Monogynous Colonies Research Articles

No major difference in growth and productivity between monogynous and polygynous colonies in the ant Myrmecina graminicola

No major difference in growth and productivity between monogynous and polygynous colonies in the ant Myrmecina graminicola

Gut Microbiome Composition of the Fire Ant Solenopsis invicta: an Integrated Analysis of Host Genotype and Geographical Distribution.

Gut symbiotic bacteria are known to be closely related to insect development, nutrient metabolism, and disease resistance traits, but the most important factors leading to changes in these communities have not been well clarified. To address this, we examined the associations between the gut symbiotic bacteria and the host genotype and geographical distribution of Solenopsis invicta in China, where it is invasive and has spread primarily by human-mediated dispersal. Thirty-two phyla were detected in the gut symbiotic bacteria of S. invicta. Proteobacteria were the most dominant group among the gut symbiotic bacteria. Furthermore, the Bray-Curtis dissimilarity matrices of the gut symbiotic bacteria were significantly positively correlated with the geographical distance between the host ant colonies, but this relationship was affected by the social form. The distance between monogyne colonies had a significant effect on the Bray-Curtis dissimilarity matrices of gut symbiotic bacteria, but the distance between polygyne colonies did not. Moreover, the Bray-Curtis dissimilarity matrices were positively correlated with Nei's genetic distance of the host but were not correlated with the COI-based genetic distance. This study provides a scientific basis for further understanding the ecological adaptability of red imported fire ants during invasion and dispersal. IMPORTANCE We demonstrated that gut microbiota composition and diversity varied among populations. These among-population differences were associated with host genotype and geographical distribution. Our results suggested that population-level differences in S. invicta gut microbiota may depend more on environmental factors than on host genotype.

Cooperation by ant queens during colony-founding perpetuates alternative forms of social organization

Key social traits, like queen number in eusocial insect colonies, have long been considered plastic, but the recent finding that colony social organization is under strict genetic control in multiple ant lineages challenges this view. This begs the question of which hardwired behavioral mechanism(s) generate alternative forms of social organization during colony development. We addressed this question in the Alpine silver ant, Formica selysi, a species with two social forms determined by a supergene. Queens that carry exclusively the M haplotype are produced by and live in monogyne (= single-queen) colonies, whereas queens that carry at least one copy of the P haplotype are produced by and live in polygyne (= multiple-queen) colonies. With extensive field samplings and laboratory experiments, we show that both types of queens successfully establish colonies independently, without being accompanied by workers, but that they do so in contrasting ways. Monogyne queens were generally intolerant of other queens and founded colonies solitarily, whereas polygyne queens were mutually attracted to each other and mainly founded colonies cooperatively. These associations persisted for months after worker emergence, suggesting that cooperative colony-founding leads to permanent multiple queening. Overall, our study shows that queens of each social form found colonies independently in the field but that P-carrying queens are more likely to cooperate, thereby contributing to perpetuate alternative forms of social organization.Significance statementUnderstanding the genetic and behavioral underpinnings of social organization is a major goal in evolutionary biology. Recent studies have shown that colony social organization is controlled by supergenes in multiple ant lineages. But the behavioral processes linking the genotype of a queen to the type of colony she will form remain largely unknown. Here, we show that in Alpine silver ants, alternative supergene genotypes are associated with different levels of social attraction and tolerance in young queens. These hardwired differences in social traits make queens carrying the P supergene haplotype more prone to cooperate and form durable associations during independent colony-founding. These findings help explain how genetic variants induce alternative forms of social organization during the ontogeny of a colony. They also illustrate how simple phenotypic differences at the individual level can result in large differences at higher levels of organization.

Distinct colony boundaries and larval discrimination in polygyne red imported fire ants (Solenopsis invicta).

Evaluating the factors that promote invasive ant abundance is critical to assess their ecological impact and inform their management. Many invasive ant species show reduced nestmate recognition and an absence of boundaries between unrelated nests, which allow populations to achieve greater densities due to reduced intraspecific competition. We examined nestmate discrimination and colony boundaries in introduced populations of the red imported fire ant (Solenopsis invicta; hereafter, fire ant). Fire ants occur in two social forms: monogyne (colonies with a single egg-laying queen) and polygyne (colonies with multiple egg-laying queens). In contrast with monogyne nests, polygyne nests are thought to be interconnected due to the reduced antagonism between non-nestmate polygyne workers, perhaps because polygyne workers habituate the colony to an odour unique to Gp-9b -carrying adults. However, colony boundaries and nestmate discrimination are poorly documented, particularly for worker-brood interactions. To delimit boundaries between field colonies, we correlated the exchange of a 15 N-glycine tracer dissolved in a sucrose solution with social form. We also evaluated nestmate discrimination between polygyne workers and larvae in the laboratory. Counter to our expectations, polygyne colonies behaved identically to monogyne colonies, suggesting both social forms maintain strict colony boundaries. Polygyne workers also preferentially fed larval nestmates and may have selectively cannibalized non-nestmates. The levels of relatedness among workers in polygyne colonies was higher than those previously reported in North America (mean±standard error: 0.269±0.037). Our study highlights the importance of combining genetic analyses with direct quantification of resource exchange to better understand the factors influencing ant invasions.

Disentangling the mechanisms linking dispersal and sociality in supergene-mediated ant social forms.

The coevolution between dispersal and sociality can lead to linked polymorphisms in both traits, which may favour the emergence of supergenes. Supergenes have recently been found to control social organization in several ant lineages. Whether and how these ‘social supergenes’ also control traits related to dispersal is yet unknown. Our goal here was to get a comprehensive view of the dispersal mechanisms associated with supergene-controlled alternative social forms in the ant Formica selysi. We measured the production and emission of young females and males by single-queen (monogyne) and multiple-queen (polygyne) colonies, the composition of mating aggregations, and the frequency of crosses within and between social forms in the wild. We found that males and females from alternative social forms did not display strong differences in their propensity to leave the nest and disperse, nor in their mating behaviour. Instead, the social forms differed substantially in sex allocation. Monogyne colonies produced 90% of the females flying to swarms, whereas 57% of the males in swarms originated from polygyne colonies. Most crosses were assortative with respect to social form. However, 20% of the monogyne females did mate with polygyne males, which is surprising as this cross has never been found in mature monogyne colonies. We suggest that the polygyny-determining haplotype free rides on monogyne females, who establish independent colonies that later become polygyne. By identifying the steps in dispersal where the social forms differ, this study sheds light on the behavioural and colony-level traits linking dispersal and sociality through supergenes.

Sex Investment Ratio and Split Sex Ratio in the Fission-Performing Ant Cataglyphis tartessica

Inclusive fitness theory predicts that the sex investment ratio should be female biased in social insects with haplodiploidy-generated relatedness asymmetry (between females and males and also among females). However, this ratio should become male biased if related females are competing with each other for resources, as it is predicted by local resource competition hypothesis. This specific situation is expected to occur in ant species that reproduce by fission, where young queens leave their mother colonies on foot to found daughter colonies. We tested this idea using the ant Cataglyphis tartessica in Donana National Park (Spain). This species is monogynous (colonies headed by a single queen), monandrous (queen mate with only one male), and reproduces by fission. Given the similarity between foraging and colony fission distances in this species, a strong local competition for resources should be expected between mother and daughter colonies. In this study, we considered investment in females the sum of the investment in gynes (virgin queens) plus the investment in the worker force that leaves with them to found a new colony. Our results show a male-biased sex investment ratio in C. tartessica of 1:8 (numerical ratio gynes/males 1:56), suggesting queen control over sexual production. In addition, we found that, during its reproductive period, this species exhibits split sex (gyne-male) production as well as split male-worker production, without any evidence of variation in relatedness asymmetry between its colonies, at the population level. An interaction between local resources competition and colony size could explain our results.

Colony fitness and garden growth in the asexual fungus-growing ant Mycocepurus smithii (Attini, Formicidae)

Nest-founding in the fungus-growing ant Mycocepurus smithii is typically by single queens (monogyny) and colonies transition to multiple queens (polygyny) as they grow larger. Here, we study the transition from monogyny to polygyny of M. smithii under lab conditions. We hypothesize that the worker-to-queen ratio affects colony growth, fungus-garden growth, and colony survival. Monogyne colonies with small gardens (0.1 g) had greater garden growth than polygyne colonies, suggesting that monogyny may be the superior strategy for small colonies after initial nest establishment. In monogyne colonies with small gardens and either 30, 60, or 90 workers, colonies with 60 workers produced the largest gardens, suggesting that an intermediate worker-to-queen ratio is optimal for monogyne colonies with small gardens. For monogyne colonies with larger gardens (0.45 g) and with either 6, 18, 60, or 90 workers, colonies with 60 or 90 workers had significantly greater garden growth than those with 6 or 18 workers. New daughter queens were produced only by colonies with a worker-to-queen ratio of 60 or 90, suggesting that only colonies with sufficient worker numbers and garden growth are stimulated to produce new queens. A single queen lays only 1.12 ± 0.06 (SE) eggs within 24 h, therefore, limiting growth of monogyne colonies. The transition from monogyny to polygyny through the addition of supernumary queens, as well as a worker-to-queen ratio of around 60, are, therefore, critical for colony growth and reproduction in M. smithii.

Joint Evolution of Asexuality and Queen Number in an Ant

Ants exhibit a striking diversity of reproductive systems, varying in traits such as the number of reproductives per colony [1], the mode of daughter production(sexual or asexual) [2], and the mode of caste determination (genetic or environmental) [3]. Species employing mixed reproductive systemspresent a unique opportunity to explore the causesand consequences of alternative breeding strategies. Mixed reproductive systems in ants include social polymorphism in colony queen number, whereby single-queen (monogyne) and multiple-queen (polygyne) colonies co-occur within species[4-7], and facultative asexuality, in which female offspring may be produced sexually or asexually within colonies [8-13]. Here, we document a remarkable confluence of multiple mixed reproductive systems in the tropical fire ant, Solenopsis geminata, in a population with three important features: (1) polygyne colonies produce workers sexually but queens asexually, whereas monogyne colonies produce both castes sexually; (2) polygyne queens mate with monogyne males to produce workers, but monogyne queens do not mate with polygyne males; and (3) different asexual/polygyne lineages evidently were founded separately by genetically distinct founder queens, which appear to have originatedfrom the same neighboring monogyne population.Multiple asexual/polygyne genomes are transmitted undiluted in this system, but sterile workers produced with sperm from a sexually-reproducing/monogynepopulation are necessary for the persistence of these lineages. The intersection of social polymorphism, facultative asexuality, and genetic caste determination marks this population of S.geminata as an embodiment of the diversityof ant reproductive systems and suggests previously unknown connections between these phenomena.

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.

An Alpine ant’s behavioural polymorphism: monogyny with and without internest aggression in Tetramorium alpestre

Social structure influences animal societies on various levels (e.g., relatedness, behaviour). In ants, both the number of matings per queen and the number of queens per colony can vary strongly. While workers from both monogynous and polygynous colonies often fight fiercely, in supercolonies (an extreme form of polygyny comprising thousands of queens in spatially separated but interconnected nests), non-nestmates interact peacefully. Studies on social and behavioural polymorphism within ant species can help elucidate their influence on genetic diversity and behaviour and the factors triggering variation in social structure and behaviour. Here, we reveal a behavioural and social polymorphism comprising monogyny with and without internest aggression in Tetramorium alpestre sampled in Tyrol, Austria. The social polymorphism is based on genetic and behavioural evidence and contrasts with the supercolonial organisation known from another location in Austria (Carinthia), 150 km away. Microsatellite genotyping using eight polymorphic loci revealed monogyny-monandry and high intranest pairwise relatedness. Interestingly, various experimental one-on-one worker encounters revealed only occasional aggressive behaviour between monogynous colonies, and thus a behavioural polymorphism. Mantel tests revealed a significant negative correlation between spatial distance and relatedness, while worker behaviour was not correlated with relatedness or spatial distance. These results indicate that behaviour might be influenced by other factors – for example, the experience of workers, ecological, chemical, and/or genetic factors not characterised in this study. However, workers distinguished nestmates from non-nestmates also when aggression was lacking. We hypothesise an adaptive value of reduced aggression. We speculate that the non-aggressive and partly aggressive encounters observed represent different options in the social structure of T. alpestre, the non-aggressiveness possibly also promoting supercolony development. The social and behavioural polymorphisms observed offer opportunities to identify the factors triggering these changes and thus further explore the behavioural and social polymorphism of this ant species.

Caste discrimination in the ant Odontomachus hastatus: What role for behavioral and chemical cues?

In social insects, the maintenance of genetic colony integrity requires resident workers to recognize any intruder with a reproductive potential and to behave appropriately to minimize fitness costs. In this study, our objective was to identify the relative contribution of the behavioral patterns and chemical cues of intruders with different fertility status on their likelihood of being accepted in monogynous colonies. Using the ponerine ant Odontomachus hastatus as a model organism, we introduced non-nestmate workers, founding queens and heterospecific workers on intact nests in the field. We demonstrated that resident workers were more aggressive toward founding queens than toward non-nestmates workers originating from the same or a distant population. Lab experiments showed that the patterns of aggression did not differ substantially between chilled and live ants, which suggests that chemical cues alone allow caste discrimination. However, the absence of behavioral cues produced more variable results in the outcome of interactions. We also showed that resident workers readily accepted non-nestmate mature queens. The analysis of cuticular profiles revealed that individuals belonging to different castes and fertility status have contrasted chemical signatures. Overall, our study revealed that workers exhibit a graded behavioral response depending on the reproductive status of intruders. We discussed the observed variation in the extent of aggression in relation to the potential fitness costs associated with acceptance or rejection error of individuals differing in fertility status.

Does Habitat Management for Northern Bobwhites Benefit the Red Imported Fire Ant?

Red imported fire ants (Solenopsis invicta) have caused damage to agricultural, economic, and wildlife resources since their accidental introduction. Previous studies have suggested that red imported fire ant (RIFA) mound densities are positively correlated to habitats maintained through disturbance. Prescribed burning and disking are two techniques commonly used to disturb portions of the landscape to maintain early successional habitats for northern bobwhite (Colinus virginianus). We tested the hypothesis that prescribed burning and disking would increase RIFA mound densities. This study was conducted in Refugio County, Texas in the Texas Coastal Prairie on Loamy Prairie range sites. Red imported fire ant mound densities were different between years (F = 5.05, df = 2, P = 0.0148). However, burning and disking had no impact (F = 0.22, df = 2, P = 0.8044) on RIFA mound densities. Initially high RIFA mound densities in our study area coupled with the territoriality of predominantly monogyne (single-queen) colonies may have limited increases in RIFA mound density in response to treatments on these study sites.

Social structure of the polygynous ant, Crematogaster osakensis

The colony structures of social insects vary greatly among species. In ant societies, the number of queens within a colony is variable during colony maturation. We investigated the social structure of a polygynous ant Crematogaster osakensis in a series of field and laboratory experiments. First, the initial colonies headed by multiple queens were found in the field. In laboratory experiments, queens that were artificially cohabited after their nuptial flight harmoniously co-existed even in the presence of newly emerged workers, suggesting that mated queens of this species can establish their colony cooperatively as primary polygynous colonies. In addition, the mating frequency of a queen was typically more than one, estimated from the sperm number stored in field-collected males and queens, and from genetic relatedness among daughters of lab-reared monogynous colonies. Second, our assessment of genetic relatedness in a mature field colony of this species revealed that dealated queens, as well as workers and alates, were relatives. The number of developed oocytes identified reproductive skew in two of five field-collected nests. Moreover, under laboratory conditions, the most fertile egg layer altered over 3 months of observation. Based on these lines of evidence, we propose that in C. osakensis, polygynous foundresses might either be unrelated and subsequently be replaced by daughter queens of particular foundresses, or be related in the first place.

Queen location and nest site preference influence colony reunification by the ant Temnothorax rugatulus

Social insect colonies adeptly make consensus decisions that emerge from distributed interactions among colony members. How consensus is accomplished when a split decision requires resolution is poorly understood. We studied colony reunification during emigrations of the crevice-dwelling ant Temnothorax rugatulus. Colonies can choose the most preferred of several alternative nest cavities, but the colony sometimes initially splits between sites and achieves consensus later via secondary emigrations. We explored the decision rules that govern reunification using artificially split colonies. When monogynous colonies were evenly divided between identical sites, the location of the queen played a decisive role, with 14 of the 16 colonies reuniting at the site that held the queen. This suggests a group-level strategy for minimizing risk to the queen by avoiding unnecessary moves. When the queen was placed in the less preferred of two sites, all 14 colonies that reunited did so at the preferred nest, despite having to move the queen. These results show that colonies balance multiple factors when reaching consensus, and that preferences for physical features of the environment can outweigh the queen’s influence.

Social Structure and Genetic Distance Mediate Nestmate Recognition and Aggressiveness in the Facultative Polygynous Ant Pheidole pallidula.

In social insects, the evolutionary stability of cooperation depends on the privileged relationships between individuals of the social group, which is facilitated by the recognition of relatives. Nestmate recognition is based on genetically determined cues and/or environmentally derived chemical components present on the cuticle of individuals. Here, we studied nestmate recognition in the ant Pheidole pallidula, a species where both single-queen (monogyne) and multiple-queen (polygyne) colonies co-occur in the same population. We combined geographical, genetic and chemical analyses to disentangle the factors influencing the level of intraspecific aggressiveness. We show that encounters between workers from neighbouring colonies (i.e., nests less than 5 m away) are on average less aggressive than those between workers from more distant colonies. Aggressive behaviour is associated with the level of genetic difference: workers from monogyne colonies are more aggressive than workers from polygyne colonies, and the intensity of aggressiveness is positively associated with the genetic distance between colonies. Since the genetic distance is correlated with the spatial distance between pairs of colonies, the lower level of aggression toward neighbours may result from their higher relatedness. In contrast, the analysis of overall cuticular hydrocarbon profiles shows that aggressive behaviour is associated neither with the chemical diversity of colonies, nor with the chemical distances between them. When considering methyl-branched alkanes only, however, chemical distances differed between monogyne and polygyne colonies and were significantly associated with aggressiveness. Altogether, these results show that the social structure of colonies and the genetic distances between colonies are two major factors influencing the intensity of agonistic behaviours in the ant P. pallidula.

Evidence of Selective Mating and Triploidy Among Two Social Forms ofSolenopsis invicta(Hymenoptera: Formicidae)

Summary A number of important behavioral and physiological traits distinguish both social forms of Solenopsis invicta Buren (Hymenoptera: Formicidae) and correlate with the Gp-9 locus within a supergene complex. These traits include fat body content, number of colony queens, dispersal, ability to initiate new colonies, size of workers, selective mortality, etc. Previous studies suggested gene flow between both social forms is unidirectional, with monogyne males mating almost exclusively with polygyne females. This study examined the genotypes of queens and their stored sperm during a mating flight in Florida where polygyne colonies predominate, and provides evidence of non-random mating; 84.6% of inseminated polygyne queens were mated to males of their own social form, and 92.4% of inseminated monogyne queens were mated by haploid males from monogyne colonies. Fertile, diploid males with unreduced sperm may be a cause for the high frequency of triploid BB alates (26.7%) and triploid polygyne alates (33.3%...

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.

Polygyny and strong genetic structuring within an isolated population of the wood ant Formica rufa

Social structuring of populations within some Formica species exhibits considerable variation going from monodomous and monogynous populations to polydomous, polygynous populations. The wood ant spe cies Formica rufa appears to be mainly monodomous and monogynous throughout most of its distribution area in central and northern Europe. Only occasionally it was mentioned that F. rufa can have both polygynous and monogynous colonies in the same geographical region. We studied an isolated polydomous F. rufa population in a deciduous mixed forest in the north-west of Belgium. The level of poly domy within the colonies varied from monodomous to 11 nests per colony. Our genetic analysis of eight variable microsatellites suggest an oligo- to polygynous structure for at least the major part of the sampled nests. Relatedness amongst nest mate workers varies considerable within the population and colonies but confirms in general a polygynous structure. Additionally high genetic diversity (e.g. up to 8 out of 11 alleles per nest for the most variable locus) and high within nest genetic variance (93%) indicate that multiple queens contribute to the gene pool of workers of the same nest. Moreover significant genetic struc turing among colonies indicates that gene flow between colonies is restricted and that exchange of workers between colonies is very limited. Finally we explain how possible factors as budding and the absence of Serviformica can explain the differences in genetic structure within this polygynous F. rufa population.

Abundance and Distribution of the Invasive Ant,Solenopsis invicta(Hymenoptera: Formicidae), in Cypress Savannas of North Carolina

AbstractThe ecological effects of invasive ants on ecosystems will depend largely on ant abundance. Cypress savannas of the southeastern United States have high conservation worth, supporting diverse and rare assemblages of species. Distance sampling was used to determine the abundance and distribution of colonies of the invasive ant, Solenopsis invicta Buren, in cypress savannas of two Carolina bays. Colonies were distributed throughout the savannas, save for areas of dense tree or shrub cover. Colony densities were much less than those reported for disturbed habitats and were similar between bays. Free-standing mounds were more common in the historically less flooded bay, and they had significantly greater volume and colony biomass as compared with these mounds in the other bay. Unlike previous studies, reporting only monogyne colonies for intact habitats of the southeast, both monogyne and polygyne colonies were present in the cypress savannas; <60% of the colonies were monogyne. Cypress savannas join a growing list of habitats, having wet sandy or loamy soils and little canopy, that have become invaded by S. invicta in the absence of anthropogenic soil disturbances. Cypress savannas resemble invaded longleaf pine savannas in vegetation physiognomy, history of fire, and dense herbaceous ground cover. While fires are critical for biodiversity, the resulting dense herbaceous ground cover may favor S. invicta. As generalist consumers and likely the most abundant ant species in these habitats, S. invicta could have important direct and indirect effects on the native communities.

Workers respond to unequal likelihood of future reproductive opportunities in an ant

In cooperatively breeding or eusocial societies, opportunities may arise for helper individuals to gain direct fitness by reproducing. However, the extent to which helpers respond differentially, in terms of their reproductive behaviour, to the probability that reproductive opportunities will arise is not fully known. In many eusocial Hymenoptera, workers lay eggs only in queenless conditions following the death of the queen or queens. Relative to polygyny (multiple queens per colony), monogyny (single queen per colony) increases the probability that queenless conditions arise. We therefore tested the hypothesis that ant workers respond differentially to queenless conditions as a function of the probability of queenlessness. We compared worker behaviour and reproduction before and after removal of queens from monogynous and polygynous colonies of the ant Leptothorax acervorum . We found that, in queenless conditions, workers from monogynous colonies were significantly more likely to lay eggs, showed a significantly reduced latency to egg laying and laid eggs at a significantly higher rate per capita than workers from polygynous colonies. In addition, before queen removal, workers that laid eggs in queenless conditions across both monogynous and polygynous colonies performed a range of behaviours associated with reproduction at significantly higher rates than nonreproductive, control workers. These ‘future reproductive’ workers also significantly reduced their rates of brood care following queen removal. These findings show that workers under monogyny reproduce more readily in queenless conditions than workers under polygyny, and that would-be reproductive workers alter their behaviour before they experience the opportunity for future reproduction. They therefore suggest that workers adaptively modulate their reproductive behaviour as a function of the likelihood of opportunities for direct reproduction arising, and that workers' behaviour is affected by the ability to gain direct fitness even when reproduction is currently not occurring. • We removed all queens from single- and multiple-queen ant colonies. • We monitored the extent of worker egg laying in queenless conditions. • Workers previously under single queens were significantly more reproductive. • Workers laying eggs when queenless differed behaviourally before queen removal. • Results suggest workers respond adaptively to the likelihood of future reproduction.