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     

Nestmate recognition and the genetic relatedness of nests in the ant Formica pratensis

Genetic relatedness of the mound-building ant Formica pratensis was determined by means of microsatellite DNA polymorphism, and its impact on nestmate recognition was tested in a population in Southern Sweden (Oeland). Recognition between nests was measured by testing aggression levels between single pairs of workers. The genetic distances of nests (Nei's genetic distance) and the spatial distance of nests were correlated and both showed a strong relation to the aggression behavior. Multiple regression analysis revealed a stronger impact of genetic relatedness rather than spatial distances on aggression behavior. Neighbouring nests were more closely related than distant nests, which may reflect budding as a possible spreading mechanism. The genetic distance data showed that nestmate recognition was strongly genetically influenced in F. pratensis. Received: 2 October 1997 / Accepted after revision: 10 January 1998     

Seasonal polydomy and unicoloniality in a polygynous population of the red wood ant Formica truncorum

Ant colonies may have a single or several reproductive queens (monogyny and polygyny, respectively). In polygynous colonies, colony reproduction may occur by budding, forming multinest, polydomous colonies. In most cases, budding leads to strong genetic structuring within populations, and positive relatedness among nestmates. However, in a few cases, polydomous populations may be unicolonial, with no structuring and intra-nest relatedness approaching zero. We investigated the spatial organisation and genetic structure of a polygynous, polydomous population of Formica truncorum in Finland. F. truncorum shifts nest sites between hibernation and the reproductive season, which raises the following question: are colonies maintained as genetic entities throughout the seasons, or is the population unicolonial throughout the season? Using nest-specific marking and five microsatellite loci, we found a high degree of mixing between individuals of the population, and no evidence for a biologically significant genetic structuring. The nestmate relatedness was also indistinguishable from zero. Taken together, the results show that the population is unicolonial. In addition, we found that the population has undergone a recent bottleneck, suggesting that the entire population may have been founded by a very limited number of females. The precise causes for unicoloniality in this species remain open, but we discuss the potential influence of intra-specific competition, disintegration of recognition cues and the particular hibernation habits of this species.     

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.     

Self-organized digging activity in ant colonies

Many ant species adjust the volume of their underground nest to the colony size. We studied whether the regulation of the volume of excavated sand could result from an interplay between recruitment processes and ant density. Experiments were performed with different group sizes of workers in the ant Messor sancta. When presented with a thin homogeneous sand disk, these groups excavated networks of galleries in less than 3 days. The excavation dynamics were logistic shaped, which suggests the existence of a double feedback system: a positive one resulting in an initial exponential growth phase, and a negative one leading the dynamics to a saturation phase. The total volume of excavated sand was almost proportional to the number of workers. We then developed a model in which we incorporated the quantitative behavioral rules of the workers digging activity. A positive feedback was introduced in the form of a recruitment process mediated by pheromones. The model predicts that the excavation dynamics should be logistic shaped and the excavation should almost stop despite the absence of any explicit negative feedback. Moreover, the model was able to reproduce the positive linear relationship between nest volume and colony size.Communicated by K. Ross     

Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size

Models based on the kin selection theory predict that in social hymenopterans, queens may favor a lower investment in the production of sexuals than workers. However, in perennial colonies, this conflict may be tuned down by colony-level selection because of the trade off between colony survival and reproductive allocation. In this study, we present a survey of sexual production in colonies of Aphaenogaster senilis, a common species of ant in the Iberian Peninsula. Similar to most species that reproduce by fission, males were found in large excess compared to gynes (172:1). Sexuals were more likely to be found in queenless than in queenright (QR) field colonies. However, we also found a few gynes and numerous males in very large QR colonies. We compared these data with those available in the literature for A. rudis, a congeneric species from North America that has independent colony founding. The sex ratio in this species was only five males for each female, and sexuals were mostly found in QR nests, irrespective of colony size. We confirmed queen inhibition of sexual production in A. senilis in laboratory experiments and provide evidence that this inhibition is mediated by a nonvolatile pheromone. To seek the potential source of such a queen pheromone, we analyzed the secretions of two conspicuous exocrine glands, the Dufour’s and postpharyngeal glands (DG and PPG, respectively) in both queens and workers. Both secretions were composed of hydrocarbons, but that of DG also contained small quantities of tetradecanal and hexadecanal. The hydrocarbon profile of the DG and PPG showed notable caste specificity suggesting a role in caste-related behavior. The PPG secretions also differed between colonies suggesting its role in colony-level recognition. We suggest that in A. senilis, there are two modes of colony fission: First, in very large colonies, gynes are produced, probably because of the dilution of the queen pheromone, and consequently one or more gynes leave the mother colony with workers and brood to found a new nest. This is beneficial at the colony level because it avoids the production of costly sexuals in small colonies. However, because the queen and workers have different optima for sexual production, we hypothesize that queens tend to overproduce the pheromone to delay their production. This in turn may drive workers to leave the mother colony during nest relocation and to produce sexuals once they are away from the queen’s influence, creating a second mode of colony fission.     

Queen dimorphism and reproductive strategies in the fire ant Solenopsis geminata (Hymenoptera: Formicidae)

Alate trapping studies of a monogyne population of the fire ant Solenopsis geminata indicate that two sizes of gynes are produced. Macrogynes, which participate in late spring and summer mating flights, are larger, fattier, and more than twice as heavy as microgynes, which participate in fall mating flights. Three patterns of gyne production were observed in 51 colonies studied: 35 produced macrogynes only, 9 produced microgynes only, and 7 produced both morphs, contributing to both summer and fall mating flights. Behavioral evidence and rearing studies suggest that macrogynes found new colonies independently, whereas microgynes achieve colony queen status by infiltrating or being adopted by established colonies. Of the total number of female alates collected from the trapped colonies, 56% were microgynes. However, because of their smaller size and lower fat content, microgynes made up only one-third of the caloric investment in female alates. By measuring the thorax lengths of queens from mature colonies, we determined that at least 56% were macrogynes and 35% or more were microgynes. These results indicate that as a reproductive strategy, colony investment in microgyne production may have at least as high a payoff as investment in macrogyne production.This is publication #24 of the Fire Ant Research Team     

Colony take-over and brood survival in temporary social parasites of the ant genus Formica

Parasites reduce host fitness, and so instigate counter adaptations by their hosts. In temporary social parasitism, usurpers must not only enter the colony unharmed, but also have their eggs reared by the host workers. We introduced parasitic Formica lugubris and Formica aquilonia queens into queen right and orphaned fragments of three host species, Formica cinerea, Formica picea and Formica fusca, and show that workers of all three host species kill over 40 % of the introduced queens within 10 days, regardless of the presence/absence of a resident queen, and parasite species. More parasite queens died in F. cinerea than in F. picea and F. fusca. There were no major differences in survival between the parasite species (except that F. lugubris survived longer than F. aquilonia in F. fusca colonies compared to F. picea colonies), but parasite queens survived longer in orphaned than in queen right fragments of F. fusca. Experimental introduction of parasite (F. aquilonia) eggs into orphaned colonies of F. fusca showed that none of the parasite eggs were reared until pupation; whereas on average, 12 % of the con-specific hetero-colonial eggs introduced in the same manner were reared until pupation. In all colonies that received parasite brood, all offspring consisted of worker-laid males, whereas the corresponding value was 50 % for colonies that received con-specific hetero-colonial brood. Thus, when the risks of entering host colonies and brood failure are combined, the rate of successful colony take-over is very low. Moreover, the host workers can to some extent alleviate the costs of parasitism by producing a final batch of own offspring.     

Colony fission affects kinship in a social insect

Establishment of new groups is an important step in the life history of a social species. Fissioning is a common mode not only in group proliferation, for instance, as a regular part of the life cycle in the honey bee, but also when multiple females reproduce in the same group, as in multiple-queen ant societies. We studied the genetic consequences of fissioning in the ant Proformica longiseta, based on DNA microsatellites. In P. longiseta, new nests arise by fissioning from the old ones when they grow large, and the daughter nests consist of workers and queens or queen pupae but never both. Our results show that fissioning is not entirely random with respect to kinship. Workers tend to segregate along kin lines, but only when the initial relatedness in the parental nests is low. Workers in a daughter nest also tend to be associated with closely related adult queens, whereas such an association is not detected between workers and queen pupae. Most queens and workers are carried to the daughter nest by a specialized group of transporting workers, suggesting active kin discrimination by them. Fissioning pattern in P. longiseta is different from that found in other social insects with regular fission (e.g., the honey bee, swarm-founding wasps), where no fissioning along kin lines has been found. It does, however, resemble fissioning in another group of social animals: primates.     

Stable relatedness structure of the large-colony swarm-founding wasp Polybia paulista

In social-insect colonies, cooperation among nestmates is generally stabilized by their high genetic similarity. Thus, fitness gained through cooperation drops quickly as the number of reproductive females (queens) increases. In this respect, wasps of the tribe Epiponini have attracted special attention, because the colonies have tens, or even hundreds of queens. It has been empirically or genetically confirmed that relatedness within nestmates can be elevated by a mechanism known as cyclical monogyny, under which new queens are produced only after the number of old queens is reduced to one. Another likely factor that can increase relatedness within nestmates under polygyny is comb partitioning by queens. If queens concentrate their egg laying on one or a subset of the available combs, then workers may be able to rear closer relatives by focusing their work on the comb where they emerged. Using microsatellite markers, we tested the hypotheses of cyclical monogyny and comb partitioning by queens increasing relatedness within nestmates under polygyny in the large-colony epiponine wasp, Polybia paulista. There were no significant differences between relatedness within combs and between combs, and thus we ruled out the possibility that each queen partitions reproduction between combs. However, as cyclical monogyny predicts, a lower effective number of queens contributed to queen production than to worker production. Cyclical monogyny explained well the observed smaller effective number of queens for new queens than that for workers, but failed to explain the stable relatedness values throughout colony cycles.Communicated by L. Keller     

Two independent mechanisms of egg recognition in worker <Emphasis Type="Italic">Formica fusca</Emphasis> ants

Informational constraints can be an important limitation on the accuracy of recognition. One potential constraint is the use of recognition information from the same sources in multiple discriminatory contexts. Worker wood ants, Formica fusca, discriminate eggs based on their maternal sources of origin in two main contexts: recognition of eggs laid by nestmate versus non-nestmate queens and recognition of worker-laid versus queen-laid eggs. We manipulated the experience of F. fusca workers in laboratory colonies to both worker-laid and queen-laid eggs by transferring eggs between colonies in order to investigate whether these two contexts of egg discrimination are independent. Experience of non-nestmate queen-laid eggs significantly increased worker acceptance of both familiar (18% accepted) and unfamiliar (10%) queen-laid eggs compared to control workers without experience of eggs other than those laid by their own colony’s queen (2%). In contrast, worker acceptance of worker-laid eggs was not affected by variation in the egg experience of workers (14% in workers from control colonies exposed only to eggs from their own colony’s queen versus 19% and 17% in workers from colonies which had received eggs laid by either a non-nestmate queen or nestmate workers, respectively). Our results suggest that these two recognition contexts do not strongly constrain each other and are different in their ontogeny. In particular, worker-laid eggs are universally discriminated against by workers from colonies with a queen whatever the egg experience of the workers, while non-nestmate queen-laid eggs are strongly discriminated against only by workers without experience of eggs laid by more than one queen.     

Prior experience with eggs laid by non-nestmate queens induces egg acceptance errors in ant workers

We studied the effect of prior experience to eggs laid by nestmate and non-nestmate queens on the acceptance of queen-laid eggs by worker wood ants, Formica fusca. We transferred eggs from a non-nestmate queen into colonies during early spring, when their own queen was recommencing egg laying. A few weeks later, workers from these “experienced” colonies accepted eggs of both familiar (44% acceptance) and unfamiliar (40%) non-nestmate queens much more than workers from control colonies (2%) that had only had previous contact with their own queen’s eggs. Thus, prior exposure to eggs laid by a non-nestmate queen induces much greater acceptance of all non-nestmate queen-laid eggs. Mechanistically, we hypothesize that exposure to eggs from several queens may increase acceptance by causing a highly permissive acceptance threshold of non-nestmate queen-laid eggs rather than by widening the template for acceptable queen-laid eggs. These novel results show that egg-discrimination behaviour in F. fusca is flexible and that workers respond to the diversity of eggs experienced in their colony.     

Compensating for the costs of polygyny in hen harriers Circus cyaneus

In polygynous species, the adults are faced with a dilemma during chick rearing. Males must decide how to distribute food between their females and food allocation patterns are often highly unequal. In turn, the females that receive less food from males have to decide how much time to invest in additional hunting. If they spend more time hunting, then they leave their young exposed to weather and predators. However, if they stay at the nest, they increase the risk of their chicks starving. One way that birds may compensate for reduced provisioning is by increasing the size of prey caught. We tested this hypothesis by comparing prey deliveries to nests of hen harriers, Circus cyaneus, with females of different breeding status. As expected, male harriers delivered less food items to the nests of polygynous females, and especially their secondary, or β females. However, both sexes were able to compensate by delivering larger items and there was no difference in the overall mass of food delivered to nests. Moreover, females spent a similar amount of time at the nest, irrespective of status, and there were no overall differences in breeding success. Our results show that polygynous female harriers can compensate for the costs of polygyny, but we suggest that their ability to do so will vary according to the abundance of both large prey and predators.     

Worker policing and nest mate recognition in the ant <Emphasis Type="Italic">Formica fusca</Emphasis>

A conflict over male production arises in social insects where workers are able to lay unfertilized male eggs. This happens because each female (queen or worker) is most closely related to her own sons and is thus predicted to reproduce. The conflict is modulated by worker policing where workers prevent each other from reproducing by aggression or egg cannibalism. In this study, we show that in the ant Formica fusca, worker policing occurs by egg cannibalism rather than by overt aggression among workers. Furthermore, we show that, contrary to bees, wasps and other ant species, egg discrimination in F. fusca is not based only on a universal queen signature chemical and that nest mate recognition of eggs occurs.     

All-offspring dispersal in a tropical mammal with resource defense polygyny

In polygynous mammals, males are usually responsible for gene flow while females are predominantly philopatric. However, there is evidence that in a few mammalian species female offspring may disperse to avoid breeding with their father when male tenure exceeds female age at maturity. We investigated offspring dispersal and local population structure in the Neotropical bat Lophostoma silvicolum. The mating system of this species is resource defense polygyny, with the resource being active termite nests, excavated by single males, which are then joined by females. We combined field observations of 14 harems during 3 years and data about the genetic structure within and between these groups, calculated with one mitochondrial locus and nine nuclear microsatellite loci. The results show that both male and female offspring disperse before maturity. In addition, we estimated life span of excavated termite nests and the duration they were occupied by the same male. Our findings suggest that long male tenure of up to 30 months is indeed a likely cause for the observed dispersal by female offspring that can reach maturity at a low age of 6 months. We suggest that dispersal by offspring of both sexes may occur quite frequently in polygynous tropical bats and thus generally may be more common in mammals than previously assumed.     

Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus

Summary The ant L. longispinosus displays geographic variation in its pattern of facultative polygyny (Fig. 2). In nature, nest density and frequency of multiple queening are positively associated over three sites. A putative causal relation between availability of vacant nest sites and polygyny was examined in New York, where a plot was seeded with additional nest sites and monitored for 24 months. Both queen number and worker number per nest on the experimental plot were reduced relative to controls (Fig. 4, Fig. 5), indicating that scarcity of available nest sites influences the pattern of polygyny in this species. The observed demographic changes resulted from fractionation of existing colonies; adding nest sites induced polydomy. Although numbers of adult ants changed with addition of nest sites, the numbers of immatures were no different after 2 years (Table 1), suggesting that the population was undergoing growth to expand into the additional sites. These results are the first direct experimental evidence linking polygyny to an ecological parameter for any ant species.     

Multiple mating and facultative polygyny in the Panamanian leafcutter ant Acromyrmex echinatior

Queen mating frequency of the facultatively polygynous ant Acromyrmex echinatior was investigated by analysing genetic variation at an (AG)_n repeat microsatellite locus in workers and sexuals of 20 colonies from a single Panamanian population. Thirteen colonies were found to be monogynous, 5 colonies contained multiple queens, whereas the queen number of 2 colonies remained unresolved. Microsatellite genotypes indicated that 12 out of 13 queens were inseminated by multiple males (polyandry). The mean queen mating frequency was 2.53 and the mean genetically effective paternity frequency was 2.23. These values range among the highest found in ants, and the results are in keeping with the high mating frequencies reported for other species of leafcutter ants. Consistent skew in the proportional representation of different patrilines within colonies was found, and this remained constant in two consecutive samples of offspring. Dissections showed that all examined queens from multiple-queen colonies were mated egg-layers. The mean relatedness value among nestmate workers in polygynous colonies was lower than that for monogynous colonies. No diploid males were detected in a sample of 70 genotyped males. Worker production of males was detected in one queenless colony. We discuss our findings in relation to known patterns of multiple maternity and paternity in other eusocial Hymenoptera. Received: 2 September 1998 / Received in revised form: 3 February 1999 / Accepted: 7 February 1999     

Reduced disease in offspring: A benefit of coloniality in sunfish

Summary Increased disease and parasitism are a well-documented cost of group living for colonial birds and mammals, but we now show that disease in offspring of fish may be reduced by nesting in colonies. The aquatic fungusSaprolegnia sp., which is a common cause of egg mortality among freshwater fishes, is more prevalent in the nests of solitary than colonial male bluegill sunfish (Lepomis macrochirus). Moreover, fungal infection decreases with nest density in colonies. This may be due in part to a behavioural advantage since colonial males can devote less time to defending eggs and more time to fanning them, which reduces fungal infection. In addition, we demonstrate experimentally that solitary nests become infected at higher rates than colonial nests, even in the absence of parental males. This suggests that colonies are encountered by spores at a lower rate and/or that the large number of nests in colonies dilutes the number of fungal spores per nest. Through one or all of these mechanisms, egg mortality in colonial nests is lowered significantly. Therefore, in some cases, disease may select for group living.     

Is the alkaloid in 2spot ladybirds (Adalia bipunctata) a defence against ant predation?

Garden black ants,Lasius niger L., in a laboratory colony, attacked three species of live ladybirds found near their nest, killing the smaller two species. A second colony was offered artificial diets containing crushed ladybirds of two species, and the ants' choice of feeding site noted. Both the diets were aversive compared to control, but that containing 7spot,Coccinella septempunctata L., was more aversive than the diet containing 2spot,Adalia bipunctata L. The implications of this lesser protection for 2spots in terms of the chemical defence of the species are discussed.     

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.