Emergence of cooperation and division of labor in the primitively eusocial wasp Ropalidia marginata.

In most primitively eusocial wasps new nests are initiated by a single female or by small groups of females. To study the emergence of division of labor (DOL) among the nest foundresses and to determine its possible effect on nest productivity we maintained newly eclosed females of Ropalidia marginata in small boxes with one, two, or three nestmate wasps of the same age per box. Only one wasp developed her ovaries and laid eggs in each box, while the other wasp(s) built the nest, brought food, and fed larvae, demonstrating the spontaneous emergence of reproductive DOL in the presence of more than one wasp. In nests with three wasps there was also a strong negative correlation between intranidal and extranidal work performed by the two nonreproductive workers, suggesting the spontaneous emergence of nonreproductive DOL; such nonreproductive DOL was absent in nests with two wasps. Both reproductive and nonreproductive DOL were modulated by dominance behavior (DB). In nests with two wasps the egg layer showed significantly more DB than the non-egg layer before nest initiation; in nests with three wasps queens showed significantly more DB than intranidal workers, which in turn showed significantly more DB than extranidal workers. Productivities of nests (as measured by total brood on the day of eclosion of the first adult) initiated by one or two wasps were not different from each other but were significantly lower than that of three wasps. Thus, nonreproductive DOL, and not merely reproductive DOL, is necessary for increase in productivity.

A place for everything and everything in its place: spatial organization of individuals on nests of the primitively eusocial wasp Ropalidia marginata.

Non-random space use is common among animals across taxa and habitats. Social insects often use space non-randomly, outside as well as inside their nests. While such non-random space use outside the nest may improve foraging efficiency, inside the nest, it is often associated with the efficient division of labour. Non-random space use by adults on their nests has been hypothesized to result from dyadic dominance interactions, non-random distribution of tasks, differential activity levels, workers avoiding their queens or prophylactic avoidance of disease spread. These hypotheses are generally derived from species in which the tasks of the workers are themselves non-randomly distributed on the nest. Here, we study the primitively eusocial wasp Ropalidia marginata, in which tasks are not distributed non-randomly, and show that 62.4% ± 16.2% of the adults nevertheless use space on their nest non-randomly. In this species, we find that non-random space use may help optimizing nutritional exchange between individuals while prophylactically minimizing disease spread among nest-mates. We did not find evidence for the roles of dominance interactions, activity levels or location of larvae in non-random space use. Spatial organization appears to be a mechanism of minimizing the costs and maximizing the benefits of social life.

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.

Current indirect fitness and future direct fitness are not incompatible.

In primitively eusocial insects, many individuals function as workers despite being capable of independent reproduction. Such altruistic behaviour is usually explained by the argument that workers gain indirect fitness by helping close genetic relatives. The focus on indirect fitness has left open the question of whether workers are also capable of getting direct fitness in the future in spite of working towards indirect fitness in the present. To investigate this question, we recorded behavioural profiles of all wasps on six naturally occurring nests of Ropalidia marginata, and then isolated all wasps in individual plastic boxes, giving them an opportunity to initiate nests and lay eggs. We found that 41% of the wasps successfully did so. Compared to those that failed to initiate nests, those that did were significantly younger, had significantly higher frequency of self-feeding behaviour on their parent nests but were not different in the levels of work performed in the parent nests. Thus ageing and poor feeding, rather than working for their colonies, constrain individuals for future independent reproduction. Hence, future direct fitness and present work towards gaining indirect fitness are not incompatible, making it easier for worker behaviour to be selected by kin selection or multilevel selection.

Homing in a tropical social wasp: role of spatial familiarity, motivation and age.

We captured foragers of the tropical social wasp Ropalidia marginata from their nests and displaced them at different distances and directions. Wasps displaced within their probable foraging grounds returned to their nests on the day of release although they oriented randomly upon release; however, wasps fed before release returned sooner, displaying nest-ward orientation. When displaced to places far from their nests, thus expected to be unfamiliar, only a third returned on the day of release showing nest-ward orientation; others oriented randomly and either returned on subsequent days or never. When confined within mosquito-net tents since eclosion and later released to places close to their nests (but unfamiliar), even fed wasps oriented randomly, and only older wasps returned, taking longer time. Thus, contrary to insects inhabiting less-featured landscapes, R. marginata foragers appear to have thorough familiarity with their foraging grounds that enables them to orient and home efficiently after passive displacement. Their initial orientation is, however, determined by an interaction of the information acquired from surrounding landscape and their physiological motivation. With age, they develop skills to home from unfamiliar places. Homing behaviour in insects appears to be influenced by evolutionarily conserved mechanisms and the landscape in which they have evolved.

Evolution of worker policing.

Workers in insect societies are sometimes observed to kill male eggs of other workers, a phenomenon known as worker policing. We perform a mathematical analysis of the evolutionary dynamics of policing. We investigate the selective forces behind policing for both dominant and recessive mutations for different numbers of matings of the queen. The traditional, relatedness-based argument suggests that policing evolves if the queen mates with more than two males, but does not evolve if the queen mates with a single male. We derive precise conditions for the invasion and stability of policing alleles. We find that the relatedness-based argument is not robust with respect to small changes in colony efficiency caused by policing. We also calculate evolutionarily singular strategies and determine when they are evolutionarily stable. We use a population genetics approach that applies to dominant or recessive mutations of any effect size.

Homing abilities of the tropical primitively eusocial paper wasp Ropalidia marginata.

Compared to our extensive knowledge about the navigation and homing abilities of ants and bees, we know rather little about these phenomena in social wasps. Here, we report the homing abilities of the tropical primitively eusocial wasp Ropalidia marginata and the factors that affect their homing success. To determine from how far these wasps can return to their nests, we transported foragers blindfold and released them at gradually increasing distances from their nests in four cardinal directions. Their homing success was determined by checking their presence on their nests on three consecutive nights. All foragers (56 individuals, 115 releases) returned back from an area of 0.73 ± 0.25 km(2) on the day of release (minimal homing area), whereas 83.8 % of the foragers (217 individuals, 420 releases) returned when we enlarged the area of release to 6.22 ± 0.66 km(2) around their nests (maximal homing area). Of 66 releases, no wasps returned from beyond the maximal homing area. The minimal homing area might be familiar to the foragers because they probably routinely forage in this area and the maximal homing area represents the maximum distances from which the wasps are capable of returning to their nests, with or without familiarity.

Reproductive queue without overt conflict in the primitively eusocial wasp Ropalidia marginata.

Colonies of the primitively eusocial wasp Ropalidia marginata consist of a single egg layer (queen) and a number of non-egg-laying workers. Although the queen is a docile individual, not at the top of the behavioral dominance hierarchy of the colony, she maintains complete reproductive monopoly. If the queen is lost or removed, one and only one of the workers [potential queen (PQ)] becomes hyperaggressive and will become the next queen of the colony. The PQ is almost never challenged because she first becomes hyperaggressive and then gradually loses her aggression, develops her ovaries, and starts laying eggs. Although we are unable to identify the PQ when the queen is present, she appears to be a "cryptic heir designate." Here, we show that there is not just one heir designate but a long reproductive queue and that PQs take over the role of egg-laying, successively, without overt conflict, as the queen or previous PQs are removed. The dominance rank of an individual is not a significant predictor of its position in the succession hierarchy. The age of an individual is a significant predictor, but it is not a perfect predictor because PQs often bypass older individuals to become successors. We suggest that such a predesignated reproductive queue that is implemented without overt conflict is adaptive in the tropics, where conspecific usurpers from outside the colony, which can take advantage of the anarchy prevailing in a queenless colony and invade it, are likely to be present throughout the year.

A crazy ants' crazy form of reproduction: Causes and consequences.

The yellow crazy ant, or the long-legged ant, Anoplolepis gracilipes (formerly Anoplolepis longipes) - named so for its meandering movements when disturbed, possibly owing to its long legs and antennae - is globallywidespread and currently classified as one of '100 of the world's worst invasive species' (Lowe et al. 2000). This status is assigned to species that are non-native in a region and cause significant negative ecological and/or socioeconomic impacts, including declines in native biodiversity, changes in native ecosystem structure and function, and the breakdown of native biogeographic realms. Possibly, themost devastating and multipronged impacts of A. gracilipes have been observed on island ecosystems, such as on Christmas Island in the Indian Ocean, where it impacted the entire island ecosystem by reducing arthropod, reptile, bird, and mammalian diversity on the forest floor and canopy, causing an 'invasional meltdown' (O'Dowd et al. 2003).

Ovarian developmental variation in the primitively eusocial wasp Ropalidia marginata suggests a gateway to worker ontogeny and the evolution of sociality.

Social insects are characterized by reproductive caste differentiation of colony members into one or a small number of fertile queens and a large number of sterile workers. The evolutionary origin and maintenance of such sterile workers remains an enduring puzzle in insect sociobiology. Here, we studied ovarian development in over 600 freshly eclosed, isolated, virgin female Ropalidia marginata wasps, maintained in the laboratory. The wasps differed greatly both in the time taken to develop their ovaries and in the magnitude of ovarian development despite having similar access to resources. All females started with no ovarian development at day zero, and the percentage of individuals with at least one oocyte at any stage of development increased gradually across age, reached 100% at 100 days and decreased slightly thereafter. Approximately 40% of the females failed to develop ovaries within the average ecological lifespan of the species. Age, body size and adult feeding rate, when considered together, were the most important factors governing ovarian development. We suggest that such flexibility and variation in the potential and timing of reproductive development may physiologically predispose females to accept worker roles and thus provide a gateway to worker ontogeny and the evolution of sociality.

The evolution of complexity in social organization-A model using dominance-subordinate behavior in two social wasp species.

Dominance and subordinate behaviors are important ingredients in the social organizations of group living animals. Behavioral observations on the two eusocial species Ropalidia marginata and Ropalidia cyathiformis suggest varying complexities in their social systems. The queen of R. cyathiformis is an aggressive individual who usually holds the top position in the dominance hierarchy although she does not necessarily show the maximum number of acts of dominance, while the R. marginata queen rarely shows aggression and usually does not hold the top position in the dominance hierarchy of her colony. In R. marginata, more workers are involved in dominance-subordinate interactions as compared to R. cyathiformis. These differences are reflected in the distribution of dominance-subordinate interactions among the hierarchically ranked individuals in both the species. The percentage of dominance interactions decreases gradually with hierarchical ranks in R. marginata while in R. cyathiformis it first increases and then decreases. We use an agent-based model to investigate the underlying mechanism that could give rise to the observed patterns for both the species. The model assumes, besides some non-interacting individuals, the interaction probabilities of the agents depend on their pre-differentiated winning abilities. Our simulations show that if the queen takes up a strategy of being involved in a moderate number of dominance interactions, one could get the pattern similar to R. cyathiformis, while taking up the strategy of very low interactions by the queen could lead to the pattern of R. marginata. We infer that both the species follow a common interaction pattern, while the differences in their social organization are due to the slight changes in queen as well as worker strategies. These changes in strategies are expected to accompany the evolution of more complex societies from simpler ones.

Interrogating an insect society.

Insect societies such as those of ants, bees, and wasps consist of 1 or a small number of fertile queens and a large number of sterile or nearly sterile workers. While the queens engage in laying eggs, workers perform all other tasks such as nest building, acquisition and processing of food, and brood care. How do such societies function in a coordinated and efficient manner? What are the rules that individuals follow? How are these rules made and enforced? These questions are of obvious interest to us as fellow social animals but how do we interrogate an insect society and seek answers to these questions? In this article I will describe my research that was designed to seek answers from an insect society to a series of questions of obvious interest to us. I have chosen the Indian paper wasp Ropalidia marginata for this purpose, a species that is abundantly distributed in peninsular India and serves as an excellent model system. An important feature of this species is that queens and workers are morphologically identical and physiologically nearly so. How then does an individual become a queen? How does the queen suppress worker reproduction? How does the queen regulate the nonreproductive activities of the workers? What is the function of aggression shown by different individuals? How and when is the queen's heir decided? I will show how such questions can indeed be investigated and will emphasize the need for a whole range of different techniques of observation and experimentation.

Queen succession in the Indian paper wasp Ropalidia marginata: On the trail of the potential queen.

Ropalidia marginata is a common primitively eusocial wasp in peninsular India. Their colonies contain a single egg-laying queen and several non-egg-laying workers. Queens and workers are morphologically indistinguishable, and individuals can change from one role to the other. Unlike most primitively eusocial species, queens of R. marginata are docile, non-aggressive and non-interactive. Nevertheless, the queens maintain a complete reproductive monopoly mediated by non-volatile pheromones. Upon the death or removal of the queen, one worker becomes temporarily hyper-aggressive and becomes the next queen within about a week; we refer to her as the 'potential queen'. Because only one individual becomes hyper-aggressive and reveals herself as the potential queen, and the other wasps never challenge her, we have been much interested in identifying the potential queen in the presence of the queen. However, we have failed to do so until recently. Here, we recount the four decades of search for the potential queen, ending with the recent resolution that emerged from applying the novel technique of multilayer network analysis. Identifying the potential queen in the presence of the previous queen is now possible by integrating behavioural information from multiple social situations to form a holistic view of the social structure of the wasps.

Can Dufour's gland compounds honestly signal fertility in the primitively eusocial wasp Ropalidia marginata?

Unlike queens of typical primitively eusocial species, Ropalidia marginata queens are docile and non-interactive, and hence cannot be using dominance to maintain their status. It appears that the queen maintains reproductive monopoly through a pheromone, of which the Dufour's gland is at least one source. Here, we reconfirm earlier results showing that queens and workers can be correctly classified on a discriminant function using the compositions of their respective Dufour's glands, and also demonstrate consistent queen-worker differences based on categories of compounds and on single compounds also in some cases. Since the queen pheromone is expected to be an honest signal of the fecundity of a queen, we investigate the correlation of Dufour's gland compounds with ovarian activation of queens. Our study shows that Dufour's gland compounds in R. marginata correlate with the state of ovarian activation of queens, suggesting that such compounds may portray the fecundity of a queen, and may indeed function as honest signals of fertility.

Regulation of reproduction in the primitively eusocial wasp Ropalidia marginata: on the trail of the queen pheromone.

Queens and workers are not morphologically differentiated in the primitively eusocial wasp, Ropalidia marginata. Upon removal of the queen, one of the workers becomes extremely aggressive, but immediately drops her aggression if the queen is returned. If the queen is not returned, this hyper-aggressive individual, the potential queen (PQ), will develop her ovaries, lose her hyper-aggression, and become the next colony queen. Because of the non-aggressive nature of the queen, and because the PQ loses her aggression by the time she starts laying eggs, we hypothesized that regulation of worker reproduction in R. marginata is mediated by pheromones rather than by physical aggression. Based on the immediate loss of aggression by the PQ upon return of the queen, we developed a bioassay to test whether the queen's Dufour's gland is, at least, one of the sources of the queen pheromone. Macerates of the queen's Dufour's gland, but not that of the worker's Dufour's gland, mimic the queen in making the PQ decrease her aggression. We also correctly distinguished queens and workers of R. marginata nests by a discriminant function analysis based on the chemical composition of their respective Dufour's glands.

The effect of age on non-reproductive division of labour in the tropical primitively eusocial wasp, Ropalidia cyathiformis.

Division of labour among workers (non-reproductive division of labour), a characteristic feature of eusocial insects enables the efficient functioning of their colonies. In many advanced insect societies division of labour is based on age (age polyethism). Primitively eusocial insects however are believed to have a weak age polyethism. Here we investigated the role of age in non-reproductive division of labour in the tropical primitively eusocial wasp, Ropalidia cyathiformis and compared it with that in Ropalidia marginata, a congeneric species that exhibits relatively strong age polyethism. Age had a significant effect on the first performance of the four tasks studied; tasks were initiated in the sequence feed larva, build, bring food and bring building material. We measured task performance as the absolute frequency of tasks performed (FTP) and the probability of performing a task relative to other tasks (PTP) and age as absolute age in days since eclosion as well as relative age compared to nestmates. FTP varied significantly with both absolute and relative age, although absolute age explained more variance. PTP varied significantly with absolute age but not always with relative age. This is contrary to R. marginata, where more variation is explained by relative age than by absolute age. There was no trade-off between intranidal and extranidal tasks in R. cyathiformis unlike in R. marginata where the frequency of intranidal tasks decreased and that of extranidal tasks increased with age. We conclude that age polyethism is weak and less flexible in R. cyathiformis compared to that in R. marginata.

Genetic relatedness does not predict the queen's successors in the primitively eusocial wasp, Ropalidia marginata.

Ropalidia marginata is a social wasp in which colonies consist of a single fertile queen and several sterile workers. If the queen is removed, one of the workers, potential queen (PQ), becomes hyperaggressive and becomes the next queen. The identity of the PQ cannot be predicted in the presence of the queen. The probability of a worker succeeding the queen is uncorrelated with her body size, dominance rank, ovarian or mating status, but imperfectly correlated with her age. Here, we investigate whether genetic relatedness help to predict the queen's successors. We constructed models based on successors being (i) most closely related to the queen, (ii) most closely related to the immediate predecessor queen/PQ, or (iii) having the highest relatedness to the majority of the workers; and (iv) having the highest average relatedness to all the workers. We predicted five successors from each of these models using pair-wise genetic relatedness estimated from polymorphic microsatellite loci. We independently performed serial queen/PQ removal experiments and compared the observed sequence of successors with the predictions from the models. The predictions of none of the models matched the experimental results; on an average 5-6 individuals predicted by the models were bypassed in the experiment. Thus, genetic relatedness is inadequate to predict the queen's successors in this species. We discuss why relatedness sometimes predicts the patterns of altruistic behaviour and sometimes not, and argue that the cost and benefit terms in Hamilton's rule, i.e. ecology, should be vigorously investigated when relatedness does not have adequate explanatory power.