for colony-level adaptive sex ratio biasing could be detected.     

The evolution of female multiple mating in social hymenoptera

Abstract The evolution of female multiple mating is a highly controversial topic, especially in social insects. Here we analyze, using comparative analyses and simulation models, the merits of two major contending hypotheses for the adaptive value of polyandry in this group. The hypotheses maintain that, respectively, the resulting genotypic diversity among offspring within a colony: (1) mitigates against the effects of parasites; or (2) favors adaptive division of labor. Only two of 11 phylogenetically uncontrolled comparative analyses supported an association between polyandry and the complexity of division of labor (measured here using worker caste polymorphism or polyethism) as proposed by hypothesis 2, and after controlling for phylogeny there were no significant associations. In contrast, a previous study demonstrated such an association for parasite load as expected under hypothesis 1. In addition, we used simulation models to track the spread of an initially rare allele for double mating in a population of single-mating alleles, thus analyzing the crucial first step from monandry to polyandry. We find that double mating evolves consistently under antagonistic coevolution given that parasites exert sufficient selection intensity. In contrast, selection for enhanced division of labor resulted in only an erratic appearance of polyandry in highly (and mostly negatively) autocorrelated environments where no coevolutionary dynamics were allowed. Together, we interpret these results to suggest that parasites, and the antagonistic coevolutionary pressures they exert, may play an important role in the evolution of polyandry in social hymenopteran populations.     

The costs and benefits of multiple mating in a mostly monandrous wasp

The taxonomically widespread nature of polyandry remains a puzzle. Much of the empirical work regarding the costs and benefits of multiple mating to females has, for obvious reasons, relied on species that are already highly polyandrous. However, this makes it difficult to separate the processes that maintain the current level of polyandry from the processes that facilitate its expression and initiated its evolution. Here we consider the costs and benefits of polyandry in Nasonia vitripennis, a species of parasitoid wasp that is “mostly monandrous” in the wild, but which evolves polyandry under laboratory culture conditions. In a series of six experiments, we show that females gain a direct fecundity and longevity benefit from mating multiply with virgin males. Conversely, mating multiply with previously mated males actually results in a fecundity cost. Sexual harassment may also represent a significant cost of reproduction. Harassment was, however, only costly during oviposition, resulting in reduced fecundity, longevity, and disrupted sex allocation. Our results show that ecological changes, in our case associated with differences in the local mating structure in the laboratory can alter the costs and benefits of mating and harassment and potentially lead to shifts in mating patterns.     

Attraction of the invasive social wasp,Vespula vulgaris,by volatiles from fermented brown sugar

The introduction of invasive social wasp species of the genus Vespula (Hymenoptera: Vespidae) to New Zealand has caused a major ecological problem, particularly in the beech forests (Nothofagus spp.) of the South Island, where they have destabilized the native bird and invertebrate biodiversity. New attractants are under investigation as part of a search for pest management solutions. Fermenting brown sugar has been previously reported as a social wasp attractant. This work was undertaken to identify compounds from fermented brown sugar attractive to social wasps. Raw fermented brown sugar was confirmed to be attractive in a field trial and 10 chemical compounds present in the headspace were positively identified by coupled gas chromatography‐mass spectrometry and synthetic references. During electroantennogram experiments, 3‐methyl‐1‐butanol, 3‐methylbutyl acetate, and ethyl hexanoate elicited high electrophysiological responses from Vespula vulgaris (L.) antennae. These compounds mediated attraction of V. vulgaris wasps in forest margins by trapping. A blend of these compounds could be used as a lure in a monitoring tool, or even a local suppression method if combined with a toxin.     

Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera

Understanding the evolution of multiple mating by females (polyandry) is an important question in behavioural ecology. Most leading explanations for polyandry by social insect queens are based upon a postulated fitness benefit from increased intracolonial genetic diversity, which also arises when colonies are headed by multiple queens (polygyny). An indirect test of the genetic diversity hypotheses is therefore provided by the relationship between polyandry and polygyny across species, which should be negative if the genetic diversity hypotheses are correct. Here, we conduct a powerful comparative investigation of the relationship between polyandry and polygyny for 241 species of eusocial Hymenoptera (ants, bees and wasps). We find a clear and significant negative relationship between polyandry and polygyny after controlling for phylogeny. These results strongly suggest that fitness benefits resulting from increased intracolonial genetic diversity have played an important role in the evolution of polyandry, and possibly polygyny, in social insects.     

Social structure of perennial Vespula squamosa wasp colonies

Many social species show variation in their social structure in response to different environmental conditions. For example, colonies of the yellowjacket wasp Vespula squamosa are typically headed by a single reproductive queen and survive for only a single season. However, in warmer climates, V. squamosa colonies sometimes persist for multiple years and can grow to extremely large size. We used genetic markers to understand patterns of reproduction and recruitment within these perennial colonies. We genotyped V. squamosa workers, pre‐reproductive queens, and males from perennial colonies in the southeastern United States at 10 polymorphic microsatellite loci and one mitochondrial DNA locus. We found that V. squamosa from perennial nests were produced by multiple reproductives, in contrast to typical annual colonies. Relatedness of nestmates from perennial colonies was significantly lower than relatedness of nestmates from annual colonies. Our analyses of mitochondrial DNA indicated that most V. squamosa perennial colonies represented semiclosed systems whereby all individuals belonged to a single matriline despite the presence of multiple reproductive females. However, new queens recruited into perennial colonies apparently mated with non‐nestmate males. Notably, perennial and annual colonies did not show significant genetic differences, supporting the hypothesis that perennial colony formation represents an instance of social plasticity. Overall, our results indicate that perennial V. squamosa colonies show substantial changes to their social biology compared to typical annual colonies and demonstrate variation in social behaviors in highly social species.     

Worker interests and male production in Polistes gallicus, a Mediterranean social wasp

The resolution of social conflict in colonies may accord with the interests of the most numerous party. In social insect colonies with single once-mated queens, workers are more closely related to the workers' sons than they are to the queens' sons. Therefore, they should prefer workers to produce males, against the queen's interests. Workers are capable of producing males as they arise from unfertilized eggs. We found Polistes gallicus to have colonies of single, once-mated queens, as determined by microsatellite genotyping of the workers, so worker interests predict worker male production. In colonies lacking queens, workers produced the males, but not in colonies with original queens. Thus worker interests were expressed only when the queen was gone. The high fraction of missing queens and early end to the colony cycle relative to climate so early in the season is surprising and may indicate a forceful elimination of the queen.     

The genetic structure of swarms and the timing of their production in the queen cycles of neotropical wasps

Kin selection theory has received some of its strongest support from analyses of within-colony conflicts between workers and queens in social insects. One of these conflicts involves the timing of queen production. In neotropical wasps, new queens are only produced by colonies with just one queen while males are produced by colonies with more queens, a pattern favoured by worker interests. We now show that new colonies, or swarms, have few queens and variable within-colony relatednesses which means that their production is not tied to new queen production. The queens in these swarms are seldom the mothers of the workers in the swarm. Therefore, either colonies producing swarms have very many queens, or queens joining daughter swarms are reproductive losers on the original colonies. As new colony production is not linked to queen production, it can occur at the ecologically optimum time, i.e. the rainy season. This disassociation between queen production and new colony production allows worker interests in sex ratios to prevail without hampering new colony production at the most favourable season, an uncoupling that may contribute to the ecological success of the Epiponini.     

Low relatedness and frequent queen turnover in the stenogastrine wasp <Emphasis Type="Italic">Eustenogaster fraterna</Emphasis> favor the life insurance over the haplodiploid hypothesis for the origin of eusociality

Summary The origin of sociality is best studied in taxa with rudimentary social development, like the stenogastrine wasp, Eustenogaster fraterna. Our study of colony structure and relatedness in this species found very small colonies aver-aging only 2.7 adult females, including a single mated, re-productive female. Microsatellite genotyping showed that adult females were related to each other but not generally as full sisters (r = 0.427 ± 0.131, 95% confidence interval). Microsatellite genotyping showed that sociality is not favored by the haplodiploid hypothesis, because relatedness of unmated females to female brood is low (r = 0.210 ± 0.171, 95% confidence interval), far lower than that among sisters in either haplodiploid or diploid species. Relatedness of unmated females to female brood is significantly lower than that of mated females to female brood (r = 0.374 ± 0.266). Mated females are also significantly more related to the male brood (r = 0.871 ± 0.168) than are unmated females (r = 0.588 ± 0.339), suggesting that unmated helpers do not generally produce sons. These results argue against an important role for exceptionally high relatedness in the origin of eusociality. One quarter of the brood could not have been the progeny of any collected female, suggesting high rates of queen turnover. In all, 7/17 nests had some brood that could not be assigned to existing adult females. These high adult mortality rates result in direct advantages to helpers in the form of colony inheritance, and indirect advantages via life insurance benefits.Received 23 October 2002; revised 13 March 2003; accepted 23 April 2003.     

The repeatability of mating failure in a polyandrous bug

Mating failure, characterized by the lack of production of offspring following copulation, is relatively common across taxa yet is little understood. It is unclear whether mating failures are stochastic occurrences between incompatible mating partners or represent a persistent, meaningful phenotype on the part of one or other sex. Here we test this in the seed bug Lygaeus simulans, by sequentially mating families of males with randomly allocated unrelated females and calculating the repeatability of mating outcome for each individual male and family. Mating outcome is significantly repeatable within individual males but not across full‐sib brothers. We conclude that mating failure represents a consistent male‐associated phenotype with low heritability in this species, affected by as yet undetermined environmental influences on males.     

Environmental and genetic influences on queen and worker body size in the social wasp Vespula maculifrons

Many social insects exhibit morphologically distinct worker and queen castes that perform different functions. These functional differences may generate unique selection regimes operating on body size. For example, queens may be under directional selection for large body size, whereas directional selection on worker body size may be limited. Such contrasting selection pressures may differentially affect levels of genetic variation associated with size variation in the two castes. This study sought to determine if genetic effects underlying phenotypic differences varied between the worker and queen castes of the social wasp Vespula maculifrons. We predicted that directional selection would remove genetic variation associated with size differences in the queen caste, whereas a lack of directional selection would tend to maintain genetic variation associated with size differences in the worker caste. We thus (1) calculated broad and narrow sense heritabilities for several morphological traits, (2) examined whether some paternal genotypes produced more morphologically diverse offspring than others, and (3) determined whether trait size variation was associated with genetic variation within colonies. We found that few morphological traits were significantly heritable, indicating that little genetic variance for those traits existed within our study population. We also found that some patrilines produced more morphologically variable offspring than others, suggesting a role of genotype in phenotypic plasticity. And finally, no significant correlations between genetic diversity arising from multiple mating by queens within colonies and trait variation in either caste were found. Overall, our findings indicate a weak effect of genotype on both worker and queen body size variation and are suggestive of a large environmental influence on morphological trait size. Moreover, our results do not indicate that levels of genetic variation underlying size variation differ substantially between castes in this species.     

Mate‐searching behavior in the invasive German wasp,Vespula germanica,in Patagonia

In order to increase the probability of reproduction, social insects can adopt various mate‐finding strategies, such as increasing densities of males at specific locations, and/or visual and chemical cues that attract the opposite sex. In field and laboratory studies we investigated strategies used by the invasive eusocial wasp Vespula germanica (Fabricius) (Hymenoptera: Vespidae). In tethered flight assays, we established contrasting flight patterns in females and males that may partly explain how related individuals distribute spatially during the mating period. We also determined experimentally, in the field and in the laboratory via olfactometer assays, that gynes produce airborne pheromonal cues that attract drones and are important during mate location. Our field trials also suggest that visual cues play a role in mate location. We conclude that in addition to aspects of the social biology of the species, an efficient mate‐location strategy can partly explain the invasion success of the species. Tools to mitigate the damage caused by yellowjackets may be developed by focusing on reproductive castes, in addition to workers.