Colony-founding Queens Research Articles

Co-founding ant queens prevent disease by performing prophylactic undertaking behaviour

BackgroundSocial insects form densely crowded societies in environments with high pathogen loads, but have evolved collective defences that mitigate the impact of disease. However, colony-founding queens lack this protection and suffer high rates of mortality. The impact of pathogens may be exacerbated in species where queens found colonies together, as healthy individuals may contract pathogens from infectious co-founders. Therefore, we tested whether ant queens avoid founding colonies with pathogen-exposed conspecifics and how they might limit disease transmission from infectious individuals.ResultsUsing Lasius niger queens and a naturally infecting fungal pathogen Metarhizium brunneum, we observed that queens were equally likely to found colonies with another pathogen-exposed or sham-treated queen. However, when one queen died, the surviving individual performed biting, burial and removal of the corpse. These undertaking behaviours were performed prophylactically, i.e. targeted equally towards non-infected and infected corpses, as well as carried out before infected corpses became infectious. Biting and burial reduced the risk of the queens contracting and dying from disease from an infectious corpse of a dead co-foundress.ConclusionsWe show that co-founding ant queens express undertaking behaviours that, in mature colonies, are performed exclusively by workers. Such infection avoidance behaviours act before the queens can contract the disease and will therefore improve the overall chance of colony founding success in ant queens.

Pesticide reduces bumblebee colony initiation and increases probability of population extinction.

Pollinators are in global decline, and agricultural pesticides are a potential driver of this. Recent studies have suggested that pesticides may significantly impact bumblebee colonies, an important and declining group of pollinators. Here we show that colony founding queens, a critical yet vulnerable stage of the bumblebee lifecycle, are less likely to initiate a colony after exposure to thiamethoxam, a neonicotinoid insecticide. Bombus terrestris queens were exposed to field-relevant levels of thiamethoxam, and two natural stressors, the parasite Crithidia bombi, and varying hibernation durations. Exposure to thiamethoxam produced a 26% reduction in the proportion of queens that laid eggs, and advanced the timing of colony initiation, although we did not detect impacts of any experimental treatment on the ability of queens to produce adult offspring during the 14-week experimental period. As expected from previous studies, hibernation duration also had an impact on egg laying, but there was no significant interaction with insecticide treatment. Modelling the impacts of a 26% reduction in colony founding on population dynamics dramatically increased the likelihood of population extinction. This shows that neonicotinoids can affect this critical stage in the bumblebee lifecycle, and may have significant impacts on population dynamics.

Nutrient allocation for somatic maintenance and worker production by the queen of the Japanese black carpenter ant, Camponotus japonicus (Hymenoptera: Formicidae)

Because queens of claustral colony-founding ants raise their first workers without foraging outside the nest, the number of first workers produced depends on the nutrient reserves of the queen when she begins to establish the colony. Although a low mortality rate of queens may be expected because they seal themselves off in the nest chambers, they do face a risk of starvation. Therefore, the queens must allocate nutrients for somatic maintenance and worker production, including the feeding of larvae. However, there are few reports on the nutrient consumption of queens. To clarify the nutrient resource utilization of claustral colony-founding queens, newly mated queens of the Japanese black carpenter ant, Camponotus japonicus (Mayr), were collected just after the nuptial flight and reared in an incubator at 25 °C in the dark. The non-lipid mass and lipid mass of the queens were measured at 0, 10, 20, 30, 40, and 52 days after the nuptial flight. A significant decline in the non-lipid mass was found in the queens after hatching of larvae. In contrast, the lipid mass of the queen decreased soon after the nuptial flight. The results indicate that the somatic maintenance of the founding queens relies exclusively on lipids, while other nutrients, such as protein, may be used for feeding the larvae.

Effects of overwintering temperature on the survival of the black garden ant (Lasius niger)

The overwintering temperatures of ants might well be elevated due to climate change. We studied whether the overwintering temperature affects the survival of the queens and whole colonies of the black garden ant, Lasius niger (Linnaeus, 1758). In two consecutive years (2009, 2010) we collected mated, colony founding queens (n=280) from the urban area of Turku, Finland. Half of the queens overwintered in +7 to +8°C and the other half in +2°C. After the overwintering period, we determined their survival rate and measured the body fat content, body size and immune defence (encapsulation rate) of overwintering queens. Using the same setup, we studied the survival of 1-year-old L. niger colonies (queen & workers). Overwintering at a lower temperature (+2°C) decreased the survival of workers. The survival of colony founding queens differed between years, but unlike with workers, the overwintering temperature did not affect their survival: neither in the colony experiment nor in the single queen experiment. All of the surviving queens managed to produce their worker offspring at the same rate. The relative amount of body fat of queens was higher for those who overwintered at a lower temperature, which is likely a result of lower energy consumption. We did not detect differences in the encapsulation rate between the temperature treatment groups. The ability of colony founding queens to tolerate wide overwintering temperature variations present in urban environments may explain the success of the colony in urban areas. As the colony grows, the overwintering chambers may extend more deeply into the ground. Thus, workers may not have to cope with such cold conditions as colony founding queens.

Thelytokous Parthenogenesis in the Ant Myrmecina nipponica (Hymenoptera: Formicidae).

Myrmecina nipponica Wheeler is a terrestrial ant nesting chiefly in the soil in forest. It is a specialized predator of oribatid mites, but also scavenges on a broad spectrum of other arthropods. In the studied population at Cape Manazuru in central Japan, M. nipponica colonies are typically monogynous, and previous dissections of queens suggested that these individuals were not inseminated, thus suggesting these ants can reproduce via thelytokous parthenogenesis. To test for thelytokous parthenogenesis in M. nipponica the spermathecae of queens (dealate gynes) from worker-containing colonies were histologically examined in detail. All specimens examined (n=5) had no spermatozoa in the spermatheca. In addition, a total of four colony-founding queens were reared in isolation in the laboratory to test whether non-inseminated females were capable of egg laying and to test whether female offspring emerged from this brood. In all of four culture replicates, only new workers were produced from the eggs those queens had laid and male offspring was absent. After the breeding experiment, the queens' spermathecae were histologically examined and no sperm were detected in their spermathecae. These results reveal that M. nipponica queens of the Manazuru population are capable of producing female offspring thelytokously. Sexual reproduction by typical gynes and also by intermorphs has been known from other local populations of M. nipponica; therefore, this species shows geographical polymorphism in sexuality.

Nosema bombi(Microsporidia: Nosematidae) and Trypanosomatid Prevalence in Spring Bumble Bee Queens (Hymenoptera: Apidae:Bombus) in Kansas

Several species of bumble bees are declining in the United States; these declining populations often show higher prevalence of Nosema bombi, a microsporidian pathogen. To date, surveys of bumble bee pathogens in the United States have only been conducted on workers and males, yet the health of a population is ultimately dependent on the success of colony-founding queens. We conducted a molecular-diagnostic survey of the prevalence of N. bombi and trypanosomatids, such as Crithidia bombi, in six species of spring queens (n = 142) collected in 2011 and 2013 at three sites in central Kansas. Nosema bombi was found in 27% of Bombus pensylvanicus and 13% of B. auricomus but was not found in the other species sampled. Trypanosomatids were only found in B. pensylvanicus (9%) during the May 2013 sampling period. The high prevalence of N. bombi in B. pensylvanicus is consistent with other surveys for this pathogen in other castes, but the high prevalence of N. bombi in B. auricomus is a novel finding. Although the conservation status of B. auricomus has not been thoroughly assessed, two recently published surveys showed that B. auricomus were less common in portions of the species' range. Based on those findings and an oft-cited link between N. bombi prevalence and bumble bee species' decline (e.g., B. pensylvanicus) in other studies, our findings suggest B. auricomus populations in Kansas may warrant further scrutiny.

Maternity-related plasticity in circadian rhythms of bumble-bee queens

Unlike most animals studied so far in which the activity with no circadian rhythms is pathological or linked to deteriorating performance, worker bees and ants naturally care for their sibling brood around the clock with no apparent ill effects. Here, we tested whether bumble-bee queens that care alone for their first batch of offspring are also capable of a similar chronobiological plasticity. We monitored locomotor activity of Bombus terrestris queens at various life cycle stages, and queens for which we manipulated the presence of brood or removed the ovaries. We found that gynes typically emerged from the pupae with no circadian rhythms, but after several days showed robust rhythms that were not affected by mating or diapauses. Colony-founding queens with brood showed attenuated circadian rhythms, irrespective of the presence of ovaries. By contrast, queens that lost their brood switched again to activity with strong circadian rhythms. The discovery that circadian rhythms in bumble-bee queens are regulated by the life cycle and the presence of brood suggests that plasticity in the circadian clock of bees is ancient and related to maternal behaviour or physiology, and is not a derived trait that evolved with the evolution of the worker caste.

Division of labor and the evolution of task sharing in queen associations of the harvester ant Pogonomyrmex californicus

Division of labor is a key factor in the ecological success of social groups. Recent work suggests that division of labor can emerge even without specific adaptations for task specialization and that it can appear in incipient social groups as a self-organizational property. We investigated experimentally how selection and self-organization may interact during the evolution of division of labor by examining task performance in groups of normally solitary versus normally social ant queens. We created social pairs of colony-founding queens from two populations of the ant Pogonomyrmex californicus, one in which queens are normally solitary and one in which queens form foundress groups, and observed their behavior during nest excavation. In both populations, one of the two queens usually performed most of the excavation, becoming the excavation specialist. We could predict which queen would become the specialist based on their relative propensities to perform the task in other contexts, consistent with a variance-based model of task specialization. The occurrence of specialization even when group members were not adapted to social life suggests that division of labor may well have been present in incipient queen groups. However, division of labor can result in cost skew among group members, and thus, paradoxically, within-group selection may constrain or even reduce specialization. Consistent with this effect, pairs of normally solitary queens were significantly more asymmetrical in their task performance than normally social pairs, in which both queens nearly always performed the behavior to some degree.

An experimental study of pleometrotic colony founding in the fire ant, Solenopsis invicta : what is the basis for association?

Many benefits and risks of cooperative colony founding (pleometrosis) have been identified, but rarely have the proximate factors that lead to association been considered. This study examined the choices queens make during the first few hours after mating, and some of the correlates of those choices. Queens had a strong affinity for preformed holes in the soil and readily used these as their initial founding chambers. This affinity was so strong that in a field experiment, the dispersion pattern of preformed holes controlled the final dispersion of colony-founding queens. Attraction to partially formed holes is thus an important cause of pleometrosis. The excavation of complete founding chambers incurred no measurable cost on the subsequent reproductive output of queens, suggesting that the primary benefit of using preformed holes is to remove the queen quickly from exposure to predation and desiccation. In the field, pairs of queens offered five equivalent preformed holes in soil were more likely to share the same hole if the holes were shallow and close together. In these experiments, queens modified preformed soil holes so that the test holes were no longer equivalent, causing the choice of queen and hole to become confounded. Laboratory experiments in plaster arenas with unmodifiable holes confirmed the field experiments: queens were more likely to share a hole when the holes were shallow than when they were deep. Because queens entering adequately deep holes seldom reemerged, this suggested that the likelihood of sharing increased with increasing contact between queens, that is, when queens were readily and frequently detected. Such contacts will also predict the future competitive environments to be experienced by incipient colonies, and may temper the tendency of queens to associate. However, experiments in which queens were exposed to high and low densities before pairing in the choice arenas failed to show an effect on the choice to join the resident queen. Queens that joined a resident queen differed in their robustness from queens that did not join. Queens choosing their own partners did no better reproductively than those assigned partners at random. Overall, this study suggests that (1) newly mated queens are under strong selection to leave the soil surface and do so by using any available holes, whether dug by another queen or of some other origin; (2) they are attracted to other queens, and are more likely to cofound as contact with the potential cofoundress becomes more frequent and (3) they choose whether or not to cofound partly on the basis of their own reproductive characteristics.

Settlement and distribution of colony-founding queens of the arboreal ant, Crematogaster ashmeadi , in a longleaf pine forest

Crematogaster ashmeadi is the dominant arboreal ant occurring on longleaf pines in the Apalachicola National Forest of northern Florida. Newly-mated C. ashmeadi queens preferentially founded colonies in abandoned beetle galleries in the dead branches of longleaf pine saplings. There was a positive association between the frequency of queens in trees, several size-related tree characteristics and the amount of insect boring activity in dead branches. The dispersion of newly-mated queens among trees was clumped, suggesting that these queens selected founding sites according to their suitability for colony founding, and that these favorable characteristics were clumped among saplings. The occurrence of founding nests was not related to the prior presence of other ants on the tree. Survival of incipient colonies during the first year was low (7.6 %), and their dispersion was not different from random. One possible explanation for this change in dispersion over the year is aggressive interference competition between incipient colonies, although random mortality cannot be discounted. Overall, the distribution of young C. ashmeadi colonies in longleaf pine saplings was probably determined by several factors including: the distribution of saplings, the distribution of suitable founding sites within these saplings, and aggressive interactions among incipient colonies, conspecifics and heterospecifics. C. ashmeadi probably gains dominance through a combination of early colonization and aggressive interference competition.

Diploid males in the bumble bee Bombus terrestris

AbstractThe frequency of colonies that produce diploid males after brother‐sister (50%) and nephew‐niece (37.5%) matings proves that in B. terrestris the sex is determined by a single multi‐allelic sex locus. The diploid males which develop normally into adults make up 50% of the diploid brood. In the laboratory the growth rate of colonies with diploid males is influenced only slightly. Of 41 colony founding queens caught out of a natural population, all produced a colony without any diploid males. Therefore, the number of sex alleles in this population is estimated to be at least 24. This means that in commercial rearing systems for bumble bees, involving several generations, the occurrence of diploid males can largely be prevented by a good scheme for crossings.

Alternative adaptations, sympatric speciation and the evolution of parasitic, inquiline ants

Inquiline ant species are workerless social parasites whose queens reproduce in colonies of other species alongside the host queens. Inquilines arise either when one non-parasitic species evolves into an inquiline parasite of another non-parasitic species (the interspecific hypothesis), or by the speciation of intraspecific inquilines from their host stock (the intraspecific hypothesis): it is unlikely that inquilines evolve from other forms of social parasite. This paper reviews the evidence for and against the inter-and intraspecific hypotheses. All inquilines are close phylogenetic relatives of their host species (loose ‘Emery's rule’), and some are their host's closest relative (strict ‘Emery's rule’). A problem for the interspecific hypothesis is how to explain the strict Emery's rule, because phylogenetic constraints on host choice are probably quite weak. By contrast, the intraspecific hypothesis has difficulty accounting for the parasites' sympatric reproductive isolation. Facultative polygyny, in which queens may found colonies alone or by adoption into an existing multi-queen colony, should promote the evolution of small intraspecific inquilines. This is because small colony-founding queens should preferentially seek adoption, which provides the opportunity to produce a sexual-only brood. We suggest that microgynes, i.e. miniature queens found in some polygynous ants, represent such parasites. We review the evidence that inquiline species have evolved intraspecifically from microgynes in Myrmica ants. The coexistence within a species of a monogynous (singly-queened) and a polygynous form is probably a phenomenon usually unconnected with inquiline evolution. The reproductive isolation of intraspecific inquilines plausibly arises from divergent breeding behaviour associated with the parasites' small size. Such divergence could involve either a temporal separation in mating episodes, with small parasites maturing early, or a spatial separation, with small males being sexually-selected to mate near the nest with small queens seeking adoption, instead of in mating aggregations. We conclude that inquiline species strictly following Emery's rule could have evolved by the intraspecific route. If so, such species provide evidence for West-Eberhard's “alternative adaptation” hypothesis that between-species diversity frequently stems from diversity within species. They also represent likely cases of sympatric speciation. We suggest work on the parasites' phytogeny, genetics, behaviour and mating biology to test these conclusions further.

Influence of Cocoons on Egg Laying of Colony-Founding Carpenter Ant Queens (Hymenoptera: Formicidae)

Patterns of brood production by colony-founding queens of Camponotus pennsylvanicus (De Geer), C. novaeboracensis (Fitch), and C. modoc Wheeler were examined. The presence of workers or larvae had either no effect or a negative one on oviposition by the queens, but the presence of cocoons stimulated oviposition. This regulation may control the worker/brood ratio or may synchronize the hatching of larvae, with the eclosion of new workers to care for them.

Studies on the south east Asian ant-plant associationCrematogaster borneensis/Macaranga: Adaptations of the ant partner

C. borneensis (Myrmicinae) lives in close association with several myrmecophytic species of the South East Asian pioneer tree genusMacaranga (Euphorbiaceae). The ants are adapted to the plants so closely that they do not survive away from it. The only food they utilize is provided as food bodies by the plant and honeydew from specific scale insects kept inside the hollow internodes. The anatomy of the digestive tract is also adapted to life on the host plant: the crop is very small and can store only minute food quantities. C. borneensis exclusively colonizes certainMacaranga species. Queens as well as workers are able to recognize their host plant species, probably by chemical cues. Colony founding queens swarm throughout the year, mostly during darkness. There is strong competition among queens for host plants. Queens do not carry scale insects on their nuptial flight. Worker ants are active day and night. Most of them patrol and collect food bodies on the younger parts of the host plant. An important characteristic is their cleaning behaviour, which results in removal of all foreign objects. Even though they are rather small, workers respond very aggressively to certain kinds of disturbance of the host plant. The ants attack most phytophagous insects and are especially effective in killing and removing small, softbodied herbivores (e.g. caterpillars). They do not possess a functional sting, but apply defensive secretion and—once biting an intruder—will not let go. Their effective alarm system results in a mass attack, which provides adequate defence for the colony and the host plant. A comparison with anotherCrematogaster species further illustrated the special adaptations ofC. borneensis to its host plant.

Genetic relatedness and colony organization in a species complex of ponerine ants

In the Rhytidoponera impressa group, populations of Type A (queenright, monogynous) colonies produce numerous colony-founding queens and have markedly female-biassed sex ratios of investment, the mean proportional investment in females (PF) being 0.824 for thirteen populations of confusa, chalybaea, and purpurea (0.839 for ten confusa populations). (All proportional means are retransformed from the angular transformation.) By contrast, Type B (worker-reproductive, usually polygynous) colonies reproduce by colony fission and show less female-biassed investment ratios, with mean PF values (12 populations, 2 species) ranging from 0.358 to 0.721, for estimates of colony fission costs ranging from 10% to 50% of the worker force. The population PF for Type A colonies shows significant positive correlations with the relative frequency (r=0.63, df= 11, P < 0.025) and density (r=0.70, df=11, P<0.01) of sympatric Type B colonies, indicating that Type A colonies compensate for male bias in the community sex ratio generated by Type B colonies. In one population (of purpurea) consisting entirely of Type A colonies, the estimated population PF was 0.736. In the absence of evidence for inbreeding or local mate competition, this suggests worker control of the investment ratio. There is a substantial amount of unexplained intrapopulation variation in colony sex ratios. Colony-level PF values for Type A colonies range from 0.00 to 1.00, and are not significantly correlated with colony size, number of alates, worker size, or weights of alates. Introduction

Biochemical changes in the crop, oesophagus and postpharyngeal gland of colony-founding red imported fire ant queens ( Solenopsis invicta)

Chemical analysis of hydrocarbons, triacylglycerols and free fatty acids present in hexane extracts of the crop, oesophagus and postpharyngeal gland of colony-founding queens of Solenopsis invicta Buren illustrates that the oesophagus enlarges into a thoracic crop concomitant with wing muscle histolysis. The flow of material goes from the crop to the oesophagus, but not to the postpharyngeal gland. In the crop and oesophagus triacylglycerols and the dominant chemical class, whereas the postpharyngeal gland contains primarily hydrocarbons. The pattern of postpharyngeal gland hydrocarbons changes between the time of insemination and 25 days after mating.

An Experimental Study on the Distribution of Heathland Ants

Brian (1964) has shown that colonies of the ant Lasius alienus (Forster) are found in high, dry, warm areas of heathland (dry heath) while colonies of the related species L. niger (L.) are found in low, wet, cooler areas (wet heath). The ant Tetramorium caespitum (L.) occupies the dry heath between these extremes and is a formidable competitor to both of the Lasius species. Furthermore, the fertilized females of L. niger and L. alienus tend to settle in those areas favoured by their own species (Brian, Hibble & Kelly 1966). Two questions can be posed: is there a process of selection by juvenile queens, during their nuptial flight, of those areas occupied by their own species? Or: are conditions in the type of heath occupied by one of the Lasius species unsuitable for the survival of colony founding queens of the other species? If this latter possibility were true it might be expected that a mechanism of territorial selection by fertilized females would arise by natural selection. It was considered that the second possibility could be tested experimentally by transplanting active colonies of one Lasius species into territory normally occupied by the other species. L. niger was chosen for this study because the more compact structure of its nest made transplantation possible.