Queen polymorphism and queen-morph related facultative polygyny in the ant, <Emphasis Type="Italic">Myrmecina graminicola</Emphasis> (Hymenoptera,Formicidae)

Summary: Polymorphism of the functional queens in Myrmecina graminicola is analyzed. Both gynomorphs (G-§§ G) and a wide range of intermorphs (I-§§ I) occur, which all are usually mated and egg-laying. Colonies having a gynomorphic queen are always monogynous, whereas about 57% of all colonies with intermorphic queens are polygynous, having two or more coexisting functional queens. The female sexual offspring of individual gynomorphic queens either consists of gynomorphs only, or exclusively of intermorphs. Intermorphic queens may have exclusively intermorphic female sexual progeny, or simultaneously both gynomorphs and intermorphs. Single colonies in laboratory culture produce the same kind of female progeny over several subsequent breeding cycles (artificially compressed "years" of 9-10 months). No environmental influence on queen morph determination could be detected. A genetically mediated queen polymorphism, as in Harpagoxenus sublaevis and Leptothorax sp. A, is suggested. Colony sizes vary considerably, with polygynous I-queen colonies being largest (57.2 - 34.3 s.d. workers), followed by G-queen colonies (44.6 - 22.7 s.d.) and monogynous I-queen colonies (34.4 - 23.7 s.d.), suggesting occasional budding of polygynous colonies.     

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.     

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.     

Production and reproductive function of intercastes inMyrmecina gvaminicola nipponica colonies (Hymenoptera: Formicidae)

Summary Many females morphologically intermediate between queens and workers were found in a northernmost population ofMyrmecina graminicola nipponica Wheeler. Dissection and morphological observation revealed that there were three categories of intercastes. Major intercastes were as large as queens in body size, with seven or more ovarioles, but had only one ocellus, unlike queens, which had three ocelli. Medium intercasts had an enlarged mesonotum, one or no ocellus and 2 to 12 ovarioles. Minor intercaste was very simlar to workers in external morphology, but had a spermatheca, unlike workers. Inseminated females constituted 75%, 40% and 28.6% in the major, medium and minor intercastes respectively. Many of the virgin medium and minor intercastes had a small disfunctional spermatheca.In queenright colonies, a single queen was inseminated and had an active ovary. In queenless colonies where the intercastes reproduced, however, some colonies were functionally monogynous, but the others polygynous. The ratio of polygynous colonies to monogynous colonies was lowest in July and highest in September, suggesting that polygyny results from newly inseminated intercastes remaining in their natal nests, although they leave those nests in the season of colonial budding. Queenless colonies containing inseminated intercastes exclusively produced intercastes, while queenright colonies almost exclusively produced queens.     

Social organization, reproductive behavior and ecology of Leptothorax acervorum (Hymenoptera, Formicidae) from the Sierra de Albarracin in central Spain

Summary: Leptothorax acervorum, an ant species with holarctic range, occurs in an isolated population in the Spanish Sierra de Albarracin. Dissection of dealate females and laboratory observations revealed that in contrast to other European populations, the colonies are monogynous, with one reproductive queen each and a variable number of virgin or mated dealate but not laying females. Most of the latter probably just hibernate in the mother nests, leaving them in the following spring, but a few remain there for longer time, without reproducing. Such colonies then are functionally monogynous. Alate females exhibit a stationary sexual calling, and mating behavior could be studied in the laboratory. Mated females return to the mother nest where they soon shed wings. When developing fertility before or after hibernation they are evicted from the nests; in nature they probably form daughter colonies. Patchy habitat and rough climatic conditions in the Sierra de Albarracin may be responsible for the particular reproductive behavior of L. acervorum in this area. The generally small size difference between queens and workers in the subgenus Leptothorax entails high costs of dispersal and colony foundation by single queens who have to forage for their first brood. Some kind of dependent colony foundation therefore is frequently met with in the subgenus. Notwithstanding the marked biological and a few slight morphological differences between central European L. acervorum and the Spanish population its taxonomic status as yet is unsettled. We refer to this population provisionally as "L. acervorum Albarracin".     

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.     

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.     

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.     

Ant workers selfishly bias sex ratios by manipulating female development.

Kin selection theory predicts that social insects should perform selfish manipulations as a function of colony genetic structure. We describe a novel mechanism by which this occurs. First, we use microsatellite analyses to show that, in a population of the ant Leptothorax acervorum, workers' relatedness asymmetry (ratio of relatedness to females and relatedness to males) is significantly higher in monogynous (single-queen) colonies than in polygynous (multiple-queen) colonies. Workers rear mainly queens in monogynous colonies and males in polygynous colonies. Therefore, split sex ratios in this population are correlated with workers' relatedness asymmetry. Together with significant female bias in the population numerical and investment sex ratios, this finding strongly supports kin-selection theory. Second, by determining the primary sex ratio using microsatellite markers to sex eggs, we show that the ratio of male to female eggs is the same in both monogynous and polygynous colonies and equals the overall ratio of haploids (males) to diploids (queens and workers) among adults. In contrast to workers of species with selective destruction of male brood, L. acervorum workers therefore rear eggs randomly with respect to sex and must achieve their favoured sex ratios by selectively biasing the final caste (queen or worker) of developing females.     

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.     

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.     

Dynamics and Consequences of Hierarchy Formation in the Ant Leptothorax sp. A

In the Nearctic ant Leptothorax sp. A, aggressive interactions among wingless intermorphic queens and primarily winged gynomorphic queens lead to the formation of dominance hierarchies, in which the highest-ranking individual is the only egg-layer in a colony. Fighting occurs during two periods of the annual cycle: in late summer, newly adopted young queens are integrated into the colony's hierarchy; after hibernation, fighting resumes and the high aggressiveness of α-queens may now lead to the emigration of β and other middle-ranking queens. The α-position appears to be very stable over successive fighting periods, though an estimate of nestmate relatedness by allozyme electrophoresis (Polyacrylamide gels and cellulose acetate plates) suggests that queen replacement occasionally occurs. The mean relatedness determined for adult workers in a functionally monogynous population of Leptothorax sp. A was 0.54 and their effective number of mothers therefore 1.5. This is lower than expected and found for monogynous colonies. Dominance rank is apparently not correlated with queen morph, weight, and size, but an influence of insemination, age, or previous reproductive experience is likely.     

REPRODUCTIVE SKEW AND SPLIT SEX RATIOS IN SOCIAL HYMENOPTERA

Abstract I present a model demonstrating that, in social Hymenoptera, split sex allocation can influence the evolution of reproductive partitioning (skew). In a facultatively polygynous population (with one to several queens per colony), workers vary in their relative relatedness to females (relatedness asymmetry). Split sex‐ratio theory predicts that workers in monogynous (single‐queen) colonies should concentrate on female production, as their relatedness asymmetry is relatively high, whereas workers in the polygynous colonies should concentrate on male production, as their relatedness asymmetry is relatively low. By contrast, queens in all colonies value males more highly per capita than they value females, because the worker‐controlled population sex ratio is too female‐biased from the queens' standpoint. Consider a polygynous colony in a facultatively polygynous population of perennial, social Hymenoptera with split sex ratios. A mutant queen achieving reproductive monopoly would gain from increasing her share of offspring but, because the workers would assess her colony as monogynous, would lose from the workers rearing a greater proportion of less‐valuable females from the colony's brood. This sets an upper limit on skew. Therefore, in social Hymenoptera, skew evolution is potentially affected by queen‐worker conflict over sex allocation.     

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.     

Back to one: consequences of derived monogyny in an ant with polygynous ancestors

The number of queens per colony is of fundamental importance in the life history of social insects. Multiple queening (polygyny), with dependent colony founding by budding, has repeatedly evolved from ancestral single queening (monogyny) and independent founding by solitary queens in waSPS, bees and ants. By contrast, the reversal to monogyny appears to be rare, as polygynous queens often lack morphological adaptations necessary for dispersal and independent colony founding. In the ant genus Cardiocondyla, monogynous species evolved from polygynous ancestors. Here, we show that queens of monogynous species found their colonies independently, albeit in an unusual way: they mate in the maternal nest, disperse on foot and forage during the founding phase. This reversal appears to be associated with the occurrence of a wing polymorphism, which reflects a trade-off between reproduction and dispersal. Moreover, queens of monogynous species live considerably longer than queens in related polygynous taxa, suggesting that queen life span is a plastic trait.     

Mating frequency and mating system of the polygynous ant, Leptothorax acervorum

Multiple mating by queens (polyandry) and the occurrence of multiple queens in the same colony (polygyny) alter patterns of relatedness within societies of eusocial insects. This is predicted to influence kin-selected conflicts over reproduction. We investigated the mating system of a facultatively polygynous UK population of the ant Leptothorax acervorum using up to six microsatellite loci. We estimated mating frequency by genotyping 79 dealate (colony) queens and the contents of their sperm receptacles and by detailed genetic analysis of 11 monogynous (single-queen) and nine polygynous colonies. Results indicated that 95% of queens were singly mated and 5% of queens were doubly mated. The corrected population mean mating frequency was 1.06. Parentage analysis of adults and brood in 17 colonies (10 monogynous, 7 polygynous) showed that female offspring attributable to each of 31 queens were full sisters, confirming that queens typically mate once. Inbreeding coefficients, queen-mate relatedness of zero and the low incidence of diploid males provided evidence that L. acervorum sexuals mate entirely or almost entirely at random. Males mated to queens in the same polygynous colony were not related to one another. Our data also confirmed that polygynous colonies contain queens that are related on average and that their workers had a mixed maternity. We conclude that the mating system of L. acervorum involves queens that mate near nests with unrelated males and then seek readoption by those nests, and queens that mate in mating aggregations away from nests, also with unrelated males.     

Morpho-physiological variability and differentiation of reproductive roles among foundresses of the primitively eusocial wasp, Belonogaster petiolata (Degeer) (Hymenoptera, Vespidae)

Summary: Pre-nesting foundresses of Belonogaster petiolata (Degeer) displayed a continuous variation in body size and ovarian development, wherein the majority (96%) of females possessed well-developed or developing ovaries. The latter indicates that most foundresses, including those that ultimately become subordinates in multiple-foundress colonies, have the potential to lay eggs when they first initiate or join nests. Relatively small differences in ovarian development between associated females at the start of the nesting season became pronounced over the course of the pre-emergence and early pre-matrifilial period concurrently with the differentiation of their roles as queens or subordinates. In pre-matrifilial colonies, ovarian development of queens was significantly greater than that of subordinates. Dominance rank and ovarian development among subordinates in pre-matrifilial colonies were not correlated, probably due to advanced ovarian regression in these females. The majority (96.5%) of foundresses from three successive nesting seasons were inseminated and would therefore have been capable of laying female-producing (i.e. worker- and queen-destined) eggs. Although queens of B. petiolata were not significantly larger than subordinates, they were the largest females in 41% of colonies. Similarly, #-foundresses were larger on average than %-foundresses. This indicates that body size may contribute to social and reproductive dominance, but is probably of secondary importance compared with hormonal and nutritional factors. These and previously published findings from B. petiolata suggest that the fitness benefits of associating with other foundresses during colony foundation may be largely mutualistic, and favoured by individual selection in addition to kin selection.     

Life-history phenotypes in populations of Brachyrhaphis episcopi (Poeciliidae) with different predator communities

Variation among populations in extrinsic mortality schedules selects for different patterns of investment in key life-history traits. We compared life-history phenotypes among 12 populations of the live-bearing fish Brachyrhaphis episcopi. Five populations co-occurred with predatory fish large enough to prey upon adults, while the other seven populations lacked these predators. At sites with large predatory fish, both sexes reached maturity at a smaller size. Females of small to average length that co-occurred with predators had higher fecundity and greater reproductive allotment than those from populations that lacked predators, but the fecundity and reproductive allotment of females one standard deviation larger than mean body length did not differ among sites. In populations with large predatory fish, offspring mass was significantly reduced. In each population, fecundity, offspring size and reproductive allotment increased with female body size. When controlling for maternal size, offspring mass and number were significantly negatively correlated, indicating a phenotypic trade-off. This trade-off was non-linear, however, because reproductive allotment still increased with brood size after controlling for maternal size. Similar differences in life-history phenotypes among populations with and without large aquatic predators have been reported for Brachyrhaphis rhabdophora in Costa Rica and Poecilia reticulata (a guppy) in Trinidad. This may represent a convergent adaptation in life-history strategies attributable to predator-mediated effects or environmental correlates of predator presence.     

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.     

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.