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     

A test of reproductive skew models in a field population of a multiple-queen ant

Determining the evolutionary basis of variation in reproductive skew (degree of sharing of reproduction among coexisting individuals) is an important task both because skew varies widely across social taxa and because testing models of skew evolution permits tests of kin selection theory. Using parentage analyses based on microsatellite markers, we measured skew among female eggs (n=32.3 eggs per colony, range=20–68) in 17 polygynous colonies from a UK field population of the ant Leptothorax acervorum. We used skew among eggs as our principal measure of skew because of the high degree of queen turnover in the study population. Queens within colonies did not make significantly unequal contributions to queen and worker adult or pupal offspring, indicating that skew among female eggs reflected skew among daughter queens. On average, both skew among female eggs (measured by the B index) and queen–queen relatedness proved to be low (means±SE=0.06±0.02 and 0.28±0.08, respectively). However, contrary to current skew models, there was no significant association of skew with either relatedness or worker number (used as a measure of productivity). In L. acervorum, predictions of the concession model of skew may hold between but not within populations because queens are unable to assess their relatedness to other queens within colonies. Additional phenomena that may help maintain low skew in the study population include indiscriminate infanticide in the form of egg cannibalism and split sex ratios that penalize reproductive monopoly by single queens within polygynous colonies.     

Extended family structure in the ant Formica paralugubris: the role of the breeding system

In populations of various ant species, many queens reproduce in the same nest (polygyny), and colony boundaries appear to be absent with individuals able to move freely between nests (unicoloniality). Such societies depart strongly from a simple family structure and pose a potential challenge to kin selection theory, because high queen number coupled with unrestricted gene flow among nests should result in levels of relatedness among nestmates close to zero. This study investigated the breeding system and genetic structure of a highly polygynous and largely unicolonial population of the wood ant Formica paralugubris. A microsatellite analysis revealed that nestmate workers, reproductive queens and reproductive males (the queens' mates) are all equally related to each other, with relatedness estimates centring around 0.14. This suggests that most of the queens and males reproducing in the study population had mated within or close to their natal nest, and that the queens did not disperse far after mating. We developed a theoretical model to investigate how the breeding system affects the relatedness structure of polygynous colonies. By combining the model and our empirical data, it was estimated that about 99.8% of the reproducing queens and males originated from within the nest, or from a nearby nest. This high rate of local mating and the rarity of long-distance dispersal maintain significant relatedness among nestmates, and contrast with the common view that unicoloniality is coupled with unrestricted gene flow among nests. Received: 8 February 1999 / Received in revised form: 15 June 1999 / Accepted: 19 June 1999     

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     

Kin conflict over caste determination in social Hymenoptera

We argue that caste determination, the process whereby females in the social Hymenoptera develop into either queens or workers, is subject to kin-selected conflict. Potential conflict arises because developing females are more closely related to their would-be offspring than to those of other females. Therefore, they may favour becoming queens contrary to the interests of other developing females and of existing queens and workers. We suggest two contexts leading to potential caste conflict. The first occurs when queens are reared in a reproductive phase following an ergonomic phase of worker production, while the second occurs when queens and workers are reared simultaneously. The first context assumes that workers' per capita contribution to colony survival and productivity falls with rising colony size. A critical feature influencing whether potential conflict is realized is the extent to which developing females can determine their own caste (“self-determination”). Self-determination is facilitated when female larvae control their own food intake and when queen-worker size dimorphism is low. We know of no strong evidence for actual conflict over caste fate arising in the first context. However, stingless bees and polygynous ants with excess queen-potential larvae that are either forced to develop as workers or are culled as adults demonstrate actual caste conflict in the second context. Caste conflict does not preclude caste regulation for “the good of the colony”, but such regulation is contingent on either the absence of potential conflict or on developing females losing control of their caste fate. Received: 22 March 1999 / Received in revised form: 15 June 1999 / Accepted: 19 June 1999     

Inbreeding in a lek-mating ant species, Pogonomyrmex occidentalis

In this paper we have two goals. First, we examine the effects of sample size on the statistical power to detect a given amount of inbreeding in social insect populations. The statistical power to detect a given level of inbreeding is largely a function of the number of colonies sampled. We explore two sampling schemes, one in which a single individual per colony is sampled for different sample sizes and a second sampling scheme in which constant sampling effort is maintained (the product of the number of colonies and the number of workers per colony is constant). We find that adding additional workers to a sample from a colony makes it easier to detect inbreeding in samples from given number of colonies; however, adding more colonies rather than more workers per colony always gives greater power to detect inbreeding. Because even relatively large amounts of sib-mating generate relatively small inbreeding coefficients, detection of even substantial deviations from random mating will require very large samples. Second, we look at the amount of inbreeding in a large population of the western harvest ant, Pogonomyrmex occidentalis. We find deviations from Hardy-Weinberg equilibrium equivalent to approximately 27% sib-mating in our population ( f = 0.09). Review of past studies on the population structure of other Pogonomyrmex species suggests that inbreeding may be a regular feature of the mating system of these ants. Although P. occidentalisis a swarm-mating species, there are a number of features of its population biology which suggest that the effective population size may be small. These include topographical variation that potentially breaks the population into demes, variation in the reproductive output of colonies, and variation in the size of reproductives produced by colonies. Received: 6 May 1996 / Accepted after revision: 6 October 1996     

Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds

A growing body of evidence suggests that social bonds have adaptive value for animals that live in social groups. Although these findings suggest that natural selection may favor the ability to cultivate and sustain social bonds, we know very little about the factors that influence the quality or stability of social bonds. Here, we draw on data derived from a 16-year study of baboons living in seven different social groups in the Amboseli basin of Kenya to evaluate the quality and stability of social bonds among females. Our results extend previous analyses, which demonstrate that females form the strongest bonds with close maternal and paternal kin, age mates (who may be paternal kin), and females who occupy similar ranks but are not maternal relatives. Here we show that the same factors influence the quality and strength of social bonds. Moreover, the results demonstrate that the quality of social bonds directly affects their stability.     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

Ecology of<Emphasis Type="Italic"> Leptothorax</Emphasis> ants: impact of food,nest sites,and social parasites

In a long-term field manipulation, we demonstrate strong reactions of Leptothorax longispinosus ant colonies to food- and nest-site supplementation. Demographic and genetic responses varied over small geographic scales, and the two ecological factors interacted with the presence of the social parasite Protomognathus americanus. We conducted a 2×2 experiment in three blocks and found that the blocks, which were less than 100 m apart, reacted very differently to the treatments. Blocks differed in degree of polygyny, intranest relatedness, colony size, productivity, and sexual investment. Furthermore, these differences were associated with the presence of slave-making ants and the local availability of nest sites. Nest-site supplementation had a strong effect only in the site with the highest prevalence of social parasites, influencing there the density and investment patterns of colonies. L. longispinosus ants in the least parasitized area were strongly affected by both food- and nest-site supplementation. There, food supplementation led to a decrease in the number of queens per colony and consequently to an increase in intranest relatedness, while colonies in nest-site-supplemented areas invested fewer resources in males and produced a female-biased allocation ratio. By contrast, in a third block with a very low intracolonial relatedness, food supplementation induced an absolute and relative higher investment in males. We conclude that ecological factors influencing social organization in insect societies cannot be studied in isolation, because the interactions among factors produce far richer responses than any one variable.Communicated by L. Sundström     

Social relationships among adult female baboons (papio cynocephalus) I. Variation in the strength of social bonds

Sociality has positive effects on female fitness in many mammalian species. Among female baboons, those who are most socially integrated reproduce most successfully. Here we test a number of predictions derived from kin selection theory about the strength of social bonds among adult female baboons. Our analyses are based on systematic observations of grooming and association patterns among 118 females living in seven different social groups in the Amboseli Basin of Kenya over a 16-year period. Females in these groups formed the strongest bonds with close kin, including their mothers, daughters, and maternal and paternal sisters. Females were also strongly attracted toward females who were close to their own age, perhaps because peers were often paternal sisters. Females’ bonds with their maternal sisters were strengthened after their mother’s deaths, whereas their relationships with their maternal aunts were weakened after their mother’s death. In addition, females formed stronger bonds with their paternal sisters when no close maternal kin were available, and they compensated for the absence of any close kin by forming strong bonds with nonrelatives. Taken together, these data suggest that social bonds play a vital role in females’ lives, and the ability to establish and maintain strong social bonds may have important fitness consequences for females.Joan B. Silk is on sabbatical at Cambridge University from September 2005 to August 2006. Tel.: +44-7929759697; Fax: +44-1223-335460.     

Resource supplements cause a change in colony sex-ratio specialization in the mound-building ant, Formica exsecta

We examine the role of food resources on split sex ratios in Formica exsecta. Models of resource-based sex allocation predict that greater resources will cause an increase in the production of reproductive females (gynes) and an increase in overall size of offspring. We experimentally increased food resources for a subset of colonies in a polygynous population with a very male-biased sex ratio. This increase in food availability caused colonies that were male specialists the prior year to switch to female production. Overall, a significantly greater proportion of food-supplemented colonies produced gynes, compared to control colonies. Moreover, food-supplemented colonies produced significantly larger workers and males (but not gynes), compared to those produced by control colonies. There was, however, no significant difference in the numerical productivity of food-supplemented and control colonies. We also measured the natural association between colony sex specialization and proximity to conifers, which typically harbor honeydew-bearing aphids (an important natural food source). In line with the view that resources play an important role for determining sex ratios in social insects, we found that female-producing colonies were significantly closer to conifers than were male-producing colonies.     

Encounter rate and task allocation in harvester ants

As conditions change, social insect colonies adjust the numbers of workers engaged in various tasks, such as foraging and nest work. This process of task allocation operates without central control; individuals respond to simple, local cues. This study investigates one such cue, the pattern of an ant's interactions with other workers. We examined how an ant's tendency to perform midden work, carrying objects to and sorting the refuse pile of the colony, is related to the recent history of the ant's brief antennal contacts, in laboratory colonies of the red harvester ant, Pogonomyrmex barbatus. The probability that an ant performed midden work was related to its recent interactions in two ways. First, the time an ant spent performing midden work was positively correlated with the number of midden workers that ant had met while it was away from the midden. Second, ants engaged in a task other than midden work were more likely to begin to do midden work when their rate of encounter per minute with midden workers was high. Cues based on interaction rate may enable ants to respond to changes in worker numbers even though ants cannot count or assess total numbers engaged in a task. Received: 1 July 1998 / Accepted: 15 November 1998     

Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors

Division of labour among workers is central to the organisation and ecological success of insect societies. If there is a genetic component to worker size, morphology or task preference, an increase in colony genetic diversity arising from the presence of multiple breeders per colony might improve division of labour. We studied the genetic basis of worker size and task preference in Formica selysi, an ant species that shows natural variation in the number of mates per queen and the number of queens per colony. Worker size had a heritable component in colonies headed by a doubly mated queen (h ²=0.26) and differed significantly among matrilines in multiple-queen colonies. However, higher levels of genetic diversity did not result in more polymorphic workers across single- or multiple-queen colonies. In addition, workers from multiple-queen colonies were consistently smaller and less polymorphic than workers from single-queen colonies. The relationship between task, body size and genetic lineage appeared to be complex. Foragers were significantly larger than brood-tenders, which may provide energetic or ergonomic advantages to the colony. Task specialisation was also often associated with genetic lineage. However, genetic lineage and body size were often correlated with task independently of each other, suggesting that the allocation of workers to tasks is modulated by multiple factors. Overall, these results indicate that an increase in colony genetic diversity does not increase worker size polymorphism but might improve colony homeostasis.     

Molecular genetic and behavioral analysis of social organization in the Asian elephant (Elephas maximus)

We report on the genetic evaluation and behavioral study of social organization in the Asian elephant (Elephas maximus). Although Asian elephants and African elephants (Loxodonta africana) were previously thought to have similar social organizations, our results demonstrate a substantial difference in the complexity and structure of Asian elephant social groupings from that described for African savanna elephants. Photographic cataloging of individuals, radio telemetry, and behavioral observations in Ruhuna National Park, Sri Lanka, enabled us to assign associated females and young to four groups with overlapping ranges. Genetic sampling of individuals from the four groups in Ruhuna National Park and three other groups in surrounding areas, conducted through PCR amplification and sequencing of mitochondrial DNA from dung, supported the matriarchal nature of female groups and the lack of inter-group transfer of females. Behaviorally and genetically, the identified social groups were best described as ”family groups”. We did not find any evidence for the existence of social groups of higher complexity than family groups. Received: 25 March 2000 / Received in revised form: 28 March 2000 / Accepted: 1 April 2000     

Young-boy networks without kin clusters in a lek-mating manakin

I use 10 years of data from a long-term study of lek-mating long-tailed manakins to relate the social network among males to their spatial and genetic structure. Previously, I showed that the network connectivity of young males predicts their future success. Here, I ask whether kinship might shape the organization of this “young-boy network”. Not surprisingly, males that were more socially distant (linked by longer network paths) were affiliated with perch zones (lek arenas) that were further apart. Relatedness (r) among males within the network decreased as social distance increased, as might be expected under kin selection. Nevertheless, any role for indirect inclusive fitness benefits is refuted by the slightly negative mean relatedness among males at all social distances within the network (overall mean r = −0.06). That is, relatedness ranged from slightly negative (−0.04) to more negative (−0.2). In contrast, relatedness in dyads for which at least one of the males was outside the social network (involving at least one blood-sampled male not documented to have interacted with other banded males) was slightly above the random expectation (mean r = 0.05). The slight variations around r = 0 among males of different categories likely reflect dispersal dynamics, rather than any influence of kinship on social organization. Relatedness did not covary with the age difference between males. These results, together with previous results for lack of relatedness between alpha and beta male partners, refute any role for kin selection in the evolution of cooperative display in this lek-mating system. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau, and R. James).     

Small queens in the ant Ectatomma tuberculatum: a new case of social parasitism

Social parasites exploit the worker force of colonies of other social insects to rear their own young. Social parasitism occurs in several Hymenoptera and is particularly common in several tribes of the ant subfamilies Myrmicinae and Formicinae. Here, we document the occurrence of miniaturized queens (microgynes) in colonies of Ectatomma tuberculatum, an ant belonging to the subfamily Ectatomminae. Behavioral observations and genetic analyses show that microgynes concentrate their reproductive efforts almost exclusively on the production of sexual offspring (microgynes and males), whereas the regular, large queens (macrogynes) produce workers in addition to sexuals. According to mitochondrial and nuclear markers, gene flow between microgynes and macrogynes is extremely limited. Whereas the co-occurrence of microgynes and macrogynes in the related species Ectatomma ruidum constitutes an intraspecific polymorphism associated with alternative dispersal tactics, microgynes found in colonies of E. tuberculatum appear to be a distinct species and to represent the first case of social parasitism in the poneromorph subfamilies of ants.     

Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens

Multiple mating is likely to be costly for ant queens and yet it is common. Whether multiple mating brings benefits to queens that outweigh the costs has, therefore, received considerable theoretical attention. Empirical tests of hypotheses have been scarce and no clear evidence has been reported. We tested the “multiple-mating-for-more-sperm” hypothesis on individual young queens in a natural population of the leafcutter ant Atta colombica, a monogynous ant characterised by very large colonies and high colony longevity. We found that the number of sperm stored by queens was positively correlated with the number of mates per queen estimated through mother-offspring analysis with microsatellite DNA markers. Queen sperm stores increased on average by 30 million sperm for each additional mate. Life-history information for Atta indicate that the number of stored sperm observed is likely to constrain the reproductive lifespan of queens in nature. Multiple mating, despite costs, may therefore enhance the fitness of Atta queens because it enables them to store more sperm. Received: 19 September 1997 / Accepted after revision: 7 December 1997     

Transmission of a pathogen in Bombus terrestris,with a note on division of labour in social insects

Summary Parasites of social insect workers can be transmitted within the colony to other, related host individuals or, alternatively, to unrelated workers of other colonies. Division of labour affects the probability of transmission, as young individuals often work inside the nest whereas older ones often leave the nest to forage. Therefore, the relative probabilities of transmission within-vs. between-nests is also affected by the delay between host infection and the shedding of propagules, i.e. the latent period of the parasite strain. We therefore hypothesized that strains of the flagellate parasite Crithidia bombi (Trypanosomatidae, Zoomastigophorea) infecting workers of the bumble bee Bombus terrestris (Hymenoptera, Apidae) could differ in their delays and coexist in a population. This would be the case if strains that are shed after a short time delay were more efficiently transmitted to other colony members, whereas strains with long delays were more efficiently transmitted to non-related workers in the population. We tested this hypothesis by experimentally varying time delay and by allowing transmission to either sister workers from the same nest or unrelated workers from other nests. Transmission of C. bombi was measured as the number of parasitic cells shed by the exposed workers after a standard period. The results showed that relatedness as such had no effect, but that delay and nest identity were highly significant effects to explain variation in transmission success. There was a significant interaction between nest identity and delay, such that bees of some colonies acted as efficient transmitters for C. bombi under short delays and vice versa. We discuss how division of labour may affect parasitism in social insects and, vice versa, how division of labour may be under selection from the effects of parasitism, using available evidence from the literature. Correspondence to: P. Schmid-Hempel     

Fertility signaling in queens of a North American ant

In most species of advanced eusocial insects, the partitioning of reproduction between nestmates is thought to be regulated by means of primer pheromones or other chemical cues, which presumably influence the behavior of co-queens and workers such that they maximize their own inclusive fitness. Here we show that in multi-queen colonies of the Nearctic ant, Leptothorax sp. A, physical dominance in concert with chemical cues, which signal the ovarian development of a queen, are used to control reproduction of competing queens and to influence worker behavior. The analysis of ranks obtained during two fighting periods in the annual colony cycle revealed a strong link between individual aggressiveness of a queen and her fertility. During the adoption of newly mated queens in autumn, the resident, egg-laying α-queen was more likely to start aggression first and keep her high rank position compared to the fighting period after hibernation. We suggest that this is proximately caused by the α-queen having much stronger developed ovaries in autumn than the young queens, whereas after hibernation, the ovaries of all queens are similarly inactive. Interactions during the first weeks after the end of hibernation and intrinsic, individual differences in aggressiveness appear to be crucial for the dominance rank achieved later. Queens which were allowed to become fertile when their nestmate queens still were kept under prolonged hibernation, were immediately socially dominant over the latter when all queens were reunited, though no aggression occurred. In another experiment, queen antagonism was prevented by spatial separation in different parts of the same nest and all queens began to lay eggs. Workers stayed preferentially with queens with high actual fecundity rather than with those which had had high social status before separation. This and further evidence suggest that ovarian status is communicated, most likely by a chemical cue perceived by co-queens and workers, affects the direction of their aggressive behavior, and allows them to discriminate among queens. Received: 5 May 1998 / Accepted after revision: 29 August 1998     

Structure and resilience of the social network in an insect colony as a function of colony size

Social interactions are critical to the organization of worker activities in insect colonies and their consequent ecological success. The structure of this interaction network is therefore crucial to our understanding of colony organization and functioning. In this paper, I study the properties of the interaction network in the colonies of the social wasp Ropalidia marginata. I find that the network is characterized by a uniform connectivity among individuals with increasing heterogeneity as colonies become larger. Important network parameters are found to be correlated with colony size and I investigate how this is reflected in the organization of work in colonies of different sizes. Finally, I test the resilience of these interaction networks by experimental removal of individuals from the colony and discuss the structural properties of the network that are related to resilience in a social network. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau, and R. James).