Sex allocation conflict in ants: when the queen rules

Insect societies are paramount examples of cooperation, yet they also harbor internal conflicts whose resolution depends on the power of the opponents. The male-haploid, female-diploid sex-determining system of ants causes workers to be more related to sisters than to brothers, whereas queens are equally related to daughters and sons. Workers should thus allocate more resources to females than to males, while queens should favor an equal investment in each sex. Female-biased sex allocation and manipulation of the sex ratio during brood development suggest that workers prevail in many ant species. Here, we show that queens of Formica selysi strongly influenced colony sex allocation by biasing the sex ratio of their eggs. Most colonies specialized in the production of a single sex. Queens in female-specialist colonies laid a high proportion of diploid eggs, whereas queens in male-specialist colonies laid almost exclusively haploid eggs, which constrains worker manipulation. However, the change in sex ratio between the egg and pupae stages suggests that workers eliminated some male brood, and the population sex-investment ratio was between the queens' and workers' equilibria. Altogether, these data provide evidence for an ongoing conflict between queens and workers, with a prominent influence of queens as a result of their control of egg sex ratio.     

Internest sex-ratio variation and male brood survival in the ant Pheidole pallidula

Sex allocation in social insects has become a general modelin tests of inclusive fitness theory, sex-ratio theory, andparent-offspring conflict. Several studies have shown that colonysex ratios are often bimodally distributed, with some coloniesproducing mainly females and others mainly males. Sex specializationmay result from workers assessing their relatedness to malebrood versus female brood, relative to the average worker-relatednessasymmetry in other colonies of their population. Workers thenadjust the sex ratio in their own interest This hypothesis assumesthat workers can recognize the sex of the brood in their colonyand selectively eliminate males. We compared the primary sexratio (at the egg stage) and secondary sex ratio (reproductivepupae and adults) of colonies in the ant Pheidole pallidula.There was a strong bimodal distribution of secondary sex ratios,with most colonies producing mainly reproductives of one sex.In contrast, there was no evidence of a bimodal distributionof primary sex ratios. The proportion of haploid eggs producedby queens was 0.35 in early spring and decreased to about 0.1in summer. Male eggs also were present in virtually all fieldcolonies sampled in July, although eggs laid at this time ofyear never give rise to males. All male brood is, therefore,selectively eliminated beginning in July and continue to beeliminated through the rest of the year. Finally, the populationsex-ratio investment was female-biased. Together, these resultsare consistent with the hypothesis that workers control thesecondary sex ratio by selectively eliminating male brood inabout half the colonies, perhaps those with high relatednessasymmetry.[Behav Ecol 7: 292–298 (1996)]     

Mode of colony foundation influences the primary sex ratio in ants

In ants, young queens can found new colonies independently (without the help of workers) or dependently (with the help of workers). It has been suggested that differences in the mode of colony founding strongly influence queen survival and colony development. This is because independent queens are constrained to produce a worker force rapidly, before they deplete their body reserves and to resist the intense intercolony competition during the founding stage. By contrast, queens that found colonies dependently remain with the workers, which probably results in a lower mortality rate and earlier production of reproductive offspring. Consequently, in species that found independently, queens of incipient colonies are expected to produce mostly worker brood by laying a lower fraction of haploid (male) eggs than queens in mature colonies; such a difference would not occur in species founding dependently. We compared the primary sex ratio (proportion of male-determined eggs) laid by queens in incipient and mature colonies of two ant species Lasius nigerLinepithema humile, showing independent and dependent modes of colony founding, respectively. As predicted L. niger queens of incipient colonies laid a lower proportion of haploid eggs than queens from mature colonies. By contrast, queens of L. humile laid a similar proportion of haploid eggs in both incipient and mature colonies. These results provide the first evidence that (1) the primary sex ratio varies according to the mode of colony foundation, and (2) queens can adjust the primary sex ratio according to the life history stage of the colony in ants. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

Influence of inbreeding in the early stages of artificially reared colonies of Bombus terrestris

In the present study on the bumblebee Bombus terrestris, we investigated the influence of inbreeding on queen fitness by comparing diapause survival and egg-laying success of queens mated with nestmate and non-nestmate males. We then compared the early stage of colonies with or without diploid males and analysed colony characteristics to identify a factor predictive of colony outcome. Diapause survival was no different between queens mated with nestmates and non-nestmates, but in the latter case, egg-laying success was significantly higher. Queens mated with nestmates gave rise to a percentage of diploid male colonies (52.6%) compatible with brother–sister coupling. We obtained 18.6% of colonies with diploid males even from queens mated with non-nestmates, indicating that the colonies of origin were in some way related or homozygous at the sex determination loci. There was no difference in the early growth stage between colonies with or without diploid males, except in the number of workers emerging in the first brood, which was significantly higher in the latter. Among diploid male colonies, the number of workers and the male/worker ratio in the first brood was highly variable and was not a good predictor of subsequent colony growth. Out of 49 colonies with diploid males that reached full development, only 11 had a sufficient size to assume that they could survive in the field or, in a commercial breeding, to be suitable for pollination purposes.     

New method to stimulate the onset of Bombus terrestris (Hymenoptera: Apidae) rearing: Using worker helpers in the presence of frozen pupae

The failure of bumblebee queens to enthusiastically start a colony under laboratory conditions may be due to lack of oviposition during an experiment, a long delay in oviposition from the termination of hibernation, and failure to rear a large first brood. In the present study, the use of frozen male pupae to start the colony with the assistance of bumblebee workers rather than fresh, young, male pupae was investigated under controlled room temperature and humidity conditions. The period of initiation of the colony decreased with an increase in the number of worker helpers from one to six. The period was as short as 3.9 days in the presence of six worker helpers. Second and third broods also started earlier with the help of workers. The rate of first worker production per egg cup was double that of the normal method (i.e. without worker helpers). Egg eating behavior of the queen was not found in the first brood if more than two workers helped the development of the larvae. Four worker helpers were found to be sufficient, as they could produce 100% colony foundation and 91.46% first worker production colonies. This study showed that using frozen old pupae is a good stimulator for colony foundation in the presence of four bumblebee worker helpers.     

Queen pheromone regulates egg production in a termite

In social insects, resource allocation is a key factor that influences colony survival and growth. Optimal allocation to queens and brood is essential for maximum colony productivity, requiring colony members to have information on the total reproductive power in colonies. However, the mechanisms regulating egg production relative to the current labour force for brood care remain poorly known. Recently, a volatile chemical was identified as a termite queen pheromone that inhibits the differentiation of new neotenic reproductives (secondary reproductives developed from nymphs or workers) in Reticulitermes speratus. The same volatile chemical is also emitted by eggs. This queen pheromone would therefore be expected to act as an honest message of the reproductive power about queens. In this study, we examined how the queen pheromone influences the reproductive rate of queens in R. speratus. We compared the number of eggs produced by each queen between groups with and without exposure to artificial queen pheromone. Exposure to the pheromone resulted in a significant decrease in egg production in both single-queen and multiple-queen groups. This is the first report supporting the role of queen pheromones as a signal regulating colony-level egg production, using synthetically derived compounds in a termite.     

Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae)

Kin selection theory predicts conflict in social Hymenoptera between the queen and workers over male parentage because each party is more closely related to its own male offspring. Some aspects of the reproductive biology of the bumble-bee Bombus terrestris support kin selection theory but others arguably do not. We present a novel hypothesis for how conflict over male parentage should unfold in B. terrestris colonies. We propose that workers delay laying eggs until they possess information showing that egg laying suits their kin-selected interests. In colonies where queens start to lay haploid eggs early, we hypothesize that this occurs when workers detect the presence of queen-produced male brood in the brood's larval stage. In colonies where queens start to lay haploid eggs late, we hypothesize that it occurs when workers detect a signal from the queen to female larvae to commence development as queens. Our hypothesis accounts for previously unexplained aspects of the timing of reproductive events in B. terrestris, provides ultimate explanations for the results of a recent study of mechanisms underlying queen-worker conflict and helps explain this species' characteristic bimodal (split) sex ratios. Therefore, kin selection theory potentially provides a good explanation for reproductive patterns in B. terrestris.     

Resource allocation in a social wasp: effects of breeding system and life cycle on reproductive decisions

Organisms must make important decisions on how to allocate resources to reproduction. We investigated allocation decisions in the social wasp Vespula maculifrons to understand how social insects make reproductive choices. We first determined how annual colonies apportioned resources to growth and reproduction by analysing developing brood. In contrast to expectations, colonies invested in both growth (workers) and reproduction (males) simultaneously. In addition, colonies showed evidence of producing males in pulses and reversing their reproductive choices by decreasing investment in males late in the season. This reversal is consistent with theory suggesting that colonies decrease production in males if fitness of late emerging males is low. To further investigate reproductive decisions within colonies, we determined if the male mates of multiply-mated queens varied in their reproductive success over time. Sperm use by queens did vary over time suggesting that male success may depend on sperm clumping within the female reproductive tract. Finally, we tested if colony sex ratio conformed to expectations under kin selection theory that nestmate relatedness would positively correlate with investment in new queens if workers controlled sex allocation. Surprisingly, the proportion of queens produced by colonies was negatively correlated with nestmate relatedness, suggesting that allocation may be shaped by advantages arising from increased genetic diversity resulting from multiple mating by queens. Overall, our study suggests that the reproductive decisions of colonies are flexible and may depend both on environmental cues arising from energetic needs of the colony and genetic cues arising from mating behaviours of queens.     

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.     

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.     

Bumblebee sex ratios: why do bumblebees produce so many males?

Sex investment ratios in populations of bumblebees are male biased, which contradicts theoretical predictions. Male-biased investment ratios in eusocial Hymenoptera are assumed to be non-stable for both the queen and her workers. In this paper, we show that male-biased sex allocation does not necessarily decrease fitness in the bumblebee Bombus terrestris. A male-biased investment ratio can be the result of an optimal allocation of resources when resources are scarce if (i) there is a large cost difference between male and female production, (ii) there is uncertainty about the amount of resources a colony can invest, and (iii) only a proportion of the investment made in an individual can be reused. This resource allocation then leads to split sex ratios depending on the amount of resources available to a bumblebee colony: colonies under low resource conditions will show a male-biased investment ratio, whereas colonies under high resource conditions allocate more resources towards females. However, the extent to which bumblebee populations show a male-biased sex allocation cannot be explained by cost differences between male and female production alone. In a recent paper, A. F. G. Bourke argued that male-biased investment ratios in bumblebee populations are a by-product of the occurrence of protandry (males emerge before females). Here we will extend Bourke''s argument and show that within a protandrous population, both protandrous and protogynous (females emerge before males) colonies exist. The existence of protandrous and protogynous colonies results in split sex ratios in time, because protogynous colonies rely on males produced by protandrous colonies (partial protandry).     

Social life-history response to individual immune challenge of workers of Bombus terrestris L.: a possible new cooperative phenomenon

Parasites typically reduce host survival or fecundity. To minimize fitness loss, hosts can make temporal adjustments of their reproductive effort. To date such plastic shifts of life‐history traits in response to parasitism are only known from solitary organisms where infected individuals can react by themselves. In the case of social insects, where brood care and reproductive effort is shared between reproductive individuals (typically the queen) and workers, adjustments of the reproductive effort would depend on collective decision‐making. We tested for this possibility by experimentally activating the immune response of individual workers in colonies of the bumblebee, Bombus terrestris L. This induction resulted, in combination with environmental conditions, in a reduction of fitness of the social unity (i.e. colony success, measured by number and biomass of offspring) and a collective response towards earlier reproduction. As both phenomena are expressed at the level of the colony, the result suggests that key elements of the use of immune defence have been maintained through the evolutionary transition to sociality.     

Parasites delay worker reproduction in bumblebees: consequences for eusociality

Workers in eusocial insects usually tend the brood of the queenand so achieve representation in the next generation throughaiding relatives to reproduce. However, workers of some eusocialspecies, such as bumblebees, are capable of reproductive activityeven in the presence of the queen (in queen-right colonies),and worker reproduction is associated with aggressive behaviorsand egg cannibalism, both of which reduce colony efficiency.Thus, factors that affect worker ovariandevelopment, a preconditionfor reproduction, can influence social harmony and colony productivity.Parasites are a ubiquitous and important part of the bioticenvironment of all organisms. Here we show that parasites playan important role in the reproductive physiology of worker bumblebeesin queen-right colonies of Bombus terrestris, affecting thepattern and timing of ovarian development and oviposition. Workersfrom colonies parasitized with the intestinal trypanosome Crithidiabombi had less developed ovaries than workers of the same agefrom unparasitized colonies. In addition, parasitized colonieswere smaller than unparasitized colonies for about the firsthalf of colony development. This generated further demographiceffects such that workers were on average younger in parasitizedthan in unparasitized colonies around the time of the onsetof worker oviposition, and worker oviposition occurred significantlylater in parasitized colonies. Workers in parasitized coloniestherefore had lower individual reproductive potential and werecooperative for a larger proportion of the colony cycle thanthose in unparasitized colonies. In this system, where transmissionof the parasite between years probably occurs only in infested,young queens, this effect may represent an adaptation on thepart of the parasite to ensure its successful passage throughthe winter. Parasites, by reducing the cost of worker cooperation,may facilitate queen control over her worker force and playan important role in moderating the social organization of eusocialinsect colonies.     

Colony structure, provisioning and sex allocation in the sweat bee Halictus ligatus (Hymenoptera: Halictidae)

Population and colony-level sex allocation and nest productivity in the eusocial sweat bee Halictus ligatus Say were studied by excavating nests during one season. The emphasis was on measuring the provision masses, which differ in size and shape depending on the sex of the egg to be laid on them (male-producing provision masses are smaller and more or less round, whereas gyne-producing provision masses are larger and 'loaf-shaped). The primary aim of this study was to test theoretical predictions about female-bias of the sex ratio in the summer brood, both on the population level and on the colony level.
The overall sex ratio of the summer brood was moderately biased towards gynes. A significant positive correlation between the overall size of provision masses (as an estimate for the degree of female bias of the nest sex ratio) and the number of eusocial workers was found. This relationship further improved in partial analyses in which the provision mass weights were adjusted for sampling date, removing the effect of protandry. Foundress size, however, had no effect on the second brood provision masses and neither was there an effect of worker number on the size of gynes and males separately. In the first brood only the size of the foundress had a consistently positive effect on the size of the provision masses and on the size of the emerging daughter workers.
The observed increase of female bias in the nest sex ratio with increasing numbers of eusocial worker bees conforms to optimization predictions following from kin-selection theory.     

Policing behaviour towards virgin egg layers in a polygynous ponerine ant

The majority of colonies of Gnamptogenys menadensis in Sulawesi lack queens and several workers ('gamergates') mate and reproduce instead. Virgin workers lay morphologically specialized trophic eggs which are fed to larvae. Some of these virgins switch to male eggs when gamergates are experimentally removed. Three distinct patterns of oogenesis thus result in: (1) trophic eggs; (2) reproductive eggs (unfertilized) laid by virgin workers; and (3) reproductive eggs laid by gamergates, whose ovarioles are always longer than those of virgin workers. We investigated the behavioural regulation of ovarian activity in virgin workers by temporarily excluding gamergates. In 12 groups of 35-45 virgins, a few workers became dominant and started to lay reproductive eggs. Once gamergates were reintroduced, sterile workers attacked and immobilized workers with enlarged ovaries (confirmed by dissection of 173 individuals), which often died as a result. Gamergates were never aggressive towards new egg layers. Aggression was not triggered by divergence in colony odours, as it was absent in control experiments in which six colonies were divided in half, with each part containing gamergates, and reunited after 50 days. Our results show that sterile workers discriminate against new egg layers, given that their ovaries are not as developed as those of gamergates. Olfactory detection of different levels of ovarian activity thus appears possible. Mesh experiments indicated that the putative pheromones are nonvolatile and require physical contact for transmission. Aggressive behaviour directed at reproducing workers can be interpreted as worker policing. In G. menadensis, worker policing results in virgins laying only trophic eggs. Copyright 1999 The Association for the Study of Animal Behaviour.     

云南短头熊蜂的繁育特性研究

短头熊蜂Bombus breviceps是云南省优势蜂种,为更好地挖掘本土熊蜂资源,繁育农业授粉蜂群,本研究从云南3个地区（屏边、个旧和昆明）收集短头熊蜂蜂王后,在相同条件下饲养,统计分析其蜂王产卵前期、工蜂发育期、蜂群生长特性、群势、产卵蜂王率及蜂群可应用率等繁育特性指标。结果表明：3个地区工蜂的发育期相同,屏边地区的蜂王产卵前期最长,蜂群始见工蜂时间及工蜂数量达到6头、30头和60头的时间也最长,均显著高于个旧地区和昆明地区（P<0.05）。3个地区短头熊蜂的群势差异不显著（P>0.05）,但昆明地区的工蜂数量最少,显著低于屏边地区和个旧地区（P<0.05）,而子代蜂王数量显著高于屏边地区和个旧地区（P<0.05）,雄性蜂数量显著高于屏边地区（P<0.05）。昆明地区的产卵蜂王率和蜂群可应用率高于屏边地区和个旧地区。总体而言,云南的短头熊蜂群势强,产卵蜂王率75%以上,蜂群可应用率均在63%以上,易于人工繁育,具有重要的授粉利用价值。     

Demography and life history characteristics of two honey bee races (Apis mellifera)

Summary Intra-colony demography and life history characteristics of neotropical Africanized and temperate European honey bearaces were compared under simulated feral conditions. Major differences in colony demography were found which nevertheless resulted in some similar reproductive characteristics. European colonies were larger than Africanized colonies, had more rapid initral growth rates of worker populations, showed better survivorship of brood and adult workers, and differed in patterns of worker age distribution. However, both races were similar in the brood and adult populations when colonies swarmed, the frequency and timing of swarming, and the number of workers in prime swarms. The factors most important in determining these colony growth and reproductive patterns were likely worker mortality rates, climate, and resource availability.     

Queen-worker conflicts over male production and sex allocation in a primitively eusocial wasp

Abstract In a colony headed by a single monandrous foundress, theories predict that conflicts between a queen and her workers over both sex ratio and male production should be intense. If production of males by workers is a function of colony size, this should affect sex ratios, but few studies have examined how queens and workers resolve both conflicts simultaneously. We conducted field and laboratory studies to test whether sex-ratio variation can be explained by conflict over male production between queen and workers in the primitively eusocial wasp Polistes chinensis antennalis.
Worker oviposition rate increased more rapidly with colony size than did queen oviposition. Allozyme and micro-satellite markers revealed that the mean frequency of workers' sons among male adults in queen-right colonies was 0.39 ± 0.08 SE (n = 22). Genetic relatedness among female nestmates was high (0.654–0.796), showing that colonies usually had a single, monandrous queen. The mean sex allocation ratio (male investment/male and gyne investments) of 46 queen-right colonies was 0.47 ± 0.02, and for 25 orphaned colonies was 0.86 ± 0.04. The observed sex allocation ratio was likely to be under queen control. For queen-right colonies, the larger colonies invested more in males and produced reproductives protandrously and/or simultaneously, whereas the smaller colonies invested more in females and produced reproductives protogynously. Instead of positive relationships between colony size and worker oviposition rate, the frequency of workers' sons within queen-right colonies did not increase with colony size. These results suggest that queens control colony investment, even though they allow worker oviposition in queen-right colonies. Eggs laid by workers may be policed by the queen and/or fellow workers. Worker oviposition did not influence the outcome of sex allocation ratio as a straightforward function of colony size.