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.     

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.     

Colony sex ratios vary with queen number but not relatedness asymmetry in the ant Formica exsecta

Split-sex-ratio theory assumes that conflict over whether to produce predominately males or female reproductives (gynes) is won by the workers in haplodiploid insect societies and the outcome is determined by colony kin structure. Tests of the theory have the potential to provide support for kin-selection theory and evidence of social conflict. We use natural variation in kinship among polygynous (multiple-queen) colonies of the ant Formica exsecta to study the associations between sex ratios and the relatedness of workers to female versus male brood (relatedness asymmetry). The population showed split sex ratios with about 89% of the colonies producing only males, resulting in an extremely male-biased investment ratio in the population. We make two important points with our data. First, we show that queen number may affect sex ratio independently of relatedness asymmetry. Colonies producing only males had greater genetic effective queen number but did not have greater relatedness asymmetry from the perspective of the adult workers that rear the brood. This lack of a difference in relatedness asymmetry between colonies producing females and those producing only males was associated with a generally low relatedness between workers and brood. Second, studies that suggest support for the relatedness-asymmetry hypothesis based on indirect measures of relatedness asymmetry (e.g. queen number estimated from relatedness data taken from the brood only) should be considered with caution. We propose a new hypothesis that explains split sex ratios in polygynous social insects based on the value of producing replacement queens.     

Swarming generates rebel workers in honeybees

According to kin selection theory, the colony kin structure of eusocial insects motivates workers' altruistic behaviors and therefore their sterility or restricted reproduction [1]. Indeed, theory and cross-species comparison confirm that workers engage in their own reproduction depending on relatedness among colony members [2, 3]. We show that in a honeybee colony, the workers switch from their typical altruistic role to a more selfish one if at their larval stage there are environmental cues of an upcoming decline in intracolony relatedness. This happens inevitably when a colony multiplies by swarming and replaces the mother queen with her daughter, because the mother queen's workers are faced with rearing the sister queen's offspring related to them half as much as between sisters. Workers developing from the mother queen's eggs immediately after swarming, in a temporarily queenless colony, had more ovarioles in their ovaries and less-developed hypopharyngeal glands producing brood food than control workers reared in queenright conditions. These "rebel" workers were more engaged in laying their own male-determined eggs than in rearing offspring, whether or not the sister queen was present in the colony. The finding of this previously unknown rebel strategy confirms that kin selection shapes both cooperation and conflict in honeybee societies.     

Caste fate conflict in swarm-founding social hymenoptera: an inclusive fitness analysis

A caste system in which females develop into morphologically distinct queens or workers has evolved independently in ants, wasps and bees. Although such reproductive division of labour may benefit the colony it is also a source of conflict because individual immature females can benefit from developing into a queen in order to gain greater direct reproduction. Here we present a formal inclusive fitness analysis of caste fate conflict appropriate for swarm-founding social Hymenoptera. Three major conclusions are reached: (1) when caste is self-determined, many females should selfishly choose to become queens and the resulting depletion of the workforce can substantially reduce colony productivity; (2) greater relatedness among colony members reduces this excess queen production; (3) if workers can prevent excess queen production at low cost by controlled feeding, a transition to nutritional caste determination should occur. These predictions generalize results derived earlier using an allele-frequency model [Behav. Ecol. Sociobiol. (2001) 50: 467] and are supported by observed levels of queen production in various taxa, especially stingless bees, where caste can be either individually or nutritionally controlled.     

Split sex ratios in the social Hymenoptera: a meta-analysis

The study of sex allocation in social Hymenoptera (ants, bees,and wasps) provides an excellent opportunity for testing kin-selectiontheory and studying conflict resolution. A queen–workerconflict over sex allocation is expected because workers aremore related to sisters than to brothers, whereas queens areequally related to daughters and sons. If workers fully controlsex allocation, split sex ratio theory predicts that colonieswith relatively high or low relatedness asymmetry (the relatednessof workers to females divided by the relatedness of workersto males) should specialize in females or males, respectively.We performed a meta-analysis to assess the magnitude of adaptivesex allocation biasing by workers and degree of support forsplit sex ratio theory in the social Hymenoptera. Overall, variationin relatedness asymmetry (due to mate number or queen replacement)and variation in queen number (which also affects relatednessasymmetry in some conditions) explained 20.9% and 5% of thevariance in sex allocation among colonies, respectively. Theseresults show that workers often bias colony sex allocation intheir favor as predicted by split sex ratio theory, even iftheir control is incomplete and a large part of the variationamong colonies has other causes. The explanatory power of splitsex ratio theory was close to that of local mate competitionand local resource competition in the few species of socialHymenoptera where these factors apply. Hence, three of the mostsuccessful theories explaining quantitative variation in sexallocation are based on kin selection.     

INTRASPECIFIC VARIATION IN ANT SEX RATIOS AND THE TRIVERS-HARE HYPOTHESIS

We consider worker-controlled sex investments in eusocial Hymenoptera (ants in particular) and assume that relatedness asymmetry is variable among colonies and that workers are able to assess the relatedness asymmetry in their own colony. We predict that such “assessing” workers should maximize their inclusive fitness by specializing in the production of the sex to which they are relatively most related, i.e., colonies whose workers have a relatedness asymmetry below the population average should specialize in males, whereas colonies whose workers have a higher than average relatedness asymmetry should specialize in making females. Our argument yields the expectation that colony sex ratios will be bimodally distributed in ant populations where relatedness asymmetry is variable owing to multiple mating, worker reproduction, and/or polygyny. No such bimodality is expected, however, in ant species where relatedness asymmetry is known to be constant, or in cases where relatedness asymmetry is supposed to be irrelevant due to allospecific brood rearing under queen control, as in the slave-making ants. Comparative data on colony sex ratios in ants are reviewed to test the predictions. The data partly support our contentions, but are as yet insufficient to be considered as decisive evidence.     

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.     

Ant workers selfishly bias sex ratios by manipulating female development.

Kin selection theory predicts that social insects should perform selfish manipulations as a function of colony genetic structure. We describe a novel mechanism by which this occurs. First, we use microsatellite analyses to show that, in a population of the ant Leptothorax acervorum, workers' relatedness asymmetry (ratio of relatedness to females and relatedness to males) is significantly higher in monogynous (single-queen) colonies than in polygynous (multiple-queen) colonies. Workers rear mainly queens in monogynous colonies and males in polygynous colonies. Therefore, split sex ratios in this population are correlated with workers' relatedness asymmetry. Together with significant female bias in the population numerical and investment sex ratios, this finding strongly supports kin-selection theory. Second, by determining the primary sex ratio using microsatellite markers to sex eggs, we show that the ratio of male to female eggs is the same in both monogynous and polygynous colonies and equals the overall ratio of haploids (males) to diploids (queens and workers) among adults. In contrast to workers of species with selective destruction of male brood, L. acervorum workers therefore rear eggs randomly with respect to sex and must achieve their favoured sex ratios by selectively biasing the final caste (queen or worker) of developing females.     

Reproductive alliances and posthumous fitness enhancement in male ants

Ants provide excellent opportunities for studying the evolutionary aspects of reproductive conflict. Relatedness asymmetries owing to the haplodiploid sex determination of Hymenoptera create substantial fitness incentives for gaining control over sex allocation, often at the expense of the fitness interests of nest-mates. Under worker-controlled split sex ratios either the reproductive interests of the mother queen (when workers male bias the sex ratio) or the father (when workers female bias the sex ratio), but never that of both parents simultaneously, are fulfilled. When workers bias sex ratios according to the frequency of queen mating, males which co-sire a colony have a joint interest in manipulating their daughter workers into rearing a more female-biased sex ratio. Here we show that males of the ant Formica truncorum achieve such manipulation by partial sperm clumping, so that the cohort-specific relatedness asymmetry of the workers in colonies with multiple fathers is higher than the cumulative relatedness asymmetry across worker cohorts. This occurs because a single male fathers the majority of the offspring within a cohort. Colonies with higher average cohort-specific relatedness asymmetry produce more female-biased sex ratios. Posthumously expressed male genes are thus able to oppose the reproductive interests of the genes expressed in queens and the latter apparently lack mechanisms for enforcing full control over sperm mixing and sperm allocation.     

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.     

Egg Cannibalism in a Facultative Polygynous Ant: Conflict for Reproduction or Strategy to Survive?

Policing, i.e. all behaviours that prevent a nestmate from reproducing, is currently observed in social insects. It is presumed to have evolved to regulate potential conflicts generated by genetic asymmetries or to enhance colony efficiency by avoiding surplus reproductives and brood. In the ant, Ectatomma tuberculatum, individual queen fecundity was similar in monogynous and polygynous colonies issued from a Mexican population. Egg cannibalism, however, occurred in the polygynous colonies. The stealing and destruction of reproductive queen‐laid eggs involved only nestmate queens, even if they were highly related. No queen appeared to monopolize reproduction in the polygynous colonies. But, the observed value of relatedness among workers differed from the expected value, suggesting an unequal sharing of reproduction between queens. We discussed whether the cannibalism of queen‐laid eggs in E. tuberculatum results from a competition for reproduction among queens or if this phenomenon is related to constraints on nutritional resources.     

Fisher's theory of the sex ratio applied to the social hymenoptera

Fisher's theory of the sex ratio may be extended to the social Hymenoptera; this extension must consider the unusual genetic structure of the Hymenoptera. Queens, workers, and laying workers generally have different equilibrial sex ratios of offspring and different equilibrial ratios of investment in offspring of the two sexes; these differences are the consequence of asymmetries in the degrees of relatedness between the queen, a worker, and a laying worker to male and female offspring. The equilibrial ratios of investment for the queen, a worker, and a laying worker are derived by finding the relative expected reproductive successes of genes in males and in reproductive females.     

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.     

Sex allocation conflict between queens and workers in Formica pratensis wood ants predicts seasonal sex ratio variation

Sex allocation theory predicts parents should adjust their investment in male and female offspring in a way that increases parental fitness. This has been shown in several species and selective contexts. Yet, seasonal sex ratio variation within species and its underlying causes are poorly understood. Here, we study sex allocation variation in the wood ant Formica pratensis. This species displays conflict over colony sex ratio as workers and queens prefer different investment in male and female offspring, owing to haplodiploidy and relatedness asymmetries. It is unique among Formica ants because it produces two separate sexual offspring cohorts per season. We predict sex ratios to be closer to queen optimum in the early cohort but more female‐biased and closer to worker optimum in the later one. This is because the power of workers to manipulate colony sex ratio varies seasonally with the availability of diploid eggs. Consistently, more female‐biased sex ratios in the later offspring cohort over a three‐year sampling period from 93 colonies clearly support our prediction. The resulting seasonal alternation of sex ratios between queen and worker optima is a novel demonstration how understanding constraints of sex ratio adjustment increases our ability to predict sex ratio variation.     

Male parentage and queen mating frequency in the bumblebee <Emphasis Type="Italic">Bombus ignitus</Emphasis> (Hymenoptera: bombinae)

Kin selection theory predicts conflict between queens and workers in the social insect colony with respect to male production. This conflict arises from the haplodiploid system of sex determination in Hymenoptera that creates relatedness asymmetries in which workers are more closely related to the sons of other workers than to those of the queen. In annual hymenopteran societies that are headed by a single queen, the mating frequency of the queen is the only factor that affects the colony kin structure. Therefore, we examined the mating structure of queens and the parentage of males in a monogynous bumblebee, Bombus ignitus, using DNA microsatellites. In the seven colonies that were studied, B. ignitus queens mated once, thereby leading to the prediction of conflict between the queen and workers regarding male production. In each of the five queen-right colonies, the majority of the males (95%) were produced by the colony’s queen. In contrast, workers produced approximately 47% of all the males in two queenless colonies. These results suggest that male production in B. ignitus is a conflict between queen and workers.     

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.     

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.     

COLONY SEX RATIOS,CONFLICT BETWEEN QUEENS AND WORKERS,AND APPARENT QUEEN CONTROL IN THE ANT PHEIDOLE DESERTORUM

Sex-ratio conflict between queens and workers was explored in a study of colony sex ratios, relatedness, and population investment in the ant Pheidole desertorum. Colony reproductive broods consist of only females, only males, or have a sex ratio that is extremely male biased. Colonies producing females (female specialists) and colonies producing males (male specialists) occur at near equal frequency in the population. Most colonies apparently specialize in producing one reproductive sex throughout their life. Allozyme analyses show that relatedness does not differ within male-specialist and female-specialist colonies and they do not appear to differ in available resources. In the population, workers are nearly three times more closely related to females than males; however, the investment sex ratio is near equal (1.01, female/male), which is consistent with queen control. Selection should be strong on workers to increase investment in reproductive females, so why do workers in male-specialist colonies produce only (or nearly only) males? One hypothesis is that queens in male-specialist colonies prevent the occurrence of reproductive females, perhaps by producing worker-biased female eggs. An earlier simulation study of genetic evolution of sex ratios in social Hymenoptera (Pamilo 1982b) predicts that such mechanisms can result in the evolution of bimodal colony sex ratios and queen control. Results on P. desertorum are generally consistent with that study; however, information is not currently available to test some of the model's predictions and assumptions.     

Trophallaxis and reproductive conflicts in social bees

In the eusocial Hymenoptera, reproductive division of labour is a key aspect of colony organisation. In most of its species, workers are sterile and are unable to reproduce, while the queen monopolises reproduction. When workers are able to reproduce, a conflict with the queen or with other workers over male production is predicted. Because this reproduction may involve costs for the colony, the potential conflict over male parentage gives rise to important questions, such as what are the proximate mechanisms that allow a queen to control the reproductive potential of its workers, and which factors make some workers fertile and others not. In the groups where it occurs, an important mechanism for the regulation of reproduction is trophallaxis (the process of mutual feeding through regurgitation that occurs in several species of social insects). Trophallaxis gives dominant individuals a trophic advantage by taking nutrients from submissive individuals. In advanced eusocial species of bees, trophallaxis may also serve as an alternative hierarchical interaction in the absence of agonistic conflicts. In this way, trophallaxis not only represents an alternative path for hierarchical interactions, but it may be evolutionary linked to intracolonial conflict among workers.