Nestmate recognition in a neotropical polygynous wasp

In social insects, nestmate recognition systems can be dynamic and modulated in response to various kinds of genetic and environmental cues. For example, multiple-queen colonies can possess weak recognition abilities relative to single-queen colonies, due to broader exposure to heritable and environmentally derived nestmate recognition cues.We conducted field experiments to examine nestmate recognition ability in a neotropical polygynous wasp, Polybia paulista. Despite the fact that the effective queen number in P. paulista is the highest ever recorded in polygynous wasps, this species exhibits a well functioning nestmate recognition system, which allows colony entry only to nestmate individuals. Similar to other social Hymenoptera, young wasps express colony specific chemical signatures within several days after emergence. This is the first study to show that the polygynous epiponine wasp is able to distinguish nestmates from non-nestmates. Received 23 May 2006; revised 6 October 2006; accepted 23 October 2006.     

Colony kin structure and breeding system in the ant genus Plagiolepis

Relatedness is a central parameter in the evolution of sociality, because kin selection theory assumes that individuals involved in altruistic interactions are related. At least three reproductive characteristics are known to profoundly affect colony kin structure in social insects: the number of reproductive queens per colony, the relatedness among breeding queens and queen mating frequency. Both the occurrence of multiple queens (polygyny) and multiple mating (polyandry) decrease within-colony relatedness, while mating among sibs increases relatedness between the workers and the brood they rear. Using DNA microsatellites, we performed a detailed genetic analysis of the colony kin structure and breeding system in three ant species belonging to the genus Plagiolepis: P. schmitzii, P. taurica and P. maura. Our data show that queens of the three species mate multiply: queens of P. maura mate with 1-2 males, queens of P. taurica with 3-11 males and queens of P. schmitzii may have 1-14 different mates. Moreover, colonies are headed by multiple queens: P. taurica and P. maura are facultatively polygynous, while P. schmitzii is obligately polygynous. Despite polyandry and polygyny, relatedness within colonies remains high because all species are characterized by sib-mating, with a fixation index F(it) = 0.25 in P. taurica, 0.24 in P. schmitzii and 0.26 in P. maura, and because the male mates of a queen are on average closely related.     

Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm

In social Hymenoptera (ants, bees, and wasps), the number of males that mate with the same queen affects social and genetic organization of the colony. However, the selective forces leading to single mating in certain conditions and multiple mating in others remain enigmatic. In this study, I investigated whether queens of the wood ant Formica paralugubris adopting different dispersal strategies varied in their mating frequency (the number of males with whom they mated). The frequency of multiple mating was determined by using microsatellite markers to genotype the sperm stored in the spermatheca of queens, and the validity of this method was confirmed by analysing mother–offspring combinations obtained from experimental single-queen colonies. Dispersing queens, which may found new colonies, did not mate with more males than queens that stayed within polygynous colonies, where the presence of numerous reproductive individuals ensured a high level of genetic diversity. Hence, this study provides no support to the hypotheses that multiple mating is beneficial because it increases genetic variability within colonies. Most of the F. paralugubris queens mated with a single male, whatever their dispersal strategy and life history. Moreover, multiple mating had little effect on colony genetic structure: the effective mating frequency was 1.11 when calculated from within-brood relatedness, and 1.13 when calculated from the number of mates detected in the sperm. Hence, occasional multiple mating by F. paralugubris queens may have no adaptive significance.     

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.     

Multiple paternity,relatedness and genetic diversity in Acromyrmex leaf-cutter ants

Multiple queen-mating occurs in many social insects, but high degrees of multiple paternity have only been found in honeybees and some yellowjacket wasps. Here we report the first case of an ant species where multiple mating reduces relatedness among female offspring to values significantly lower than 0.5. Genetic analysis of a Panamanian population of the leaf-cutter ant Acromyrmex octospinosus showed that queens mate with at least 4 to 10 males. The detected (minimum) genetically effective paternity of nestmate females was 3.9 and estimates of mean relatedness among nestmate females were ca. 0.33. This implies that multiple queen-mating in Acromyrmex octospinosus reduces relatedness to 44% of the value in full-sib colonies (0.75), realizing 84% of the maximum reduction (to 0.25) that would be obtained with an infinite number of matings. Queens of Panamanian Acromyrmex octospinosus mate with more males than sympatric queens of Atta colombica, which is contrary to the positive relationship between queen-mating frequency and colony size found across more distantly related ant species. Possible selective forces that maintain high queen-mating frequencies in leaf-cutter ants are discussed.     

Colony sex ratios vary with queen number but not relatedness asymmetry in the ant Formica exsecta

Split-sex-ratio theory assumes that conflict over whether to produce predominately males or female reproductives (gynes) is won by the workers in haplodiploid insect societies and the outcome is determined by colony kin structure. Tests of the theory have the potential to provide support for kin-selection theory and evidence of social conflict. We use natural variation in kinship among polygynous (multiple-queen) colonies of the ant Formica exsecta to study the associations between sex ratios and the relatedness of workers to female versus male brood (relatedness asymmetry). The population showed split sex ratios with about 89% of the colonies producing only males, resulting in an extremely male-biased investment ratio in the population. We make two important points with our data. First, we show that queen number may affect sex ratio independently of relatedness asymmetry. Colonies producing only males had greater genetic effective queen number but did not have greater relatedness asymmetry from the perspective of the adult workers that rear the brood. This lack of a difference in relatedness asymmetry between colonies producing females and those producing only males was associated with a generally low relatedness between workers and brood. Second, studies that suggest support for the relatedness-asymmetry hypothesis based on indirect measures of relatedness asymmetry (e.g. queen number estimated from relatedness data taken from the brood only) should be considered with caution. We propose a new hypothesis that explains split sex ratios in polygynous social insects based on the value of producing replacement queens.     

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.     

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.     

Polygynous supercolonies of the acacia‐ant Pseudomyrmex peperi,an inferior colony founder

In ant–plant protection mutualisms, plants provide nesting space and nutrition to defending ants. Several plant–ants are polygynous. Possessing more than one queen per colony can reduce nestmate relatedness and consequently the inclusive fitness of workers. Here, we investigated the colony structure of the obligate acacia‐ant Pseudomyrmex peperi, which competes for nesting space with several congeneric and sympatric species. Pseudomyrmex peperi had a lower colony founding success than its congeners and thus, appears to be competitively inferior during the early stages of colony development. Aggression assays showed that P. peperi establishes distinct, but highly polygynous supercolonies, which can inhabit large clusters of host trees. Analysing queens, workers, males and virgin queens from two supercolonies with eight polymorphic microsatellite markers revealed a maximum of three alleles per locus within a colony and, thus, high relatedness among nestmates. Colonies had probably been founded by one singly mated queen and supercolonies resulted from intranidal mating among colony‐derived males and daughter queens. This strategy allows colonies to grow by budding and to occupy individual plant clusters for time spans that are longer than an individual queen’s life. Ancestral states reconstruction indicated that polygyny represents the derived state within obligate acacia‐ants. We suggest that the extreme polygyny of Pseudomyrmex peperi, which is achieved by intranidal mating and thereby maintains high nestmate relatedness, might play an important role for species coexistence in a dynamic and competitive habitat.     

The role of queens in colonies of the swarm-founding wasp Parachartergus colobopterus

Social insect queens reproduce while workers generally do not. Queens may also have other behavioural roles in the colony. In small, independent-founding colonies of social wasps, the dominant queen physically enforces her interests over those of the workers and serves as a pacemaker of the colony, stimulating workers to forage and engage in other tasks. By contrast, in large-colony, swarm-founding wasps, the collective interests of the workers are fulfilled in sex allocation and production of males, whether or not they coincide with the interests of the queens. The behavioural role of the queens in such species has not been extensively studied. We investigated the role of the queens both in regulating worker activity and in reducing the numbers of reproductively active queens in the swarm-founding epiponine wasp Parachartergus colobopterus. We found no evidence that queens regulate worker activity, as they were rarely involved in any interactions. Worker activity may be self-organized, without centralized active control by anyone. Furthermore, we found no evidence that the reduction in queen number characteristic of this tribe of wasps occurs in response to aggression among queens. The reduction in queen number may be a result of worker treatment of queens, although worker discrimination against some queens was not obvious in our data. i Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

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.     

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.     

Sociogenetic organization of the ants Myrmica ruginodis and Myrmica lobicornis: Number,relatedness and longevity of reproducing individuals

The number and relationships of reproducing individuals create the observed genetic heterogeneity within a social insect colony. These are referred to as sociogenetic organization and were studied in the red ants M. ruginodis and M. lobicornis. Direct observations of the queen numbers were obtained by excavating colonies. The effective number of reproducing individuals was estimated from genetic relatedness based on genotype frequency data. Sociogenetic organization of colonies of both species is simple. The number of queens is low, single mating of queens is the rule and queen to queen variation in worker production is minor. The important variables of sociogenetic organization are the number and relatedness of coexisting queens in polygynous colonies. Queen nestmates are related on average by 0.405 in polygynous colonies of M. ruginodis, showing that colonies recruit their own daughters as new reproductives. The distribution of queen number in M. ruginodis indicates that the study population contains both microgyna and macrogyna types of the species. The large proportion of colonies where the resident queen(s) is not the mother of the workers shows that the average life span of a queen is short and colonies are serially polygynous.     

Shape differences rather than size differences between castes in the Neotropical swarm-founding wasp <Emphasis Type="Italic">Metapolybia docilis</Emphasis> (Hymenoptera: Vespidae,Epiponini)

Background  

Swarm-founding epiponine wasps are an intriguing group of social insects in which colonies are polygynic (several queens share reproduction) and differentiation between castes is often not obvious. However, caste differences in some may be more pronounced in later phases of the colony cycle.     

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.     

Experimental manipulation of queen number affects colony sex ratio investment in the highly polygynous ant Formica exsecta

In polygynous (multiple queens per nest) ants, queen dispersal is often limited with young queens being recruited within the parental colony. This mode of dispersal leads to local resource competition between nestmate queens and is frequently associated with extremely male-biased sex ratios at the population level. The queen-replenishment hypothesis has been recently proposed to explain colony sex ratio investment under such conditions. It predicts that colonies containing many queens (subject to high local resource competition) should only produce males, whereas colonies hosting few queens (reduced or no local resource competition) should produce new queens in addition to males. We experimentally tested this hypothesis in the ant Formica exsecta by manipulating queen number over three consecutive years in 120 colonies of a highly polygynous population. Queens were transferred from 40 colonies into another 40 colonies while queen number was not manipulated in 40 control colonies. Genetic analyses of worker offspring revealed that our treatment significantly changed the number of reproductive queens. The sex ratio of colonies was significantly different between treatments in the third breeding season following the experiment initiation. We found that, as predicted by the queen-replenishment hypothesis, queen removal resulted in a significant increase in the proportion of colonies that produced new queens. These results provide the first experimental evidence for the queen-replenishment hypothesis, which might account for sex ratio specialization in many highly polygynous ant species.     

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.     

Egg Cannibalism in a Facultative Polygynous Ant: Conflict for Reproduction or Strategy to Survive?

Policing, i.e. all behaviours that prevent a nestmate from reproducing, is currently observed in social insects. It is presumed to have evolved to regulate potential conflicts generated by genetic asymmetries or to enhance colony efficiency by avoiding surplus reproductives and brood. In the ant, Ectatomma tuberculatum, individual queen fecundity was similar in monogynous and polygynous colonies issued from a Mexican population. Egg cannibalism, however, occurred in the polygynous colonies. The stealing and destruction of reproductive queen‐laid eggs involved only nestmate queens, even if they were highly related. No queen appeared to monopolize reproduction in the polygynous colonies. But, the observed value of relatedness among workers differed from the expected value, suggesting an unequal sharing of reproduction between queens. We discussed whether the cannibalism of queen‐laid eggs in E. tuberculatum results from a competition for reproduction among queens or if this phenomenon is related to constraints on nutritional resources.     

The social consequences of honey bee polyandry: the effects of kinship on worker interactions within colonies

Honey bees, Apis mellifera L., are polyandrous and several males simultaneously father offspring within a single colony. The relatedness of female colony members therefore varies with their paternity: workers encounter both patrilineal full sister (r¯=0·75) and non-patrilineal half-sister (r¯=0·25) nestmates. The impact of this intra-colony genetic variation on social grooming and trophallaxis (liquid food exchange) among workers in colonies consisting of two phenotypically-distinct worker patrilines was examined. Workers in these colonies groomed and fed a disproportionately large number of full sisters despite a tendency to encounter a disproportionately large number of half-sisters. Thus, workers actively discriminated between full and half-sisters. This patrilineal discrimination occurred both in colonies with laying queens and in a queenless colony rearing replacement queens. These results suggest that intracolony genetic variation may have a major effect on colony social organization.