Effects of foundress number on brood raids and queen survival in the fire ant Solenopsis invicta

In several ant species, colonies are founded by small groups of queens (pleometrosis), which coexist until the first workers eclose, after which all but one queen is killed. It has been hypothesized that, by producing a larger cohort of workers, cooperating queens may increase colony success during brood raids, a form of competition in which brood and workers from losing nests are absorbed into winning colonies. To test whether this benefit is sufficient to favor pleometrosis, newly mated queens of the fire ant Solenopsis invicta were assembled in groups of one, two, three, or four, reared in the laboratory until the first workers eclosed, then planted in the field in replicated assemblages. The proportion of colonies engaging in brood raids increased with average foundress number per nest and with colony density but was unaffected by variance in foundress number among interacting colonies. Within mixed assemblages of single-queen and multiple-queen colonies, queen number had no effect on the likelihood of engaging in raids or the probability of nest survival through the brood raiding period. However, following nearly 30% of raids, queens moved to new nests and displaced the resident queens. When queen relocation and subsequent mortality were accounted for, it was found that the survival of queens from four-queen groups was substantially higher than that of solitary queens. By contrast, the survival of queens from two-queen colonies was no greater than that of solitary queens. These results show that the competitive advantages of multiple-queen colonies are sufficient to counterbalance the increased mortality of queens within groups only when the number of foundresses is greater than two and when colonies are founded at high density. When colonies lose brood raids, the workers appear to abandon their mothers to join surviving colonies. However, in laboratory experiments, queens attempting to enter foreign nests were significantly more likely to displace the resident queen if their own daughters were present within the invaded nest. Thus, workers may be able to bias the probability that their mother rejoins them and displaces competing queens.     

Queen longevity,queen adoption,and posthumous indirect fitness in the facultatively polygynous ant Myrmica tahoensis

In many polygynous ant species, established colonies adopt new queens secondarily. Conflicts over queen adoption might arise between queens and workers of established colonies and the newly mated females seeking adoption into nests. Colony members are predicted to base adoption decisions on their relatednesses to other participants, on competition between queens for colony resources, and on the effects that adopted queens have on colony survivorship and productivity. To provide a better understanding of queen-adoption dynamics in a facultatively polygynous ant, colonies of Myrmica tahoensis were observed in the field for 4 consecutive years and analyzed genetically using highly polymorphic microsatellite DNA markers. The extreme rarity of newly founded colonies suggests that most newly mated queens that succeed do so by entering established nests. Queens are closely related on average (rˉ = 0.58), although a sizable minority of queen pairs (29%) are not close relatives. An experiment involving transfers of queens among nests showed that queens are often accepted by workers to which they are completely unrelated. Average queen numbers estimated from nest excavations (harmonic mean = 1.4) are broadly similar to effective queen numbers inferred from the genetic relatedness of colony members, suggesting that reproductive skew is low in this species. Queens appear to have reproductive lifespans of only 1 or 2 years. As a result, queens transmit a substantial fraction of their genes posthumously (through the reproduction of related nestmates), in comparison to direct and indirect reproduction while they are alive. Thus queens and other colony members should often accept new queens when doing so will increase colony survivorship, in some cases even when the adopted queens are not close relatives. Received: 20 February 1996/Accepted after revision: 25 May 1996     

Lack of detectable nepotism in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

Multiple-queen (polygyne) colonies of the introduced fire ant Solenopsis invicta present a paradox for kin selection theory. Egg-laying queens within these societies are, on average, unrelated to one another, and the numbers of queens per colony are high, so that workers appear to raise new sexuals that are no more closely related to them than are random individuals in the population. This paradox could be resolved if workers discriminate between related and unrelated nestmate sexuals in important fitness-related contexts. This study examines the possibility of such nepotism using methods that combine the following features: (1) multiple relevant behavioral assays, (2) colonies with an unmanipulated family structure, (3) multiple genetic markers with no known phenotypic effects, and (4) a statistical technique for distinguishing between nepotism and potentially confounding phenomena. We estimated relatedness between interactants in polygyne S. invicta colonies in two situations, workers tending egg-laying queens and workers feeding maturing winged queens. In neither case did we detect a significant positive value of relatedness that would implicate nepotism. We argue that the non-nepotistic strategies displayed by these ants reflect historical selection pressures experienced by native populations, in which nestmate queens are highly related to one another. The markedly different genetic structure in native populations may favor the operation of stronger higher-level selection that effectively opposes weaker individual-level selection for nepotistic interactions within nests. Received: 28 June 1996 / Accepted after revision: 6 October 1996     

Variation in colony structure in the subterranean termite Reticulitermes flavipes

The genetic organization of colonies of the subterranean termite Reticulitermes flavipes in two subpopulations in Massachusetts was explored using five polymorphic allozymes and double-strand conformation polymorphism (DSCP) analysis of the mitochondrial control region. Empirically obtained estimates of worker relatedness and F-statistics were compared with values generated by computer simulations of breeding schemes to make inferences about colony organization. In one study site (G), worker genotypes indicated the presence of a mixture of colonies headed by monogamous outbred primary reproductives and colonies headed by inbreeding neotenic reproductives, both colony types having limited spatial ranges. A second site (S) was dominated by several large colonies with low relatedness among nestmates. Mixed DSCP haplotypes in three colonies indicated that nestmates had descended from two or three unrelated female reproductives. Computer simulations of breeding schemes suggested that positive colony inbreeding coefficients at site S resulted from either commingling of workers from different nests or different colonies. Such an exchange of workers between nests corresponds to the multiple-site nesting lifetype of many subterranean termites and resembles colony structure in polycalic Formica ants. Our study demonstrates considerable variation in R. flavipes colony structure over a small spatial scale, including colonies headed by monogamous outbred primary reproductives, colonies containing multiple inbred neotenic reproductives and large polydomous colonies containing the progeny of two or more unrelated queens, and suggests that the number of reproductives and nestmate relatedness change with colony age and size.     

Polygyny in the Neotropical termite Nasutitermes corniger: life history consequences of queen mutualism

Summary ecological aspects of monogyny and polygyny in social insect colonies are important in comparing individual queen reproductive success. Inseminated, fecund, multiple foundresses are common in some groups of ants and eusocial wasps, but true polygyny in termites has not previously been studied. One third of Nasutitermes corniger (Isoptera: Termitidae) colonies sampled in areas of young second growth in Panama contained from 2–33 primary queens (not supplementary or neotenic reproductives). All queens in polygynous associations were fully pigmented, physogastric egg layers within a single royal cell. Multiple kings were found less frequently; true polyandry is apparently restricted to immature polygynous colonies.Data on queen weight and morphological features, and on colony composition, show that queens in polygynous nests are young and that a transition from polygyny to monogyny probably occurs after several years. The escalated growth rate of multiple queen colonies removes them from the vulnerable incipient colony size class more rapidly than colonies initiated by a single foundress, and gives them sufficient neuter support staff (workers and soldiers) to enable earlier production of fertile alates. Using a population model (Leslie matrix) I construct isoclines of equal population growth which show values of early age class probability of survival and reproductive output favoring monogyny or polygyny under individual selection. This model of queen mutualism accounts for the risk of a female in a polygynous group not succeeding as the final surviving queen.Multiple primary queens are considered rare in termites, but a review of the literature demonstrates that they may be more widespread than is currently recognized. Polygyny in termites has received scant attention but is of significance as an example of a further ecological and evolutionary convergence between the phylogenetically independent orders Isoptera and Hymenoptera.     

Colony foundation and polygyny in the ant Formica podzolica

We document the variation in number of queens occurring naturally in founding, immature and mature nests of the ant Formica podzolica, and compare development of colonies and survivorship of queens in experimental nests started with 1–16 foundresses. Number of queens per nest was associated with stage of colony development. Most nests were monogynous, but 20% of immature nests (n = 66) and 25% of mature nests (n = 92) were oligogynous or polygynous. Colonies were usually established by single queens (i.e., haplometrosis), but colony establishment by multiple queens (i.e., pleometrotis) was also common, occurring in 27% of founding nests (n = 492). Foundress groups in the field were small ( = 1.47 ± 0.04 queens/nest), and large groups experienced high mortality and low productivity in artificial nests. Therefore, the many queens (up to 140) in some immature and mature colonies were probably secondarily pleometrotic. Experimental nests started with 1–4 queens were more successful than those initiated by 8 or 16 queens. Small groups (2–4 queens) produced more pupae before the first nests reared workers than single foundresses or larger groups (8 or 16 queens). Although single foundresses were less productive than queens in small groups, they experienced greater survivorship and less weight loss than queens in pleometrotic associations. Besides low productivity, queen mortality and weight loss were greatest in large groups.     

Colony founding,queen dominance and oligogyny in the Australian meat ant Iridomyrmex purpureus

Summary Field observations and laboratory experiments demonstrate that in the Australian meat ant, Iridomyrmex purpureus, the modes of colony founding are remarkably diverse. New colonies can originate from single foundresses (haplometrosis), or foundress associations (pleometrosis), or by colony budding, or the adoption of newly-mated queens that dig founding chambers next to mature nests (probably their natal nests, as workers protect them and may help them dig). Readoption of foundresses and pleometrosis lead to the coexistence of several queens in one nest. We discovered a striking antagonistic behavior among coexisting queens in young colonies, in the form of ritualized antennation bouts. These interactions result in a reproductive rank order in which dominant queens inhibit egg-laying by subordinates, but escalation into physical fighting is rare. Workers ignore queen dominance interactions and treat all queens equally. The first quantitative ethogram of dominance display behavior between multiple ant queens, and its reproductive consequences, is presented. As a colony grows, queens become intolerant of each other's presence and permanently separate within the nest. Once separated, queens appear to be equal in status, laying approximately equal numbers of eggs. All queens continue to be tolerated by workers, even when the colony has reached a size of several thousand workers and begun to produce reproductives. Such mature nests of I. purpureus fulfill the criteria of oligogyny, defined by worker tolerance toward more than one queen and antagonism among queens, such that a limited number of fully functional queens are spaced far apart within a single colony. Oligogynous colonies can arise in this species by pleometrotic founding (primary oligogyny) or by adoption of queens into existing nests (secondary oligogyny). The adaptive significance of the complex system of colony founding, queen dominance and oligogyny in I. purpureus is discussed.     

Intranest relatedness and nestmate recognition in the meadow ant Formica pratensis (R.)

The impact of intranest relatedness on nestmate recognition was tested in a population of polydomous and monodomous nests of the mound-building ant Formica pratensis. Nestmate recognition was evaluated by testing aggression levels between 37 pairs of nests (n=206 tests). Workers from donor colonies were placed on the mounds of recipient nests to score aggressive interactions among workers. A total of 555 workers from 27 nests were genotyped using four DNA microsatellites. The genetic and spatial distances of nests were positively correlated, indicating budding and/or fissioning as spread mechanisms. Monodomous and polydomous nests did not show different aggression levels. Aggression behavior between nests was positively correlated with both spatial distance and intranest relatedness of recipient colonies, but not with genetic distance or intranest relatedness of donor colonies. Multiple regression analysis revealed a stronger effect of spatial distance than of genetics on aggression behavior in this study, indicating that the relative importance of environment and genetics can be variable in F. pratensis. Nevertheless, the positive regression between intranest relatedness of recipient colonies and aggression in the multiple analysis supports earlier results that nestmate recognition is genetically influenced in F. pratensis and further indicates that foreign label rejection most likely explains our data.     

Intraspecific parasitism and split sex ratios in a monogynous and monandrous ant (Leptothorax nylanderi)

Sex ratios were bimodally distributed in a population of the monogynous and monandrous ant Leptothorax nylanderi during each of 3 study years. The population-wide investment ratios suggested worker control of sex allocation. Nest-level variation in the proportional investment in virgin queens was not affected by the presence or absence of a queen and only slightly by collecting year, but was correlated with nest size, total sexual investment and, unexpectedly, with differences in nestmate relatedness: small, low-investment nests and nests with several worker lineages produced male-biased sex ratios. Colonies containing several worker lineages arise from usurpation of mature colonies by unrelated founding queens and the fusion of unrelated colonies under strong nest site limitation. In contrast to facultatively polygynous and polyandrous species of social insects, where workers can maximize their inclusive fitness by adjusting sex ratios according to the degree of relatedness asymmetry, workers in mixed colonies of L. nylanderi do not benefit from manipulating sex allocation, as here relatedness asymmetries appear to be the same as in homogeneous colonies. Received: 7 December 1999 / Received in revised form: 29 February 2000 / Accepted: 13 March 2000     

Levels of selection in a social insect: a review of conflict and cooperation during honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) queen replacement

The extended phenotype of a social insect colony enables selection to act at both the individual level (within-colony selection) and the colony level (between-colony selection). Whether a particular trait persists over time depends on the relative within- and between-colony selection pressures. Queen replacement in honey bee colonies exemplifies how selection may act at these different levels in opposing directions. Normally, a honey bee colony has only one queen, but a colony rears many new queens during the process of colony reproduction. The replacement of the mother queen has two distinct phases: queen rearing, where many queens develop and emerge from their cells, and queen elimination, where most queens die in a series of fatal duels. Which queens are reared to adulthood and which queens ultimately survive the elimination process depends on the strength and direction of selection at both the individual and colony levels. If within-colony selection is predominant, then conflict is expected to occur among nestmates over which queens are produced. If between-colony selection is predominant, then cooperation is expected among nestmates. We review the current evidence for conflict and cooperation during queen replacement in honey bees during both the queen rearing and queen elimination phases. In particular, we examine whether workers of different subfamilies exhibit conflict by acting nepotistically toward queens before and after they have emerged from their cells, and whether workers exhibit cooperation by collectively producing queens of high reproductive quality. We conclude that although workers may weakly compete through nepotism during queen rearing, workers largely cooperate to raise queens of similar reproductive potential so that any queen is suitable to inherit the nest. Thus it appears that potential conflict over queen replacement in honey bees has not translated into actual conflict, suggesting that between-colony selection predominates during these important events in a colonys life cycle.Communicated by A. Cockburn     

Genetic influence on caste in the ant Camponotus consobrinus

Genetic influences on polyethism within social insect colonies are well known, suggesting that the determination of caste (soldiers and minor workers) may also be genetically mediated. The Australian sugar ant Camponotus consobrinus is suitable for such a study, having soldiers and minor workers that follow a complex allometry. Further, although most C. consobrinus colonies are monogynous, 13 of 42 surveyed using microsatellites were found to be polygynous. Thus, although a minority of colonies were polygynous, the great majority of queens live in polygynous colonies. From the 29 monogynous colonies studied, we inferred that the queens are monandrous. Ants from four polygynous colonies were assigned to families on the basis of microsatellite genotypes, after measurements had been taken of head width and scape length. These measurements reflect a complex allometry interpretable as soldier and minor worker growth curves with a large changeover zone. Genetic influence on caste determination was examined by testing for differences between families within colonies in the distribution of scape lengths, residuals from the overall colony allometric curve, and proportions of soldiers and minor workers (as determined by head width falling above or below the inflection point of the overall colony allometric curve). Families in all four colonies differed significantly in caste proportions and in head-width distributions, and three of the four colonies showed significant differences between families in residuals from the overall colony growth curve. Nested ANOVAs using head widths and scape-length residuals showed that when the effect of family is removed, intercolony differences in allometry are negligible. This evidence indicates genetic rather than environmental causes for the observed differences between families. We speculate that this variation may reflect some selective advantage to within-colony heterogeneity between families or that selective differences are few between a wide array of family growth patterns. Received: 16 June 1999 / Received after revision: 13 September 1999 / Accepted: 25 September 1999     

High degree of polyandry in Apis dorsata queens detected by DNA microsatellite variability

Workers of six colonies of the giant honeybee Apis dorsata from Sabah, Malaysia (five colonies) and Java (one colony) were genotyped using single locus DNA fingerprinting. The colonies from Sabah nested in colony aggregations of 5 and 28 nests respectively on two trees. Three DNA microsatellite loci (A14, A76, A88) with a total of 27 alleles provided sufficient genetic variability to classify the workers into distinct sub-families revealing the degree of polyandry of the queens. Queens mated on average with 30.17 ± 5.98 drones with a range from 19 to 53. The average effective number of matings per queen was 25.56 ± 11.63. In the total sample of 192 workers, 22 individuals were found that were not offspring of the colony's queen. Three of these were potentially drifted offspring workers from genotyped queens of colonies nesting on the same tree.     

Queen acceptance and the complexity of nestmate discrimination in the Argentine ant

In most social insect species, individuals recognize and behave aggressively towards non-nestmate conspecifics to maintain colony integrity. However, introduced populations of the invasive Argentine ant, Linepithema humile, exhibit pronounced variation in intraspecific aggression denoting diversity in nestmate recognition behavior, which possibly shapes their social structure and the varying levels of unicoloniality observed among these populations. One approach to better understand differential aggression behaviors towards conspecifics and recognition cue perception and response in L. humile is to examine variation in nestmate discrimination capability among genetically distinct colonies under different social contexts. Consequently, we investigated the dynamics of queen and worker recognition in southeastern US L. humile queenless and queenright colonies by measuring rates of non-nestmate worker and queen adoption and intercolony genetic similarity. Aggression levels between colony pairs differed and were associated with non-nestmate worker, but not queen adoption. Adoption of queens and workers was a function of host colony origin, while colony queen number affected adoption of queens, but not workers, with queens more readily accepted by queenless hosts. Fecundity of adopted non-nestmate queens was comparable to that of rejected non-nestmate and host colony queens, suggesting that queen fecundity did not affect adoption decisions. Genetic similarity between colonies ranged from 30 to 77% alleles shared, with more genetically similar colonies showing lower levels of intraspecific aggression. Non-nestmate queens and workers that were more genetically similar to host colony workers were more likely to be adopted. We provide the first evidence for the role of L. humile colony queen number on queen discrimination and suggest an effect of resident queens on worker conspecific acceptance thresholds. Our findings indicate a role for genetically based cues in L. humile nestmate recognition. However, subtle discrimination capability seems to be influenced by the social context, as demonstrated by more frequent recognition errors in queenless colonies.     

The independent origin of a queen number bottleneck that promotes cooperation in the African swarm-founding wasp, Polybioides tabidus

When cooperation is based on shared genetic interests, as in most social insect colonies, mechanisms which increase the genetic similarity of group members may help to maintain sociality. Such mechanisms can be especially important in colonies with many queens because within-colony relatedness drops quickly as queen number increases. Using microsatellite markers, we examined the Old World, multiple-queen, swarm-founding wasp Polybioides tabidus which belongs to the ropalidiine tribe, and found that relatedness among the workers was four times higher than what would be expected based on queen number alone. Relatedness was elevated by a pattern of queen production known as cyclical oligogyny, under which, queen number varies, and daughter queens are produced only after the number of old queens has reduced to one or a very few. As a result, the queens are highly related, often as full sisters, elevating relatedness among their progeny, the workers. This pattern of queen production is driven by collective worker control of the sex ratios. Workers are three times more highly related to females than to males in colonies with a single queen while they are more equally related to males and females in colonies with more queens. As a result of this difference, workers will prefer to produce new queens in colonies with a single queen and males in colonies with many queens. Cyclical oligogyny has also evolved independently in another group of swarm-founding wasps, the Neotropical epiponine wasps, suggesting that collective worker control of sex ratios is widespread in polistine wasps. Received: 22 May 2000 / Revised: 24 August 2000 / Accepted: 4 September 2000     

Genotypic differences in brood rearing in honey bee colonies: context-specific?

Summary Three experiments were performed to determine whether brood care in honey bee colonies is influenced by colony genetic structure and by social context. In experiment 1, there were significant genotypic biases in the relative likelihood of rearing queens or workers, based on observations of individually labeled workers of known age belonging to two visually distinguishable subfamilies. In experiment 2, no genotypic biases in the relative likelihood of rearing drones or workers was detected, in the same colonies that were used in experiment 1. In experiment 3, there again were significant genotypic differences in the likelihood of rearing queens or workers, based on electrophoretic analyses of workers from a set of colonies with allozyme subfamily markers. There also was an overall significant trend for colonies to show greater subfamily differences in queen rearing when the queens were sisters (half- and super-sisters) rather than unrelated, but these differences were not consistent from trial to trial for some colonies. Results of experiments 1 and 3 demonstrate genotypic differences in queen rearing, which has been reported previously based on more limited behavioral observations. Results from all three experiments suggest that genotypic differences in brood care are influenced by social context and may be more pronounced when workers have a theoretical opportunity to practice nepotism. Finally, we failed to detect persistent interindividual differences in bees from either subfamily in the tendency to rear queen brood, using two different statistical tests. This indicates that the probability of queen rearing was influenced by genotypic differences but not by the effect of prior queen-rearing experience. These results suggest that subfamilies within a colony can specialize on a particular task, such as queen rearing, without individual workers performing that task for extended periods of time.     

Sociogenetic organization of the red ant Myrmica rubra

Knowledge of the sociogenetic organization determining the kin structure of social insect colonies is the basis for understanding the evolution of insect sociality. Kin structure is determined by the number and relatedness of queens and males reproducing in the colonies, and partitioning of reproduction among them. This study shows extreme flexibility in these traits in the facultatively polygynous red ant Myrmica rubra. Relatedness among worker nestmates varied from 0 to 0.82. The most important reason for this variation was the extensive variation in the queen number among populations. Most populations were moderately or highly polygynous resulting in low relatedness among worker nestmates, but effectively monogynous populations were also found. Polygynous populations also often tend to be polydomous, which is another reason for low relatedness. Coexisting queens were positively related in two populations out of five and relatedness was usually similar among workers in the same colonies. Due to the polydomous colony organization and short life span of queens, it was not possible to conclusively determine the importance of unequal reproduction among coexisting queens, but it did not seem to be important in determining the relatedness among worker nestmates. The estimates of the mating frequency by queens remained ambiguous, which may be due to variation among populations. In some populations relatedness among worker nestmates was high, suggesting monogyny and single mating by queens, but in single-queen laboratory nests relatedness among the worker offspring was lower, suggesting that multiple mating was common. The data on males were sparse, but indicated sperm precedence and no relatedness among males breeding in the same colony. A comparison of social organizations and habitat requirements of M. rubra and closely related M. ruginodis suggested that habitat longevity and patchiness may be important ecological factors promoting polygyny in Myrmica. Received: 15 May 1995/Accepted after revision: 17 October 1995     

Queen primer pheromone affects conspecific fire ant (<Emphasis Type="Italic">Solenopsis invicta</Emphasis>) aggression

Monogyne fire ant, Solenopsis invicta, colony workers are territorial and are aggressive toward members of other fire ant colonies. In contrast, polygyne colony workers are not aggressive toward non-nestmates, presumably due to broader exposure to heritable and environmentally derived nestmate recognition cues (broad template). Workers from both monogyne and polygyne fire ant colonies execute newly mated queens after mating flights. We discovered that monogyne and polygyne queens have a remarkable effect on conspecific recognition. After removal of their colony queen, monogyne worker aggression toward non-nestmate conspecifics quickly drops to merely investigative levels; however, heterospecific recognition/aggression remains high. Queenless monogyne or polygyne worker groups were also not aggressive toward newly mated queens. Queenless worker groups of both forms that adopted a monogyne-derived newly mated queen became aggressive toward non-nestmate workers and newly mated queens. We propose that the powerful effect of fire ant queens on conspecific nestmate recognition is caused by a queen-produced recognition primer pheromone that increases the sensitivity of workers to subtle quantitative differences in nestmate recognition cues. This primer pheromone prevents the adoption of newly mated queens (regulation of reproductive competition) in S. invicta and when absent allows queenless workers to adopt a new queen readily. This extraordinary discovery has broad implications regarding monogyne and polygyne colony and population dynamics.     

Colony life history and demography of a swarm-founding social wasp

Colonies of social insects are sometimes viewed as superorganisms. The birth, reproduction, and death of colonies can be studied with demographic measures analogous to those normally applied to individuals, but two additional questions arise. First, how do adaptive colony demographies arise from individual behaviors? Second, since these superorganisms are made up of genetically distinct individuals, do conflicts within the colony sometimes modify and upset optima for colonies? The interplay between individual and superindividual or colony interests appears to be particularly complex in neotropical, swarm-founding, epiponine wasps such as Parachartergus colobopterus. In a long-term study of this species, we censused 286 nests to study colony-level reproduction and survivorship and evaluated individual-level factors by assessing genetic relatedness and queen production. Colony survivorship followed a negative exponential curve very closely, indicating type II survivorship. This pattern is defined by constant mortality across ages and is more characteristic of birds and other vertebrates than of insects. Individual colonies are long-lived, lasting an average of 347 days, with a maximum of over 4.5 years. The low and constant levels of colony mortality arise in part from colony initiation by swarming, nesting on protected substrates, and an unusual expandable nest structure. The ability to requeen rapidly was also important; relatedness data suggest that colonies requeen on average once every 9–12 months. We studied whether colony optima with respect to the timing of reproduction could be upset by individual worker interests. In this species, colonies are normally polygynous but new queens are produced only after a colony reaches the monogynous state, a result which is in accord with the genetic interests of workers. Therefore colony worker interests might drive colonies to reproduce whenever queen number happens to cycled down to one rather than at the season that is otherwise optimal. However, we found reproduction to be heavily concentrated in the rainy season. The number of new colonies peaked in this season as did the percentages of males and queens. Relatedness among workers reached a seasonal low of 0.21–0.27, reflecting the higher numbers of laying queens. This seasonality was achieved in part by a modest degree of synchrony in the queen reduction cycle. Worker relatedness reached peaks of around 0.4 in the dry season, reflecting a decrease to a harmonic mean queen number of about 2.5. Thus, a significant number of colonies must be approaching monogyny entering the rainy season. Coupled with polygynous colonies rearing only males (split sex ratios), this makes it possible for a colony cycle driven by selfish worker interests to be consistent with concentrating colony reproduction during a favorable season.     

Queen number, queen cycling and queen loss: the evolution of complex multiple queen societies in the social wasp genus Ropalidia

Complex, highly integrated societies have evolved from simpler societies repeatedly, and the social insects provide an excellent model system for understanding increasing complexity and integration. In the paper wasps, large societies, known as swarm-founding, have evolved repeatedly from smaller societies, known as independent-founding. Swarm-founding colonies have many more queens than independent-founding colonies, which should dramatically reduce relatedness, posing a challenge to cooperation. However, in each instance, swarm-founding species have also evolved a cyclical pattern of queen reduction which elevates relatedness despite high queen numbers. The genus Ropalidia provides an excellent system in which to study the transition to swarm-founding because it has both independent and swarm-founding species. We studied the Australian independent-founding wasp Ropalidia revolutionalis to better understand the evolution of multiple queens and their periodic reductions in swarm-founding wasps. Using microsatellite genetic markers we genotyped queens, workers and brood from 37 colonies and found that while most colonies had a single queen, three of the colonies had multiple queens at or immediately prior to the time of collection. An additional seven colonies had had multiple co-occurring queens earlier in the season. We also found that colonies experienced many queen losses, and that founding queens were gradually lost until they were replaced by a new cohort of daughter queens in many colonies. This pattern is similar to the periodic reductions and replacements in swarm-founding wasps and suggests that multiple queens and queen cycling evolved relatively early in the shift to swarm-founding in Ropalidia.Communicated by R. Page     

Promiscuous honeybee queens generate colonies with a critical minority of waggle-dancing foragers

Honeybees present a paradox that is unusual among the social Hymenoptera: extremely promiscuous queens generate colonies of nonreproducing workers who cooperate to rear reproductives with whom they share limited kinship. Extreme polyandry, which lowers relatedness but creates within-colony genetic diversity, produces substantial fitness benefits for honeybee queens and their colonies because of increased disease resistance and workforce productivity. However, the way that these increases are generated by individuals in genetically diverse colonies remains a mystery. We assayed the foraging and dancing performances of workers in multiple-patriline and single-patriline colonies to discover how within-colony genetic diversity, conferred to colonies by polyandrous queens, gives rise to a more productive foraging effort. We also determined whether the initiation by foragers of waggle-dance signaling in response to an increasing sucrose stimulus (their dance response thresholds) was linked to patriline membership. Per capita, foragers in multiple-patriline colonies visited a food source more often and advertised it with more waggle-dance signals than foragers from single-patriline colonies, although there was variability among multiple-patriline colonies in the strength of this difference. High-participation patrilines emerged within multiple-patriline colonies, but their more numerous foragers and dancers were neither more active per capita nor lower-threshold dancers than their counterparts from low-participation patrilines. Our results demonstrate that extreme polyandry does not enhance recruitment effort through the introduction of low-dance-threshold, high-activity workers into a colony’s population. Rather, genetic diversity is critical for injecting into a colony’s workforce social facilitators who are more likely to become engaged in foraging-related activities, so boosting the production of dance signals and a colony’s responsiveness to profitable food sources.