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.     

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.     

Gene expression patterns associated with caste and reproductive status in ants: worker‐specific genes are more derived than queen‐specific ones

Variation in gene expression leads to phenotypic diversity and plays a central role in caste differentiation of eusocial insect species. In social Hymenoptera, females with the same genetic background can develop into queens or workers, which are characterized by divergent morphologies, behaviours and lifespan. Moreover, many social insects exhibit behaviourally distinct worker castes, such as brood‐tenders and foragers. Researchers have just started to explore which genes are differentially expressed to achieve this remarkable phenotypic plasticity. Although the queen is normally the only reproductive individual in the nest, following her removal, young brood‐tending workers often develop ovaries and start to reproduce. Here, we make use of this ability in the ant Temnothorax longispinosus and compare gene expression patterns in the queens and three worker castes along a reproductive gradient. We found the largest expression differences between the queen and the worker castes (~2500 genes) and the smallest differences between infertile brood‐tenders and foragers (~300 genes). The expression profile of fertile workers is more worker‐like, but to a certain extent intermediate between the queen and the infertile worker castes. In contrast to the queen, a high number of differentially expressed genes in the worker castes are of unknown function, pointing to the derived status of hymenopteran workers within insects.     

Contrasting population genetic structure for workers and queens in the putatively unicolonial ant Formica exsecta

The theory of inclusive fitness provides a powerful explanation for reproductive altruism in social insects, whereby workers gain inclusive fitness benefit by rearing the brood of related queens. Some ant species, however, have unicolonial population structures where multiple nests, each containing numerous queens, are interconnected and individuals move freely between nests. In such cases, nestmate relatedness values may often be indistinguishable from zero, which is problematic for inclusive fitness-based explanations of reproductive altruism. We conducted a detailed population genetic study in the polygynous ant Formica exsecta, which has been suggested to form unicolonial populations in its native habitat. Analyses based on adult workers indeed confirmed a genetic structuring consistent with a unicolonial population structure. However, at the population level the genetic structuring inferred from worker pupae was not consistent with a unicolonial population structure, but rather suggested a multicolonial population structure of extended family-based nests. These contrasting patterns suggest limited queen dispersal and free adult worker dispersal. That workers indeed disperse as adults was confirmed by mark-recapture measures showing consistent worker movement between nests. Together, these findings describe a new form of social organization, which possibly also characterizes other ant species forming unicolonial populations in their native habitats. Moreover, the genetic analyses also revealed that while worker nestmate relatedness was indistinguishable from zero at a small geographical scale, it was significantly positive at the population level. This highlights the need to consider the relevant geographical scale when investigating the role of inclusive fitness as a selective force maintaining reproductive altruism.     

Proximate Determinants of Reproductive Skew in Polygyne Colonies of the Ant Formica fusca

Understanding the determinants of reproductive skew (the partitioning of reproduction among co‐breeding individuals) is one of the major questions in social evolution. In ants, multiple‐queen nests are common and reproductive skew among queens has been shown to vary tremendously both within and between species. Proximate determinants of skew may be related to both queen and worker behaviour. Queens may attempt to change their reproductive share through dominance interactions, egg eating and by changing individual fecundity. Conversely, workers are in a position to regulate the reproductive output of queens when rearing the brood. This paper investigates queen behaviour at the onset of egg laying and the effect of queen fecundity and worker behaviour on brood development and reproductive shares of multiple queens in the ant Formica fusca. The study was conducted in two‐queen laboratory colonies where the queens produced only worker offspring. The results show that in this species reproductive apportionment among queens is not based on dominance behaviour and aggression, but rather on differences in queen fecundity. We also show that, although the queen fecundity at the onset of brood rearing is a good indicator of her final reproductive output, changes in brood composition occur during brood development. Our results highlight the importance of queen fecundity as a major determinant of her reproductive success. They furthermore suggest that in highly derived polygyne species, such as the Formica ants, direct interactions as a means for gaining reproductive dominance have lost their importance.     

Genetic determination of female castes in a hybridogenetic desert ant

In most social insects, the brood is totipotent and environmental factors determine whether a female egg will develop into a reproductive queen or a functionally sterile worker. However, genetic factors have been shown to affect the female's caste fate in a few ant species. The desert ant Cataglyphis hispanica reproduces by social hybridogenesis. All populations are characterized by the coexistence of two distinct genetic lineages. Queens are almost always found mated with a male of the alternate lineage than their own. Workers develop from hybrid crosses between the genetic lineages, whereas daughter queens are produced asexually via parthenogenesis. Here, we show that the association between genotype and caste in this species is maintained by a ‘hard‐wired’ genetic caste determination system, whereby nonhybrid genomes have lost the ability to develop as workers. Genetic analyses reveal that, in a rare population with multiple‐queen colonies, a significant proportion of nestmate queens are mated with males of their own lineage. These queens fail to produce worker offspring; they produce only purebred daughter queens by sexual reproduction. We discuss how the production of reproductive queens through sexual, intralineage crosses may favour the stability of social hybridogenesis in this species.     

Significant reproductive skew in the facultatively polygynous ant Pheidole pallidula

Reproductive skew - the extent to which reproduction is unevenly shared between individuals in a social group - varies greatly between and within animal species. In this study, we investigated how queens share parentage in polygynous (multiple queen) colonies of the Mediterranean ant Pheidole pallidula. We used highly polymorphic microsatellites markers to determine parentage of gynes (new queens), males and workers in P. pallidula field colonies. The comparison of the genotypes of young and adult workers revealed a very low queen turnover (less than 2%). The first main finding of the study of reproductive skew in these colonies was that there was a significant departure from equal contribution of queens to gyne, male and worker production. Reproductive skew was greater for male production than for queen and worker production. There was no relationship between the magnitude of the reproductive skew and the number of reproductive queens per colony, their relatedness and the overall colony productivity, some of the factors predicted to influence the extent of reproductive skew. Finally, our study revealed for the first time a trade-off in the relative contribution of nestmate queens to gyne and worker production. The queens contributing more to gyne production contributed significantly less to worker production.     

Workers' sons rescue genetic diversity at the sex locus in an invasive honey bee population

The hallmark of eusociality is the division of labour between reproductive (queen) and nonreproductive (worker) females. Yet in many eusocial insects, workers retain the ability to produce haploid male offspring from unfertilized eggs. The reproductive potential of workers has well‐documented consequences for the structure and function of insect colonies, but its implications at the population level are less often considered. We show that worker reproduction in honey bees can have an important role in maintaining genetic diversity at the sex locus in invasive populations. The honey bee sex locus is homozygous‐lethal, and, all else being equal, a higher allele number in the population lead to higher mean brood survival. In an invasive population of the honey bee Apis cerana in Australia, workers contribute significantly to male production: 38% of male‐producing colonies are queenless, and these contribute one‐third of all males at mating congregations. Using a model, we show that such male production by queenless workers will increase the number of sex alleles retained in nascent invasive populations following founder events, relative to a scenario in which only queens reproduce. We conclude that by rescuing sex locus diversity that would otherwise be lost, workers' sons help honey bee populations to minimize the negative effects of inbreeding after founder events and so contribute to their success as invaders.     

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

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

Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants

The process of reproductive caste determination in eusocial insect colonies is generally understood to be mediated by environmental, rather than genetic factors. We present data demonstrating unexpected genetic differences between reproductive castes in a variant of the rough harvester ant, Pogonomyrmex rugosus var. fuscatus. Across multiple loci, queens were consistently more homozygous than expected, while workers were more heterozygous. Adult colony queens were divided into two highly divergent genetic groups, indicating the presence of two cryptic species, rather than a single population. The observed genetic differences between castes reflect differential representation of heterospecific and conspecific patrilines in these offspring groups. All workers were hybrids; by contrast, winged queens were nearly all pure-species. The complete lack of pure-species workers indicates a loss of worker potential in pure-species female offspring. Hybrids appear to be bipotential, but do not normally develop into reproductives because they are displaced by pure-species females in the reproductive pool. Genetic differences between reproductive castes are expected to be rare in non-hybridizing populations, but within hybrid zones they may be evolutionarily stable and thus much more likely to occur.     

Reproductive specialization in multiple-queen colonies of the ant Formica exsecta

In polygynous (multiple queens per nest) colonies of socialinsects, queens can increase their reproductive share by layingmore eggs or by increasing the proportion of eggs that developinto reproductive individuals instead of workers. We used polymorphicmicrosatellite loci to determine the genetically effective contributionof queens to the production of gynes (new queens), males, and2 different cohorts of workers in a polygynous population ofthe ant Formica exsecta. For this purpose, we developed a newmethod that can be used for diploid and haplodiploid organismsto quantify the degree of reproductive specialization amongbreeders in societies where there are too many breeders to ascertainparentage. Using this method, we found a high degree of reproductivespecialization among nest-mate queens in both female- and male-producingcolonies (sex ratio is bimodally distributed in the study population).For example, a high effective proportion of queens (25% and79%, respectively) were specialized in the production of malesin female- and male-producing colonies. Our analyses furtherrevealed that in female-producing colonies, significantly fewerqueens contributed to gyne production than to worker production.Finally, we found significant changes in the identity of queenscontributing to different cohorts of workers. Altogether, thesedata demonstrate that colonies of F. exsecta, and probably thoseof many other highly polygynous social insect species, are composedof reproductive individuals differing in their investment togynes, males, and workers. These findings demonstrate a newaspect of the highly dynamic social organization of complexanimal societies.     

Cheaters sometimes prosper: targeted worker reproduction in honeybee (Apis mellifera) colonies during swarming

Kin selection theory predicts that honeybee (Apis mellifera) workers should largely refrain from producing their own offspring, as the workers collectively have higher inclusive fitness if they rear the sons of their mother, the queen. Studies that have quantified levels of ovary activation and reproduction among workers have largely supported this prediction. We sampled pre‐emergent male pupae and adult workers from seven colonies at regular intervals throughout the reproductive part of the season. We show that the overall contribution of workers to male (drone) production is 4.2%, nearly 40 times higher than is generally reported, and is highest during reproductive swarming, when an average of 6.2% of the males genotyped are worker‐produced. Similarly, workers in our samples were 100 times more likely to have active ovaries than previously assumed. Worker reproduction is seasonally influenced and peaks when colonies are rearing new queens. Not all worker subfamilies contribute equally to reproduction. Instead, certain subfamilies are massively over‐represented in drone brood. By laying eggs within the period in which many colonies produce virgin queens, these rare worker subfamilies increase their direct fitness via their well‐timed sons.     

Selectable components of sex allocation in colonies of the honeybee (Apis mellifera L.)

Colonies of social insects that undergo fission as a componentof reproduction produce large excesses of males. Hypothesesto explain this phenomenon have assumed that the workers thatconstitute the entourage for the new queen (or queens) representinvestment in female reproductives. Selection for optimal colonysex allocation then leads to an increase in production of malesthat balances the investment in females based on their relativereproductive values. We show that the construction of comb dedicatedto the production of males (drone comb) versus workers (workercomb) is a component of sex investment under the control ofcolony workers. Relative comb construction was highly correlatedwith the relative investment in male and worker brood. Coloniesthat invested relatively more in their total numbers of malesinvested less in the dry weight of individual workers. Coloniesthat had more adult workers produced a greater number of malesand workers, but colony size did not affect the proportionalinvestment in drone comb or brood. Genetic variability was foundfor the number of adult workers in colonies, the amount of dronecomb produced, the amount of worker comb produced, and the dryweight of adult workers, suggesting that sex allocation is aselectable trait in honeybees.     

A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis

Reproduction by workers is rare in honey bee colonies that have an active queen. By not producing their own offspring and preventing other workers from producing theirs, workers are thought to increase their inclusive fitness due to their higher average relatedness towards queen-produced male offspring compared with worker-produced male offspring. But there is one exception. Workers of the Cape honey bee, Apis mellifera capensis, are able to produce diploid female offspring via thelytokous parthenogenesis and thus produce clones of themselves. As a result, worker reproduction and tolerance towards worker-produced offspring is expected to be more permissive than in arrhenotokous (sub)species where worker offspring are male. Here we quantify the extent to which A. m. capensis workers contribute to reproduction in queenright colonies using microsatellite analyses of pre-emergent brood. We show that workers produced 10.5% of workers and 0.48% of drones. Most of the workers' contribution towards the production of new workers coincided with the colonies producing new queens during reproductive swarming.     

Colony structure and reproductive sharing among queens in a tropical paper wasp, <Emphasis Type="Italic">Polistes olivaceus</Emphasis>

Reproductive partitioning among group members is a key feature in social Hymenoptera. We investigated the genetic colony structure of a tropical paper wasp Polistes olivaceus, with an emphasis on variation in the number of queens and reproductive sharing among queens. Among 22 P. olivaceus colonies, 6 were monogynous, 9 polygynous, and 7 were queenless. Adults and brood (eggs and larvae) were genotyped based on six polymorphic microsatellite loci. In each of the polygynous colonies, progenies were assigned to their mothers using maximum-likelihood methods. Nestmate queens were full sisters. The vast majority of reproduction appeared to be monopolized by the dominant queen (α), and the overall reproductive skews were 0.63 ± 0.04 (B index) and 0.97 ± 0.02 (S _c index). Although all nestmate queens had equal reproductive potential, the high magnitude of reproductive skew was enigmatic in this species. Although 9.55 ± 2.07 workers contained developed ovaries in 11 of 15 queen-right colonies, they were unrelated to the nestmate queens but related to each other as full sisters, suggesting that they were the remaining offspring of superseded queens. In 2 of the 11 colonies, we detected male eggs produced by reproductive workers. On average, 7.27 % of the total genotyped male eggs were derived from reproductive workers among the colonies. These results suggest three possibilities regarding the presence of reproductive workers in the P. olivaceus colonies: drifting between colonies, putative remaining offspring from superseded queens, and the offspring of unrelated females who joined the colonies and reproduced there. We found no worker-derived larvae or adult males, suggesting that male eggs were removed by nestmates at some point between oviposition and hatching.     

Host queen killing by a slave-maker ant queen: when is a host queen worth attacking?

A new colony of the slave-making ant Polyergus breviceps is initiated when a newly mated gyne invades a host nest and kills the resident queen. This process seems to result in chemical camouflage of the invading gyne and allows her to usurp the position of colony reproductive. Young, recently mated Formica gynes, however, are not attacked. To determine whether worker and/or immature presence is the basis for aggression, we placed eggs, larvae, pupae and workers from mature F. gnava queens with newly mated F. gnava queens and observed the responses of introducedP. breviceps queens. Because no newly mated gyne was attacked, we tested newly mated F. gnava queens (1) once they had produced eggs, (2) when the offspring reached the larval, pupal and callow stages of development, and (3) every 2 weeks until aggression ensued. Eventually all F. gnava queens were attacked but only 29 weeks after having mated. Thus, although offspring are the ultimate benefit from attacking an established F. gnava queen,P. breviceps queens detect mature queens using another time-dependent feature that is reliably indicative of reproductive status. The similarity of host queen hydrocarbon profiles, often correlated with reproductive status in other ant species, suggests that other compounds reflect queen fecundity and produce a kairomonal effect, or that another cue signals host queen and colony suitability. Our findings indicate P. breviceps gynes have evolved to respond aggressively to a host gyne cue that appears long after mating, preventing attacks on gynes without the workers necessary for colony founding.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

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.     

Prediction of social structure and genetic relatedness in colonies of the facultative polygynous stingless bee Melipona bicolor (Hymenoptera, Apidae)

Stingless bee colonies typically consist of one single-mated mother queen and her worker offspring. The stingless bee Melipona bicolor (Hymenoptera: Apidae) shows facultative polygyny, which makes this species particularly suitable for testing theoretical expectations concerning social behavior. In this study, we investigated the social structure and genetic relatedness among workers from eight natural and six manipulated colonies of M. bicolor over a period of one year. The populations of M. bicolor contained monogynous and polygynous colonies. The estimated genetic relatedness among workers from monogynous and polygynous colonies was 0.75 ± 0.12 and 0.53 ± 0.16 (mean ± SEM), respectively. Although the parental genotypes had significant effects on genetic relatedness in monogynous and polygynous colonies, polygyny markedly decreased the relatedness among nestmate workers. Our findings also demonstrate that polygyny in M. bicolor may arise from the adoption of related or unrelated queens.     

Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca

Potential reproductive conflicts are common in social insects and may occur between and within castes. In multiqueen (polygyne) colonies of ants, reproductive conflicts among coexisting queens may be resolved by aggressive interactions and/or by pheromonal signalling. Pheromonal signals may be directed at workers, which may adjust the reproductive shares of queens behaviourally. Workers are expected to favour a queen that is more likely to be their mother and to produce offspring of close kin to them. We used microsatellite markers to study reproductive partitioning between cobreeding Formica fusca queens in a laboratory experiment where workers received a choice between two queens. We expected queens of this species to communicate their reproductive status by chemical communication, because no aggressive interactions between queens have been observed. We found that queens of different reproductive status (with majority, minority or no production) differed in their cuticular hydrocarbon (CHC) profiles. The fecundity of a queen was associated with worker behaviour; the higher a queen's fecundity, the more attention she received from workers. Our results suggest that a queen fecundity signal is encoded in her CHC profile and acts as a pheromone for workers, which respond to the signal by discriminating between queens. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Variation in patriline reproductive success during queen production in orphaned colonies of the thelytokous ant Cataglyphis cursor

In genetically diverse insect societies (polygynous or polyandrous queens), the production of new queens can set the ground for competition among lineages. This competition can be very intense when workers can reproduce using thelytoky as worker lineages that manage to produce new queens gain a huge benefit. Selection at the individual level might then lead to the evolution of cheating genotypes, i.e. genotypes that reproduce more than their fair share. We studied the variation in reproductive success among worker patrilines in the thelytokous and highly polyandrous ant Cataglyphis cursor. Workers produce new queens by thelytoky in orphaned colonies. The reproductive success of each patriline was assessed in 13 orphaned colonies using genetic analysis of 433 workers and 326 worker-produced queens. Our results show that patrilines contributed unequally to queen production in half of the colonies, and the success of patrilines was function of their frequencies in workers. However, over all colonies, we observed a significant difference in the distribution of patrilines between workers and worker-produced queens, and this difference was significant in three of 13 colonies. In addition, six colonies contained a low percentage of foreign workers (drifters), and in one colony, they produced a disproportionably high number of queens. Hence, we found some evidence for the occurrence of rare cheating genotypes. Nevertheless, cheating appears to be less pronounced than in the Cape Honey bee, a species with a similar reproductive system. We argue that worker reproduction by parthenogenesis might not be common in natural populations of C. cursor.