Sociogenetic Organization Research Articles

Genetic Diversity in Pioneer Ants: The Cardiocondyla shuckardi Group

The myrmicine ant genus Cardiocondyla consists of around 80 species of small, inconspicuous ants, which live mainly in subtropical and tropical Africa, Eurasia, and Australia. Several species have been accidentally introduced to America and have also invaded numerous originally ant-free islands around the world. The diversity of life histories in this genus, with lethally fighting wingless males, dominance hierarchies among queens, and considerable variation in the sociogenetic organization of colonies across species, has made it an interesting model to investigate the evolution and behavioral ecology of reproductive strategies. Taxa of the African Cardiocondyla shuckardi group are of particular interest, as in a phylogeny they lie between facultatively polygynous species with fatal male competition and monogynous species with mutually tolerant males. Studies on male behavior and sociogenetics in C. “venustula,” a widespread member of the C. shuckardi group, showed that males defend small territories inside their subterraneous nests. At the same time, they revealed a surprisingly large variability in mtDNA haplotypes both within and between populations in South Africa, Angola, and Côte d’Ivoire. As the different lineages are very similar in morphology and nuclear markers, more research is needed to clarify the very confused taxonomic situation in this fascinating group of ants.

Population structure and sociogenetic organisation in a species with ergatoid queens, the desert ant Ocymyrmex robustior

In ants, reproductive division of labour is typically associated with queen-worker dimorphism. In some species with ergatoid queens (wingless worker-like queens), this polymorphism is drastically reduced and virgin queens may integrate the worker force. While ergatoid queens have been described in several species, their colony and population genetic structure remain largely unstudied. Here, we investigated the population structure and sociogenetic organisation of the desert ant Ocymyrmex robustior. All Ocymyrmex species have only ergatoid queens that are worker-sized. Workers, queens, and males from a large population were genotyped at ten polymorphic microsatellite loci. Our results show that the study population is genetically structured, consistent with dependent colony foundation. Genetic analyses revealed that 17.6% of the males were diploid; diploid males are fertile, siring triploid females. Nests were typically headed by a single queen, and queens were strictly monandrous. However, several nests in the population shared matrilines, indicating polygyny, polydomy, dependent colony foundation, serial polygyny, or a combination of these processes. Dissections reveal that workers lay eggs in both queenright and queenless nests, while virgin ergatoid queens lay eggs in queenright nests only. However, our genetic analyses show that male offspring in queenright nests are all queen-produced, suggesting worker policing and/or trophic egg laying.

High inter-colonial variation in worker nestmate relatedness and diverse social structure in a desert ant from Mongolia

Ants of the genus Cataglyphis have a broad distribution and display a remarkable degree of variation in life-history traits between species, making them an excellent model system for comparative studies, but the biology of many key species remains unknown. In this study we present the first data on the most easterly distributed member of the genus, Cataglyphis aenescens from Mongolia. We collected workers and brood from 40 colonies from a population located on the outskirts of Sainshand, in south-eastern Mongolia, and genotyped them with microsatellite markers. In the population studied, our data strongly suggest that this species is monodomous, facultatively polygynous and exhibits a low level of polyandry compared to most other Cataglyphis species. The large worker size variation observed within colonies was not related to the level of genetic relatedness. We found no evidence of genetic isolation by distance based on workers and no evidence of thelytokous reproduction by queens as occurs in some other species. Although the sociogenetic organisation of this species could not be completely resolved, it is clear that there is a sharp contrast between C. aenescens and its closest congener, C. cursor. This underlines the variability of various life-history traits exhibited within the group, and we discuss the new findings in light of the available biological and phylogenetic information.

Sociogenetic organisation of two desert ants

Desert ants of the genus Cataglyphis evolved a remarkable diversity in their reproductive strategies. In Cataglyphis species where social organisation was described so far, colonies are headed by one or multiple queens, queens being singly or multiply mated, and workers and/or queens possess the ability to reproduce asexually via thelytokous parthenogenesis. Here, we investigate the social organisation of C. bombycina (group bombycinus) and C. theryi (group albicans) using highly polymorphic microsatellite markers. Our results show that both species are characterized by monogynous colonies and multiply mated queens, supporting the idea that polyandry is an ancestral trait of the genus. No evidence for parthenogenetic reproduction by queens was found. One distinctive feature of the species C. bombycina among the genus is the presence of a morphologically distinct soldier caste, with highly developed scythe blades jaws. In the only colony where a significant number of soldiers have been sampled, the distribution of patrilines is fundamentally different between the soldier and the worker caste. This result suggests a genetic contribution to worker caste determination in this species, and certainly awaits further investigation.

Multiple mating and supercoloniality in Cataglyphis desert ants

In social organisms, the breeding system corresponds to the number of breeders in a group, their genetic relationships, and the distribution of reproduction among them. Recent, genetically based studies suggest an amazing array of breeding system and reproductive strategies in desert ants of the genus Cataglyphis. Using highly polymorphic DNA microsatellites, we performed a detailed analysis of the breeding system and population genetic structure of two Cataglyphis species belonging to the same phylogenetic group: C. niger and C. savignyi. Our results show that both species present very different breeding systems. C. savignyi colonies are headed by a single queen and populations are multicolonial. Remarkably, queens show one of the highest mating frequency reported in ants (Mp = 9.25). Workers can reproduce by both arrhenotokous and thelytokous parthenogenesis. By contrast, colonies of C. niger are headed by several, multiply mated queens (Mp = 5.17), and they are organized in supercolonial populations made of numerous interconnected nests. Workers lay arrhenotokous eggs only. These results illustrate the high variability in the socio-genetic organization that evolved in desert ants of the genus Cataglyphis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 866–876.

Colony genetic structure in the Australian jumper ant Myrmecia pilosula

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.

Survival and growth of parasitic Maculinea alcon caterpillars (Lepidoptera, Lycaenidae) in laboratory nests of three Myrmica ant species

The Alcon blue butterfly (Maculinea alcon) parasitizes the nests of several Myrmica ant species. In Denmark, it uses M. rubra and M. ruginodis, but never M. scabrinodis. To further examine the basis of this specificity and local co-adaptation between host and parasite, the pattern of growth and survival of newly-adopted caterpillars of M. alcon in Myrmica subcolonies was examined in the laboratory. M. alcon caterpillars were collected from three populations differing in their host use, and reared in laboratory nests of all three ant species collected from each M. alcon population. While there were differences in the pattern of growth of caterpillars from different populations during the first few months after adoption, which depended on host ant species and the site from which the ants were collected, there was no evidence of major differences in final size achieved. Survival was, however, much higher in nests of M. rubra than in nests of M. ruginodis and M. scabrinodis, even for caterpillars from a population that is never known to use M. rubra as a host in the field. The caterpillars of M. alcon thus do not show local adaptation in their pattern of growth and survival, but instead show a pattern that may reflect different nestmate recognition abilities of the host ants, related to their sociogenetic organisation. The pattern of observed host ant use in the field seems to result from a combination of differences in local host availability and locally adapted infectivity, modulated by smaller differences in survivorship in the nests of the different host ants.

Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum

Sweat bees (Halictidae) exhibit great interspecific and intraspecific diversity in their social organisation, yet there is remarkably little information on the sociogenetic organisation of any species. Lasioglossum malachurum is a eusocial sweat bee with an annual lifecycle that exhibits considerable variation in its social organisation across its wide geographic range from northern to southern Europe. We collected all adults from 31 L. malachurum nests at Eichkogl, Austria, near the latitudinal centre of its distribution, and genotyped 148 workers using 5 highly variable microsatellite loci developed for this species. Nests were often queenless (48% of nests) during the second phase of worker activity, when colonies were provisioning the sexual brood. Pedigree reconstruction and estimates of nestmate genetic relatedness demonstrated that nests often (32% of nests) contained alien workers, probably as a result of worker drifting from their natal to a foreign nest. Queen effective mating frequency was variable (harmonic mean me = 1.24), but sometimes high (maximum 2.7). These data demonstrate that nests of L. malachurum do not have a classical eusocial sociogenetic organisation (monogyny, monandry) and thereby pose a challenge to exclusively relatedness based arguments for the evolution of eusociality in the taxon.

Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee, Lasioglossum malachurum, as revealed by microsatellites.

The sweat bees (Family Halictidae) are a socially diverse taxon in which eusociality has arisen independently numerous times. The obligate, primitively eusocial Lasioglossum malachurum, distributed widely throughout Europe, has been considered the zenith of sociality within halictids. A single queen heads a colony of smaller daughter workers which, by mid-summer, produce new sexuals (males and gynes), of which only the mated gynes overwinter to found new colonies the following spring. We excavated successfully 18 nests during the worker- and gyne-producing phases of the colony cycle and analysed each nest's queen and either all workers or all gynes using highly variable microsatellite loci developed specifically for this species. Three important points arise from our analyses. First, queens are facultatively polyandrous (queen effective mating frequency: range 1-3, harmonic mean 1.13). Second, queens may head colonies containing unrelated individuals (n = 6 of 18 nests), most probably a consequence of colony usurpation during the early phase of the colony cycle before worker emergence. Third, nonqueen's workers may, but the queen's own workers do not, lay fertilized eggs in the presence of the queen that successfully develop into gynes, in agreement with so-called 'concession' models of reproductive skew.

Queen-worker conflict over male production and the sex ratio in a facultatively polyandrous bumblebee, Bombus hypnorum: the consequences of nest usurpation

Evolutionary conflicts among social hymenopteran nestmates are theoretically likely to arise over the production of males and the sex ratio. Analysis of these conflicts has become an important focus of research into the role of kin selection in shaping social traits of hymenopteran colonies. We employ microsatellite analysis of nestmates of one social hymenopteran, the primitively eusocial and monogynous bumblebee Bombus hypnorum, to evaluate these conflicts. In our 14 study colonies, B. hypnorum queens mated between one and six times (arithmetic mean 2.5). One male generally predominated, fathering most of the offspring, thus the effective number of matings was substantially lower (1-3.13; harmonic mean 1.26). In addition, microsatellite analysis allowed the detection of alien workers, those who could not have been the offspring of the queen, in approximately half the colonies. Alien workers within the same colony were probably sisters. Polyandry and alien workers resulted in high variation among colonies in their sociogenetic organization. Genetic data were consistent with the view that all males (n = 233 examined) were produced by a colony's queen. Male parentage was therefore independent of the sociogenetic organization of the colony, suggesting that the queen, and not the workers, was in control of the laying of male-destined eggs. The population-wide sex ratio (fresh weight investment ratio) was weakly female biased. No evidence for colony-level adaptive sex ratio biasing could be detected.

Queen–worker conflict over male production and the sex ratio in a facultatively polyandrous bumblebee,Bombus hypnorum: the consequences of nest usurpation

AbstractEvolutionary conflicts among social hymenopteran nestmates are theoretically likely to arise over the production of males and the sex ratio. Analysis of these conflicts has become an important focus of research into the role of kin selection in shaping social traits of hymenopteran colonies. We employ microsatellite analysis of nestmates of one social hymenopteran, the primitively eusocial and monogynous bumblebeeBombus hypnorum, to evaluate these conflicts. In our 14 study colonies,B. hypnorumqueens mated between one and six times (arithmetic mean 2.5). One male generally predominated, fathering most of the offspring, thus the effective number of matings was substantially lower (1–3.13; harmonic mean 1.26). In addition, microsatellite analysis allowed the detection of alien workers, those who could not have been the offspring of the queen, in approximately half the colonies. Alien workers within the same colony were probably sisters. Polyandry and alien workers resulted in high variation among colonies in their sociogenetic organization. Genetic data were consistent with the view that all males (n = 233 examined) were produced by a colony’s queen. Male parentage was therefore independent of the sociogenetic organization of the colony, suggesting that the queen, and not the workers, was in control of the laying of male‐destined eggs. The population‐wide sex ratio (fresh weight investment ratio) was weakly female biased. No evidence for colony‐level adaptive sex ratio biasing could be detected.

Sociogenetic responses to ecological variation in the ant Myrmica punctiventris are context dependent

Models of social evolution predict a strong relationship between ecological factors and sociogenetic organization in social insects (e.g. queen number, nestmate relatedness and population structure). Despite a large body of coherent theory, empirical support for these predictions is weak. Here we report the results of an experiment that manipulated two ecological parameters, food and nestsite availability, thought to be important for a population of the forest ant Myrmica punctiventris. Earlier work had shown that the sociogenetic structure varies between two populations of this species, and an ecological experiment in one of the populations (in Vermont) revealed that food supplementation had the strongest effects on nestmate relatedness. We repeated the experiment in the second population (in New York) and obtained strikingly different results. We show that nestsite supplementation had the strongest effect in the New York population, and that adding both food and nestsites affected nestmate relatedness in a direction opposite to that reported from the Vermont study. These results show that the ecological context is critically important for understanding the determinants of colony structure in ants. Furthermore, comparison of our data with that of a previous study shows that social organization in New York is temporally unstable. Thus, not only do ecological factors strongly influence social organization, but their influence can vary over time. Our study underscores the need for detailed information on the natural history and ecology of social species.

Sociogenetic organization of the red ant Myrmica rubra

Knowledge of the sociogenetic organization determining the kin structure of social insect colonies is the basis for understanding the evolution of insect sociality. Kin structure is determined by the number and relatedness of queens and males reproducing in the colonies, and partitioning of reproduction among them. This study shows extreme flexibility in these traits in the facultatively polygynous red ant Myrmica rubra. Relatedness among worker nestmates varied from 0 to 0.82. The most important reason for this variation was the extensive variation in the queen number among populations. Most populations were moderately or highly polygynous resulting in low relatedness among worker nestmates, but effectively monogynous populations were also found. Polygynous populations also often tend to be polydomous, which is another reason for low relatedness. Coexisting queens were positively related in two populations out of five and relatedness was usually similar among workers in the same colonies. Due to the polydomous colony organization and short life span of queens, it was not possible to conclusively determine the importance of unequal reproduction among coexisting queens, but it did not seem to be important in determining the relatedness among worker nestmates. The estimates of the mating frequency by queens remained ambiguous, which may be due to variation among populations. In some populations relatedness among worker nestmates was high, suggesting monogyny and single mating by queens, but in single-queen laboratory nests relatedness among the worker offspring was lower, suggesting that multiple mating was common. The data on males were sparse, but indicated sperm precedence and no relatedness among males breeding in the same colony. A comparison of social organizations and habitat requirements of M. rubra and closely related M. ruginodis suggested that habitat longevity and patchiness may be important ecological factors promoting polygyny in Myrmica.

Reproductive skew and genetic relatedness inLeptothoraxants

Optimization models for the evolution of high reproductive skew in animal societies predict that high skew is evolutionarily stable only if group members are closely related. In the ant genus Leptothorax, nestmate queens differ remarkably in their behaviour: whereas in some species, queens fight and form social and reproductive dominance hierarchies (\`functional monogyny'), in others they appear to ignore each other and lay eggs at more or less similar rates (\`polygyny'). A comparative analysis of the sociogenetic organization of Leptothorax colonies indicates that: (i) worker and queen relatedness are surprisingly high even in most polygynous species; and (ii) reproductive skew as estimated from egg laying rates or the ovarian development of nestmate queens does not strongly affect the genetic structure of the colonies. In functionally monogynous species, a frequent exchange of the dominant queen apparently lowers the average relatedness among adult nestmates. In some polygynous species, on the other hand, mechanisms other than aggressive competition among queens keep relatedness from decreasing. Cyclical changes in queen number per colony and a negative influence of high queen number on the production of female sexuals may be important in this context. Preliminary relatedness estimates from virgin female sexuals from polygynous colonies of three Leptothorax species seem to indicate an association of high skew and high queen relatedness as predicted by the skew models. This result, however, does not necessarily mean that high relatedness causes high skew: as young queens are readopted mostly into their native colonies after mating, high relatedness and high skew may be mutually reinforcing.

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

AbstractThe 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.

Genetic population structure and sociogenetic organisation in Formica truncorum (Hymenoptera; Formicidae)

The genetic population structure and the sociogenetic organization of the red wood ant Formica truncorum were compared in two populations with monogynous colonies and two populations with polygynous colonies. The genetic population structure was analysed by measuring allele frequency differences among local subsets of the main study populations. The analysis of sociogenetic organisation included estimates of nestmate queen and nestmate worker relatedness, effective number of queens, effective number of matings per queen, relatedness among male mates of nestmate queens and relatedness between queens and their male mates. The monogynous populations showed no differentiation between subpopulations, whereas there were significant allele frequency differences among the subpopulations in the polygynous population. Workers, queens and males showed the same genetical population structure. The relatedness among nestmate workers and among nestmate queens was identical in the polygynous societies. In three of the four populations there was a significant heterozygote excess among queens. The queens were related to their male mates in the polygynous population analysed, but not in the monogynous ones. The data suggest limited dispersal and partial intranidal mating in the populations with polygynous colonies and outbreeding in the populations having monogynous colonies. Polyandry was common in both population types; about 50% of the females had mated at least twice. The males contributed unequally to the progeny, one male fathering on average 75% of the offspring with double mating and 45–80% with three or more matings.