Population genetics and history of the introduced fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), in Australia

Abstract  The red imported fire ant, Solenopsis invicta , a damaging invasive pest, was discovered in February 2001 in Brisbane, Australia at two sites, Fisherman Islands and suburban Richlands-Wacol. Using four microsatellite loci and the protein marker Gp-9 , we compared the two infestations with each other, and with potential source populations in North and South America to better understand the history of their introduction to Brisbane. Based on an analysis of molecular variance, as well as a maximum likelihood tree of colonies from the two Australian sites, we found that the two sites were genetically distinct and were almost certainly introduced separately. All of the colonies at Fisherman Islands were monogynous, headed by a single queen, while the Richlands-Wacol site had a mixture of single-queen monogynous and multiple-queen polygynous colonies. However, the monogynous and polygynous colonies at the Richlands-Wacol site were not genetically distinct from each other, and probably constitute a single, mixed introduction. Based on allele frequencies at the microsatellite loci, and Gp-9 , both Australian infestations were more similar to North American populations than to South American, though the Fisherman Islands infestation was intermediate, making it difficult to assign. Thus, there has been one introduction from either a North or South American monogynous population at Fisherman Islands, and one introduction from a mixed monogynous/polygynous North American population at Richlands-Wacol. These findings have implications for the control of the current infestations, as well as for the quarantine regulations necessary to prevent additional introductions to Australia.     

Evolutionary implications of polygyny in the Argentine ant,Iridomyrmex humilis (Mayr) (Hymenoptera: Formicidae): an experimental study

A comparison of several physiological parameters of queens of Iridomyrmex humilis in experimental monogynous and polygynous colonies showed that queens in monogynous colonies became heavier, had more developed ovaries and laid about twice as many eggs. Workers in monogynous colonies were more attracted to queens, which therefore probably received more food. This may partially explain the higher weight and fecundity of queens in monogynous colonies of Iridomyrmex humilis and possibly other ant species. In polygynous colonies, queens differed greatly in their fecundity. These differences did not appear to be the result of a dominance hierarchy. These results are discussed from an evolutionary point of view. Two hypotheses of mutualism and colony level selection are proposed as an alternative to kin selection which is unlikely to be the exclusive selective influence in the evolution of polygyny either in I. humilis or in most other ant species.     

Social structure varies with elevation in an Alpine ant

Insect societies vary greatly in social organization, yet the relative roles of ecological and genetic factors in driving this variation remain poorly understood. Identifying how social structure varies along environmental gradients can provide insights into the ecological conditions favouring alternative social organizations. Here, we investigate how queen number variation is distributed along elevation gradients within a socially polymorphic ant, the Alpine silver ant Formica selysi. We sampled low‐ and high‐elevation populations in multiple Alpine valleys. We show that populations belonging to different drainage basins are genetically differentiated. In contrast, there is little genetic divergence between low‐ and high‐elevation populations within the same drainage basin. Thus, elevation gradients in each of the drainage basins represent independent contrasts. Whatever the elevation, all well‐sampled populations are socially polymorphic, containing both monogynous (= one queen) and polygynous (= multiple queen) colonies. However, the proportion of monogynous colonies per population increases at higher elevation, while the effective number of queens in polygynous colonies decreases, and this pattern is replicated in each drainage basin. The increased prevalence of colonies with a single queen at high elevation is correlated with summer and winter average temperature, but not with precipitation. The colder, unpredictable and patchy environment encountered at higher elevations may favour larger queens with the ability to disperse and establish incipient monogynous colonies independently, while the stable and continuous habitat in the lowlands may favour large, fast‐growing polygynous colonies. By highlighting differences in the environmental conditions favouring monogynous or polygynous colonies, this study sheds light on the ecological factors influencing the distribution and maintenance of social polymorphism.     

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.     

Asymmetric assortative mating and queen polyandry are linked to a supergene controlling ant social organization

Nonrecombining genomic variants underlie spectacular social polymorphisms, from bird mating systems to ant social organization. Because these “social supergenes” affect multiple phenotypic traits linked to survival and reproduction, explaining their persistence remains a substantial challenge. Here, we investigate how large nonrecombining genomic variants relate to colony social organization, mating system and dispersal in the Alpine silver ant, Formica selysi. The species has colonies headed by a single queen (monogynous) and colonies headed by multiple queens (polygynous). We confirmed that a supergene with alternate haplotypes—Sm and Sp—underlies this polymorphism in social structure: Females from mature monogynous colonies had the Sm/Sm genotype, while those from polygynous colonies were Sm/Sp and Sp/Sp. Queens heading monogynous colonies were exclusively mated with Sm males. In contrast, queens heading polygynous colonies were mated with Sp males and Sm males. Sm males, which are only produced by monogynous colonies, accounted for 22.9% of the matings with queens from mature polygynous colonies. This asymmetry between social forms in the degree of assortative mating generates unidirectional male‐mediated gene flow from the monogynous to the polygynous social form. Biased gene flow was confirmed by a significantly higher number of private alleles in the polygynous social form. Moreover, heterozygous queens were three times as likely as homozygous queens to be multiply mated. This study reveals that the supergene variants jointly affect social organization and multiple components of the mating system that alter the transmission of the variants and thus influence the dynamics of the system.     

Polymorphic social organization in an ant

Identifying species exhibiting variation in social organization is an important step towards explaining the genetic and environmental factors underlying social evolution. In most studied populations of the ant Leptothorax acervorum, reproduction is shared among queens in multiple queen colonies (polygyny). By contrast, reports from other populations, but based on weaker evidence, suggest a single queen may monopolize all reproduction in multiple queen colonies (functional monogyny). Here we identify a marked polymorphism in social organization in this species, by conclusively showing that functional monogyny is exhibited in a Spanish population, showing that the social organization is stable and not purely a consequence of daughter queens overwintering, that daughter queen re-adoption is frequent and queen turnover is low. Importantly, we show that polygynous and functionally monogynous populations are not genetically distinct from one another based on mtDNA and nDNA. This suggests a recent evolutionary divergence between social phenotypes. Finally, when functionally monogynous and polygynous colonies were kept under identical laboratory conditions, social organization did not change, suggesting a genetic basis for the polymorphism. We discuss the implications of these findings to the study of reproductive skew.     

Polygyny reduces rather than increases nestmate discrimination cue diversity in Formica exsecta ants

Although the majority of social insect colonies are headed by a single queen, some species possess nests that contain numerous reproductive queens (polygyny), a trait that is particularly widespread amongst the ants. Polygyny is often associated with a lack of conspecific inter-nest aggression between workers. This is hypothesised to result from increased nestmate cue diversity within nests, since polygynous nests are more genetically diverse than monogynous nests. Alternatively, it may reflect the common origin of polygynous nests that form polydomous networks. We exploit the recent discovery that the nestmate discrimination system in the ant Formica exsecta is based on cuticular hydrocarbons to investigate cue (Z9-alkenes) diversity in several monogynous and polygynous populations. Contrary to previous predictions, in all polygynous populations, the variation between nests in the Z9-alkene profiles was reduced relative to that found in monogynous populations. However, nest-specific Z9-alkene profiles with little variation amongst nestmate workers were still maintained irrespective of nest type or population. This suggests a very effective gestalt mechanism that homogenises the chemical discrimination cues, despite genetic diversity within colonies. Although the reduction in variation between nests was associated with reduced worker aggression on the population level, it cannot totally explain the weak aggression associated with polygynous populations.     

Population genetics of the socially polymorphic ant <Emphasis Type="Italic">Formica podzolica</Emphasis>

Summary. We used microsatellite markers to analyze the hierarchical genetic structure of the North American mound building ant, Formica podzolica. About one-third of all colonies were headed by a single queen (monogynous) whose effective mating frequency was close to one (nestmate worker relatedness r = 0.70), while the remaining colonies were polygynous, with low average nestmate relatedness (r = 0.16). The low worker relatedness found in most polygynous colonies furthermore suggested that the numbers of queens in polygynous colonies of this ant are usually high. Contrary to what has been described from other ants with a queen number dichotomy, we did not find an effect of social form variation on the partitioning of genetic variation above the level of the colony. We found no significant differentiation between the sympatric social forms of F. podzolica, nor did differentiation among populations appear to be affected by colony social organization. These unexpected patterns of genetic structure may have resulted from differences either in the spatial distribution of the social forms or in their social flexibility.Received 12 January 2004; revised 23 February 2004; accepted 10 March 2004.     

Social and genetic characteristics of geographically isolated populations in the ant Formica cinerea

The ant Formica cinerea in northern Europe has geographically isolated populations that were examined using five microsatellite loci. The populations differ widely regarding the social organization of colonies. Based on genetic relatedness (r) among worker nest mates, the populations were classified as M type with monogynous (single queen) colonies (r > 0.59), as P type with polygynous colonial networks (r < 0.1), or as intermediate with weakly polygynous colonies (0.16 < r < 0.47). The social types showed weak geographical clustering, but the overall distribution indicated that the shift between the social types has occurred several times. The geographically isolated populations had slightly reduced levels of genetic diversity compared to populations from areas where the species is abundant and continuously distributed. Many of the isolated populations consisted of monogynous or weakly polygynous colonies, making their effective population sizes small, and some of them also showed weak bottleneck effects. The overall level of microsatellite diversity within populations was relatively high and differentiation among populations low, indicating recent connections. Isolation of populations may thus be a new phenomenon resulting from reduction of suitable habitats. At the local level, we obtained limited support from a group of nearby subpopulations in southern Finland to the hypothesis that the P type is connected to restricted dispersal. Other P type populations did not, however, show similar elevated levels of differentiation.     

Sex allocation in a facultatively polygynous ant: between-population and between-colony variation

We investigated sex allocation in three U.K. populations ofthe facultatively polygynous ant Leptothorax acervorum over1-3 years. The first main finding was that, across sites, thepopulation sex-investment ratio changed from significantly femalebiased to significantly male biased with increasing polygyny.This was consistent with workers controlling sex allocationand reacting to changes in their population-level relatedness asymmetry.It was also consistent with local resource competition due to reproductionby colony budding under polygyny. Worker control was supportedby the finding that queen number had no effect on sex allocationamong polygynous colonies. The second main result was that monogynouscolonies consistently produced more female-biased sex-investmentratios than polygynous colonies in one site only (Santon). Theresults from Santon supported both the relative relatednessasymmetry hypothesis and the idea of sex ratio compensationdue to colony budding. The workers' response to their population-levelrelatedness asymmetry reinforced the case for relatedness asymmetrybeing influential at the colony level. The other populationscould have lacked split sex ratios because polygynous colonieswere either comparatively rare or common, making them behaveas almost entirely monogynous (Aberfoyle) or polygynous (Roydon) populations.In Roydon, this was consistent with the inference from allozyme datathat monogynous and polygynous colonies did not differ in theirworker relatedness asymmetries. The final principal findingwas that, of hypotheses linking the colony sex-investment ratiowith sexual productivity, there was support for the constantfemale hypothesis but not for the constant male, cost variation,or multifaceted parental investment hypotheses.     

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.     

A morphological comparison of alates between monogynous and polygynous colonies of Myrmica kotokui in northernmost Japan

Summary: Social structure and sexual size of two populations of Myrmica kotokui were compared. Most of the colonies were polygynous in one population and monogynous in the other. Mean body size of the queens was larger in the monogynous population than in the polygynous population. Although the polygynous population contained many large queens, their wing length was significantly shorter than that of queens in the monogynous population. Some females in the polygynous population were intermorphic between typical workers and queens, while the females of the monogynous population were clearly divided into worker and queen castes without any intermorphic females. The body size of the males showed a large variation and the mean was not significantly different between the two populations.     

The influence of social structure on brood survival and development in a socially polymorphic ant: insights from a cross‐fostering experiment

Animal societies vary in the number of breeders per group, which affects many socially and ecologically relevant traits. In several social insect species, including our study species Formica selysi, the presence of either one or multiple reproducing females per colony is generally associated with differences in a suite of traits such as the body size of individuals. However, the proximate mechanisms and ontogenetic processes generating such differences between social structures are poorly known. Here, we cross‐fostered eggs originating from single‐queen (= monogynous) or multiple‐queen (= polygynous) colonies into experimental groups of workers from each social structure to investigate whether differences in offspring survival, development time and body size are shaped by the genotype and/or prefoster maternal effects present in the eggs, or by the social origin of the rearing workers. Eggs produced by polygynous queens were more likely to survive to adulthood than eggs from monogynous queens, regardless of the social origin of the rearing workers. However, brood from monogynous queens grew faster than brood from polygynous queens. The social origin of the rearing workers influenced the probability of brood survival, with workers from monogynous colonies rearing more brood to adulthood than workers from polygynous colonies. The social origin of eggs or rearing workers had no significant effect on the head size of the resulting workers in our standardized laboratory conditions. Overall, the social backgrounds of the parents and of the rearing workers appear to shape distinct survival and developmental traits of ant brood.     

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.     

Prediction of social structure and genetic relatedness in colonies of the facultative polygynous stingless bee Melipona bicolor (Hymenoptera, Apidae)

Stingless bee colonies typically consist of one single-mated mother queen and her worker offspring. The stingless bee Melipona bicolor (Hymenoptera: Apidae) shows facultative polygyny, which makes this species particularly suitable for testing theoretical expectations concerning social behavior. In this study, we investigated the social structure and genetic relatedness among workers from eight natural and six manipulated colonies of M. bicolor over a period of one year. The populations of M. bicolor contained monogynous and polygynous colonies. The estimated genetic relatedness among workers from monogynous and polygynous colonies was 0.75 ± 0.12 and 0.53 ± 0.16 (mean ± SEM), respectively. Although the parental genotypes had significant effects on genetic relatedness in monogynous and polygynous colonies, polygyny markedly decreased the relatedness among nestmate workers. Our findings also demonstrate that polygyny in M. bicolor may arise from the adoption of related or unrelated queens.     

Variation of colony types in the antFormica cinerea

Summary Formica cinerea is a rare ant species in northern Europe where it occurs in few isolated populations. Estimates of genetic relatedness among worker nestmates revealed very different colonial structures. Relatedness was g = 0.81 in one population, and g = –0.03 and = 0.01 in two others. These results indicate that some populations of the species have mainly monogynous colonies (perhaps with monandrous queens), whereas others consist of polygynous and possibly polydomous colonies. Genetic differentiation of closely located populations suggests restricted dispersal.     

Colony sex ratios vary with breeding system but not relatedness asymmetry in the facultatively polygynous ant Pheidole pallidula

Abstract.— We investigated sex allocation in a Mediterranean population of the facultatively polygynous (multiple queen per colony) ant Pheidole pallidula . This species shows a strong split sex ratio, with most colonies producing almost exclusively a single-sex brood. Our genetic (microsatellite) analyses reveal that P. pallidula has an unusual breeding system, with colonies being headed by a single or a few unrelated queens. As expected in such a breeding system, our results show no variation in relatedness asymmetry between monogynous (single queen per colony) and polygynous colonies. Nevertheless, sex allocation was tightly associated with the breeding structure, with monogynous colonies producing a male-biased brood and polygynous colonies almost only females. In addition, sex allocation was closely correlated with colony total sexual productivity. Overall, our data show that when colonies become more productive (and presumably larger) they shift from monogyny to polygyny and from male production to female production, a pattern that has never been reported in social insects.     

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.     

Queen/worker thorax volume ratios and nest-founding strategies in ants

Queen/worker thorax volume ratios were calculated in nine monogynous, seven polygynous and eight parasitic ant species in order to determine whether mode of nest founding is reflected in relative gyne size. A significant difference in this ratio was found between monogynous (independent nest founders) and polygynous and parasitic species (dependent nest founders). Thorax volume ratio in ants appears to be independent of actual gyne or worker size and can be used as a relative measure sure of colony investment in the gynes. Furthermore, thorax volume ratio seems to reflect the mode of nestfounding behaviour when compared between species within genera as well as among species in general. Polygyny is discussed as a nest-founding strategy that is selected for when nest founding by single gynes is difficult and costly. In addition, secondary benefits could be gained by polygynous colonies since investment in gyne size could be decreased.     

GENETIC VARIABILITY,QUEEN NUMBER,AND POLYANDRY IN SOCIAL HYMENOPTERA

Several hypotheses have been put forward to explain the adaptive significance of interspecific variation in mating frequencies by eusocial hymenopteran queens. Four of these hypotheses assert that polyandry is advantageous to queens because of the resultant increase in genetic variability within colonies (referred to as the “GV” hypotheses). Here we compare the frequency of polyandry between monogynous (single-queen) and polygynous (multiple-queen) ant species to test the hypotheses that (1) multiple mating functions primarily to increase intracolonial genetic variability, and (2) mating has costs (such as increased energetic losses or risk of predation or venereal disease). If one of the GV hypotheses is true and mating is costly, the frequency of polyandry should be lower in polygynous species (in which the presence of multiple queens results in low relatedness among workers) than in monogynous species. As predicted by the GV hypotheses, polyandry is less common among polygynous than among monogynous species. Furthermore, it seems that the causal relationship underlying this association is that the number of matings by queens depends on the number of queens present in the colony (rather than the number of queens being influenced by the number of matings), which also supports the GV hypotheses together with the assumption that mating has costs.