Solitary Foundresses Research Articles

Experimental disruption of social structure reveals totipotency in the orchid bee, Euglossa dilemma.

Eusociality has evolved multiple times across the insect phylogeny. Social insects with greater levels of social complexity tend to exhibit specialized castes with low levels of individual phenotypic plasticity. In contrast, species with simple social groups may consist of totipotent individuals that transition among behavioral and reproductive states. However, recent work has shown that in simple social groups, there can still be constraint on individual plasticity, caused by differences in maternal nourishment or social interaction. It is not well understood how these constraints arise, ultimately leading to the evolution of nonreproductive workers. Some species of orchid bees form social groups of a dominant and-one to two subordinate helpers where all individuals are reproductive. Females can also disperse to start their own nest as a solitary foundress, which includes a nonreproductive phase characterized by ovary inactivation, not typically expressed by subordinates. Little is known about individual flexibility across these trajectories. Here, using the orchid bee Euglossa dilemma, we assess the plasticity of subordinate helpers, finding that they are capable of the same behavioral, physiological, transcriptomic, and chemical changes seen in foundresses. Our results suggest that the lack of nonreproductive workers in E. dilemma is not due to a lack of subordinate plasticity.

Shared reproduction and sex ratio adjustment to clutch size in a socially polymorphic orchid bee

AbstractNests of the primitively eusocial orchid beeEuglossa viridissimaare generally founded by a solitary female but can be reactivated by female offspring, in the presence or absence of the mother. The population therefore exists of solitary and social nests that co‐occur in an area. A female can stay as a subordinate helper under a dominant female or disperse to become a solitary foundress. Yet, the costs and benefits of the different social phenotypes are so far little understood. Here, we compared solitary and social nests of orchid bees. We used offspring of solitary and social nests to calculate offspring sex ratio, and applied molecular markers to calculate intranidal relatedness, infer maternity and test whether sociality may have a genetic component. We found that social nests had on average more brood than solitary nests. The overall sex ratio in the population did not differ from 1:1. However, social nests tended to produce a split sex ratio with some nests producing mainly males and others mainly female offspring. Regardless of social phenotype, the number of offspring was correlated with the sex ratio, with smaller nests having a more female‐biased offspring. In social nests, not all offspring resulted from a single‐mated mother, which was also the case for some solitary nests. This suggests shared reproduction in social nests and may be an indication that intraspecific parasitism and nest takeover are not uncommon. Structure analyses did not reveal different genetic background of the two social phenotypes. Our results suggest that there is no clear benefit that favours one of the two social phenotypes over the other and that the population is kept at balance in terms of sex ratio.

To leave or to stay: direct fitness through natural nest foundation in a primitively eusocial wasp

Dispersing from the natal nest to found new nests is an avenue for gaining direct fitness for workers in some primitively eusocial insects, especially in species with a perennial nesting cycle where males are present throughout the year. Such nest foundation is difficult to study in nature or in small laboratory cages. Hence, we have investigated the dynamics of nest foundation by workers of the primitively eusocial wasp Ropalidia marginata inside closed walk-in cages so that we could locate and observe every event of nest foundation. Starting with nine parent nests we observed the dispersal of female workers that initiated 9 single-foundress and 20 multiple-foundress nests. Wasps congregated outside their parent nests and engaged in dominance–subordinate interactions before initiating multiple foundress nests. The most dominant wasps of such aggregations became queens, and among the others, some joined the new nests as cofoundresses to become workers while the others remained in the parent nests. Solitary foundresses never participated in such off-nest aggregations. Solitary foundresses and future queens of multiple foundress nests engaged in self-feeding behaviour outside their parent nests, a behaviour not performed by wasps that did not initiate new nests. Queens of new nests gained immediate direct fitness. Although the cofoundresses continued to gain only indirect fitness, they are expected to have a higher probability of gaining direct fitness in the future as compared to the corresponding probability in their much larger parent nests. These findings underscore the importance of direct fitness in the evolution of cooperation in primitively eusocial insects.

WASPnest: a worldwide assessment of social Polistine nesting behavior.

Cooperative breeding decreases the direct reproductive output of subordinate individuals, but cooperation can be evolutionarily favored when there are challenges or constraints to breeding independently. Environmental factors, including temperature, precipitation, latitude, high seasonality, and environmental harshness have been hypothesized to correlate with the presence of cooperative breeding. However, to test the relationship between cooperation and ecological constraints requires comparative data on the frequency and variation of cooperative breeding across differing environments, ideally replicated across multiple species. Paper wasps are primitively social species, forming colonies composed of reproductively active dominants and foraging subordinates. Adult female wasps, referred to as foundresses, initiate new colonies. Nests can be formed by a single solitary foundress (noncooperative) or by multiple foundress associations (cooperative). Cooperative behavior varies within and among species, making paper wasps species well suited to disentangling ecological correlates of variation in cooperative behavior. This data set reports the frequency and extent of cooperative nest founding for 87 paper wasp species. Data were assembled from more than 170 published sources, previously unpublished field observations, and photographs contributed by citizen scientists to online natural history repositories. The data set includes 25,872 nest observations and reports the cooperative behavioral decisions for 45,297 foundresses. Species names were updated to reflect modern taxonomic revisions. The type of substrate on which the nest was built is also included, when available. A smaller population-level version of this data set found that the presence or absence of cooperative nesting in paper wasps was correlated with temperature stability and environmental harshness, but these variables did not predict the extent of cooperation within species. This expanded data set contains details about individual nests and further increases the power to address the relationship between the environment and the presence and extent of cooperative breeding. Beyond the ecological drivers of cooperation, these high-resolution data will be useful for future studies examining the evolutionary consequences of variation in social behavior. This data set may be used for research or educational purposes provided that this data paper is cited.

Morphological Differences between Reproductive and Non-reproductive Females in the Social Wasp Mischocyttarus consimilis Zikán (Hymenoptera: Vespidae)

Phenotypic divergence plays an important role in establishment of the reproductive division of labor among castes in social insects; however, little is known about this subject in independent-founding polistine wasps. In this study, we investigated morphological differences among foundresses from associative and solitary foundations, as well as among females produced in different phases of the colony cycle in Mischocyttarus consimilis Zikán. Our results showed that the alpha foundress had significantly greater body size than auxiliary foundresses, although it did not differ in size from solitary foundresses. In addition, the alpha foundress had greater ovarian development than their auxiliary and solitary foundresses. We also demonstrated that gynes were significantly larger than workers. These results therefore suggest that the phenotype of females emerging in colonies M. consimilis can vary with the progress of the colony cycle, and that body size and ovarian condition are closely linked to the function performed by the foundress.

Queen signal should be honest to be involved in maintenance of eusociality: chemical correlates of fertility in Ropalidia marginata

Queens of many social insect species are known to maintain reproductive monopoly by pheromonal signalling of fecundity. Queens of the primitively eusocial wasp Ropalidia marginata appear to do so using secretions from their Dufour’s glands, whose hydrocarbon composition is correlated with fertility. Solitary nest foundresses of R. marginata are without nestmates; hence expressing a queen signal can be redundant, since there is no one to receive the signal. But if queen pheromone is an honest signal inextricably linked with fertility, it should correlate with fertility and be expressed irrespective of the presence or absence of receivers of the signal, by virtue of being a byproduct of the state of fertility. Hence we compared the Dufour’s gland hydrocarbons and ovaries of solitary foundresses with queens and workers of post-emergence nests. Our results suggest that queen pheromone composition in R. marginata is a byproduct of fertility and hence can honestly signal fertility. This provides important new evidence for the honest signalling hypothesis.

Shift from independent to dependent colony foundation and evolution of ‘multi-purpose’ ergatoid queens in Mystrium ants (subfamily Amblyoponinae)

Division of labour improves fitness in animal societies. In ants, queens reproduce, whereas workers perform all other tasks. However, during independent colony founding, queens live as solitary insects and must be totipotent, especially in species where they need to forage. In many ants, solitary founding has been replaced by dependent founding, where queens are continuously helped by nestmate workers. Little is known about the details of this evolutionary transition. Mystrium rogeri from Madagascar and Mystrium camillae from Southeast Asia (subfamily Amblyoponinae) have winged queens, but three congeneric species from Madagascar reproduce with permanently wingless queens instead. We show that this ‘ergatoid’ caste has distinct body proportions in all three species, expressing a mixture of both queen and worker traits. Ergatoid queens have functional ovaries and spermatheca, and tiny wing rudiments. They can be as numerous as workers within a colony, but only a few mate and reproduce, whereas most behave as sterile helpers. The shape of their mandibles makes them unsuited for hunting and, together with a lack of metabolic reserves (i.e. in the form of wing muscles), this means that ergatoid queens cannot be solitary foundresses. In comparison with winged queens, ergatoid queens are less costly per capita and they experience lower mortality. They remain in their natal colonies where they can either reproduce or function as helpers, making them a ‘multi-purpose’ caste. Within the Amblyoponinae, ergatoid queens replace winged queens in Onychomyrmex as well. However, in this genus, ergatoid queens are ‘sole-purpose’, few are produced each year and they reproduce but do not work. Hence, different types of ergatoid queens evolved to replace winged queens in ants. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 198–207.

Survival and productivity benefits to social nesting in the sweat bee Megalopta genalis (Hymenoptera: Halictidae)

Facultatively solitary and eusocial species allow for direct tests of the benefits of group living. We used the facultatively social sweat bee Megalopta genalis to test several benefits of group living. We surveyed natural nests modified for observation in the field weekly for 5 weeks in 2003. First, we demonstrate that social and solitary nesting are alternative behaviors, rather than different points on one developmental trajectory. Next, we show that solitary nests suffered significantly higher rates of nest failure than did social nests. Nest failure apparently resulted from solitary foundress mortality and subsequent brood orphanage. Social nests had significantly higher productivity, measured as new brood cells provisioned during the study, than did solitary nests. After accounting for nest failures, per capita productivity did not change with group size. Our results support key predictions of Assured Fitness Return models, suggesting such indirect fitness benefits favor eusocial nesting in M. genalis. We compared field collections of natural nests to our observation nest data to show that without accounting for nest failures, M. genalis appear to suffer a per capita productivity decrease with increasing group size. Calculating per capita productivity from collected nests without accounting for the differential probabilities of survival across group sizes leads to an overestimate of solitary nest productivity.

Costs and benefits of joint colony founding in Australian Acacia thrips

Facultative joint colony founding by social insects (pleometrosis) provides an outstanding opportunity to analyze the costs and benefits of sociality. Pleometrosis has been documented for a range of social insects, but most studies on the adaptive benefits of this behavior are restricted to the Hymenoptera. In this study, we provide the first analysis of costs and benefits associated with pleometrosis for Australian Dunatothrips, which form domiciles by glueing together phyllodes (leaves) of their Acacia host plant. In Dunatothrips aneurae, the distribution of foundress numbers per nest indicated that females formed associations non-randomly. Furthermore, average group size was independent of both the number of foundresses on the host plant and the number of mature colonies, suggesting that this behavior was not simply a response to limited availability of nesting sites. Although per capita reproduction declined with increasing group size, we also identified two benefits of pleometrosis: (1) individual foundresses in groups had higher survival than solitary foundresses during the brood development period, and (2) larger colony sizes resulting from pleometrosis provided a benefit later in colony development, because a higher proportion of D. aneurae adults survived invasions by the kleptoparasite Xaniothrips mulga when colony size was larger. These results demonstrate that the reproductive costs of pleometrosis are at least partially counterbalanced by survival benefits.

Number of queens in founding associations of the ponerine ant Pachycondyla villosa

In the ant Pachycondyla villosa, new colonies are usually started cooperatively by two or more young queens who establish a dominance order with a division of labour. Co-founding can lead to primary polygyny, where queens stay together after workers have emerged. Here we show that two queens associations are the most common (47%) and also the most stable in the field. When offered additional nest sites in the laboratory, two-queen associations did not split, whereas larger associations did so. We also show that solitary foundresses always accepted experimentally introduced alien queens, while these were attacked and sometimes killed in queen associations. The removal of dominant alpha queens from three-queen associations resulted in beta queens obtaining the dominant role and sometimes the destruction of the existing eggs. It appears that two queens suffice for a successful association and that pleometrosis is favoured by ecological constrains, such as nest-site limitation.

Comparative Biology of a Novel Strain of Russian Wheat Aphid (Homoptera: Aphididae) on Three Wheat Cultivars

In spring 2003, several outbreaks of the Russian wheat aphid, Diuraphis noxia (Mordvilko), were reported in fields of supposedly resistant wheat cultivars ('Stanton', 'Halt', and 'Prairie Red') in eastern Colorado. We conducted two laboratory experiments to compare the biological performance of this new biotype 2 (B2) to that of two D. noxia collections of biotype 1 (B1) from western Kansas by using three wheat cultivars as host plants: 'Trego', a susceptible cultivar, and Stanton and Halt, two cultivars with different genetic sources of resistance. Survival of solitary nymphs from first instar to adult for the two clones of B1 on Trego was 96 and 90%, respectively, compared with 67 and 43% on Stanton, and 65 and 57% on Halt. In contrast, B2 had 60% survival on Trego, 43% survival on Halt, and 85% survival on Stanton. One clone of B1 required longer to mature on Halt compared with Trego or Stanton, but no other differences in developmental time among cultivars were significant. The standardized fecundity of solitary foundresses of the B1 clones was 19.6 and 20.1 nymphs on Trego, compared with 4.6 and 0.9 on Stanton, and 2.8 and 1.1 on Halt, respectively, over the same period. In contrast, fecundity of B2 was 21.1, 20.8, and 19.7 on Trego, Stanton, and Halt, respectively. When larger colonies developed on individual plants over longer periods, Trego supported the largest number of B1 aphids by experiment's end, whereas Stanton and Halt yielded the largest numbers of B2. The order of overall plant damage was Trego > Stanton > Halt when infested with B1, with no significant differences for B2. Trego had more pronounced leaf rolling than other cultivars, independent of biotype. Collectively, the results suggest that D. noxia B2 from Colorado has evolved cross-virulence to both Dn4- and Dny-based resistance sources.

Clutch size: a major sex ratio determinant in fig pollinating wasps?

Under local mate competition, sex ratio theory predicts that increasing numbers of ovipositing females (foundresses) on a site should lead to higher proportions of males in their broods. Fig pollinators have confirmed this prediction. It is also predicted that with decreasing clutch size, solitary foundresses should produce increasing proportions of sons. We show this to be true. Further, when several females compete, brood size decreases. As a result, the proportion of males increases, and this could provide a mechanistic explanation of sex ratio response to numbers of colonizing females. Therefore, sex ratio data on fig wasps need to be reassessed to determine whether females ‘count’ other foundresses, as is generally accepted, or whether they simply ‘count’ the number of eggs that they lay. To cite this article: F. Kjellberg et al., C. R. Biologies 328 (2005).

Variation in cuticular hydrocarbon signatures, hormonal correlates and establishment of reproductive dominance in a polistine wasp

In many social insects the relationship between reproductive dominance and physiological correlates is poorly understood. Recent evidence now strongly suggests that cuticular hydrocarbons are important in reproductive differentiation in these societies where they are used as signals of ovarian activity in reproductive females. In this study we investigated the relationship between reproductive dominance, size of the corpora allata (CA, producer of Juvenile Hormone, JH) and the proportions of cuticular hydrocarbons present on the cuticle in overwintering foundresses and both associative (polygynous) and solitary (monogynous) pre-emergence colonies of the social wasp Polistes dominulus. Size of the CA was positively correlated with ovarian development in polygynous colonies. In contrast, solitary foundresses possessed significantly smaller CAs than dominant foundresses from polygynous nests, yet ovarian activity was similar for both female types. CA size variation was associated with variation in cuticular hydrocarbon proportions. Overwintering, solitary, dominant and subordinate (from associative nests) females all possessed distinctive cuticular chemical profiles revealed by multivariate discriminant analyses. Our data indicate that the social environment strongly affects reproductive physiology in this wasp, and we discuss the role of cuticular hydrocarbons in reproductive signaling in P. dominulus and other social insects.

Social organization in experimentally assembled colonies of Ropalidia marginata : comparison of introduced and natal wasps

In the primitively eusocial wasp, Ropalidia marginata worker behaviour cannot be explained satisfactorily by the haplodiploidy hypothesis due to the existence of polyandry, serial polygyny and movement of wasps between nests, which reduce intra-colony genetic relatedness to levels lower than the value expected between a solitary foundress and her offspring. We introduced wasps eclosing from one set of colonies into other colonies separated by a distance of 10 km or more, to examine the possibility of kin recognition and task specialization under conditions of low intracolony relatedness. Introduced wasps were readily accepted into unrelated foster colonies, where they performed most of the behaviours and tasks shown by the natal wasps. We found no evidence of kin recognition or task specialization among natal and introduced wasps. Introduced wasps sometimes became replacement queens in spite of the presence of natal wasps. Taken together with previous observations, these results lend support to the idea that factors other than genetic relatedness must play a prominent role in the evolution of worker behaviour in Ropalidia marginata.

Do Social Wasps Choose Nesting Strategies Based on Their Brood Rearing Abilities?

Primitively eusocial wasp nests may be founded by one or a group of females. The solitary foundress builds a nest, lays eggs, defends her brood from parasites and predators, and forages to feed her growing larvae, all by herself, at least until the eclosion of her first daughter. In multiple-foundress nests, only one individual normally assumes the role of dominant queen or egg layer while the remaining cofoundresses act as subordinate workers, building the nest and foraging for food and building material and laying few or no eggs [1, 2].

Demographic predisposition to the evolution of eusociality: a hierarchy of models.

I present a hierarchy of models that illustrate, within the framework of inclusive fitness theory, how demographic factors can predispose a species to the evolution of eusociality. Delayed reproductive maturation lowers the inclusive fitness of a solitary foundress relative to that of a worker. Variation in age at reproductive maturity makes the worker strategy more profitable to some individuals than to others and thus predicts the coexistence of single-foundress and multiple-foundress nesting associations. Delayed reproductive maturation and variation in age at reproductive maturity also select for mixed reproductive strategies so that some individuals whose reproductive maturation is expected to be delayed can first act as workers and later switch over to the role of a queen or foundress. Assured fitness returns shows how identical mortality rates can have different consequences for workers and solitary nest foundresses because a solitary foundress will have to necessarily survive for the entire duration of development of her brood, whereas a worker can hope to get proportional fitness returns for short periods of work. In concert with assured fitness returns, delayed reproductive maturation and variation in age at reproductive maturity become more powerful in selecting for worker behavior, and mixed reproductive strategies become available to a wider range of individuals. These phenomena provide a consistently more powerful selective advantage for the worker strategy than do genetic asymmetries created by haplodiploidy.

On testing the role of genetic asymmetries created by haplodiploidy in the evolution of eusociality in the Hymenoptera

The haplodiploid genetic system found in all Hymenopterans creates an asymmetry in genetic relatedness so that full-sisters are more closely related to each other than a mother is to her daughters. Thus Hymenopteran workers who rear siblings can obtain higher inclusive fitness compared to individuals who rear offspring. However, polyandry and polygyny reduce relatedness between workers and their sisters and thus tend to break down the genetic asymmetry created by haplodiploidy. Since the advent of electrophoretic analysis of variability at enzyme loci, several estimates of intra-colony genetic relatedness in the Hymenoptera have been published. To test the role of the genetic asymmetry created by haplodiploidy in the evolution of eusociality, I assume that workers are capable of investing in their brothers and sisters in their ratio of relatedness to them. I then compute ahaplodiploidy threshold, which is the threshold relatedness to sisters required for workers to obtain a weighted mean relatedness of 0.5 to siblings and thus break even with solitary foundresses. When workers rear mixtures of sisters and brothers in an outbred population, the value of this threshold is 0.604. An examination of the distribution of 185 estimates of mean genetic relatedness between sisters in Hymenopteran colonies shows that the values are well below the expected 0.75 for full sisters, both in higly eusocial as well as in primitively eusocial species although relatedness values in the latter are higher than in the former. Of the 177 estimates with standard error, 49 are significantly lower than the haplodiploidy threshold and 22 are significantly higher. Of the 35 species studied only 6 have one or more estimates that are significantly higher than the haplodiploidy threshold. For more than half the estimates, the probability of the relatedness value being above the haplodiploidy threshold is less than 0.5. Reanalysis of these data using 0.5 as the threshold does not drastically alter these conclusions. I conclude that the genetic asymmetry created by haplodiploidy is, in most cases, insufficient by itself either topromote the origin of eusociality or tomaintain the highly eusocial state.

Evolution of eusociality: the advantage of assured fitness returns

Delineation of the selective pressures responsible for the evolution ol sterile worker castes found in social insect colonies remains a major unsolved problem in evolutionary biology. There has therefore been a great deal of interest in suggesting ways by which the inclusive fitness of sterile workers can potentially be larger than those of solitary nest-builders. Queller’s (1989) head-start hypothesis ( Proc. natn. Acad. Sci. U.S.A. 86, 3224) suggests that workers may gain relatively more inclusive fitness because they have access to young of various ages which can be quickly brought to the age of independence, whereas a solitary foundress has to survive for the entire duration of the development of her brood. I argue here that Queller's quantitative analysis is incorrect because it gives an unfair advantage to workers, either by giving full credit of rearing an offspring to a worker who only cared for it for a short while or, by assuming that a worker can do much more work per unit time than a solitary foundress. I show, however, that workers do indeed have an advantage over solitary foundresses because they have assured fitness returns, even if in small amounts, for short periods of work. This results from a different reckoning from that used by Queller and gives a more moderate advantage, arising essentially from saving the wasted effort that occurs when lone foundress nests fail. Using field and laboratory data on the primitively eusocial wasp Ropalidia marginata , and re-analysing data on the four species of polistine wasps used by Queller, I show that such an ‘assured fitness returns' model provides a selective pressure for the evolution of worker behaviour which is at least about as strong as that of haplodiploidy, but free from such requirements of the latter as high levels of worker-brood genetic relatedness and ability of workers to manipulate brood sex ratios.

Solitary and eusocial nests in a population of Augochlorella striata (Provancher) (Hymenoptera; Halictidae) at the northern edge of its range

Augochlorella striata was studied at the northern limit of its range. The study population contained a mixture of solitary and social nest foundresses. Eusocial foundresses produced 1 or 2 workers before switching to a male biased brood. Solitary foundresses produced males first. Cells vacated by eclosed offspring were reused late in summer. A female biased brood resulted from cell reuse in both solitary and eusocial nests. Workers were slightly smaller than their mothers and were sterile although most of them mated. In comparison to published data from a Kansas population of this species, the Nova Scotia population had i) a lower proportion of multiple foundress nests, ii) a smaller worker brood and iii) a briefer period of foraging activity but iv) comparable overall nest productivity.