Colony specificity of Dufour gland secretions in a functionally monogynous ant

Summary. Queens in colonies of the small myrmicine ant, Leptothorax gredleri Mayr 1855 (Hymenoptera, Formicidae) engage in dominance interactions and form social hierarchies, in which typically only the top-ranking queen lays eggs. Occasionally, queen antagonism escalates to violent mandible fighting, during which the sting is used to apply Dufour gland secretions onto the cuticle of the opponent. Contaminated queens often are attacked by nestmate workers. Here we show that the chemical composition of the Dufour gland is colony-specific and that workers can discriminate between secretions from their own and other colonies. Our findings suggest that Dufour gland secretions are involved in the establishment of hierarchies within a colony. When invading an alien colony the queen presumably employs the secretions during the expulsion of the resident queen. Apparently, Dufour gland secretions play a role in intraspecific queen competition similar to that in slave-making and inquiline formicoxenine ants, where they function as "propaganda substances" in an interspecific context. Received 7 July 1998; accepted 15 September 1998.     

Mixed messages: fertility signaling interferes with nestmate recognition in the monogynous ant Camponotus floridanus

Chemical communication is crucial for the organization of social insect colonies. However, with the heavy use of one communication modality, problems may arise such as the interference of different types of information. This study investigated how information about fertility and colony membership is integrated in the ant Camponotus floridanus. We introduced into mature, queenright colonies (a) the nestmate queen, (b) a nestmate worker, (c) a foreign, high-fertility queen, (d) a foreign, low-fertility queen, and (e) a foreign worker. As expected, workers did not attack their nestmate queen or a nestmate worker but responded aggressively to foreign workers and foreign, low-fertility queens. Surprisingly, workers did not attack foreign, high-fertility queens. Chemical analysis demonstrated that the cuticular hydrocarbon profile of C. floridanus encodes information about fertility status in queens and workers and colony membership in workers. We suggest that ants respond to this information in the cuticular hydrocarbon profile: individuals with strong fertility signals are accepted regardless of their colony membership, but individuals without strong fertility signals are tolerated only if their cuticular hydrocarbon profile matches that of colony members. Learning how social insects respond to multiple types of information presented together is critical to our understanding of the recognition systems that permit the complex organization of social insect colonies.     

Serial polygyny and colony genetic structure in the monogynous queenless ant Diacamma cyaneiventre

Serial polygyny, defined as the temporal succession of several reproductive females in a colony, occurs in some monogynous social insects and has so far attracted little attention. Diacamma cyaneiventre is a queenless ponerine ant found in the south of India. Colonies are headed by one singly mated worker, the gamergate. After the death of the gamergate or her absence following colony fission, the gamergate is replaced by a newly eclosed nestmate worker. After a replacement, colonies go through short-lived periods in which two matrilines of sisters co-occur. This is a situation which can be described as serial polygyny. To measure the consequences of serial polygyny, a genetic analysis was performed on 449 workers from 46 colonies of D. cyaneiventre using five microsatellite loci. The presence of more than one matriline among workers of the same nest was detected in 19% of colonies, indicating a recent change of gamergate. The average genetic relatedness among nestmate workers was 0.751 and did not significantly differ from the theoretical expectation under strict monogyny and monandry (0.75). A simple analytical model of the temporal dynamics of serial polygyny was developed in order to interpret these results. We show that the rate of gamergate turnover relative to the rate of worker turnover is the crucial parameter determining the level of serial polygyny and its effect on the genetic structure of colonies. This parameter, estimated from our data, confirms that serial polygyny occurs in D. cyaneiventre but is not strong enough to influence significantly the average genetic relatedness among workers.     

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     

Queen and worker policing in the monogynous and monandrous ant, Diacamma sp.

Policing behavior that prevents workers from laying male eggs was examined in the monogynous and monandrous ponerine ant Diacamma sp. from Japan, in which a singly mated worker called a “gamergate” reproduces as the functional queen in each colony. Since oviposition by virgin workers is rare in the presence of a gamergate, we separated a portion of workers from the gamergates and induced their oviposition experimentally. When orphaned workers had started to oviposit, they were returned to the original colonies, where they continued to lay eggs for a while. The gamergates and other workers interfered with the laying workers by aggressively taking and finally eating the eggs. In total, 60% and 29% of the worker-derived eggs were eaten by gamergates and non-mother workers, respectively. The observed worker-worker interactions were not driven simply by competition to leave own sons, because non-laying non-orphaned workers interfered with worker reproduction. Furthermore, orphaned workers were usually attacked by non-orphaned workers soon after colony reunification. These results indicate that both queen policing by gamergates and worker policing in this species are mechanisms inhibiting worker oviposition. The gamergate contribution to policing was proportionately larger than that of workers, but among virgin workers, the relationship between dominance rank and contribution to policing was not clear. But about 11% of the eggs were not policed and were added to egg piles, especially in large colonies. Worker policing in a monandrous and monogynous eusocial Hymenoptera contrasts to other recent findings, and possible genetic, social, and ecological factors for its evolution in Diacamma sp. are discussed. Received: 16 November 1998 / Received in revised form: 9 February 1999 / Accepted: 21 February 1999     

Dominance orders in the ponerine ant Pachycondyla apicalis (Hymenoptera,Formicidae)

Summary Intracolony aggression among workers of the neotropical ponerine ant species Pachycondyla apicalis leads to dominance orders. Antagonistic interactions can entail either overt physical attacks with the subordinate individual often exhibiting a submissive posture or the robbing and destruction of eggs laid by nestmates. The single queen, however, was never observed either attacking or being attacked by any colony member. The hierarchical structure among workers consists of one dominant individual and several subordinates; the relationships among subordinate workers are unclear, however. We report for the first time a natural (nonmanipulated) change in the social status of individuals within an ant dominance order. Dominant workers usually had better developed ovaries, laid more eggs and were more frequently observed attending the egg pile than subordinate individuals. This pattern became even more striking when the queen was excluded from the colony. These results indicate that workers of P. apicalis lay eggs even in the presence of the queen. It is possible that some of these haploid eggs may develop into males.Offprint requests to: B. Holldobler     

Dominance orders,worker reproduction,and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis

Summary In a queenright colony of the monogynous slave-making ant Harpagoxenus sublaevis, a subset of workers formed a linear dominance order in which dominance was corrlated with ovarian development, frequency of trophallaxis, length of time spent in the nest, but not body size. Identical dominance orders occurred in queenless colonies. Experiments in which the top-ranking workers were removed from queenless colonies demonstrated that worker dominance behaviour inhibits egg-laying in subordinates. A similar removal experiment showed queens restrict dominance behaviour and egg-laying in workers, probably pheromonally. Observations of slave raids indicated ovary-developed workers spent significantly less time scouting for slaves, and tended to participate less in slave raids, than workers without ovarian development. These findings suggest that potentially fertile H. sublaevis workers aggressively compete for egg-laying rights, consume extra food for egg development, and safeguard their reproductive futures by avoiding risks outside the nest. Hence worker reproduction in this species strongly influences the colony's social structure, nutrient flow, and division of labour, even though all workers in a colony are full sisters. I hypothesize that worker reproduction was formerly even more prevalent in H. sublaevis, with workers following the strategy of raising sisters and producing sons predicted by kinship theory. Its continued existence despite queen opposition conceivably results from selection on orphaned workers to reproduce, and the inability of slave-maker workers to raise female-biased broods. The social organization of H. sublaevis therefore highlights the importance both of worker reproduction and of the concomitant queen-worker conflict over male parentage in Hymenopteran social evolution.     

Queen fertility, egg marking and colony size in the ant Camponotus floridanus

In ant societies, workers do not usually reproduce but gain indirect fitness benefits from raising related offspring produced by the queen. One of the preconditions of this worker self-restraint is sufficient fertility of the queen. The queen is, therefore, expected to signal her fertility. In Camponotus floridanus, workers can recognize the presence of a highly fertile queen via her eggs, which are marked with the queen's specific hydrocarbon profile. If information on fertility is encoded in the hydrocarbon profile of eggs, we expect workers to be able to differentiate between eggs from highly and weakly fertile queens. We found that workers discriminate between these eggs solely on the basis of their hydrocarbon profiles which differ both qualitatively and quantitatively. This pattern is further supported by the similarity of the egg profiles of workers and weakly fertile queens and the similar treatment of both kinds of eggs. Profiles of queen eggs correspond to the cuticular hydrocarbon profiles of the respective queens. Changes in the cuticular profiles are associated with the size of the colony the queen originates from and her current egg-laying rate. However, partial correlation analysis indicates that only colony size predicts the cuticular profile. Colony size is a buffered indicator of queen fertility as it is a consequence of queen productivity within a certain period of time, whereas daily egg-laying rate varies due to cyclical oviposition. We conclude that surface hydrocarbons of eggs and the cuticular profiles of queens both signal queen fertility, suggesting a major role of fertility signals in the regulation of reproduction in social insects.     

Dominance and reproduction in a parthenogenetic lizard

Summary In most vertebrates, males and females are believed to differ in terms of their investment in offspring. Dominance theory suggests that one way individuals of the sex with lower parental investment can increase reproductive success would be to dominate others of the same sex. The dominant competitors are thought to achieve preferred access to mates, and thus, have greater reproductive success than subordinates.Reproduction in parthenogenetic Cnemidophorus uniparens normally proceeds without males, but individuals exhibit mounting behaviors in captivity that are typical of closely related Cnemidophorus species that reproduce sexually. Thus, these animals provide an unusual opportunity to study the effects of behavior on reproduction apart from copulation and fertilization. In this study relationships between dominance and reproduction were investigated in the unisexual lizard species, C. uniparens. Dominance hierarchies were rapidly established and maintained in the laboratory by agonistic encounters among individuals. The number of times an individual charged its cagemates was positively correlated with the number of clutches and eggs laid. Also, dominant animals who charged their cagemates were likely to win agonistic encounters; recipients of charges usually fled. Hierarchies based on different behaviors were not all related to reproduction. Charges as a predictor of dominance was unrelated to body length, percent increase in body length and time spent in the basking site. However, individuals with a high percent increase in body length spent more time basking. This is likely a result of the increased energy demands of growth in addition to reproduction. Physiological stress as measured by plasma corticosterone titers was unrelated to dominance. We suggest that dominance is an important factor affecting reproduction in C. uniparens.     

Graded recruitment in a ponerine ant

Summary (1) The giant tropical ant, Paraponera clavata, exhibits graded recruitment responses, depending on the type, quantity, and quality of a food source. More ants are initially recruited to a large prey or scavenge item than to a large quantity of sugar water. (2) Individual ants encountering prey items gauge the size and/or unwieldiness of the item, regardless of the weight, when determining whether to recruit. (3) The trail pheromone of this species is often used as an orientation device by individual ants, independent of recruitment of nestmates. (4) It is proposed that the foraging behavior of P. clavata represents one of the evolutionary transitions from the independent foraging activities of the primitive ants to the highly coordinated cooperative foraging activities of many higher ants.     

Dominance and competition in an herbivorous lizard

Summary A study of social organization in an herbivorous lizard Ctenosaura hemilopha investigated the role of dominance in group member behavior. Attention focused on a very populous (16 ind.) colony to examine causes and effects of crowding with respect to competitive factors. Lizards were colonial, with a top-rank male, one or more adult females, and various subadults and juveniles. Top-rank males defended harems, with colonies female-biased (1:4 in focal colony). Dominance hierarchy was observed, with females more aggressive than males, except for the top-rank male. Group awareness facilitated adaptive responses to threatening dominants and predators. Strong correlations existed among individual size, rank, and aggression. Top-rank male aggressiveness was partly explained by harem defense. Food resource competition, which causes aggression in female insectivorous lizards, did not explain female C. hemilopha behavior. Response to predators, predator fecal pellet analysis, and tail break frequencies implicate crevice escape sites for predator avoidance as a prime controller of social and population structure in these lizards.     

Colony level sex allocation in a polygynous and polydomous ant

The colony-level sex allocation pattern of eusocial Hymenoptera has attracted much attention in recent studies of evolutionary biology. We conducted a theoretical and empirical study on this subject using the dolichoderine ant Technomyrmex albipes. This ant is unusual in having a dispersal polymorphism in both males and females. New colonies are founded by an alate female after mating with one or more alate males in the nuptial flight. In mature colonies, the reproductive role of the foundress queen is taken over by wingless offspring (supplementary reproductives). Mature colonies are extremely polygynous, with many wingless queens reproducing through intea-colonial mating with wingless males (inbreeding), and producing both alate and wingless sexuals. The population sex ratio of wingless sexuals was found to be extremely female-biased, while the population allocation ratio of alates was almost 1:1. This result suggests that there is local mate competition among wingless sexuals. A specific model for this extraordinary life cycle predicted that the asymmetry of regression relatedness (b _f/b _m) will disappear during the first few generations of wingless reproductives after the foundress dies. If colonies begin to produce alates after several wingless generations, this undermines the hypotheses for intercolonial sex ratio variation based on the relatedness asymmetry. We compared the magnitude of variation in sex ratios and other characteristics between two levels (within-colony-inter-nest and between-colony). Although there was considerable within-colony variation in all the examined characteristics, between-colony variances were always larger. This means that allocation is important at the whole-colony level, not that of the nest. There was no apparent correlation between the sex ratio of alates and colony size. Furthermore, partial correlation analysis indicated that neither the number of workers nor investment in alates explained the variation in the sex ratio of alates. The only factor which was significantly correlated with the sex ratio of alates was the sex ratio of wingless sexuals (a positive correlation). We conclude that both the alate and wingless sex ratios may be influenced by a common primary sex ratio at the egg stage, the variance of which may have genetic components. In the wingless sexuals, partial correlation analysis indicated that colony size and the number of workers explained the sex allocation ratio. The number of wingless females was strongly (positively) correlated with the total investment in wingless sexuals, while the number of males showed no such correlation. There is, however, no convincing explanation for the variation in sex allocation ratio of wingless sexuals, because the estimates of investment in wingless males may have a large sampling error. Correspondence to: K. Tsuji     

Reproductive conflicts and egg discrimination in a socially polymorphic ant

The ability to discriminate against competitors shapes cooperation and conflicts in all forms of social life. In insect societies, workers may detect and destroy eggs laid by other workers or by foreign queens, which can contribute to regulate reproductive conflicts among workers and queens. Variation in colony kin structure affects the magnitude of these conflicts and the diversity of cues used for discrimination, but the impact of the number of queens per colony on the ability of workers to discriminate between eggs of diverse origin has so far not been investigated. Here, we examined whether workers from the socially polymorphic ant Formica selysi distinguished eggs laid by nestmate workers from eggs laid by nestmate queens, as well as eggs laid by foreign queens from eggs laid by nestmate queens. Workers from single- and multiple-queen colonies discriminated worker-laid from queen-laid eggs, and eliminated the former. This suggests that workers collectively police each other in order to limit the colony-level costs of worker reproduction and not because of relatedness differences towards queens’ and workers’ sons. Workers from single-queen colonies discriminated eggs laid by foreign queens of the same social structure from eggs laid by nestmate queens. In contrast, workers from multiple-queen colonies did not make this distinction, possibly because cues on workers or eggs are more diverse. Overall, these data indicate that the ability of F. selysi workers to discriminate eggs is sufficient to restrain worker reproduction but does not permit discrimination between matrilines in multiple-queen colonies.     

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 dominance modifies behavioral rhythm in a queenless ant

Social insects provide an intriguing model system in chronobiology. Typically, an egg-laying queen exhibits arrhythmicity in activity while foraging worker has clear rhythmicity. In the queenless ant, Diacamma sp., from Japan, colony members lack morphological caste, and reproductive differentiation occurs as a consequence of dominance hierarchy formation. Their specialized dominance interaction “gemmae mutilation”, provide us a fascinating model system to investigate the effect of social dominance on rhythmic ontogeny. Measurement of individual rhythms revealed that they have clear circadian rhythm at eclosion but it is diminished by social mutilation of gemmae. Moreover, unlike highly eusocial species, mated egg-layer (i.e., gamergate) possessed a circadian rhythm even after mating in Diacamma. Measurement of colony-level rhythms revealed that gemmae mutilations are performed in the limited time of the day, but foraging occurs around-the-clock. The above finding is a novel form of temporal organization in social insects, providing a new insight in morphologically casteless species. We discuss the causes and consequences of rhythmic variability in social organization.     

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     

Colony fusion causes within-colony variation in a parthenogenetic ant

The evolutionary stability of cooperation and altruism in colonies of social insects requires that nestmates be to some extent related. An efficient system of discrimination against non-nestmates protects the nest against unrelated conspecifics, which might exploit or parasitize the colony. The co-occurrence of unrelated individuals in mature colonies therefore is a rare event that deserves more attention. Here, we report on the relatively common incidence of colony fusion in the ant Platythyrea punctata. Workers of this ant can produce genetically identical female offspring from unfertilized eggs through thelytokous parthenogenesis. Consequently, the majority of colonies has a “clonal structure” and consists of individuals with identical multilocus genotypes. Nevertheless, field observations indicate that a surprisingly large percentage of colonies contain workers belonging to two or more different genetic lineages. Much of this genetic heterogeneity is incompatible with eventual recombination or mutation events, but instead appears to result from colony fusion or the adoption of unrelated individuals. Indeed, colonies of P. punctata from the Dominican Republic and Barbados readily merged in the laboratory and, after elimination of one of the two reproductive workers, formed stable, genetically heterogeneous colonies. We discuss the possible causes and benefits of colony fusion in natural populations.     

Plasticity of social organization in a forest ant species

We manipulated availability of food and nesting sites in one population of the forest ant Myrmica punctiventris. The manipulations produced significant changes in relatedness structure, reproductive allocation, and response to hierarchical selection. Food availability appeared to have a consistently stronger influence on these aspects of social organization than did availability of nesting sites. We interpret our experimental results in light of observed differences between populations, and discuss implications for kin selection dynamics. Received: 30 July 1998 / Accepted after revision: 31 October 1998     

Dominance and survival of dippers Cinclus cinclus

Survival of dippers Cinclus cinclus in the wild was studied in relation to their dominance. Dominance was assessed amongst groups of temporary captives in a laboratory arena. Adults tended to be more dominant than juveniles, and within age classes males generally dominated females. Dominant individuals also sang more. Logistic regression was used to examine survival in the wild in relation to dominance and other factors. Annual survival of juvenile males was negatively related to dominance during the previous autumn. No significant effects of dominance on winter or annual survival were found amongst females or adult males. Dominance effects on overwinter survival approached significance for adult females, however, and were significant for both winter and annual survival when the data from adult females and juvenile males were combined. None of the other factors considered, which included body size, song frequency and year, had a significant effect on overwinter or annual survival. We concluded that dominance either had no influence on survival, or had a negative effect particularly on dippers of intermediate status. We were unable to show if dominance had a direct effect, however, or acted indirectly on survival via an unidentified factor we did not examine. Received: 23 June 1994/Accepted after revision: 28 October 1995