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.     

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.     

BIDIRECTIONAL SHIFTS IN COLONY QUEEN NUMBER IN A SOCIALLY POLYMORPHIC ANT POPULATION

The breeding system of social organisms affects many important aspects of social life. Some species vary greatly in the number of breeders per group, but the mechanisms and selective pressures contributing to the maintenance of this polymorphism in social structure remain poorly understood. Here, we take advantage of a genetic dataset that spans 15 years to investigate the dynamics of colony queen number within a socially polymorphic ant species. Our study population of Formica selysi has single‐ and multiple‐queen colonies. We found that the social structure of this species is somewhat flexible: on average, each year 3.2% of the single‐queen colonies became polygynous, and conversely 1.4% of the multiple‐queen colonies became monogynous. The annualized queen replacement rates were 10.3% and 11.9% for single‐ and multiple‐queen colonies, respectively. New queens were often but not always related to previous colony members. At the population level, the social polymorphism appeared stable. There was no genetic differentiation between single‐ and multiple‐queen colonies at eight microsatellite loci, suggesting ongoing gene flow between social forms. Overall, the regular and bidirectional changes in queen number indicate that social structure is a labile trait in F. selysi, with neither form being favored within a time‐frame of 15 years.     

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.     

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.     

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.     

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.     

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.     

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.     

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.