Brood development into sexual females depends on the presence of a queen but not on temperature in an ant dispersing by colony fission,Aphaenogaster senilis

Abstract. 1. In eusocial insects, colony fission is a mode of dispersal by which a young queen leaves her nest with some workers to found a new colony. In these species, adult females (workers and the queen) should allocate most resources to increasing their colony size, which constrains the possibility of fission. In contrast, developing diploid larvae should have a preference for becoming a queen and having their own offspring, rather than becoming workers and rearing the offspring of other females. 2. In the ant Aphaenogaster senilis, queens are produced in very small numbers, suggesting that adult females control larval development. We used a 6‐year series of data on more than 300 nests to determine the annual cycle of worker and queen production. Although both overlapped, the latter mostly occurred in the second half of the summer, after a major peak of worker emergence. Young queens were also often produced in nests whose reproductive queen had died, thus allowing her replacement. Overall, we estimate that only 0.07% of diploid larvae actually develop into gynes. 3. Laboratory experiments indicated that brood is bipotent until the second larval instar. Diploid larval development into queen was favoured by the removal of the mother queen, but was not affected by rearing temperature. 4. Our data suggest that most diploid broods are forced by the adults to develop into workers rather than into gynes. However, when the queen is not present due to death or after a fission event, a few larvae are allowed to develop into gynes. One way for workers to limit the development of larvae might be by controlling the amount of food they receive.     

It's good to be queen: classically eusocial colony structure and low worker fitness in an obligately social sweat bee

Lasioglossum malachurum, a bee species common across much of Europe, is obligately eusocial across its range but exhibits clear geographic variation in demography and social behaviour. This variation suggests that social interactions between queens and workers, opportunities for worker oviposition, and patterns of relatedness among nest mates may vary considerably, both within and among regions. In this study, we used three microsatellite loci with 12-18 alleles each to examine the sociogenetic structure of colonies from a population at Agios Nikolaos Monemvasias in southern Greece. These analyses reveal that the majority of colonies exhibit classical eusocial colony structure in which a single queen mated to a single male monopolizes oviposition. Nevertheless, we also detect low rates of multiqueen nest founding, occasional caste switching by worker-destined females, and worker oviposition of both gyne and male-producing eggs in the final brood. Previous evidence that the majority of workers show some ovarian development and a minority (17%) have at least one large oocyte contrasts with the observation that only 2-3% of gynes and males (the so-called reproductive brood) are produced by workers. An evaluation of the parameters of Hamilton's Rule suggests that queens benefit greatly from the help provided by workers but that workers achieve greater fitness by provisioning and laying their own eggs rather than by tending to the queen's eggs. This conflict of interest between the queen and her workers suggests that the discrepancy between potential and achieved worker oviposition is due to queen interference. Comparison of relatedness and maternity patterns in the Agios Nikolaos Monemvasias population with those from a northern population near Tübingen, Germany, points to a north-south cline of increasingly effective queen control of worker behaviour.     

Effects of brood manipulation costs on optimal sex allocation in social hymenoptera

In eusocial Hymenoptera, queens and workers are in conflict over optimal sex allocation. Sex ratio theory, while generating predictions on the extent of this conflict under a wide range of conditions, has largely neglected the fact that worker control of investment almost certainly requires the manipulation of brood sex ratio. This manipulation is likely to incur costs, for example, if workers eliminate male larvae or rear more females as sexuals rather than workers. In this article, we present a model of sex ratio evolution under worker control that incorporates costs of brood manipulation. We assume cost to be a continuous, increasing function of the magnitude of sex ratio manipulation. We demonstrate that costs counterselect sex ratio biasing, which leads to less female-biased population sex ratios than expected on the basis of relatedness asymmetry. Furthermore, differently shaped cost functions lead to different equilibria of manipulation at the colony level. While linear and accelerating cost functions generate monomorphic equilibria, decelerating costs lead to a process of evolutionary branching and hence split sex ratios.     

Colony social organization of <Emphasis Type="Italic">Lasioglossum malachurum</Emphasis> Kirby (Hymenoptera,Halictidae) in southern Greece

Summary We studied the nesting and social biology of two aggregations of the obligately eusocial halictine bee Lasioglossum malachurum at Agios Nikolaos Monemvasias (ANM) in southern Greece. Observations and nest excavations carried out from May to June 2000, revealed social and demographic variation between aggregations and years at ANM, as well as notable differences between these and other European populations. In southern Greece, the colony cycle includes multiple broods: the first two broods comprise only workers, whereas the third brood comprises workers, males, and gynes. Although pleometrosis is unknown in other populations, in the ANM region, as many as 10% of nests have more than one foundress. Newly emerged workers and gynes exhibit non-overlapping size distributions, but a few queens are worker-sized, indicating that workers occasionally overwinter and become foundresses. Although the vast majority of workers are unmated and most exhibit no ovarian development, an increase in worker ovarian development at the time of male production suggests that many males may develop from worker-laid eggs. Worker reproduction seems to be inhibited by the presence of queens, and annual variation in queen mortality may underlie annual variation in worker ovarian development. Across Europe, the major demographic and social differences among L. malachurum populations are in the number of worker broods and the extent of worker ovarian development. This contrasts with the results of a principal components analysis of social traits among 15 social L. (Evylaeus) populations, which shows that interspecific social variation is defined by the proportion of males in the early brood, the proportion of workers mated, queen-worker size dimorphism, gyne overwintering locale, and the proportion of workers with developed ovaries.Received 17 June 2002; revised 16 January 2002; accepted 27 January 2003.     

Genetic relatedness and population structure in the social wasp,Mischocyttarus mexicanus (Hymenoptera: Vespidae)

Summary In primitively eusocial wasps workers often retain the ability to become queens, so their continued performance in the worker role is partly dependent on elevated genetic relatedness between workers and the brood they rear. In colonies of the social wasp,Mischocyttarus mexicanus, workers were related to female pupae by 0.29±0.12, a value that is significantly below the full sister value of 0.75, but not significantly below 0.50, worker relatedness to daughters. Though individuals often build new nests within meters of their natal nest, there was no genetic population structure discernable among four nest clusters, or inbreeding of any kind.     

A mechanical signal biases caste development in a social wasp

Understanding the proximate mechanisms of caste development in eusocial taxa can reveal how social species evolved from solitary ancestors. In Polistes wasps, the current paradigm holds that differential amounts of nutrition during the larval stage cause the divergence of worker and gyne (potential queen) castes. But nutrition level alone cannot explain how the first few females to be produced in a colony develop rapidly yet have small body sizes and worker phenotypes. Here, we provide evidence that a mechanical signal biases caste toward a worker phenotype. In Polistes fuscatus, the signal takes the form of antennal drumming (AD), wherein a female trills her antennae synchronously on the rims of nest cells while feeding prey-liquid to larvae. The frequency of AD occurrence is high early in the colony cycle, when larvae destined to become workers are being reared, and low late in the cycle, when gynes are being reared. Subjecting gyne-destined brood to simulated AD-frequency vibrations caused them to emerge as adults with reduced fat stores, a worker trait. This suggests that AD influences the larval developmental trajectory by inhibiting a physiological element that is necessary to trigger diapause, a gyne trait.     

Social behavior and brood decline in reproductive-phase colonies ofBelonogaster petiolata (Degeer) (Hymenoptera: Vespidae)

Colonies ofBelonogaster petiolata in Gauteng (South Africa) produced reproductive offspring (gynes and males) in late January and early February of each nesting season; their appearance was associated with a decline in worker and brood numbers. Brood decline could commence in the presence of a dominant, reproductively active queen, and loss or removal of the queen was not followed directly by cessation of nest growth and brood care. An older worker usually took over the α-position in queenless colonies. Several factors appear to contribute to brood decline and, ultimately, termination of the colony cycle in this species. These include (1) cessation of the supply of solid food to colonies (and particularly their larvae) during the reproductive phase, (2) a decrease in the worker/larva ratio during the latter phase due to the progressive loss of workers, (3) increasing number of gynes and males, and (4) an adult priority over food reception from foragers.     

Queen recruitment and split sex ratios in polygynous colonies of the ant Formica exsecta

Sex ratios in social insects have become a general model for tests of inclusive fitness theory, sex ratio theory and parent–offspring conflict. In populations of Formica exsecta with multiple queens per colony , sex ratios vary greatly among colonies and the dry-weight sex ratio is extremely male-biased, with 89% of the colonies producing males but no gynes (reproductive females). Here we test the queen-replenishment hypothesis, which was proposed to explain sex ratio specialization in this and other highly polygynous ants (i.e. those with many queens per nest). This hypothesis proposes that, in such ants, colonies produce gynes to recruit them back into the colony when the number of resident queens falls below a given threshold limiting colony productivity or survival. We tested predictions of the queen-replenishment hypothesis by following F. exsecta colonies across two breeding seasons and relating the change in effective queen number with changes in sex ratio, colony size and brood production. As predicted by the queen-replenishment hypothesis, we found that colonies that specialized in producing females increased their effective queen number and were significantly more likely to specialize in male production the following year. The switch to male production also coincided with a drop in productivity per queen as predicted. However, adoption of new queens did not result in a significant increase in total colony productivity the following year. We suggest that this is because queen production comes at the expense of worker production and thus queen production leads to resource limitation the following year, buffering the effect of greater queen number on total productivity.     

Adaptive colony sex ratios in primitively eusocial bees

Colony-level predictions about sex-ratio optimization in eusocial Hymenoptera are different from the ones that apply to the population level. A recent empirical study on the sweat bee Halictus rubicundus has revealed a distinct pattern in the colony sex ratio of the summer brood: eusocial colonies produced more female-biased sex ratios and non-eusocial colonies produce more male-biased sex ratios. These data are consistent with theoretical hypotheses as put forward by Trivers and Hare and several later authors. When interpreted in the light of these theoretical contentions, the sex-ratio variation in Halictus rubicundus appears to be adaptive for workers, replacement queens and - under reasonable additional assumptions - also for foundresses.     

Unexpected benefit of a social parasite for a key fitness component of its ant host

Numerous invertebrates inhabit social insect colonies, including the hoverfly genus Microdon, whose larvae typically live as brood predators. Formica lemani ant colonies apparently endure Microdon mutabilis infections over several years, despite losing a considerable fraction of young, and may even produce more gynes. We present a model for resource allocation within polygynous ant colonies, which assumes that whether an ant larva switches development into a worker or a gyne depends on the quantity of food received randomly from workers. Accordingly, Microdon predation promotes gyne development by increasing resource availability for surviving broods. Several model predictions are supported by empirical data. (i) Uninfected colonies seldom produce gynes. (ii) Infected colonies experience a short-lived peak in gyne production leading to a bimodal distribution in gyne production. (iii) Low brood : worker ratio is the critical mechanism controlling gyne production. (iv) Brood : worker ratio reduction must be substantial for increased gyne production to become noticeable.     

The kin selection theory of genomic imprinting and modes of reproduction in the eusocial Hymenoptera

Genomic imprinting is known from flowering plants and mammals but has not been confirmed for the Hymenoptera even though the eusocial Hymenoptera are prime candidates for this peculiar form of gene expression. Here, the kin selection theory of genomic imprinting is reviewed and applied to the eusocial Hymenoptera. The evidence for imprinting in eusocial Hymenoptera with the typical mode of reproduction, involving the sexual production of diploid female offspring, which develop into workers or gynes, and the arrhenotokous parthenogenesis of haploid males, is also reviewed briefly. However, the focus of this review is how atypical modes of reproduction, involving thelytokous parthenogenesis, hybridisation and androgenesis, may also select for imprinting. In particular, naturally occurring hybridisation in several genera of ants may provide useful tests of the role of kin selection in the evolution of imprinting. Hybridisation is expected to disrupt the coadaptation of antagonistically imprinted loci, and thus affect the phenotypes of hybrids. Some of the limited data available on hybrid worker reproduction and on colony sex ratios support predictions about patterns of imprinting derived from kin selection theory.     

Inbreeding and reproductive investment in the ant Formica exsecta

In social animals, inbreeding depression may manifest by compromising care or resources individuals receive from inbred group members. We studied the effects of worker inbreeding on colony productivity and investment in the ant Formica exsecta. The production of biomass decreased with increasing inbreeding, as did biomass produced per worker. Inbred colonies produced fewer gynes (unmated reproductive females), whereas the numbers of males remained unchanged. As a result, sex ratios showed increased male bias, and the fraction of workers increased among the diploid brood. Males raised in inbred colonies were smaller, whereas the weight of gynes remained unchanged. The results probably reflect a trade-off between number and quality of offspring, which is expected if the reproductive success of gynes is more dependent on their weight or condition than it is for males. As males are haploid (with the exception of abnormal diploid males produced in very low frequencies in this population), and therefore cannot be inbred themselves, the effect on their size must be mediated through the workers of the colony. We suggest the effects are caused by the inbred workers being less proficient in feeding the growing larvae. This represents a new kind of social inbreeding depression that may affect sex ratios as well as caste fate in social insects.     

Split sex ratios in perennial social Hymenoptera: a mixed evolutionary stable strategy from the queens' perspective?

In social Hymenoptera, relatedness asymmetries due to haplodiploidy often generate conflicts of genetic interest between queens and workers. Split sex ratios are common in ant populations and may result from such conflicts, with workers favoring the production of males in some colonies and of gynes in others. Such intercolonial differences may result from variations in relatedness asymmetries among colony members, but several examples are now known in which this hypothesis does not hold. We develop here a simple model assuming monogynous, monoandrous, worker-sterile, perennial colonies without dispersal restrictions. Workers may eliminate eggs of either sex and determine the caste of the female brood, but the queen controls the number of eggs of each sex she lays. In such conditions, we demonstrate that split sex ratios can result from queens adopting a mixed evolutionary stable strategy (ESS), with one option being to put a strict limit to the number of diploid eggs available and the alternative one to provide diploid eggs ad lib. In the former situation, workers should raise all diploid eggs as workers and release only male sexuals. In the latter, workers should adjust the caste ratio so as to reach the maximum sexual productivity for the colony, which is entirely invested into gynes. For a particular relative investment in gynes at the population level, between 0.5 (ESS under full queen control) and 0.75 (ESS under full worker control), an equilibrium is reached at which both strategies yield an equal genetic payoff to the queen. Male-specialized colonies are predicted to be equally abundant but less populous and less productive than gyne-specialized ones. Available data on the monogyne form of the fire ant, Solenopsis invicta, suggest that this model may apply in this case, although more specific studies are required to test these predictions.     

The biology of the primitively eusocial Augochloropsis iris (Schrottky, 1902) (Hymenoptera, Halictidae)

Summary: This work investigated Augochloropsis iris, its annual colony cycle, brood size and survival rate, caste differentiation, and sex ratio, and is the first detailed account of a clearly eusocial species of this genus. The population studied is located in the Campos do Jordão State Park, São Paulo, Brazil. The annual colony cycle extends from August to March and consists of three phases of cell provisioning separated by two phases of inactivity, and followed by an emergence of future queens and males. Provisioning during the first phase is carried primarily out by solitary females. The daughters, after emerging from the cells, remain in the natal nests, carrying out foraging activities, while the mother engages in reproduction. New nests are initiated during each of the provisioning phases by solitary females, principally by females from the second-phase brood which, soon after emerging from the cells, leave their natal nests to found their own nests, which they provision during the third phase. The females resulting from the third-phase brood in general mate and excavate their own nests, in which they diapause, with provisioning delayed until the following August. On average, the queens are significantly larger (5%) than the workers. In general, the workers do not have developed ovaries, but all are mated. Kin selection can be accepted as the selective force responsible for worker behavior of A. iris in eusocial colonies when the queen has mated once and semisocial colonies if the queen mated only once. The percentage of males produced in the first, second and third broods and in the brood of new nests founded by solitary females active in the second and third phases was: 20.7%, 22.2%, 13.3% and 0.0% respectively. The resultant sex ratio of the third brood suggests that the third-phase workers of eusocial nests are at least in partial control of their colony's sex ratios, in cases where the queens mated only once.     

Availability and depletion of fat reserves in halictid foundress queens with a focus on solitary nest founding

Foundress queens of social Hymenoptera require considerable amounts of energy for survival, solitary nest founding, provisioning of the first brood, and egg production. Energy reserves in insects mostly consist of fat. We investigated how hibernation and the subsequent flight season, especially the solitary nest founding phase, influenced the abdominal fat content of gynes in the primitively eusocial sweat bee, Lasioglossum malachurum (Hymenoptera, Halictidae). In our study population, sexuals are produced in both the second and the third broods. Emerging gynes of the third brood had significantly more fat than those of the second brood, whereas there was no such difference in males. As expected, fat reserves in samples of female sexuals caught at emergence, after hibernation, during solitary nest founding, and at the end of the social phase of the nest cycle indicate a severe decrease of reserves that was highest during the 7 weeks of the solitary founding phase. Thus, the amount of fat reserves of foundress queens seems to be crucial, particularly for nest founding. However, investment of energy reserves in the solitary nest founding phase has probably to be balanced with the subsequent social phase in a way that maximizes the queen’s fitness. Possible consequences for the complexity and progress of the nest cycle are discussed.     

Sex-ratio conflict between queens and workers in eusocial Hymenoptera: mechanisms, costs, and the evolution of split colony sex ratios

Because workers in the eusocial Hymenoptera are more closely related to sisters than to brothers, theory predicts that natural selection should act on them to bias (change) sex allocation to favor reproductive females over males. However, selection should also act on queens to prevent worker bias. We use a simulation approach to analyze the coevolution of this conflict in colonies with single, once-mated queens. We assume that queens bias the primary (egg) sex ratio and workers bias the secondary (adult) sex ratio, both at some cost to colony productivity. Workers can bias either by eliminating males or by directly increasing female caste determination. Although variation among colonies in kin structure is absent, simulations often result in bimodal (split) colony sex ratios. This occurs because of the evolution of two alternative queen or two alternative worker biasing strategies, one that biases strongly and another that does not bias at all. Alternative strategies evolve because the mechanisms of biasing result in accelerating benefits per unit cost with increasing bias, resulting in greater fitness for strategies that bias more and bias less than the population equilibrium. Strategies biasing more gain from increased biasing efficiency whereas strategies biasing less gain from decreased biasing cost. Our study predicts that whether queens or workers evolve alternative strategies depends upon the mechanisms that workers use to bias the sex ratio, the relative cost of queen and worker biasing, and the rates at which queen and worker strategies evolve. Our study also predicts that population and colony level sex allocation, as well as colony productivity, will differ diagnostically according to whether queens or workers evolve alternative biasing strategies and according to what mechanism workers use to bias sex allocation.     

The relationship of provision weight to adult weight and sex ratio in the solitary bee, Ceratina calcarata

ABSTRACT.

• 1 The female of the solitary bee Ceratina calcarata (Robertson) (Hymenoptera: Anthophoridae) excavates a tunnel in a pithy twig and then constructs and provisions a linear series of brood cells that make up her nest.
• 2 Adult females are, on the average, 1.3 times heavier than the males, a significant difference (P<0.001). There is no difference between the sexes in the amount of weight gained per unit of larval food.
• 3 Larger females occur because their provision masses are, on the average, 1.3 times heavier than male-producing provision masses, a significant difference (P<0.001).
• 4 Because mothers invest more time and energy in their daughters, Fisher's theory predicts that they should produce more sons. When available resources are fewer in a given year as reflected in lighter provision masses, more males are produced during the year.
• 5 The observed sex ratio did not differ significantly from the expected, calculated as mean female weight/mean male weight and was male-biased.
• 6 Unlike species which nest in pre-formed tunnels, the sex of any brood cell except the innermost is random with respect to that cell's position in the nest and the tunnel's depth and diameter. The innermost position contained offspring with a female biased sex ratio (P<0.005).

     

Sex investment ratios in eusocial Hymenoptera support inclusive fitness theory

Inclusive fitness theory predicts that sex investment ratios in eusocial Hymenoptera are a function of the relatedness asymmetry (relative relatedness to females and males) of the individuals controlling sex allocation. In monogynous ants (with one queen per colony), assuming worker control, the theory therefore predicts female‐biased sex investment ratios, as found in natural populations. Recently, E.O. Wilson and M.A. Nowak criticized this explanation and presented an alternative hypothesis. The Wilson–Nowak sex ratio hypothesis proposes that, in monogynous ants, there is selection for a 1 : 1 numerical sex ratio to avoid males remaining unmated, which, given queens exceed males in size, results in a female‐biased sex investment ratio. The hypothesis also asserts that, contrary to inclusive fitness theory, queens not workers control sex allocation and queen–worker conflict over sex allocation is absent. Here, I argue that the Wilson–Nowak sex ratio hypothesis is flawed because it contradicts Fisher's sex ratio theory, which shows that selection on sex ratio does not maximize the number of mated offspring and that the sex ratio proposed by the hypothesis is not an equilibrium for the queen. In addition, the hypothesis is not supported by empirical evidence, as it fails to explain ‘split’ (bimodal) sex ratios or data showing queen and worker control and ongoing queen–worker conflict. By contrast, these phenomena match predictions of inclusive fitness theory. Hence, the Wilson–Nowak sex ratio hypothesis fails both as an alternative hypothesis for sex investment ratios in eusocial Hymenoptera and as a critique of inclusive fitness theory.     

Effects of nest size and dispersion on brood production in a North American population of wood ant Formica fusca (Hymenoptera: Formicidae)

We examined several key parameters of the population ecology of a North American population of Formica fusca (L.), including nest dispersion, colony size and brood production. Physical nest size was significantly correlated with colony size, and colony size, in turn, was significantly correlated with brood production. Sex allocation was male biased, although larger nests were more likely to produce reproductive female brood (gynes). Neither nest temperature nor moisture level was significantly correlated with brood production. Formica fusca nests in this population had a comparatively low average nearest-neighbor distance with a significantly even pattern of dispersion, which suggests relatively high intraspecific competition. However, nearest-neighbor distance was not significantly associated with either colony size or relative brood production.     

Dominance hierarchy among workers changes with colony development in Polistes japonicus (Hymenoptera, Vespidae) paper wasp colonies with a small number of workers

Dominance hierarchy in the primitively eusocial wasp Polistes japonicus was analysed in four colonies for two periods: (1) the first-brood period, when only early emerging workers are present on the nest, and (2) the mixed-brood period, when the first and second (last) broods are present on the nest. The rank in the dominance hierarchy was determined based on a sociogram showing a dominance–subordinance relationship for all pairs of workers. During the first-brood period, older workers were likely to be more dominant (older dominance hierarchy), while the rank of workers was reversed during the mixed-brood period, with younger workers being likely to be more dominant (younger dominance hierarchy). However, the oldest and youngest workers were not always the top-ranked workers in the dominance hierarchy during the first- and mixed-brood periods, respectively, and during the mixed-brood period no younger dominance hierarchy was evident when the first or second brood was analysed separately. Higher ranked workers displayed dominance behaviour more frequently, and the lowest ranked worker hardly displayed dominance behaviour. Most workers displayed dominance behaviours primarily towards the worker ranked immediately below in the dominance hierarchy during the mixed-brood period but not during the first-brood period. The bodies of younger workers were larger for the mixed brood, but not for the first brood in some colonies or the second brood in all colonies. The association between body size and rank in the dominance hierarchy was negative during the first-brood period and positive during the mixed-brood period, with a nearly significant trend also seen even when the analysis was limited to the second brood. To explain the above temporal change from an older dominance hierarchy to a younger dominance hierarchy, we propose the hypothesis that the probability of a worker inheriting the colony increases rapidly with colony development, and consequently younger larger workers attempt to move up the dominance hierarchy in order to produce their own offspring by becoming the superseder late in colony development, rather than working harmoniously so as to boost the overall production of reproductive progeny for a colony, which is the strategy adopted early in colony development.