Optimal investment allocation in primitively eusocial bees: a balance model based on resource limitation of the queen

The classical model of colony dynamics developed by Macevicz and Oster predicts that optimal colony fitness in annual eusocial insects is achieved by a bang-bang strategy of reproduction: exclusive production of workers (ergonomic phase) followed by exclusive production of sexuals (reproductive phase). We propose an alternative model that assumes colony development in discrete broods and a limited overall investment potential of the queen. Based on the costs for producing eggs, workers, and sexuals and efficiency of individuals we predict the optimal number of workers and sexuals in the colony for each brood of the colony cycle that maximizes overall colony fitness. To link our model assumptions to the real world we chose model parameters according to field data of the halictid bee Lasioglossum malachurum. However, our model is representative of a large number of species with an annual life cycle and with discrete broods. Our model shows that the optimal partitioning of resources, i.e. the optimal workers/sexuals ratio depends on rearing cost for sexuals as well as productivity of workers but not on the queens’ total investment, egg cost, or rearing cost for workers. In complete accordance to Macevicz and Oster we predict a bang-bang reproduction strategy despite the differences in the basic assumptions. Potential deviations from this strategy and transitions from social to solitary breeding are discussed in the framework of our model. Received 31 October 2006; revised 29 March 2007; accepted 17 April 2007.     

Workers, sexuals, or both? Optimal allocation of resources to reproduction and growth in annual insect colonies

Understanding decisions about the allocation of resources into colony growth and reproduction in social insects is one of the challenging issues in sociobiology. In their seminal paper, Macevicz and Oster predicted that, for most annual insect colonies, a bang–bang strategy should be favoured by selection, i.e. a strategy characterised by an “ergonomic phase” with exponential colony growth followed by a “reproductive phase” with all resources invested into the production of sexuals. Yet, there is empirical evidence for the simultaneous investment into the production of workers and sexuals in annual colonies (graded control). We, therefore, re-analyse and extend the original model of Macevicz and Oster. Using basic calculus, we can show that sufficiently strong negative correlation between colony size and worker efficiency or increasing mortality of workers with increasing colony size will favour the evolution of graded allocation strategies. By similar reasoning, graded control is predicted for other factors limiting colony productivity (for example, if queens’ egg laying capacity is limited).     

Sex‐allocation conflict and sexual selection throughout the lifespan of eusocial colonies

Models of sex‐allocation conflict are central to evolutionary biology but have mostly assumed static decisions, where resource allocation strategies are constant over colony lifespan. Here, we develop a model to study how the evolution of dynamic resource allocation strategies is affected by the queen‐worker conflict in annual eusocial insects. We demonstrate that the time of dispersal of sexuals affects the sex‐allocation ratio through sexual selection on males. Furthermore, our model provides three predictions that depart from established results of classic static allocation models. First, we find that the queen wins the sex‐allocation conflict, while the workers determine the maximum colony size and colony productivity. Second, male‐biased sex allocation and protandry evolve if sexuals disperse directly after eclosion. Third, when workers are more related to new queens, then the proportional investment into queens is expected to be lower, which results from the interacting effect of sexual selection (selecting for protandry) and sex‐allocation conflict (selecting for earlier switch to producing sexuals). Overall, we find that colony ontogeny crucially affects the outcome of sex‐allocation conflict because of the evolution of distinct colony growth phases, which decouples how queens and workers affect allocation decisions and can result in asymmetric control.     

Caste regulation in the pharaoh's ant Monomorium pharaonis: the influence of queens on the production of new sexual forms

ABSTRACT. In colonies of Monomorium pharaonis (L.), the presence of fertile queens normally prevents the production of new queens and males (sexuals). The inhibitory effect of the presence of fertile queens is not shared by virgin queens or by freshly killed dead queens, but can be substituted by the artificial introduction of eggs. Moreover, fertile queens made sterile by exposure to a Juvenile Hormone analogue lose their ability to prevent the rearing of new sexuals. Thus, the inhibitory action of queens is mediated via the eggs that they lay, such that the rearing of new sexuals is limited to the times when either the number or fecundity of extant queens is reduced. Workers appear able to detect changes in the number of eggs present in the colony. When eggs are plentiful (i.e. when queens are laying at maximum rates), only worker brood is reared, but if egg numbers decline, workers will respond by rearing a new batch of males and queens. This method of caste regulation is highly efficient, and the inhibitory action of eggs on the production of sexuals is comparable to the action of 'queen substances' reported in some other social insects.     

Host choice in the phoretic mite Parasitellus fucorum (Mesostigmata: Parasitidae): which bumblebee caste is the best?

Host caste recognition may be important for the dispersal of phoretic mites associated with social insects. All developmental stages of the mite Parasitellus fucorum (Acari: Mesostigmata: Parasitidae) live in the nests of bumblebees (Hymenoptera: Apidae: Bombus). Dispersal occurs by specialised phoretic instars, deutonymphs, which attach to adult bumblebees. Since bumblebee colonies are annual and only young queens overwinter, deutonymphs that are able to discriminate between bumblebee castes and preferentially attach to queens should be favoured by selection. In the field, deutonymphs of P. fucorum were found to be phoretic on bumblebee workers and queens, and in behavioural experiments all castes proved to be attractive as carriers for the mites. However, they preferred queens that had hibernated as carriers when they could choose between workers and queens. In a further experiment, when given a choice, deutonymphs switched from males to young queens but never transferred from a queen to a male. These results suggest that deutonymphs preferentially attach to queens but may also use other castes for transport. Those dispersing on workers and males may try to switch to queens later. Host-switching is possible during copulation and on flowers, where bees of all castes forage. Received: 14 November 1997 / Accepted: 16 February 1998     

A heritable component in sex ratio and caste determination in a Cardiocondyla ant

Studies on sex ratios in social insects provide among the most compelling evidence for the importance of kin selection in social evolution. The elegant synthesis of Fisher's sex ratio principle and Hamilton's inclusive fitness theory predicts that colony-level sex ratios vary with the colonies' social and genetic structures. Numerous empirical studies in ants, bees, and wasps have corroborated these predictions. However, the evolutionary optimization of sex ratios requires genetic variation, but one fundamental determinant of sex ratios - the propensity of female larvae to develop into young queens or workers ("queen bias") - is thought to be largely controlled by the environment. Evidence for a genetic influence on sex ratio and queen bias is as yet restricted to a few taxa, in particular hybrids. Because of the very short lifetime of their queens, ants of the genus Cardiocondyla are ideal model systems for the study of complete lifetime reproductive success, queen bias, and sex ratios. We found that lifetime sex ratios of the ant Cardiocondyla kagutsuchi have a heritable component. In experimental single-queen colonies, 22 queens from a genetic lineage with a highly female-biased sex ratio produced significantly more female-biased offspring sex ratios than 16 queens from a lineage with a more male-biased sex ratio (median 91.5% vs. 58.5% female sexuals). Sex ratio variation resulted from different likelihood of female larvae developing into sexuals (median 50% vs. 22.6% female sexuals) even when uniformly nursed by workers from another colony. Consistent differences in lifetime sex ratios and queen bias among queens of C. kagutsuchi suggest that heritable, genetic or maternal effects strongly affect caste determination. Such variation might provide the basis for adaptive evolution of queen and worker strategies, though it momentarily constrains the power of workers and queens to optimize caste ratios.     

Multiple functions of fire ant Solenopsis invicta mandibular gland products

Alarm pheromones of social insects are best known for their role in the defence and maintenance of colony integrity. Previous studies with the fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae) demonstrate that the mandibular glands of workers (sterile females) and male and female sexuals produce an alarm pheromone, 2‐ethyl‐3,6‐dimethylpyrazine. The function of alarm pheromones in worker ants is well understood and divergent from the function of these compounds in the winged sexual forms. The present study quantifies the amount of pyrazine in the mandibular glands from male and female alate sexuals, as well as queens. Pyrazine production in female alates starts in the late pupal stage and increases until they reach mating flight‐ready maturity; however, after mating flight participation, the pyrazine level declines by >50%. Interestingly, mature male alates lose >85% of their mandibular gland pyrazine during mating flight activity. The results of the present study indicate that male and female sexuals use mandibular gland secretions for mating flight initiation and during mating flights. Furthermore, the ontogeny of mandibular gland products (pyrazine as the marker) from newly‐mated queens to mature colony queens shows a more than two‐fold increase in the amount of pyrazine by 6 months after mating. However, this is followed by a decline to trace amounts in mature colony queens (>2 years old), suggesting a function for mandibular gland products during colony development. Multifunctional use of social insect pheromones is well documented and data are reported in the present study suggesting new roles for mandibular gland products in fire ants.     

Colony pace: a life-history trait affecting social insect epidemiology

Among colonies of social insects, the worker turnover rate (colony ‘pace’) typically shows considerable variation. This has epidemiological consequences for parasites, because in ‘fast-paced’ colonies, with short-lived workers, the time of parasite residence in a given host will be reduced, and further transmission may thus get less likely. Here, we test this idea and ask whether pace is a life-history strategy against infectious parasites. We infected bumblebees (Bombus terrestris) with the infectious gut parasite Crithidia bombi, and experimentally manipulated birth and death rates to mimic slow and fast pace. We found that fewer workers and, importantly, fewer last-generation workers that are responsible for rearing sexuals were infected in colonies with faster pace. This translates into increased fitness in fast-paced colonies, as daughter queens exposed to fewer infected workers in the nest are less likely to become infected themselves, and have a higher chance of founding their own colonies in the next year. High worker turnover rate can thus act as a strategy of defence against a spreading infection in social insect colonies.     

Advantages and disadvantages of large colony size in a halictid bee: the queen's perspective

The size of the group of social species might influence basicaspects of productivity and social interactions. In many primitivelysocial insects, foundress queens are basically in control ofthe number of workers in their first brood. We examined factorsthat might influence the optimal number of workers a queen shouldproduce during the solitary founding phase in Lasioglossum malachurum(Hymenoptera, Halictidae). A priori, it seems plausible thatshe should produce as many workers as possible (1) to maximizecolony productivity and (2) to minimize the impact of broodparasitoids. However, there might also be unfavorable consequencesof a large colony size from the queen's perspective. First,the queen might incur disproportionately high costs that decreaseher potential for subsequent reproduction. Second, the queenmight not be able to suppress the development of ovaries ina large number of workers. As a clear advantage of a large colonysize, we found an increased production of sexuals. Contraryto our expectation, in the first worker phase, nests that wereparasitized by Sphecodes bees had more workers than did unparasitizednests. We found no evidence that the production of the firstworker brood entailed costs to the queen. However, the degreeof development of worker ovaries increased with colony size,and some degree of development was detectable with as few asfour workers. This study shows that the number of workers aqueen produces might depend on the interaction of several factors,some of which have not been considered in detail yet.     

Sex ratio conflict and worker production in eusocial hymenoptera

The best known of the conflicts occurring in eusocial Hymenoptera is queen-worker conflict over sex ratio. So far, sex ratio theory has mostly focused on optimal investment in the production of male versus female sexuals, neglecting the investment in workers. Increased investment in workers decreases immediate sexual productivity but increases expected future colony productivity. Thus, an important issue is to determine the queen's and workers' optimal investment in each of the three castes (workers, female sexuals, and male sexuals), taking into account a possible trade-off between production of female sexuals and workers (both castes developing from diploid female eggs). Here, we construct a simple and general kin selection model that allows us to calculate the evolutionarily stable investments in the three castes, while varying the identity of the party controlling resource allocation (relative investment in workers, female sexuals, and male sexuals). Our model shows that queens and workers favor the investment in workers that maximizes lifetime colony productivity of sexual males and females, whatever the colony kin structure. However, worker production is predicted to be at this optimum only if one of the two parties has complete control over resource allocation, a situation that is evolutionarily unstable because it strongly selects the other party to manipulate sex allocation in its favor. Queens are selected to force workers to raise all the males by limiting the number of eggs they lay, whereas workers should respond to egg limitation by raising a greater proportion of the female eggs into sexual females rather than workers as a means to attain a more female-biased sex allocation. This tug-of-war between queens and workers leads to a stable equilibrium where sex allocation is between the queen and worker optima and the investment in workers is below both parties' optimum. Our model further shows that, under most conditions, female larvae are in strong conflict with queens and workers over their developmental fate because they value their own reproduction more than that of siblings. With the help of our model, we also investigate how variation in queen number and number of matings per queen affect the level of conflict between queens, workers, and larvae and ultimately the allocation of resource in the three castes. Finally, we make predictions that allow us to test which party is in control of sex allocation and caste determination.     

Avoid mistakes when choosing a new home: Nest choice and adoption of Leptothorax ant queens

In ants, mating and colony founding are critical steps in the life of ant queens. Outside of their nests, young queens are exposed to intense predation. Therefore, they are expected to have evolved behavior to accurately and quickly locate a nesting place. However, data on the early life history of female reproductives are still lacking. Leptothorax gredleri is a suitable model organism to study the behavior of young queens. Reproductives can be reared under artificial conditions and readily mate in the laboratory. After mating, L. gredleri queens have the options to found solitarily, seek adoption into another colony, or return into their natal nest. In this study, we investigated the decision-making processes of female sexuals before and after mating. In particular, we tested whether female sexuals use chemical cues to find their way back to the nest, studied if they prefer their own nest over other nesting sites and followed the adoption dynamics of mated queens over 8 weeks (plus hibernation and spring). We showed that female sexuals and freshly mated queens spent more time on substrate previously used by workers from their own colony and from another colony than on a blank substrate. This discriminatory capability of queens appears to be lost in old, reproductive queens. Nest choice experiments showed that female sexuals and freshly mated queens can distinguish their own nest while old mated queens’ do not. When reintroduced in their maternal colony, young queens were readily adopted, but a few weeks later aggression against young queens led to their emigration from the maternal nest and eventually also death.     

Does the diapause experience of bumblebee queens Bombus terrestris affect colony characteristics?

1. Bumblebee colonies show much variation in the number of workers, drones, and queens produced. Because this variation prevails even when colonies are kept under identical conditions, it does not seem to be caused by extrinsic factors but rather by differences between founding queens. 2. The most likely factor that could cause differences between queens is diapause. Although colonies are raised under standardised conditions, the queens often experience diapause of different length. If there are costs associated with diapause that influence post‐diapause reproduction, the diapause history of the queens could affect colony characteristics. 3. Here, several colony characteristics are compared: number of first and second brood workers; total number of workers, drones, and queens; energy spent on sexuals; sex ratio; rate of worker production; time to emergence of first reproductive; and colony lifetime. Colonies were used where the queens experienced a diapause treatment of 0 (nondiapause queens), 2, and 4 months. 4. Although no proof was found for the existence of costs associated with diapause, the colony characteristics of nondiapause queens were significantly different from those of diapause queens. Colonies of nondiapause queens produced the lowest number of workers but the highest number of young queens. 5. It is argued that these nondiapause colonies are more time‐constrained than diapause colonies because nondiapause colonies produce two generations within the same season and should therefore be more efficient in producing sexual offspring. 6. Moreover, nondiapause colonies should rear a more female‐biased sex ratio because they can be certain of the presence of males produced by other (diapause) colonies.     

Review. Lifelong commitment to the wrong partner: hybridization in ants

The extraordinary lifelong partner commitment in social insects is expected to increase choosiness in both sexes and therefore to be associated with particularly low hybridization frequencies. Yet, more and more studies reveal that in many ant taxa hybrids are surprisingly common, with up to half of all female sexuals receiving sperm from allospecific males in extreme cases. In a few ant species, hybridization has led to the evolution of reproductively isolated new lineages with a bizarre system of genetic caste differentiation: colonies produce hybrid workers and pure-lineage female sexuals. This requires that colonies either contain multiple queens or that queens mate multiple times. In most other cases, hybridization appears to be an evolutionary dead end and fertile hybrid queens are rarely found. In such cases, haplodiploid sex determination appears to decrease the costs of mating with an allospecific male. As long as hybrid workers are viable, a cross-mated queen can partially rescue its fitness by producing males from unfertilized eggs. Mating with an allospecific partner may thus be an option for queens when conspecific mates are not available. The morphological similarity of most ant males, perhaps resulting from the lack of sexual conflict, may similarly contribute to the commoness of hybridization.     

The influence of queens of the antParatrechina flavipes on daughter and non-daughter workers, for the suppression of sexual production

The influence that the queen ofParatrechina flavipes (Smith) (Hymenoptera: Formicidae) has upon workers was investigated in field and laboratory nests. There was no significant difference in sexual production, either of gynes or males, between field queenright and queenless nests of the ant. A replicated laboratory experiment revealed that workers lay fewer eggs and rear fewer sexual larvae in the presence of their mother queen, while this reduction is not observed in workers with influence of non-mother queens. The results seem to support the queen's signal hypothesis by Keller & Nonacs (1993). The contradiction is explained by workers rearing sexuals in queenless satellite nests. There exists a probably complex regulation of the transfer of larvae between satellite and mother nests.     

Lack of inbreeding avoidance in the Argentine ant Linepithema humile

Although workers might increase their inclusive fitness by favoringcloser over more distant kin, evidence suggest that nepotismgenerally does not occur within colonies of social insects.It has been suggested that this may be due to the cost of recognitionerrors. We tested whether recognition occurs in a system wherea better than random ability to recognize kin should be selected for. Using DNA microsatellites, we show that sexuals of theArgentine ant Linepithema humile fail to use genetic cues toavoid sib-mating. When offspring of two queens were allowedto mate, the percentage of matings among siblings was not significantlylower than expected under the hypothesis of random mating.The finding that sexuals fail to use genetic cues to avoid sib-matings cannot be attributed to the cost of recognitionerrors because any recognition system that would lead to abetter than random ability to avoid sib-mating should be selectedfor when there are costs to inbreeding. These data are thusconsistent with the view that kin recognition mediated solelyby genetic cues might be intrinsically error prone within coloniesof social insects.     

Bumblebees at an alpine site in northern Sweden: temporal development, population size, and plant utilization

The bumblebee community in an alpine valley in northern Sweden was studied for two seasons. Only two species of bumblebees, Bombus alpinus and B. hyperboreus. are common at the site. Bombus hyperhoreus is an obligate nest parasite on B. alpinus : the latter species is four times more abundant than the former. The number of captures on any given day was very low. However, the number of queens foraging in the area was estimated by a mark-reacapture method to ca 350 specimens, indicating that the queens forage over large areas. The dates for capturing queens carrying pollen in their corbiculae and the emergence of workers and males indicate that the queens only have time to produce one batch (or possibly two overlapping batches) of workers. The utilization of different plant species corresponds well with their flowering phenology at the site. The unspecialized flowers of Saxifraga oppositifolia are the main pollen and nectar source in the early part of the season. The bumblebees switch to Astragalus alpinus and Bartsia alpina as soon as they come into flower: these species show a typical bee pollination syndrome, the corbicular loads most commonly consisted of 91-100% of pollen from a single species. The change in flower utilization and the composition of the corbicular loads give no support for the hypothesis that aretie bumblebees should be more generalistic in their foraging than temperate species. The preference for Astragalus and Bartsia will probably have an effect on outcrossing in late-flowering specimens of Saxifraga oppositifolia , which has a very extended flowering period.     

Production of Early Diploid Males by European Colonies of the Invasive Hornet Vespa velutina nigrithorax

The invasive yellow-legged hornet Vespa velutina nigrithorax was accidentally introduced in Europe in the early 2000s. As is the case in colonies of other wasp and hornet species, V. velutina colonies are known to produce sexuals (males and new queens) at the end of the summer. We show that early-stage colonies in French populations frequently produce males well before the usual reproductive period. The vast majority of the males produced are diploid, which is consistent with the loss of genetic diversity previously reported in introduced populations in France. Since males do not participate in colony activities, the production of early diploid males at the expense of workers is expected to hamper colony growth and, ultimately, decrease the expansion of the species in its invasive range in Europe.     

Queen number influences the timing of the sexual production in colonies of Cardiocondyla ants

Wingless males of the ant genus Cardiocondyla engage in fatal fighting for access to female sexual nestmates. Older, heavily sclerotized males are usually capable of eliminating all younger rivals, whose cuticle is still soft. In Cardiocondyla sp. A, this type of local mate competition (LMC) has turned the standard pattern of brood production of social insects upside down, in that mother queens in multi-queen colonies produce extremely long-lived sons very early in the life cycle of the colony. Here, we investigated the emergence pattern of sexuals in two species with LMC, in which males are much less long-lived. Queens of Cardiocondyla obscurior and Cardiocondyla minutior reared their first sons significantly earlier in multi-queen than in single-queen societies. In addition, first female sexuals also emerged earlier in multi-queen colonies, so that early males had mating opportunities. Hence, the timing of sexual production appears to be well predicted by evolutionary theory, in particular by local mate and queen-queen competition.     

No evidence that reproductive bumblebee workers reduce the production of new queens

Kin selection theory predicts potential conflict between queen and workers over male parentage in hymenopteran societies headed by one, singly mated queen, because each party is more closely related to its own male offspring. In ‘late-switching’ colonies of the bumblebee Bombus terrestris, i.e. colonies whose queens lay haploid eggs relatively late in the colony cycle, workers start to lay male eggs shortly after the queen lays the female eggs that will develop into new queens. It has been hypothesized that this occurs because workers recognize, via a signal given by the queen instructing female larvae to commence development as queens, that egg laying is now in their kin-selected interest. This hypothesis assumes that aggressive behaviour in egg-laying workers does not substantially reduce the production of new queens, which would decrease the workers' fitness payoff from producing males. We tested the hypothesis that reproductive activity inB. terrestris workers does not reduce the production of new queens. We used microsatellite genotyping to sex eggs and hence to select eight size-matched pairs of ‘late-switching’ colonies from a set of commercial colonies. From one colony of each pair we removed every egg-laying or aggressive worker observed. From the other colony, we simultaneously removed a nonegg-laying, nonaggressive worker. Removed workers were replaced with young workers from separate colonies at equal frequencies within the pair. There was no significant difference in queen productivity between colonies with reduced or normal levels of egg-laying or aggressive workers. Therefore, as predicted, reproductive B. terrestris workers did not significantly reduce the production of new queens.     

Weight changes in adult hornets,Vespa affinis (Hymenoptera: Vespidae)

Summary After sexuals emerge from their cells, they remain within the nest for 8–11 days (males) or 13–14 days (queens). During this time their weight increases (males 38 %, queens 40 %) due to the laying down of fat in the gaster. The weight of workers does not change over the same period. The fat is utilized by the queen during the 4–5 month overwintering period. When queens emerge in spring their weight is at its lowest, and they feed on nectar. Ovarian development, which was delayed during winter, now begins. During summer, queens again gain weight but this is now due to the development of the ovaries. The queen lives for about 1 year.