Highly polymorphic microsatellite loci in the facultatively eusocial hover wasp,Liostenogaster flavolineata and cross‐species amplification

We describe eight polymorphic microsatellite loci for facultatively eusocial hover wasps (Hymenoptera: Stenogastrinae). Loci were isolated from a partial genomic library of Liostenogaster flavolineata DNA, enriched for GA repeats and an unenriched library of Liostenogaster vechti DNA. We present our results of cross‐species amplification in three species: L. flavolineata, L. vechti and Parischnogaster alternata.     

Rank and colony defense against conspecifics in a facultatively eusocial hover wasp

An important benefit of social living is increased capacityfor defense. Highly eusocial species have often evolved a fightingcaste for this purpose, but many facultatively eusocial insectsand cooperatively breeding vertebrates lack morphological castesand the decision to defend or not can depend on costs and benefitsto each individual. Defense by subordinates in a social groupcan be regarded as a form of helping, and helping input oftenvaries among subordinates of different age or size. Severalhypotheses attempt to explain variation in helping effort, includingthe effects of relatedness and differences in the costs of helping.Evidence for these hypotheses is mixed and often lacks dataon the rank of subordinates, an important determinant of expectedfuture fitness. We examined individual variation in propensityto defend the nest against conspecifics in the tropical hairy-facedhover wasp Liostenogaster flavolineata. Prior to experimentation,we determined the positions of all wasps in the age-based queueto inherit the single egg-laying position in each L. flavolineatagroup. Two approaches were then used: observations of defenseagainst natural intrusions by conspecifics and experimentaltrials where wasps were presented attached to a wire. Higherranks were more likely to defend the nest than lower ranks,opposite to the pattern previously documented for another formof helping: foraging effort. Possible explanations for thisresult are that higher ranked females are better defenders andthat they suffer a larger decrease in expected future fitnesswhen an intruder usurps their position in the inheritance queue.     

Characterization of 12 polymorphic microsatellite markers for a facultatively eusocial sweat bee (Megalopta genalis)

We developed a library of twelve polymorphic di- and tri-nucleotide microsatellite markers for Megalopta genalis, a facultatively eusocial sweat bee. We tested each locus in a panel of 23 unrelated females and found 7-20 alleles per locus. Observed and expected heterozygosities ranged from 0.65 to 0.96 and from 0.69 to 0.95 respectively. None of the loci deviated from Hardy-Weinberg equilibrium proportions or was found to be in gametic disequilibrium.     

Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns

Successful Polistes dominulus nests can be started by one ormore nest founding queens (foundresses). Consequently, thereis much interest in the specific benefits that induce cooperationamong foundresses. Here, we experimentally demonstrate one majorbenefit of cooperation, namely that multiple foundresses increasecolony productivity. This increase is close to the value predictedby subtracting the productivity of undisturbed single-foundresscolonies from the productivity of undisturbed multiple-foundresscolonies. However, we found no evidence that an associatingfoundress' contribution to colony growth is preserved if shedisappears (assured fitness returns). Our correlational datasuggest that cooperation provides survival benefits, multiple-foundresscolonies are more likely to survive to produce offspring thanare single-foundress colonies, and individual foundresses inmultiple-foundress groups are less likely to disappear beforeworker emergence than foundresses nesting alone. Therefore,association provides substantial productivity and survival benefitsfor cooperating foundresses.     

Colony founding in the primitively eusocial wasp, Ropalidia marginata (Hymenoptera: Vespidae)

Abstract.

• 1 In a 16-month study in Bangalore, India, about 35% of the newly founded colonies of Ropalidia marginata were single foundress colonies and the remainder were multiple foundress colonies with two to twenty-two individuals.
• 2 Larger colonies did not have a significantly higher per capita productivity, did not produce significantly heavier progeny and did not produce them significantly faster than smaller colonies did.
• 3 Predation by the hornet Vespa tropica appeared to be independent of group size.
• 4 Single foundress colonies failed more often but not often enough to make them have a lower average per capita productivity, compared to multiple foundress colonies.
• 5 Some of the advantages of multiple foundress associations came from the greater predictability of their attaining the mean per capita productivity, the relatively lower rates of usurpation experienced by them compared to single foundress colonies, and the opportunities provided by queen turnovers for workers to become replacement queens and gain direct individual fitness.

     

Colony-level sex ratio selection in the eusocial Hymenoptera

We present an inclusive fitness model on worker-controlled sex investments in eusocial Hymenoptera which expands the existing theory for random mating populations as formulated by Trivers and Hare (1976) and Benford (1978). We assume that relatedness asymmetry is variable among colonies — owing to multiple mating, worker reproduction and polygyny — and that workers are able to assess the relatedness asymmetry in their own colony. A simple marginal value argument shows that “assessing” workers maximize their inclusive fitness by specializing on the production of the sex to which they are relatively more related than the average worker in the population is related to that sex. The model confirms our earlier verbal argument on this matter (Boomsma and Grafen, 1990) and gives further quantitative predictions of the optimal sex ratio of relatedness-asymmetry classes for both infinite and finite, random mating populations. It is shown that in large populations all but one of the relatedness-asymmetry classes should specialize on the production of one sex only. The remaining, balancing class is selected to compensate any bias induced by the other class(es) such that the population sex ratio reflects the relatedness asymmetry of that balancing class. In the absence of worker-reproduction, the sex ratio compensation by the balancing-class is generally close to 100%, unless the population is very small. In the Discussion we address explicitly the likelihood of our relatedness-assessment hypothesis and other assumptions made in the model. The relationship of our model with previous theory on sex allocation in eusocial Hymenoptera is worked out in the Appendix.     

Using social parasitism to test reproductive skew models in a primitively eusocial wasp

Remarkable variation exists in the distribution of reproduction (skew) among members of cooperatively breeding groups, both within and between species. Reproductive skew theory has provided an important framework for understanding this variation. In the primitively eusocial Hymenoptera, two models have been routinely tested: concessions models, which assume complete control of reproduction by a dominant individual, and tug-of-war models, which assume on-going competition among group members over reproduction. Current data provide little support for either model, but uncertainty about the ability of individuals to detect genetic relatedness and difficulties in identifying traits conferring competitive ability mean that the relative importance of concessions versus tug-of-war remains unresolved. Here, we suggest that the use of social parasitism to generate meaningful variation in key social variables represents a valuable opportunity to explore the mechanisms underpinning reproductive skew within the social Hymenoptera. We present a direct test of concessions and tug-of-war models in the paper wasp Polistes dominulus by exploiting pronounced changes in relatedness and power structures that occur following replacement of the dominant by a congeneric social parasite. Comparisons of skew in parasitized and unparasitized colonies are consistent with a tug-of-war over reproduction within P. dominulus groups, but provide no evidence for reproductive concessions.     

Genetic relatedness and population structure in the social wasp,Mischocyttarus mexicanus (Hymenoptera: Vespidae)

Summary In primitively eusocial wasps workers often retain the ability to become queens, so their continued performance in the worker role is partly dependent on elevated genetic relatedness between workers and the brood they rear. In colonies of the social wasp,Mischocyttarus mexicanus, workers were related to female pupae by 0.29±0.12, a value that is significantly below the full sister value of 0.75, but not significantly below 0.50, worker relatedness to daughters. Though individuals often build new nests within meters of their natal nest, there was no genetic population structure discernable among four nest clusters, or inbreeding of any kind.     

Population structure of Leptothorax ambiguus,a facultatively polygynous and polydomous ant species

We examined the genetic and spatial structure of Leptothorax ambiguus in a Vermont site. Nests of this tiny ant species have variable queen number and comprise larger polydomous colonies, as do their closest relatives in North America. Nests are patchily distributed in the forest, and sometimes occur in local abundance. We collected 121 nests in four years from plots in which all nests were mapped; furthermore, we subjected nests collected in two separate years to starch gel electrophoresis and estimated relatedness according to the Queller—Goodnight (1989) algorithm. Queens that share a nest site also share 33% of their alleles on average, and relatedness among worker nestmates is about 0.5. The existence of diploid males and nonzero F-values demonstrate inbreeding in this species, an unusual phenomenon for social insects in general. Mapping data showed that nests with like genotypes tended to cluster in space, forming polydomous colonies. Colonies consisted of 1–6 nest subunits, and about half of all colonies were polygynous. We compare these features of L. ambiguus to its close relative L. longispinosus and a European congener L. acervorum. These comparisons allow us to conclude that an interplay between ecological and genetic factors produces the observed pattern of multiple queening and nest spatial distribution in this species.     

Egg size and reproductive allocation in eusocial thrips

Reproductive allocation, in terms of fecundity and egg size,has been given little consideration in eusocial societies. Tobegin to address this, absolute and body size–adjustedegg volumes were compared, along with fecundity, between thefoundress and her subfertile soldier offspring in the eusocial,gall-inducing thrips, Kladothrips hamiltoni, Kladothrips waterhousei,and Kladothrips habrus, and a congeneric, Kladothrips morrisi,with fully fecund soldiers. Soldiers produced significantlylarger eggs than the foundress in all species except K. morrisi,where egg volumes did not differ. After accounting for bodysize, soldiers produced significantly smaller eggs than thefoundress in K. morrisi and marginally so in K. waterhousei,but egg sizes did not differ in K. hamiltoni and K. habrus.When egg size and fecundity data are combined, K. morrisi soldiersinvest less in reproduction than the foundress, and in conjunctionwith other life-history features the species can be consideredeusocial. Maximum likelihood analyses reveal relatively lowreproductive allocation skew in the ancestral lineages and highskew in the derived lineages, but the trend is not significantwhen fecundity and egg size are considered separately. Gallsize covaried negatively with soldier-to-foundress relativebody size–adjusted egg size and reproductive allocationand marginally so with fecundity, suggesting that gall sizeis a determinant of egg size and fecundity trade-offs in eusocialthrips and providing the strongest support to date that gallsize has featured in the social evolution of this clade. Thisstudy highlights that data on fecundity alone may be insufficientfor assessing reproductive division of labor.     

Helping behaviour in facultatively eusocial hover wasps: an experimental test of the subfertility hypothesis

A candidate explanation for the evolution of eusociality is that helpers are physiologically constrained such that helping is their only realistic option. We tested this subfertility hypothesis in a species of facultatively eusocial hover wasp (Hymenoptera, Stenogastrinae: Liostenogaster flavolineata) by seeing whether helpers that were forced to nest on their own were able to mature their own eggs. One focal helper was left alone on each of 22 nests, from which all other adult wasps (including the dominant) were permanently removed. After 18 days, all but one of the 19 focal helpers that remained on their nests had ovarian development and insemination status characteristic of dominants, and the majority had probably laid eggs. This was in striking contrast to the reproductive status of other helpers removed from the same nests at the start of the experiment. These results provide convincing experimental evidence that females do not become helpers because of some unconditional physiological constraint. There is currently no unequivocal support for the subfertility hypothesis in facultatively eusocial Hymenoptera lacking morphological castes. Copyright 1999 The Association for the Study of Animal Behaviour.     

A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta)

Measurement of reproductive skew in social groups is fundamentalto understanding the evolution and maintenance of sociality,as it determines the immediate fitness benefits to helpers ofstaying and helping in a group. However, there is a lack ofstudies in natural populations that provide reliable measuresof reproductive skew and the correlates of reproductive success,particularly in vertebrates. We present results of a study thatuses a combination of field and genetic (microsatellite) dataon a cooperatively breeding mongoose, the meerkat (Suricatasuricatta). We sampled 458 individuals from 16 groups at twosites and analyzed parentage of pups in 110 litters with upto 12 microsatellites. We show that there is strong reproductiveskew in favor of dominants, but that the extent of skew differsbetween the sexes and between different sites. Our data suggestthat the reproductive skew arises from incest avoidance andreproductive suppression of the subordinates by the dominants.     

Queen number and genetic relatedness in a neotropical wasp, Polybia occidentalis

We found that genetic relatedness among Polybia occidentalisworkers was .26±0.057, a value high enough to make altruisticbehavior by workers relatively easy to explain. This comparativelyhigh level of relatedness can be attributed to close relatednessamong queens of .57±0.077 and to great variation amongcolonies in numbers of queens. The harmonic mean of queen numberis 3.1 queens per colony, which is much lower than the arithmeticmean of 10.6 queens per colony. These results are consistentwith a colony cycle called cyclical oligogyny, that is characterizedby a reduction in queen number from colony initiation to colonyreproduction. We did not find any evidence that one or a fewqueens monopolized egg laying or that there was any inbreeding,both of which have been hypothesized to increase relatednessamong workers. Another factor that can increase relatednessamong workers and the brood they rear is withincolony segregationon the basis of relatedness. We found that combmate pupae aresignificantly more closely related to each other (r = .41) thanthey are to pupae in other combs (r = .33), but we have notinvestigated whether workers take advantage of these relatednesspatterns. This distribution of relatedness among combs willoccur if queens do not lay eggs randomly throughout the nest,but concentrate their egg laying on one or a subset of the availablecombs.     

Significant reproductive skew in the facultatively polygynous ant Pheidole pallidula

Reproductive skew - the extent to which reproduction is unevenly shared between individuals in a social group - varies greatly between and within animal species. In this study, we investigated how queens share parentage in polygynous (multiple queen) colonies of the Mediterranean ant Pheidole pallidula. We used highly polymorphic microsatellites markers to determine parentage of gynes (new queens), males and workers in P. pallidula field colonies. The comparison of the genotypes of young and adult workers revealed a very low queen turnover (less than 2%). The first main finding of the study of reproductive skew in these colonies was that there was a significant departure from equal contribution of queens to gyne, male and worker production. Reproductive skew was greater for male production than for queen and worker production. There was no relationship between the magnitude of the reproductive skew and the number of reproductive queens per colony, their relatedness and the overall colony productivity, some of the factors predicted to influence the extent of reproductive skew. Finally, our study revealed for the first time a trade-off in the relative contribution of nestmate queens to gyne and worker production. The queens contributing more to gyne production contributed significantly less to worker production.     

High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis

Explaining the evolution of helping behaviour in the eusocial insects where nonreproductive (“worker”) individuals help raise the offspring of other individuals (“queens”) remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on nontropical species, where seasonality causes family groups to disperse; cofoundresses forming new nests the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here, we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes—Polistes canadensis. Using both microsatellites and newly developed single nucleotide polymorphism markers, we show that adult cofoundresses are highly related and that brood production is monopolized by a single female across the nesting cycle. Nonreproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life history and ecologies when considering the evolution of reproductive strategies.     

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.     

Kin selection, relatedness, and worker control of reproduction in a large-colony epiponine wasp, Brachygastra mellifica

Hamilton's kin selection theory predicts conflicts of interestamong relatives, even within highly cooperative social insectsocieties. Because workers are the most numerous caste, collectiveworker interests may be an important force in determining theoutcome of conflicts. In this study, we used genotypes fromtwo DNA microsatellite loci to show that two kinds of collectiveworker interests are satisfied in Brachygastra mellifica, amember of the multiqueen epiponine wasps. First, from the highrelatedness of queens (0.66) and the fact that queens are singlymated (shown by genotyping their stored sperm), we calculatedthat new queens are reared in colonies with a harmonic meanof 1.2 old queens, whereas males are reared in colonies withmuch higher queen numbers. This split sex ratio result is predictedunder worker control. It matches other studies of epiponines,but B. mellifica has much larger mature colonies (averaging7951 adults) with many more queens (averaging 398), showingthe pattern holds for large-colony species. Second, we reportthe first genetic data on parentage of males in epiponines andshow that these are also consistent with collective worker interests.Workers are on average significantly more related to queensthan to other workers (r = .37 versus .23) and should thereforesuppress each other and allow the queens to lay haploid (male)eggs. Though many workers have developed ovaries and could layeggs, the genetic analyses showed that most or all males comefrom queens.     

Reproductive skew and group size: an N-person staying incentive model

Transactional models of social evolution emphasize that dominantbreeders may donate parcels of reproduction to subordinatesin return for peaceful cooperation. We develop a general transactionalmodel of reproductive partitioning and group size for N-persongroups when (1) expected group output is a concave (decelerating)functiong[N] of the number N of group members, and (2) thesubordinates may receive fractions of total group reproduction("staying incentives") just sufficient to induce them to stayand help the dominant instead of breeding solitarily. We focusespecially on "saturated" groups, that is, groups that havegrown in size just up to the point where subsequent joining by subordinates is no longer beneficial either to them (in parent-offspring groups) or to the dominant (in symmetric-relatedness groups).Decreased expected output for solitary breeding increases thesaturated group size and decreases the staying incentives.Increased relatedness decreases both the saturated group sizeand the staying incentives. However, in saturated groups withsymmetric relatedness, an individual subordinate's staying incentive converges to 1 — g[N^* — 1]/g[N^*]) regardless ofrelatedness, where N^* is the size of a saturated group, providedthat the g[N] function near the saturated group size N^* isapproximately linear. Thus, staying incentives can be insensitiveto relatedness in saturated groups, although the dominant's total fraction of reproduction (total skew) will be more sensitive.The predicted ordering for saturated group size is: Parent-fullsibling offspring = non-relatives > symmetrically relatedrelatives. Strikingly, stable groups of non-relatives can formfor concaveg[N] functions in our model but not in previousmodels of group size lacking skew manipulation by the dominant.Finally, symmetrical relatedness groups should tend to breakup by threatened ejections of subordinates by dominants, whereas parent-offspring groups should tend to breakup via unforceddepartures by subordinates.     

Worker biting interactions and task performance in a swarm-founding eusocial wasp (Polybia occidentalis, Hymenoptera: Vespidae)

Workers in many insect societies interact via body contact withtheir nest mates, and social biting and other forms of contactmay play a general role in regulating task performance. HereI present evidence that social biting affects task performancewithout direct reproductive conflict in Polybia occidentalis,a swarm-founding eusocial wasp. Polybia occidentalis workersengaged in social biting with nest mates. Most workers thatwere active on the nest surface participated in biting interactions,but individuals differed significantly in their rates of biting and of being bitten. Rates of being bitten corresponded withnonreproductive task performance: more biting was directedat foragers than nonforagers, and foraging rates were correlatedwith rates of being bitten. Furthermore, some on-nest workersinitiated foraging activity immediately after they were bitten.Together these patterns suggest that social biting influencesforaging rates by increasing workers' probabilities of leavingthe nest. Variation in biting rates did not correspond withdifferences in reproductive physiology: highly active bitersand recipients did not differ in body size or in ovary development.In P. occidentalis and in other eusocial insects with largeworker forces, biting and other types of social contact amongworkers may regulate task performance independently of directreproductive competition.