Polygyny,relatedness and nest founding in the polygynous myrmicine ant Leptothorax acervorum (Hymenoptera; Formicidae)

Summary There is high within-nest relatedness for functional queens (with corpora lutea), nonfunctional queens (without corpora lutea), and workers in polygynous nests of Leptothorax acervorum. The high functional queen relatedness suggests that young mated queens are adopted back to their mother nest. Functional queen relatedness does not change with the number of queens present in the nest, suggesting that the number of generations of queens, on average two to three, is rather stable. Worker relatedness decreases with increasing number of functional queens per nest (Tables 5, 6). The number of queens contributing offspring to the nest (mothers), estimated from worker and functional queen relatedness, is lower than the number of functional queens, particularly in highly polygynous nests. Estimates of number of mothers in monogynous nests indicate that these nests previously were polygynous (Table 7). There is no correlation between nest relatedness and distance between nests, and budding-off, if present, thus appears to be a rare mode of nest founding (Table 8). There are no indications of inbreeding in the two populations studied since the frequency of heterozygotes is as high as expected from random mating (Table 4). Most likely, polygyny is the rule in L. acervorum and serves to secure the presence of queens in the nest.     

Oligogyny by unrelated queens in the carpenter ant, Camponotus ligniperdus

Multilocus DNA fingerprinting and microsatellite analysis were used to determine the number of queens and their mating frequencies in colonies of the carpenter ant, Camponotus ligniperdus (Hymenoptera: Formicidae). Only 1 of 61 analyzed queens was found to be double-mated and the population-wide effective mating frequency was therefore 1.02. In the studied population, 8 of 21 mature field colonies (38%) contained worker, male, or virgin queen genotypes which were not compatible with presumed monogyny and therefore suggested oligogyny, i.e., the cooccurrence of several mutually intolerant queens within one colony. Estimated queen numbers in oligogynous colonies ranged between two and five. According to the results of the genetic analysis, most of the queens coexisting in oligogynous colonies were not closely related. Pleometrosis is very rare and queenless colonies adopt mated queens both in the laboratory and field. Therefore, the most plausible explanation for the origin of oligogynous colonies in C. ligniperdus is the adoption of unrelated queens by orphaned mature colonies. The coexistence of unrelated, but mutually intolerant queens in C. ligniperdus colonies demonstrates that oligogyny should be considered as a phenomenon distinct from polygyny. Received: 18 December 1997 / Accepted after revision: 20 June 1998     

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.     

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     

Behavioral ecology of the neotropical termite-hunting ant Pachycondyla (= Termitopone) marginata: colony founding,group-raiding and migratory patterns

This study provides the first detailed field account of colony founding, group-raiding and migratory habits in the neotropical termite-hunting ant rPachycondyla marginata, in a semi-deciduous forest in south-east Brazil. New colonies can originate by haplometrosis, pleometrosis, or colony fission. Incipient colonies with multiple foundresses persisted longer in the field, and most excavated nests contained more than one dealated female. A total of 202 group raids by P. marginata were registered, and in all cases the raided termite species was Neocapritermes opacus. Nearly 20% of the workers within a colony engage with raiding activity. Colonies of P. marginata hunt for termites approximately every 2–3 weeks, and group-raids may last for more than 24 h. Target termite nests are up to 38 m from the ant colony, and occasionally two nests are simultaneously raided by one ant colony. Raiding ants carry 1 or 2 paralysed prey, and nearly 1600 termites can be captured during a 9-h raid. Migration by P. marginata colonies lasted over 2 days and covered distances of 2-97 m (n = 48). Average residence time at a given location was 150 days. Three basic migratory patterns were noted: colony fission (only part of the colony moves), long-distance migrations, and short-distance migrations. Both raiding and migratory activities appeared to be strongly affected by seasonal factors. The group raiding and migratory patterns of P. marginata are compared with other ant taxa with similar habits. It is concluded that P. marginata presents a rudimentary form of the so-called army ant behavior, which is highly developed in the subfamilies Dorylinae and Ecitoninae. The extremely specialized diet of P. marginata and the associated high costs of migration are features likely to prevent it from evolving a full army ant life pattern.     

Individual and collective decision-making during nest site selection by the ant Leptothorax albipennis

Social insect colonies possess remarkable abilities to select the best among several courses of action. In populous societies with highly efficient recruitment behaviour, decision-making is distributed across many individuals, each acting on limited local information with appropriate decision rules. To investigate the degree to which small societies with less efficient recruitment can also employ distributed decision-making, we studied nest site selection in Leptothorax albipennis. Colonies were found to make sophisticated choices, taking into account not only the intrinsic qualities of each site, but also its value relative to the available options. In choices between two sites, individual ants were able to visit both sites, compare them and choose the better one. However, most ants encountered only one site in the course of an emigration. These poorly informed ants also contributed to the colony's decision, because their probability of initiating recruitment to a site depended on its quality. This led to shorter latencies between discovery and recruitment to a superior site, and so created greater amplification via positive feedback of the population at the better site. In short, these small colonies make use of a distributed mechanism of information processing, but also take advantage of direct decision-making by well-informed individuals. The latter feature may in part stem from the limitations of their social structure, but may also reflect the stringent demand for unanimous decisions by house-hunting colonies of any size.     

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

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

Worker discrimination among queens in newly founded colonies of the fire ant Solenopsis invicta

Although colonies of the fire ant Solenopsis invicta are often founded by small groups of queens, all but one of the queens are soon eliminated due to worker attacks and queen fighting. The elimination of supernumerary queens provides an important context for tests of discrimination by the workers, since the outcome of these interactions strongly affects the workers' inclusive fitness. To test whether workers in newly founded colonies discriminate among nestmate queens, paired cofoundresses were narrowly separated by metal screens that prevented direct fighting, but through which the workers could easily pass. Soon after the first workers completed development, they often attacked one of the queens; these attacks were strongly associated with queen mortality. When one queen's brood was discarded, so that the adult workers were all the daughters of just one queen, the workers were significantly less likely to bite their mother than the unrelated queen; however, this tendency was comparatively weak. Queens kept temporarily at a higher temperature to increase their rate of investment in brood-rearing lost weight more rapidly than paired queens and were subsequently more likely to be attacked and killed by workers. Workers were more likely to bite queens that had been temporarily isolated than queens that remained close to brood and workers. When queens were not separated by screens, the presence of workers stimulated queen fights. These results show that workers discriminate strongly among equally familiar queens and that discrimination is based more on the queens' condition and recent social environment than on kinship. Received: 9 June 1998 / Accepted after revision: 10 October 1998     

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

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

Mutual pheromonal inhibition among queens in polygyne colonies of the fire ant Solenopsis invicta

Summary Decrease in individual reproductive output with increasing numbers of reproductives is a general feature of social insect colonies. The previously described negative relationship between the fecundity of individual queens and number of resident queens in polygyne (multiple-queen) colonies of the fire ant Solenopsis invicta appears to result from mutual pheromonal inhibition. In an experimental test for the presence of fecundity reducing pheromones, corpses of functional (egg-laying) queens were found to effectively inhibit the fecundity of functional queens, suggesting that queen-produced pheromones suppress egg production in such queens. Evidence concerning a possible mechanism mediating this inhibition was also obtained. Treatment of queens with methoprene, a juvenile hormone (JH) analog, increased ovary development, suggesting that fecundity in functional queens may be mediated by the level of endogenous JH. These findings are consistent with the occurrence of mutual pheromonal inhibition among queens achieved by suppression of endogenous JH titers.     

Brood production and lineage discrimination in the red harvester ant (Pogonomyrmex barbatus)

In contrast to the system of caste determination in most social insects, reproductive caste determination in some populations of Pogonomyrmex barbatus has a genetic basis. Populations that exhibit genetic caste determination are segregated into two distinct, genetic lineages. Same-lineage matings result in female reproductives, while inter-lineage matings result in workers. To investigate whether founding P. barbatus queens lay eggs of reproductive genotype, and to determine the fate of those eggs, we genotyped eggs, larvae, and pupae produced by naturally inseminated, laboratory-raised queens. We show that founding dependent lineage queens do lay eggs of reproductive genotype, and that the proportion of reproductive genotypes decreases over the course of development from eggs to larvae to pupae. Because queens must mate with a male of each lineage to produce both workers and female reproductives, it would benefit queens to be able to distinguish males of the two lineages. Here we show that P. barbatus males from the two genetic lineages differ in their cuticular hydrocarbon profiles. Queens could use male cuticular hydrocarbons as cues to assess the lineage of males at the mating aggregation, and possibly keep mating until they have mated with males of both lineages.     

High genetic relatedness among nestmate queens in the polygynous ponerine ant Gnamptogenys striatula in Brazil

Gnamptogenys striatula is a polygynous ant species, in which all workers are potentially able to mate. The reproductive status, relatedness and pedigree relationships among nestmate queens and winged females in a Brazilian population were investigated. We collected all the sexual females of 12 colonies (2–44 queens per colony, plus 2–18 winged females in 3 colonies). Dissections revealed that 98% of the queens were inseminated and that the queens in the most polygynous colonies did not lay equal numbers of eggs. The sexual females and a sample of the population were genotyped using eight microsatellite markers. Relatedness among nestmate queens was among the highest recorded to date (0.65±0.25), and tests of pedigree relationship showed that they were likely to be full-sisters, and sometimes cousins. Mated winged females were always full-sisters, the estimated genetically effective queen numbers were low and tests of pedigree relationship showed that only a few queens in the colony could be the mothers. These results suggest that the high queen-queen relatedness in polygynous colonies of G. striatula is maintained by an unusual mechanism: winged females are mostly produced by only one or a few queens, and these groups of full-sisters are recruited back into their original nest after mating. Received: 26 November 1999 / Revised: 7 September 2000 / Accepted: 7 September 2000     

Colony founding,queen dominance and oligogyny in the Australian meat ant Iridomyrmex purpureus

Summary Field observations and laboratory experiments demonstrate that in the Australian meat ant, Iridomyrmex purpureus, the modes of colony founding are remarkably diverse. New colonies can originate from single foundresses (haplometrosis), or foundress associations (pleometrosis), or by colony budding, or the adoption of newly-mated queens that dig founding chambers next to mature nests (probably their natal nests, as workers protect them and may help them dig). Readoption of foundresses and pleometrosis lead to the coexistence of several queens in one nest. We discovered a striking antagonistic behavior among coexisting queens in young colonies, in the form of ritualized antennation bouts. These interactions result in a reproductive rank order in which dominant queens inhibit egg-laying by subordinates, but escalation into physical fighting is rare. Workers ignore queen dominance interactions and treat all queens equally. The first quantitative ethogram of dominance display behavior between multiple ant queens, and its reproductive consequences, is presented. As a colony grows, queens become intolerant of each other's presence and permanently separate within the nest. Once separated, queens appear to be equal in status, laying approximately equal numbers of eggs. All queens continue to be tolerated by workers, even when the colony has reached a size of several thousand workers and begun to produce reproductives. Such mature nests of I. purpureus fulfill the criteria of oligogyny, defined by worker tolerance toward more than one queen and antagonism among queens, such that a limited number of fully functional queens are spaced far apart within a single colony. Oligogynous colonies can arise in this species by pleometrotic founding (primary oligogyny) or by adoption of queens into existing nests (secondary oligogyny). The adaptive significance of the complex system of colony founding, queen dominance and oligogyny in I. purpureus is discussed.     

The evolution of polyandry by queens in social Hymenoptera: the significance of the timing of removal of diploid males

Summary Multiple mating by queens in social Hymenoptera with single locus sex determination may be an adaptation to reduce the effect of genetic load caused by the production of diploid males, if there is a concave relationship between queen fitness and the proportion of diploid male offspring in the colony. In this situation queens should be selected to reduce the variance in the production of diploid male offspring by multiple mating. It has been suggested that this concave relationship occurs in species such as the honey bee, Apis mellifera, in which reproduction occurs near the peak of colony population. This paper suggests that the timing of diploid male removal may influence mating frequency, with early removal of diploid males favoring multiple mating and late removal of diploid males favoring single mating. This idea is explored in two ways. A mathematical model shows that cell use in the brood area of species that rear young in cells will be more efficient with multiple mating. This would favor multiple mating in species, such as the honey bee, in which brood rearing is constrained by the usable area of the brood chamber. Secondly, comparison of polyandrous honey bees (early removal of diploid males as young larvae) with monandrous fire ants, Solenopsis invicta, and Melipona bees (non-removal of immature diploid males) suggests that in the species without diploid male removal, variance reduction may reduce queen fitness. Suggestions are made for testing this hypothesis.     

Resource allocation,brood production and cannibalism during colony founding in the fire ant,Solenopsis invicta

Summary The colony founding characteristics of newly mated fire ant queens from monogyne colonies were studied in the field and in the laboratory under haplo- and pleometrotic conditions. Initial queen weight (live) was not correlated with subsequent progeny production. During founding, queens lost a mean of 54% of their lean weight, 73% of their fat weight and 67% of their energy content. The percentage of fat decreased from 44% to 33%. Queens lost weight or energy in relation to the amount of progeny they produced (Figs. 1, 2). The efficiency of the conversion of queen to progeny increased as more progeny were produced, leading to a decline in the unit cost of progeny (Fig. 3). The more minims a queen produced, the lower the mean weight of these minims and the faster they developed (Fig. 4). In a field experiment on pleometrotic founding, total brood increased with queen number, peaked between four and seven queens and declined with 10 queens (Fig. 5). Brood developed faster at the sunny, warmer site, but total production and queen survival was higher at the shady site. As queen density increased, production per queen decreased as a negative exponential in which the exponent estimated sensitivity of brood production to queen-crowding and the constant estimated the production by solo queens (Fig. 9). These effects of queen number were confirmed in laboratory experiments. The decrease of production per queen was small and not always detectable during the egg-laying phase, but brood attrition was always strong during the larval period and increased with queen number (Figs. 8, 10). While airborne factors may have contributed to this inhibition, most of the brood reduction was due to other causes, probably cannibalism. For a given number of minims, increased queen number increased the mean weight of these minims, an effect that resulted both from a lower minim production per queen and from cannibalism of dead queens by survivors (Fig. 11). Cannibal queens lost much less weight to produce a given number of minims than unfed control queens, and these minims were heavier (Fig. 12).     

Energy use and allocation in the Florida harvester ant, Pogonomyrmex badius: are stored seeds a buffer?

Limitation of a necessary resource can affect an organism’s investment into growth and reproduction. Pogonomyrmex harvester ants store vast quantities of seeds in their nests that are thought to buffer the ants when external resources are not available. This research uses externally controlled food availability to examine how resource shortage affects colony investment, resource use, and resource distribution within the nest. Colonies were either starved or supplemented with resources for 2 months, beginning at the onset of reproductive investment and ending immediately before nuptial flights. Fed colonies invested more in overall production, proportionally more in reproduction relative to growth and in female reproductives relative to males. Stored seeds in starved colonies did not buffer production in this study. However, worker fat reserves were depleted in starved colonies, indicating that fat reserves fuel the spring bout of production. In starved colonies, worker fat reserves were depleted evenly throughout the nest, distributing the burden of starvation on all workers regardless of caste and age. A reallocation of diploid eggs into female workers rather than reproductives best explains the observed change in sex ratio investment between treatments. The redistribution of resources into growth relative to reproduction in starved colonies is consistent with life history theory for long-lived organisms, switching from current to future reproduction when resources are scarce.