Facultative polygyny in Ectatomma tuberculatum (Formicidae, Ectatomminae)

Summary. Polygyny, the presence of several mated queens within the same colony, is widespread in insect societies. This phenomenon is commonly associated with ecological constraints such as limited nest sites. In habitats where solitary nest foundation is risky, monogynous colonies can reintegrate young daughter queens (secondary polygyny). We studied the reproductive structure (i.e. queen number) of the ectatommine ant Ectatomma tuberculatum from Bahia State, Brazil. This species was found to present facultative polygyny: out of a total of 130 colonies collected, 39.2% were monogynous, while 43.8% were polygynous. Polygynous colonies had significantly more workers than monogynous ones. Queen number in polygynous colonies ranged from 2 to 26, with an average of 4 ± 4 queens per colony. All nestmate queens were egg-layers with no apparent dominance hierarchy or agonistic behavior. Non-nestmate queens were adopted by monogynous colonies suggesting that polygyny is secondary, originating through queen adoption. This species is characterized by an open recognition system, which probably allows a switch from monogynous to polygynous colonies. The behavioral acts of queens showed that resident queens remained frequently immobile on or near the brood, contrarily to alien or adopted queens and gynes. In addition, monogynous queens showed no behavioral or physiological (i.e. by ovarian status) differences in comparison with polygynous ones. Secondary or facultative polygyny, probably associated with queen adoption, may have been favored in particular environmental conditions. Indeed, by increasing colony productivity (i.e. number of workers) and territory size (by budding and polydomy), polygyny could uphold E. tuberculatum as a dominant species in the mosaic of arboreal ants in Neotropical habitats.Received 7 April 2004; revised 11 November 2004; accepted 15 November 2004.     

Stenamma debile (Hymenoptera, Formicidae): Facultative polygyny, and an extreme 1997 sex ratio

Summary: Monogynous and a high proportion of truly polygynous colonies of Stenamma debile were found in populations of this small and inconspicuous ant in southern Germany. Moreover, dissections revealed that queens of different age may co-occur in one nest. Thus polygyny is not only an outcome of pleometrosis. Probably young queens sometimes join the mother colonies.¶Practically no female sexuals were reared in the 1997 brood of 29 colonies, thus a population-level sex ratio of &gif1; was recorded. It is likely that such an extreme sex ratio is atypical for this species, suggesting substantial year-to-year variation in sex ratios. Variation of sex ratios over several years has been reported for other ant species, too, but rarely to such an extent. The reason for the failure of queen production in 1997 was perhaps an unusual sequence of warm and cold periods in the spring which may have caused a re-determination of the queen-destined hibernated larvae to become workers, while male larvae were reared in ordinary numbers.     

Reproductive conflicts in polyandrous and polygynous ant Formica sanguinea

The occurrence of multiple reproductives within an ant colony changes the balance between indirect fitness benefits and reproductive competition. We test whether the number of matings by an ant queen (polyandry) correlates negatively with the number of reproductive queens in the colony (polygyny), whether the patrilines and matrilines differ in their contribution to the sexual and worker progeny and whether there is an overall reproductive skew. For these aims, we genotyped both worker and sexual offspring from colonies of the ant Formica sanguinea in three populations. Most colonies were monogynous, but eight (11%) were polygynous with closely related queens. Most queens in the monogynous colonies (86%) had mated with multiple males. The effective paternity was lower than the actual number of mates, and the paternity skew was significant. Furthermore, in some monogynous colonies, the patrilines were differently represented in the worker pupae and sexual pupae produced at the same time. Likewise, the matrilines in polygynous colonies were differently present in worker pupae and male offspring. The effective number of matings by a queen was significantly lower in polygynous colonies (mean m_e = 1.68) than in monogynous colonies (means 2.06–2.61). The results give support to the hypotheses that polyandry and polygyny are alternative breeding strategies and that reproductive competition can lead to different representation of patrilines and matrilines among the sexual and worker broods.     

Nesting patterns,ecological correlates of polygyny and social organization in the neotropical arboreal ant <Emphasis Type="Italic">Odontomachus hastatus</Emphasis> (Formicidae,Ponerinae)

Queen number varies in the population of O. hastatus in SE Brazil. Here, we evaluate how nesting ecology and colony structure are associated in this species, and investigate how reproduction is shared among nestmate queens. Queen number per colony is positively correlated with nesting space (root cluster of epiphytic bromeliads), and larger nest sites host larger ant colonies. Plant samplings revealed that suitable nest sites are limited and that nesting space at ant-occupied bromeliads differs in size and height from the general bromeliad community. Dissections revealed that queens in polygynous colonies are inseminated, have developed ovaries, and produce eggs. Behavioral observations showed that reproduction in polygynous colonies is mediated by queen–queen agonistic interactions that include egg cannibalism. Dominant queens usually produced more eggs. Field observations indicate that colonies can be initiated through haplometrosis. Polygyny in O. hastatus may result either from groups of cofounding queens (pleometrosis) or from adoption of newly mated queens by established colonies (secondary polygyny). Clumping of bromeliads increases nest space and probably adds stability through a strong root system, which may promote microhabitat selection by queens and favor pleometrosis. Rainstorms that frequently knock down bromeliads can be a source of colony break-up and may promote polygyny. Bromeliads are limited nest sites and may represent a risk for young queens leaving a suitable nest, thus favoring secondary polygyny. Although proximate mechanisms mediating queen number are poorly understood, this study suggests that heterogeneous microhabitat conditions probably contribute to the coexistence of variable forms of social structure in O. hastatus.     

Effect of mono- and polygyne social forms on transmission and spread of a microsporidium in fire ant populations

Thelohania solenopsae is a pathogen of the red imported fire ant, Solenopsis invicta, which debilitates queens and eventually causes the demise of colonies. Reductions of infected field populations signify its potential usefulness as a biological control agent. Thelohania solenopsae can be transmitted by introducing infected brood into a colony. The social forms of the fire ant, that is, monogyny (single queen per colony) or polygyny (multiple queens per colony), are associated with different behaviors, such as territoriality, that affect the degree of intercolony brood transfer. T. solenopsae was found exclusively in polygyne colonies in Florida. Non-synchronous infections of queens and transovarial transmission favor the persistence and probability of detecting infections in polygynous colonies. However, queens or alates with the monogyne genotype can be infected, and infections in monogyne field colonies have been reported from Louisiana and Argentina. Limited independent colony-founding capability and shorter dispersal of alate queens with the polygyne genotype relative to monogyne alates may facilitate the maintenance of infections in local polygynous populations. Demise of infected monogyne colonies can be twice as fast as in polygyne colonies and favors the pathogen's persistence in polygyne fire ant populations. The social form of the fire ant reflects different physiological and behavioral aspects of the queen and colony that will impact T. solenopsae spread and ultimate usefulness for biological control.     

Plasticity in queen number and social structure in the invasive Argentine ant (Linepithema humile)

In many polygynous social insect societies, ecological factors such as habitat saturation promote high queen numbers by increasing the cost of solitary breeding. If polygyny is associated with constrained environments, queen number in colonies of invasive social insects should increase as saturation of their new habitat increases. Here I describe the variation in queen number, nestmate relatedness, and nest size along a gradient of time since colonization in an invading population of Argentine ants (Linepithema humile) in Haleakala, Hawaii. Nest densities in this population increase with distance from the leading edge of the invasion, reaching a stable density plateau approximately 80 m from the edge (> 2 years after colonization). Although the number of queens per nest in Haleakala is generally lower than previously reported for Argentine ants, there is significant variation in queen number across this population. Both the observed and effective queen numbers increase across the density gradient, and nests in the center of the population contain queen numbers three to nine times higher than those on the edge of the invasion. The number of workers per nest is correlated with queen number, and nests in the center are six times larger than nests at the edge. Microsatellite analysis of relatedness among nestmates reveals that all nests in the Haleakala population are characterized by low relatedness and have evidence of multiple reproducing queens. Relatedness values are significantly lower in nests in the center of the population, indicating that the number of reproducing queens is greater in areas of high nest density. The variation in queen number and nestmate relatedness in this study is consistent with expectations based on changes in ecological constraints during the invasion of a new habitat, suggesting that the social structure of Argentine ant populations is strongly influenced by ecological factors. Flexibility in social structure may facilitate persistence in variable environments and may also confer significant advantages to a species when introduced into new areas.     

Facultative polygyny in the plant-ant Petalomyrmex phylax (Hymenoptera: Formicinae): sociogenetic and ecological determinants of queen number

In polygynous ants it has been proposed that the coexistence of several queens in a colony evolved as a response to ecological, social and genetic parameters. We present demographic, histological and genetic data showing that the plant-ant Petalomyrmex phylax is facultatively and secondarily polygynous. Polygyny is functional, lowers the reproductive output per queen, and is a kin-selected trait as new queens accepted in polygynous colonies are highly related females that never left their natal colony. The degree of polygyny varies according to a geographical gradient. Northern colonies can be strongly polygynous, while at the southern edge of the species' distribution, colonies are almost exclusively monogynous. However, ecological studies of the host-plant populations revealed that this cline could not be explained by variations in the degree of nest site limitation. We discuss selective costs and benefits associated with these social structures, and propose that this cline may result from historical processes such as selection of a more dispersive strategy along a colonization front.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 133–151.     

Facultative polygyny and habitat succession in boreal ants

High dispersal risks of ant queens make staying in the natal patch more attractive than long range dispersal. These alternative strategies and the mode of colony founding determine the average number of queens in the population. Increasing competition and queen predation make independent colony founding increasingly difficult and the only option for new queens to reproduce in the habitat patch may be to enter an existing colony. The effect of nest-site availability to the number of queens was studied in successional spruce-dominated taiga forests in facultatively polygynous ants Myrmica ruginodis, M. sulcinodis, Leptothorax acervorum, Formica sanguinea and F. truncorum. Decreasing relatedness among worker nestmates supports an association between increasing habitat age and polygyny to some extent. M. sulcinodis and L. acervorum persist in this type of taiga only for a relatively short period. Relatedness varied only slightly among populations, but lower relatedness estimated in other studies suggested higher levels of polygyny in older populations. In M. ruginodis there was more variation in relatedness and it was possibly connected to the relative proportions of the two social forms of the species. In F. sanguinea and F. truncorum the decrease in relatedness with increasing age of the habitat was clearest. Other factors favouring limited dispersal and acceptance of new queens in the colonies are, however, hard to separate.     

Polygyny in the nest-site limited acacia-ant Crematogaster mimosae

Polygyny is common in social insects despite inevitable decreases in nestmate relatedness and reductions to the inclusive fitness returns for cooperating non-reproductive individuals. We studied the prevalence and mode of polygyny in the African acacia-ant Crematogaster mimosae. These ants compete intensively with neighboring colonies of conspecifics and with three sympatric ant species for resources associated with the whistling-thorn acacias in which they all obligately nest. We used the genotypes of alate males at ten microsatellite loci to reconstruct queen genotypes and found that C. mimosae colonies are frequently secondarily polygynous, in that they include multiple closely related (and sometimes full-sib) queens, and (more rarely) unrelated queens. We also found that individual queens in both monogynous and polygynous colonies had mated with multiple males, making C. mimosae an interesting example of simultaneous polygyny and polyandry. The presence of polygyny in C. mimosae and the intense competition for nest-sites between C. mimosae and its conspecifics support the association between nest-site limitation and polygyny. Polygyny may allow for increased worker populations and a competitive advantage, as inter-colony conflicts are typically won by the colony with the larger number of workers.     

Colony genetic structure in the Australian jumper ant <Emphasis Type="Italic">Myrmecia pilosula</Emphasis>

Eusocial insects vary significantly in colony queen number and mating frequency, resulting in a wide range of social structures. Detailed studies of colony genetic structure are essential to elucidate how various factors affect the relatedness and the sociogenetic organization of colonies. In this study, we investigated the colony structure of the Australian jumper ant Myrmecia pilosula using polymorphic microsatellite markers. Nestmate queens within polygynous colonies, and queens and their mates, were generally unrelated. The number of queens per colony ranged from 1 to 4. Queens were estimated to mate with 1–9 inferred and 1.0–11.4 effective mates. This is the first time that the rare co-occurrence of polygyny and high polyandry has been found in the M. pilosula species group. Significant maternity and paternity skews were detected at the population level. We also found an isolation-by-distance pattern, and together with the occurrence of polygynous polydomy, this suggests the occurrence of dependent colony foundation in M. pilosula; however, independent colony foundation may co-occur since queens of this species have fully developed wings and can fly. There is no support for the predicted negative association between polygyny and polyandry in ants.     

Intraspecific support for the polygyny-vs.-polyandry hypothesis in the bulldog ant Myrmecia brevinoda

The number of queens per colony and the number of matings per queen are the most important determinants of the genetic structure of ant colonies, and understanding their interrelationship is essential to the study of social evolution. The polygyny-vs.-polyandry hypothesis argues that polygyny and polyandry should be negatively associated because both can result in increased intracolonial genetic variability and have costs. However, evidence for this long-debated hypothesis has been lacking at the intraspecific level. Here, we investigated the colony genetic structure in the Australian bulldog ant Myrmecia brevinoda. The numbers of queens per colony varied from 1 to 6. Nestmate queens within polygynous colonies were on average related (r(qq) = 0.171 ± 0.019), but the overall relatedness between queens and their mates was indistinguishable from zero (r(qm) = 0.037 ± 0.030). Queens were inferred to mate with 1-10 males. A lack of genetic isolation by distance among nests indicated the prevalence of independent colony foundation. In accordance with the polygyny-vs.-polyandry hypothesis, the number of queens per colony was significantly negatively associated with the estimated number of matings (Spearman rank correlation R = -0.490, P = 0.028). This study thus provides the rare intraspecific evidence for the polygyny-vs.-polyandry hypothesis. We suggest that the high costs of multiple matings and the strong effect of multiple mating on intracolonial genetic diversity may be essential to the negative association between polygyny and polyandry and that any attempt to empirically test this hypothesis should place emphasis upon these two key underlying aspects.     

Restricted effective queen dispersal at a microgeographic scale in polygynous populations of the ant Formica exsecta

Ecological constraints on effective dispersal have been suggested to be a key factor influencing social evolution in animal societies as well as the shift from single queen colonies (monogyny) to multiple queen colonies (polygyny) in ants. However, little is known about the effective dispersal patterns of ant queens. Here we investigate the microgeographic genetic structure of mitochondrial haplotypes in polygynous populations of the ant Formica exsecta, both between pastures and among nests within pastures. An analysis of molecular variance revealed a very high genetic differentiation (phiST = 0.72) between pastures, indicating that queens rarely disperse successfully between pastures, despite the fact that pastures were sometimes as close as 1 km. Most of the pastures contained only a single haplotype, and haplotypes were frequently distinct between nearby pastures and even between groups of nests within the same pasture. In the three pastures that contained several haplotypes, haplotypes were not randomly distributed, the genetic differentiation between nests being phiST = 0.17, 0.52, and 0.69. This indicates that most queens are recruited within their parental colonies. However, a large proportion of nests contained more than one haplotype, demonstrating that colonies will sometimes accept foreign queens. The relatedness of mitochondrial genes among nestmates varied between 0.62 and 0.75 when relatedness was measured within each pasture and ranged between 0.72 and 1.0 when relatedness was assessed with all pastures as a reference population. Neighboring nests were more genetically similar than distant ones, and there was significant isolation by distance. This pattern may be due to new nests being formed by budding or by limited effective queen dispersal, probably on foot between neighboring nests. These results show that effective queen dispersal is extremely restricted even at a small geographical scale, a pattern consistent with the idea that ecological constraints are an important selective force leading to the evolution and maintenance of polygyny.     

The frequency of multi‐queen colonies increases with altitude in a Nearctic ant

1. Most ants in boreal and alpine habitats are facultatively polygynous, i.e. their colonies may contain one or several queens. It was investigated how the proportion of polygynous colonies varies along an elevation gradient from 60 to 2700 m in the Nearctic ant Temnothorax rugatulus (Emery). 2. Across all populations, the proportion of polygynous colonies was positively correlated with altitude. The correlation was considerably stronger when only populations in the narrow area of the Chiricahua Mts, Arizona, were compared. 3. The dominance of polygynous colonies at high altitudes may be associated with selection against solitary colony founding by young queens. In areas with short summers and long winters, hibernation mortality of solitarily founding queens may select for alternative reproductive tactics, such as polygyny and colony founding by budding. 4. Colony founding tactics need to be taken into account to more fully understand altitudinal and latitudinal patterns of ant faunas.     

Polygyny and polyandry in small ant societies

Social insects, ants in particular, show considerable variation in queen number and mating frequency resulting in a wide range of social structures. The dynamics of reproductive conflicts in insect societies are directly connected to the colony kin structure, thus, the study of relatedness patterns is essential in order to understand the evolutionary resolution of these conflicts. We studied colony kin structure and mating frequencies in two closely related Neotropical ant species Pachycondyla inversa and Pachycondyla villosa. These represent interesting model systems because queens found new colonies cooperatively but, unlike many other ant species, they may still co-exist when the colony becomes mature (primary polygyny). By using five specific and highly variable microsatellite markers, we show that in both species queens usually mate with two or more males and that cofounding queens are always unrelated. Polygynous and polyandrous colonies are characterized by a high genetic diversity, with a mean relatedness coefficient among worker nestmates of 0.27 (+/- 0.03 SE) for P. inversa and 0.31 (+/- 0.05 SE) for P. villosa. However, relatedness among workers of the same matriline is high (0.60 +/- 0.03 in P. inversa, 0.62 +/- 0.08 in P. villosa) since males that mated with the same queen are on average closely related. Hence, we have found a new taxon in social Hymenoptera with high queen-mating frequencies and with intriguing mating and dispersal patterns of the sexuals.     

QUEEN NUMBER IN COLONIES OF SOCIAL HYMENOPTERA AS A KIN-SELECTED ADAPTATION

Using a series of kin-selection models, I examine factors that favor multiple egg-laying queens (polygyny) in eusocial Hymenoptera colonies. One result is that there is a theoretical conflict of interest between the founding queens and their daughter workers over how many and which individuals should be the extra reproductives. Both castes should prefer their full sisters. Therefore, primary polygyny (multiple related foundresses) may favor queens while secondary polygyny (related queens added to mature colonies) may favor workers. Polygyny, itself, was found to be favored by high colony survivorship and low probability of queens contributing eggs to successive broods. Polygyne colonies, however, did not need to produce more offspring per brood to be selectively favored; they could be half as productive per brood as monogyne ones and still have higher lifetime fitness under some conditions. For reproductive data from eight ant species with both monogyne and polygyne colonies, the model generates results that are consistent with a kin-selection explanation of polygyny in all of them. It is proposed that queen number is an ecologically flexible trait that is influenced by a broad set of factors but is not necessarily linked to specific habitat types. Furthermore, neither polygyny nor monogyny may be reliably considered as the primitive or ancestral Hymenopteran social system. The optimal queen number within a species may evolutionarily increase or decrease, depending on the direction of environmental change.     

Inbreeding and kinship in the ant Plagiolepis pygmaea

In ants the presence of multiple reproductive queens (polygyny) decreases the relatedness among workers and the brood they rear, and subsequently dilutes their inclusive fitness benefits from helping. However, adoption of colony daughters, low male dispersal in conjunction with intranidal (within nest) mating and colony reproduction by budding may preserve local genetic differences, and slow down the erosion of relatedness. Reduced dispersal and intranidal mating may, however, also lead to detrimental effects owing to competition and inbreeding. We studied mating and dispersal patterns, and colony kinship in three populations of the polygynous ant Plagiolepis pygmaea using microsatellite markers. We found that the populations were genetically differentiated, but also a considerable degree of genetic structuring within populations. The genetic viscosity within populations can be attributed to few genetically homogeneous colony networks, which presumably have arisen through colony reproduction by budding. Hence, selection may act at different levels, the individuals, the colonies and colony networks. All populations were also significantly inbred (F=0.265) suggesting high frequencies of intranidal mating and low male dispersal. Consequently the mean regression relatedness among workers was significantly higher (r = 0.529-0.546) than would be expected under the typically reported number (5-35) of queens in nests of the species. Furthermore, new queens were mainly recruited from their natal or a neighbouring related colony. Finally, the effective number of queens coincided with that found upon excavation, suggesting low reproductive skew.     

Parentage,reproductive skew and queen turnover in a multiple-queen ant analysed with microsatellites.

We investigated the fine genetic structure of colonies of the ant, Leptothorax acervorum, to examine how queens share parentage (skew) in a social insect with multiple queens (polygyny). Overall, 494 individuals from eight polygynous field colonies were typed at up to seven microsatellite loci each. The first main finding was that surprisingly many sexual progeny (60% of young queens and 49% of young males) were not the offspring of the extant queens within their colonies. This implies that a high turnover (brief reproductive lifespan) of queens within colonies could be an important feature of polygyny. The second main result was that in most colonies relatedness among sexual progeny fell significantly below that expected among full siblings, proving that these progeny were produced by more than one singly-mated queen, but that skew in two colonies where the data permitted its calculation was moderate to high. However, relative to a German population, the study population is characterized by low queen-queen relatedness and low skew in female production, which is in line with the predictions of skew theory.     

Mitochondrial markers in the ant Leptothorax rugatulus reveal the population genetic consequences of female philopatry at different hierarchical levels

Leptothorax rugatulus, an abundant North American ant, displays a conspicuous queen size polymorphism that is related to alternative reproductive tactics. Large queens participate mainly in mating flights and found new colonies independent of their mother colony. In contrast, small queens do not found new colonies independently, but seek readoption into their natal nest which results in multiple-queen colonies (polygyny). Populations differ strongly in the ratio of small to large queens, the prevalent reproductive tactic and colony social structure, according to ecological parameters such as nest site stability and population density. This study compares the genetic structure of two strongly differing populations within the same mountain range. Data from microsatellites and mitochondrial DNA give no evidence for alien reproductives in polygynous colonies. The incidence of alien workers in colonies (as determined by mitochondrial haplotype) was low and did not differ between monogynous and polygynous colonies. We found significant population viscosity (isolation-by-distance) at the mitochondrial level in only the predominantly polygynous population, which supports the theoretical prediction that female philopatry leads to mtDNA-specific population structure. Nuclear and mitochondrial genetic diversity was similar in both populations. The genetic differentiation between the two investigated populations was moderate at the mitochondrial level, but not significantly different from zero when measured with microsatellites, which corroborates limited dispersal of females (but not males) at a larger scale.     

Behavioral Plasticity in Ant Queens: Environmental Manipulation Induces Aggression among Normally Peaceful Queens in the Socially Polymorphic Ant Leptothorax acervorum

The behavioral traits that shape the structure of animal societies vary considerably among species but appear to be less flexible within species or at least within populations. Populations of the ant Leptothorax acervorum differ in how queens interact with other queens. Nestmate queens from extended, homogeneous habitats tolerate each other and contribute quite equally to the offspring of the colony (polygyny: low reproductive skew). In contrast, nestmate queens from patchy habitats establish social hierarchies by biting and antennal boxing, and eventually only the top-ranking queen of the colony lays eggs (functional monogyny: high reproductive skew). Here we investigate whether queen-queen behavior is fixed within populations or whether aggression and high skew can be elicited by manipulation of socio-environmental factors in colonies from low skew populations. An increase of queen/worker ratio and to a lesser extent food limitation elicited queen-queen antagonism in polygynous colonies from Nürnberger Reichswald similar to that underlying social and reproductive hierarchies in high-skew populations from Spain, Japan, and Alaska. In manipulated colonies, queens differed more in ovarian status than in control colonies. This indicates that queens are in principle capable of adapting the magnitude of reproductive skew to environmental changes in behavioral rather than evolutionary time.     

The determinants of queen size in a socially polymorphic ant

In social animals, body size can be shaped by multiple factors, such as direct genetic effects, maternal effects, or the social environment. In ants, the body size of queens correlates with the social structure of the colony: colonies headed by a single queen (monogyne) generally produce larger queens that are able to found colonies independently, whereas colonies headed by multiple queens (polygyne) tend to produce smaller queens that stay in their natal colony or disperse with workers. We performed a cross‐fostering experiment to investigate the proximate causes of queen size variation in the socially polymorphic ant Formica selysi. As expected if genetic or maternal effects influence queen size, eggs originating from monogyne colonies developed into larger queens than eggs collected from polygyne colonies, be they raised by monogyne or polygyne workers. In contrast, eggs sampled in monogyne colonies were smaller than eggs sampled in polygyne colonies. Hence, eggs from monogyne colonies are smaller but develop into larger queens than eggs from polygyne colonies, independently of the social structure of the workers caring for the brood. These results demonstrate that a genetic polymorphism or maternal effect transmitted to the eggs influences queen size, which probably affects the social structure of new colonies.