Colony foundation and polygyny in the ant Formica podzolica

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

Effects of the social environment on the survival and fungal resistance of ant brood

The phenotype of social animals can be influenced by genetic, maternal and environmental effects, which include social interactions during development. In social insects, the social environment and genetic origin of brood can each influence a whole suite of traits, from individual size to caste differentiation. Here, we investigate to which degree the social environment during development affects the survival and fungal resistance of ant brood of known maternal origin. We manipulated one component of the social environment, the worker/brood ratio, of brood originating from single queens of Formica selysi. We monitored the survival of brood and measured the head size and ability to resist the entomopathogenic fungus Beauveria bassiana of the resulting callow workers. The worker/brood ratio and origin of eggs affected the survival and maturation time of the brood and the size of the resulting callow workers. The survival of the callow workers varied greatly according to their origin, both in controls and when challenged with B. bassiana. However, there was no interaction between the fungal challenge and either the worker/brood ratio or origin of eggs, suggesting that these factors did not affect parasite resistance in the conditions tested. Overall, the social conditions during brood rearing and the origin of eggs had a strong impact on brood traits that are important for fitness. We detected a surprisingly large amount of variation among queens in the survival of their brood reared in standard queenless conditions, which calls for further studies on genetic, maternal and social effects influencing brood development in the social insects.     

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

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

Seasonal nestmate recognition in the ant Formica exsecta

Under favorable conditions, the mound-building ant Formica exsecta may form polydomous colonies and can establish large nest aggregations. The lack of worker aggression towards nonnestmate conspecifics is a typical behavioral feature in such social organization, allowing for a free flux of individuals among nests. However, this mutual worker toleration may vary over the seasons and on spatial scales. We studied spatio-temporal variation of worker–worker aggression within and among nests of a polydomous F. exsecta population. In addition, we determined inter- and intracolony genetic relatedness by microsatellite DNA genotyping and assessed its effect on nestmate recognition. We found significant differences in the frequency of worker exchange among nests between spring, summer, and autumn. Moreover, we found significant seasonal variation in the level of aggression among workers of different nests. Aggression levels significantly correlated with spatial distance between nests in spring, but neither in summer nor in autumn. Multiple regression analysis revealed a stronger effect of spatial distances rather than genetic relatedness on aggressive behavior. Because nestmate discrimination disappeared over the season, the higher aggression in spring is most plausibly explained by cue intermixing during hibernation.     

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     

Fire ant polymorphism: the ergonomics of brood production

Summary Social organization is generally assumed to increase colony efficiency and survival; however, little quantitative information is available to support this assumption. Polymorphism is an important aspect of labor division in colonies of the fire ant, Solenopsis invicta. Our objective was to investigate the effect of fire ant polymorphism on brood production efficiency. We set up standardized polymorphic colonies with a full range of worker sizes and artificial monomorphic colonies that contained only small, medium or large workers respectively. Polymorphic colonies produced brood at about the same rate as colonies composed of only small workers (Fig. 2A). Colonies composed of only medium workers produced about 30% less brood, and colonies composed of only large workers produced little or no brood at all. This pattern was independent of colony size; however, smaller colonies (0.75 g, live weight) produced almost twice as much brood per gram of workers as larger colonies (3.0g). Additional experiments revealed that the size of workers in the artificial monomorphic colonies affected all stages of brood rearing. Large workers not only inhibited the development of early and late instar larvae (Fig 4), but also reduced the queen's oviposition rate (Fig. 3). Brood production efficiency on an energetic basis was determined by dividing the grams of brood produced per unit time by the energetic costs expended for the maintenance and production of each worker size class. Worker maintenance costs were estimated from respiration while production costs were determined from the caloric content of worker tissue divided by their average longevity. Worker respiration per milligram body weight decreased about 40% as body size increased (Fig. 5). Large workers lived about 50% longer than small workers (Fig. 6) and contained 9% more energy per milligram of tissue (Fig. 7). Energetic efficiency in polymorphic colonies was approximately 10% higher than in colonies composed of only small workers (Fig. 9). In other words, when food supplies are limiting, polymorphism may offer a slight advantage in brood production.     

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

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

Slave addition increases sexual production of the facultative slave-making ant Formica subnuda

Formica subnuda is a facultative slave-making ant, and colonies without slaves are often found. We studied the effect of slave workers on sexual production of F. subnuda by experimentally increasing the proportion of slaves. We added c. 4000 worker pupae of the ant F. podzolica to 15 F. subnuda colonies and kept 15 colonies as controls. The following year we excavated all colonies, counted the proportion of slaves, the total number of workers (colony size) and the number of sexual offspring. The proportion of slaves was significantly higher in the slave-added colonies than in the control colonies. The total production of sexual offspring increased 57% in the treatment colonies in comparison to the controls. When colony size was adjusted to the number of sexual offspring, the treatment colonies produced significantly more sexual offspring than the controls. Slave addition did not alter sex ratios. We suggest that two alternative mechanisms, not mutually exclusive, caused the increase of sexual production in F. subnuda colonies: (1) Most of the added pupae were consumed and stored as fat body in workers at the end of the experimental year; the following spring the excess fat was metabolized and fed to the developing sexual larvae, or (2) a proportion of the added pupae hatched to become slaves; the following spring these slaves foraged actively for protein-rich food for the developing sexual offspring. Received: 27 April 1995/Accepted after revision: 23 October 1995     

Maximization of foraging efficiency and resource defense by group retrieval in the ant Formica schaufussi

Summary Workers of the ant Formica schaufussi forage as individuals and cooperate in groups to retrieve arthropod prey. In 2 sample years, group-transported prey were on average 6.8 and 4.7 times heavier than individually retrieved items, and the average loading ratios of groups were greater than the loading ratios of single foragers. Retrieval group size was adjusted to prey size, and prey transport velocity for individuals and groups tended to decrease with increasing prey weight. The efficiency of individual and group retrieval, estimated from calculations of the prey delivery rate to the nest (PDR) achieved by each foraging mode, varied as a function of prey size. Individual retrieval maximized PDR at a prey weight of 19.5 mg, and group transport maximized PDR at 190 mg. Although the PDR maxima of an individual in a group and a solitary forager were approximately equal, depending on prey size, group transport may maximize foraging efficiency. Group transport also decreased interference competition from sympatric ant species. Group-transported prey having a greater likelihood of successful retrieval were within the size range of prey that maximized foraging efficiency. Transport group size appeared to be more important in prey defense than in increasing prey transport velocity, suggesting an important role of group size in competitive ability.Offprint requests to: J.F.A. Traniello     

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.     

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     

Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics

Social groups are at particular risk for parasite infection, which is heightened in eusocial insects by the low genetic diversity of individuals within a colony. To combat this, adult ants have evolved a suite of defenses to protect each other, including the production of antimicrobial secretions. However, it is the brood in a colony that are most vulnerable to parasites because their individual defenses are limited, and the nest material in which ants live is also likely to be prone to colonization by potential parasites. Here, we investigate in two ant species whether adult workers use their antimicrobial secretions not only to protect each other but also to sanitize the vulnerable brood and nest material. We find that, in both leaf-cutting ants and weaver ants, the survival of the brood was reduced and the sporulation of parasitic fungi from them increased, when the workers nursing them lacked functional antimicrobial-producing glands. This was the case for both larvae that were experimentally treated with a fungal parasite (Metarhizium) and control larvae which developed infections of an opportunistic fungal parasite (Aspergillus). Similarly, fungi were more likely to grow on the nest material of both ant species if the glands of attending workers were blocked. The results show that the defense of brood and sanitization of nest material are important functions of the antimicrobial secretions of adult ants and that ubiquitous, opportunistic fungi may be a more important driver of the evolution of these defenses than rarer, specialist parasites.     

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     

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.     

A new technique to identify and assess the dispersion of eggs of individual brood parasites

Summary A new technique for identifying eggs of brood parasites to individual females is presented. Twenty-six undeveloped brown-headed cowbird eggs were removed from nests on a small study area in eastern Kansas. Proteins from their yolks were subjected to starch gel electrophoresis. Electromorphs are completely of maternal origin, and results from a separate sample from California showed that electromorphs do not differ among eggs from an individual cowbird. Combinations of electromorphs at four polymorphic loci identified eggs to seven hypothetical females. The binomial probability that two or more of eight females (fieldwork suggested no more than 7–8 females laying on the site) share a particular combination was calculated from an off-site, independent sample of eggs. Six of seven of these probabilities were below 5%. Eggs collected directly from two females matched two of the electromorph combinations. Discriminant function analyses on 11 egg variables correctly classified 95.7% of the eggs to the group in which they were placed by electromorph combination. Patterns of dispersion of the eggs of individuals over host species, time and space were assessed. Despite small sample sizes, it is clear that individuals are not host-specific and overlap considerably in their laying areas.     

Interference by wood ant influences size selection and retrieval rate of prey by Formica fusca

Summary Dominance relations between the territorial wood ant Formica polyctena and the submissive F. fusca generate testable predictions on the mechanisms of their coexistence. Here I tested the influence of interference competition by the dominant F. polyctena on the foraging of F. fusca. In the presence of F. polyctena, the activity and the retrieval rate of items of F. fusca decreased significantly. When F. fusca were given a choice between small chironomids and flies a hundred times heavier they selected nearly always flies in the absence of wood ants; when disturbed F. fusca took proportionately more chironomids. In nature, irrespective of distance from the wood-ant mound the size distribution of potentially available food items was the same. F. fusca collected smaller items close to the wood-ant mound, where the density of interfering wood ants was high, than far from it. Also, F. polyctena carried larger protein items from the outskirts of its territory than from the center. The items of F. fusca were on average smaller than those of F. polyctena although the item-size overlap was substantial. When encountering a F. polyctena, those F. fusca workers carrying a fly always lost their booty to the dominant but always managed to bring the chironomids to the nest. F. fusca and F. polyctena were equally efficient in detecting single chironomids placed on the surface of ground, but the presence of either species decreased the discovery rate of the other. This implies mutual exploitation competition between the species for the locally most abundant protein resource. F. polyctena found single flies faster than F. fusca. In an earlier study I showed that close to the wood-ant mound the colony size and production of sexual offspring of F. fusca were reduced. I suggest that the suppressed colony success of F. fusca is attributable to the diminished size and decreased retrieval rate of prey items close to the woodant mound abounding with interfering wood-ant foragers.     

Colony genetic diversity affects task performance in the red ant Myrmica rubra

High relatedness and low genetic diversity among individuals in a group is generally considered crucial to the evolution of cooperative behaviour. However, in about a third of social insect species, intracolonial genetic diversity is increased because of derived polyandry (multiple mating by queens) and/or polygyny (multiple reproductive queens). Several studies have shown that increased intracolonial genetic diversity can enhance task performance in honey bees, but evidence of such effect in other social insects is still lacking. Why increased genetic diversity has evolved in some, but not all species, is a fundamental question in sociobiology. In this study, we investigated the effect of intracolonial genetic diversity on the task of nest migration, using the facultatively polyandrous and polygynous red ant Myrmica rubra. Genetic diversity significantly affected migration speed, but its effects were context dependent. Migration speed correlated positively with genetic diversity in one experiment in which migrations were into a known nest site, due to quicker transfer of brood into the new nest once consensus was reached. However, in a another experiment in which migration included scouting for new nest sites, migration speed correlated negatively with genetic diversity, due to slower discovery of new nest sites and slower transfer of brood into the new nest. Our results show for the first time that genetic diversity affects task performance in a social insect other than the honeybee, but that it can produce contrasting effects under different conditions.     

Testing the limits of social resilience in ant colonies

Social resilience is the ability of Leptothorax ant colonies to re-assemble after dissociation, as caused, for example, by an emigration to a new nest site. Through social resilience individual workers re-adopt their spatial positions relative to one another and resume their tasks without any time being wasted in worker respecialisation. Social resilience can explain how an efficient division of labour can be maintained throughout the trials and tribulations of colony ontogeny including the, often substantial, period after the queen dies when the ability to conserve worker social relationships may be essential for efficiency to be maintained. The mechanism underlying social resilience is, therefore, expected to be robust even in the absence of many of the colony’s components, such as the queen, the brood and even a large proportion of the workers. Such losses are likely, given the ecology of this genus. Using sociotomy experiments, we found that social resilience can occur in the absence of the queen. Furthermore, the spatial component of social resilience can occur even when the queen, the brood, as well as a large proportion of the workers, are all absent simultaneously and hence many of the tasks are missing. We conclude, therefore, that social resilience is indeed robust. This does not, however, preclude worker flexibility in response to changes in task supply and demand. We propose a possible sorting mechanism based on worker mobility levels which might explain the robustness underlying this phenomenon. Received: 25 October 1999 / Accepted: 1 April 2000