Queenless Ants Research Articles

Hostility prevents the tragedy of the commons in metapopulation with asymmetric migration: Alessonfromqueenlessants.

A colony of the queenless ant species, Pristomyrmex punctatus, can broadly be seen as consisting of small-body sized worker ants and relatively larger body-sized cheater ants. Hence, in the presence of intercolony migration, a set of constituent colonies act as a metapopulation exclusively composed of cooperators and defectors. Such a setup facilitates an evolutionary game-theoretic replication-selection model of population dynamics of the ants in a metapopulation. Using the model, we analytically probe the effects of territoriality induced hostility. Such hostility in the ant metapopulation proves to be crucial in preventing the tragedy of the commons, specifically, the workforce, a social good formed by cooperation. This mechanism applies to any metapopulation-not necessarily the ants-composed of cooperators and defectors where interpopulation migration occurs asymmetrically, i.e., cooperators and defectors migrate at different rates. Furthermore, our model validates that there is evolutionary benefit behind the queenless ants' behavior of showing more hostility towards the immigrants from nearby colonies than those from the far-off ones. In order to calibrate our model's parameters, we have extensively used the data available on the queenless ant species, P. punctatus.

Genotype-Based Recognition Among Individuals of the Social Insect Pristomyrmex Punctatus (Japanese Queenless Ant) from Geographically Divergent Populations

The queenless ant, Pristomyrmex punctatus (F. Smith) reproduces parthenogenetically. The workers lay unfertilized eggs, which develop into female workers. This mode of reproduction generates hereditary clones. A previous research shows that when genetically monomorphic colonies were split, the workers tended to reassemble after being split into two groups, but when genetically polymorphic colonies split, they remained as two separate colonies. However, it remains unclear whether the workers can recognize individual genotype. Here, it was investigated whether individuals from geographically divergent, genetically monomorphic colonies would assemble with individuals of the same genotype. Two artificially fused colonies were prepared, A and B, comprising 200 individuals and 100 individuals, respectively. Each half of the artificially fused colony was composed of workers from two different genetically monomorphic source colonies. The workers assembled as a single colony when the genotype of the source colonies was identical. However, when the genotypes of source colonies were different, the workers did not assemble into one colony, but split into two groups according to genotype. These results suggest that P. punctatus can potentially recognize individual genotype, and select colony members based on an individual’s genotype.

Japanese Queenless Ants, Pristomyrmex punctatus, Prefer the Traces of Both Nestmates and Strangers in Nest Selection

Conspecific avoidance may influence the spatial distribution of colonies in some ants. House-hunting ants (Temnothorax albipennis) avoid nesting in areas where non-nestmates have nested previously. However, no reports are available on conspecific avoidance during nest selection in other ants. In the present study, we investigated nest selection in another nomadic species, the Japanese queenless ant, Pristomyrmex punctatus. Two-choice tests revealed that, similar to house-hunting ants, P. punctatus preferred nests soiled by nestmates to clean nests. However, unlike house-hunting ants, P. punctatus also preferred nests soiled by non-nestmates to a clean nest. Given the choice between a nest soiled by nestmates and one soiled by strangers, P. punctatus, unlike house-haunting ants, showed no significant preference. Thus, conspecific avoidance in nest selection was not observed in P. punctatus. Interspecific differences in ecological factors may drive the evolution of different nest selection strategies.

Do Japanese Queenless Ants Pristomyrmex punctatus (F. Smith) Exhibit Genotype-based Kin Recognition During Colony Formation?

The queenless ant, Pristomyrmex punctatus (F. Smith) reproduces parthenogenetically. Workers lay unfertilized eggs, which develop into female workers. This mode of reproduction generates hereditary clones, though a colony is not necessarily constructed from single clonal line. In a previous study, where a colony was separated into two subcolonies, it was found that genetically monomorphic colonies tended to reassemble but genetically polymorphic colonies did not. Here, we used multiple clonal colonies to investigate whether P. punctatus could recognize “individual” relatedness and assemble with subcolony members of the same clonal type. Results show individuals did not assemble with individuals of the same clonal type in each subcolony. This suggests they cannot recognize individual relatedness.

Influence of Queen and Diet on Nestmate Recognition and Cuticular Hydrocarbon Differentiation in a Fission-Dispersing Ant,Aphaenogaster senilis

In social insects, colony fission is a particular mode of dispersal by which an adult colony splits into two or more independent nests. In the monogynous ant Aphaenogaster senilis, field data suggest that new queens may be produced in queenless daughter nests after nest relocation. Because workers do not fly, colony fission limits dispersal distance, leading young sister colonies to compete together and with the mother queen. In the present study we analysed the effects of queen loss and diet change on nestmate recognition. Queenright colonies were separated into two queenless and one queenright fragments. One queenless group received the same food as the queenright group, while the other queenless group received a different diet for 150 days. Recognition bioassays revealed that aggression between queenright and queenless former nestmates increased progressively until day 20, when they could no longer be reunited. Different diets also induced aggression between orphaned groups. Chemical analyses indicated that cuticular hydrocarbon profiles were already different between groups after 5 days. Overall, our results are in accordance with the graded model of nestmate recognition and suggest that the loss of the mother queen progressively leads to the independence of the related nests after fission. This may also allow queenless ants to merge again with their mother colony during a short time window after fission.

Conflict over the timing of breeder replacement in vertebrate and invertebrate societies

Conflicts over reproduction are common in social groups, where they often result in more or less pronounced reproductive skew. Conflicts are greatest in groups of reproductively totipotent individuals where a single breeder of each sex monopolizes reproduction. Skew models investigate how reproduction is divided among group members, i.e. how the conflict is settled. Here, we investigate the conflict over the timing of breeder replacement.Using a genetic model we show that some non-breeding individuals should challenge the breeder under a wide set of conditions, rather than queue for a breeding vacancy. Consequently, societies of totipotent individuals may be the stage of an almost perpetual conflict between the breeder and helpful reproductives. However, the outcome of this conflict may be determined by non-breeding individuals that are not helpful reproductives (policing behaviours), or constrained by ecological conditions such as high costs of independent breeding or incest avoidance. We discuss our model in the light of skew models and model of matricide, and review the literature of highly skewed vertebrate and invertebrate societies of totipotent individuals (naked and Damaraland mole-rats, African wild dogs, dwarf mongooses, queenless ants, Polistine wasps). This cross-taxonomic review reveals that some non-breeders attempt to replace the breeder or position themselves so as to be able to do so when the opportunity arises, which supports the predictions of the model.

Cuticular Hydrocarbons Provide Reliable Cues of Fertility in the Ant Gnamptogenys striatula

In ca. 150 species of queenless ants, a specialized queen caste is rare or absent, and mated workers take over the role of the queen in some or all of the colonies. Previously, it has been shown that reproduction in queenless ants is regulated by a combination of dominance behavior and chemical fertility signaling. It is unknown, however, whether chemical signals alone can sufficiently regulate reproduction. To investigate this possibility, we studied reproductive regulation in the facultatively queenless ant Gnamptogenys striatula, a species where dominance behavior is rare or absent. Active egg layers and infertile workers showed qualitative and quantitative differences in their cuticular hydrocarbon profile. Five long-chain methyl alkanes, 3,13- and 3,15-dimethyl pentriacontane, 3,13- and 3,15-dimethyl heptentriacontane, and 3,11,15-trimethyl heptentriacontane occurred only on the cuticles of virgin and mated egg layers. Pronounced quantitative differences were found in a further 27 alkenes; alkanes; and mono-, di-, and trimethyl alkanes. Workers that had recently stopped laying eggs had profiles similar to infertile workers, and mating status did not affect this chemical pattern. We conclude that the cuticular hydrocarbon profiles of G. striatula workers provide reliable information about their current fertility. In the interest of colony productivity, this allows reproduction to be regulated without the use of aggression.

Reproductive conflicts and mutilation in queenless Diacamma ants

Reproductive conflicts are particularly intense in queenless ants because colonies are made up of totipotent workers, all potentially able to mate and produce female offspring. After a gamergate (a mated egg-laying worker) dies, aggressive interactions determine her replacement. In Diacamma , the single gamergate systematically mutilates newly emerged workers (callows) and consequently they can never mate. New callows are expected to resist because, once mutilated, they cannot replace the gamergate. In D. ceylonense and D. australe , we studied the behaviour of new callows confronted with dominant individuals of different fertility or age. Faced with a young unmutilated worker (the future gamergate with poorly developed ovaries), callows were aggressive, whereas they did not resist gamergates. We interpret this dichotomy in terms of reproductive differentials between actors and victims. We discuss the selective advantages of mutilation relative to dominance hierarchies which other queenless ants use to regulate monogyny. Mutilation seems to maximize colony productivity by creating irreversibly sterile helpers from newly emerged individuals.

Estimating the rate of gamergate turnover in the queenless ant Diacamma cyaneiventre using a maximum likelihood model

In monogynous ants, the death of the queen gener- ally implies the death of the colony. However, queen replace- ment by either unrelated or related queen has been described in few species. In queenless ants from the genus Diacamma, the single reproductive worker (gamergate) is replaced by one of her daughters (or occasionally by a sister). From a long-term genetic survey of nests of D. cyaneiventre, we es- timated the rate of gamergate turnover as well as the lifespan of workers and gamergate tenure using a maximum likeli- hood model developed for this purpose. We specifi cally compared the genotypes of two cohorts of workers sampled at 2 and 16 months interval from the same nests, using fi ve microsatellite markers. To improve the accuracy of the esti- mates, we also used in the model the nests from the same population sampled only once and analysed by Andre et al. (2001). The model indicates that the possibility of the same nest not sheltering the same colony at two different sampling dates (colony turnover) was not signifi cantly different from zero in our sample. The likelihood of the model was maxi- mal for a probability of gamergate change pg = 0.005 per day (i.e. a gamergate tenure of 200 days) and a worker lifespan w = 60 days, indicating that the gamergate 's tenure is about 3 times longer than workers' expected lifespan in the popula- tion studied. Moreover, the genetic analysis of the gamergate and brood in three colonies excavated completely, reveals that colony fi ssion can occur just after a gamergate replace- ment with the sister of the new gamergate reproducing in the new propagule.

Biogenic amine levels, reproduction and social dominance in the queenless ant Streblognathus peetersi

Social harmony often relies on ritualized dominance interactions between society members, particularly in queenless ant societies, where colony members do not have developmentally predetermined castes but have to fight for their status in the reproductive and work hierarchy. In this behavioural plasticity, their social organisation resembles more that of vertebrates than that of the "classic" social insects. The present study investigates the neurochemistry of the queenless ant species, Streblognathus peetersi, to better understand the neural basis of the high behavioural plasticity observed in queenless ants. We report measurements of brain biogenic amines [octopamine, dopamine, serotonin] of S. peetersi ants; they reveal a new set of biogenic amine influences on social organisation with no common features with other "primitively organised societies" (bumble bees) and some common features with "highly eusocial" species (honey bees). This similarity to honey bees may either confirm the heritage of queenless species from their probably highly eusocial ancestors or highlight independent patterns of biogenic amine influences on the social organisation of these highly derived species.

Hormonal correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi

In colonies of the queenless ant Streblognathus peetersi, dominance interactions produce a reproductive hierarchy in which one individual, the alpha, is capable of producing offspring while her subordinates remain infertile. Based on differences between behaviour and cuticular hydrocarbon profiles, the subordinates can be further divided into high and low ranking workers. Although it had been shown previously that alphas treated with a juvenile hormone analog lose their reproductive status, little was known of the endocrinological basis of dominance in this species. To elucidate the underlying endocrinology of these three ranks, we measured the individual in vitro rate of juvenile hormone (JH) production of excised corpora allata, and the ecdysteroid titer of pooled hemolymph samples. Production of JH was highest in low-ranking workers, intermediate in high rankers, and almost undetectable in alphas. Ecdysteroid titers were low for low rankers, but were more than twice as high for both high rankers and alphas. The results support the hypothesis that JH suppresses ovarian function in these queenless ants, and suggest that ecdysteroids may be responsible for stimulating vitellogenin production. The possible role of these hormones as behavioural modulators is also discussed.

Dominance hierarchies reduce the number of hopeful reproductives in polygynous queenless ants

In many animal societies aggressive interactions regulate essential features such as feeding order and reproductive rights. Because aggressive interactions are costly the number of individuals competing for direct reproduction (hopeful reproductives) affects colony productivity. Using mathematical models, based on the costs/benefits trade-off for a worker to attempt to become a reproductive, we determine the number of hopeful reproductives expected to occur in insect societies with totipotent workers and several reproductives. The model is based on the biology of the polygynous queenless ant Rhytidoponera confusa (Formicidae: Ectatomminae), where every worker can potentially reproduce but only a few actually do, but is valid for all societies with totipotent individuals. We compare the number of hopeful reproductives predicted in the absence of a dominance hierarchy and with a linear dominance hierarchy, and we investigate the effects of colony size, relatedness, and mortality. The models show that a linear dominance hierarchy reduces the number of hopeful reproductives, and additional unpublished models show that this reduction is lower in non-linear hierarchies. Dominance hierarchies are thus favoured by natural selection. Larger colony size and higher mortalities result in longer hierarchy, whereas higher relatedness shortens hierarchy length. These predictions were successfully tested with eight colonies of R. confusa.

Differentiation of the reproductive tract between dominant and subordinate workers in the Japanese queenless ant Diacamma sp.

AbstractIn queenless ants, gamergates (mated egg‐laying workers) fulfil the reproductive task normally reserved for the queen. Every worker is a potential gamergate, thus we expect pronounced conflicts over sexual reproduction within their colonies. In the queenless ant genus Diacamma, gamergates inhibit nest mates from mating by aggressively removing (‘mutilating’) a pair of small appendages on the thorax, termed gemmae, shortly after eclosion. Dissection and serial sectioning of the reproductive tracts of both mutilated and unmutilated individuals of Diacamma sp. from Japan at different ages revealed that mutilation inhibits the development of the bursa copulatrix and the spermatheca, two structures fundamental for sexual reproduction. The precursor of the bursa copulatrix develops into a fully functional structure in unmutilated individuals, whereas it degenerates irreversibly in mutilated callows. Experimental manipulations showed that the removal of the gemmae is not the sole factor regulating this development. The spermathecal epithelium and accessory spermathecal gland of unmutilated individuals are thicker than that of mutilated individuals, indicating a higher degree of activity in the former. Mutilated females are therefore left incapable of copulating and less competent for long‐time sperm storage.

Crossing the taxonomic divide: conflict and its resolution in societies of reproductively totipotent individuals

Reproduction in groups may be unequal, with one or a few individuals monopolizing direct reproduction assisted by nonbreeding helpers. In social insects this has frequently led to a pronounced queen-worker dichotomy and a loss of reproductive totipotency among workers. However, in some invertebrate and all vertebrate societies, all or most individuals remain reproductively totipotent. In these groups, conflicts of interest over reproduction are potentially greatest. Here, we synthesize previous analyses of reproductive conflict, aggression and breeder replacement in haplodiploid societies of totipotent individuals and extend them to cover diploid (vertebrate) examples. We test predictions arising from this approach using the best-studied invertebrate (Dinoponera queenless ants) and vertebrate (naked mole-rat, Heterocephalus glaber) examples, although in principle our analysis applies to all similar groups. We find that premature replacement of a parent breeder by nonbreeders (overthrow) is rare. Dominant coercive control of nonbreeders by the breeder is often unnecessary and honest signalling of breeder vitality can maintain group stability and resolve conflicts over reproduction. We hope that by providing an explicit transfer of social theory between ants and naked mole-rats we will stimulate further cross-taxonomic studies that will greatly broaden our understanding of sociality.

Fertility signalling and reproductive skew in queenless ants

Social insects often show an extreme reproductive skew. In queenless ants, colonies consist of morphologically identical workers that can all potentially reproduce sexually. Similarly to that in social vertebrates, aggression in these ants functions to select the reproductive(s). We investigated the mechanisms underlying reproductive skew in the monogynous queenless ant Streblognathus peetersi . Behavioural observations of disturbed hierarchies were integrated with physiological measures of fertility (vitellogenin titre in the haemolymph) and chemical analysis of cuticular hydrocarbons, which are putative fertility pheromones. This multifaceted approach revealed that the colony reproductive is determined as a result of aggression between high-ranking workers, but once an alpha is established, chemical signalling is enough to maintain reproductive skew. As already reported in several species of ants and also in a social wasp, egg layers have distinct profiles of cuticular hydrocarbons compared with infertile workers. Importantly, ‘high rankers’ who are unable to lay eggs also have a specific cuticular profile; this is consistent with their intermediate state of fertility indicated by vitellogenin levels. Rather than just ovarian activity, the cuticular hydrocarbon profile thus reveals the individual hormonal state that underlies reproductive activity. We compare the fertility signal in queenless ants with the ‘badge of status’ reported in various birds. We discuss the evolutionary stability of this communication system and give special emphasis to ecological constraints and the high degree of intracolonial relatedness typical of social insects.

Reproductive conflict in animal societies: hierarchy length increases with colony size in queenless ponerine ants

Dominance interactions determine reproductive status in many animal societies, including many cooperatively breeding vertebrates and eusocial Hymenoptera without queen-worker dimorphism. Typically, the dominant individual monopolises reproduction, and subordinates behave like helpers. In Dinoponera queenless ants, workers are totipotent females and can potentially reproduce, yet only the top-ranking worker actually reproduces. Individual workers ranked immediately below the dominant breeder worker (gamergate) are hopeful reproductives. Whether or not a worker benefits from joining the hierarchy of high-ranking workers depends on the trade-off between the probability of becoming dominant and reproducing directly, and the colony-level cost of an additional lazy high ranker. Inclusive fitness models predict that the length of the dominance hierarchy depends on relatedness, colony size, and the linearity of the hierarchy. Here, we test the effect of colony size by comparing hierarchy length among three species that differ in colony size (Dinoponera australis: median=14 workers, quartiles=10 and 19 workers; D. gigantea: median=41, quartiles=33 and 74; D. quadriceps: median=78, quartiles=55 and 90). Although difficulties in defining where the hierarchy ends hamper comparisons, the results are in broad agreement with the predictions. Hierarchies are close to the predicted lengths and are longer in species with larger colonies (one, three and three workers in the three species in order from smallest to largest colony vs two, three and four predicted). These conclusions are further supported by determining Kokko and Lindstrom's λ index of skew, which is smaller (i.e. characteristic of a longer hierarchy) in species with larger colonies.

Policing in queenless ponerine ants

Potential reproductive conflicts are common in insect societies. One process that can reduce or suppress conflict is policing. We review worker and "queen" policing in queenless ponerine ants. Queenless ants are an important model system for the study of intracolony reproductive conflict. Policing is widespread in queenless ants because workers are totipotent, so that additional potential conflicts occur in comparison to species where workers cannot mate, and these additional conflicts are frequently reduced by policing. Policing is more diverse than suggested by the examples known in other social insects. In almost all species of social Hymenoptera it can include preventing workers from reproducing by killing worker-laid eggs, but in queenless ants it can additionally include immobilisation or mutilation of workers attempting to reproduce by replacing the gamergate (i.e. mated worker with a queen-like role) or by becoming an extra gamergate. Policing by both workers and by the gamergate are important. Policing can be facultative. Depending on the age of the gamergate, workers can prevent her replacement by immobilising challenging workers or they can favour replacement by immobilising the gamergate. The initial definition of policing was inspired by species in which workers retain ovaries but cannot mate. We broaden the definition to include species, such as queenless ants, where females are totipotent, thereby including not only conflict over male production but also over gamergate replacement and gamergate number. Finally, we compare policing with punishment and dominance hierarchy. Policing is not always punishment and it does not necessarily entail dominance relationships.

Dominance Interactions Regulate Worker Mating in the Polygynous Ponerine AntGnamptogenys menadensis

In queenless ants, workers compete aggressively to be reproductives instead of sterile helpers. To limit the number of reproductives, either mating or egg‐laying by mated workers can be regulated. InGnamptogenys menadensis, all mated workers reproduce, and field data presented here indicate that mating is not random. We removed gamergates experimentally (n=16 groups) to induce mating and gamergate replacement. Virgin workers engaged in agonistic interactions, allowing us to classify them into two groups: dominants performed antennal boxing and biting, while subordinates did not. However, a few subordinates cooperated to immobilize individual dominant workers. This effectively reduced the number of dominants because immobilized dominants became subordinates. Six to 12 wks after the removal of reproductives, between one and eight dominants per colony started to perform ‘sexual calling’ outside the nest entrance. Sixteen (out of 33) dominants mated with foreign males introduced in five experimental groups. None of the subordinate workers mated. The probability of mating is thus regulated by dominance interactions among workers and immobilizations initiated by infertile workers in this polygynous queenless ant.

Reproduction versus work in queenless ants: when to join a hierarchy of hopeful reproductives?

Many animal societies contain few breeders and many helpers. In some species, individuals can become either helpers or breeders, and breeding is often restricted to high rankers in a dominance hierarchy. In social Hymenoptera with no morphological queen caste, all females have the potential to become dominant and reproduce. In our model, females involved in the hierarchy do not work and gain direct fitness if they become alpha following death of the current alpha, while females not in the hierarchy gain indirect fitness by working. Using an inclusive-fitness model combined with models of alpha replacement in slightly different types of near-linear hierarchies, we determined the critical rank (i.e., optimal hierarchy length) for which the gain in fitness by entering the hierarchy as a hopeful reproductive equals the cost caused by a reduced worker force. High relatedness decreases the hierarchy length by lowering the potential benefit of entering the hierarchy. In contrast, large colony size increases the hierarchy length because the cost of each non-working high ranker is relatively lower. The model predicts a hierarchy of five workers in the queenless ant Dinoponera quadriceps, close to empirical data which show that in a colony of about 100 females, the top 5 carry out 72.8% of the aggressive interactions. The model is also used to make several testable predictions about the effect on hierarchy length of (1) variation in colony size and (2) variation in worker reproductive options between species of the queenless ants genus Diacamma.

Absence of sex-differential brood raising by workers in Diacamma sp. from Japan

To optimally allocate resources between workers, reproductive females, and males, ant workers have to be able to identify the sex of larvae and raise them differently. The ability of workers to discriminate between the sexes in the brood was tested in colonies of queenless ponerine ants, Diacamma sp., from Japan. The ratio of male eggs in the egg pile was increased experimentally. This manipulation resulted in a corresponding increase in the ratio of adult males, suggesting that Diacamma workers do not raise the sexes differently.