The role of juvenile hormone in dominance behavior,reproduction and cuticular pheromone signaling in the caste-flexible epiponine wasp, <Emphasis Type="Italic">Synoeca surinama</Emphasis>

Background

The popular view on insect sociality is that of a harmonious division of labor among two morphologically distinct and functionally non-overlapping castes. But this is a highly derived state and not a prerequisite for a functional society. Rather, caste-flexibility is a central feature in many eusocial wasps, where adult females have the potential to become queens or workers, depending on the social environment. In non-swarming paper wasps (e.g., Polistes), prospective queens fight one another to assert their dominance, with losers becoming workers if they remain on the nest. This aggression is fueled by juvenile hormone (JH) and ecdysteroids, major factors involved in caste differentiation in most eusocial insects. We tested whether these hormones have conserved aggression-promoting functions in Synoeca surinama, a caste-flexible swarm-founding wasp (Epiponini) where reproductive competition is high and aggressive displays are common.

Results

We observed the behavioral interactions of S. surinama females in field nests before and after we had removed the egg-laying queen(s). We measured the ovarian reproductive status, hemolymph JH and ecdysteroid titers, ovarian ecdysteroid content, and analyzed the cuticular hydrocarbon (CHC) composition of females engaged in competitive interactions in both queenright and queenless contexts. These data, in combination with hormone manipulation experiments, revealed that neither JH nor ecdysteroids are necessary for the expression of dominance behaviors in S. surinama. Instead, we show that JH likely functions as a gonadotropin and directly modifies the cuticular hydrocarbon blend of young workers to match that of a reproductive. Hemolymph ecdysteroids, in contrast, are not different between queens and workers despite great differences in ovarian ecdysteroid content.

Conclusions

The endocrine profile of S. surinama shows surprising differences from those of other caste-flexible wasps, although a rise in JH titers in replacement queens is a common theme. Extensive remodeling of hormone functions is also evident in the highly eusocial bees, which has been attributed to the evolution of morphologically defined castes. Our results show that hormones which regulate caste-plasticity can lose these roles even while caste-plasticity is preserved.

     

Intergenerational effect of juvenile hormone on offspring in <Emphasis Type="Italic">Pogonomyrmex</Emphasis> harvester ants

Parents can influence the phenotypes of their offspring via a number of mechanisms. In harvester ants, whether female progeny develop into workers or daughter queens is strongly influenced by the age and temperature conditions experienced by their mother, which is associated with variation in maternal ecdysteroid deposition in fertilized eggs. In many insects, juvenile hormone (JH) is antagonistic to ecdysteroid release, suggesting that seasonal and age-based variation in maternal JH titers may explain maternal effects on offspring size and reproductive caste. To test this hypothesis, we artificially increased maternal JH titers with methoprene, a JH analog, in laboratory colonies of two Pogonomyrmex populations exhibiting genetic caste determination. Increasing maternal JH resulted in a 50% increase in worker body size, as well as a sharp reduction in total number of progeny reared, but did not alter the genotype of progeny reared to adulthood. The intergenerational effect of JH manipulation was not mediated by a reduction in ecdysteroid deposition into eggs; instead, changes in egg size, trophic egg availability or brood/worker ratio may have altered the nutritional environment of developing larvae. Egg ecdysteroid content was significantly negatively correlated with natural variation in worker body size, however, suggesting that there are multiple independent routes by which queens can modify offspring phenotypes.     

Functional Monogyny and Dominance Hierarchy in the Queenless Ponerine Ant Pachycondyla (=Bothroponera) sp. in West Java,Indonesia (Hymenoptera,Formicidae, Ponerinae)

Social organization of the queenless ponerine ant Pachycondyla (Bothroponera) sp. was studied in Bogor, West Java, Indonesia. Colonies had no morphologically distinct queens. Worker number per colony was 11 on average. Most colonies contained multiple mated workers (gamergates), however, only one of them laid eggs, whereas additional gamergates were sterile or ovipositing at a low rate, indicating that this ant species shows functional monogyny. Some virgin workers also developed their oocytes and actually laid eggs. Ritualized dominant — subordinate behavior was frequently observed and a linear dominance hierarchy was established among workers. The topranking individual was a fertile gamergate. Sterile gamergates positioned in lower ranks and they often engaged in foraging. Among virgin workers, callows and young workers monopolized higher ranks.     

Evolution of wingless reproductives in ants: weakly specialized ergatoid queen instead of gamergates in Platythyrea conradti

Platythyrea conradti is the only species in this genus with ergatoid (= permanently wingless) queens. Colonies lack gamergates (unlike other species in this genus), yet aggressive interactions among queen and workers define a hierarchy. A single fertile queen has the top rank and highranking workers do not lay eggs, except when the queen dies. Colonial reproduction by both alate queens (independent foundation) and gamergates (fission) seems the ancestral state in Platythyrea. Independent foundation can be selected against in some species, causing the loss of alate queens for economic reasons. Thus gamergates become the only reproductives, except in P. conradti in which queens became ergatoid. Gamergates and ergatoid queens are two mutually redundant reproductive phenotypes that allow colonial reproduction by fission. Received 1 July 2005; revised 10 November 2005; accepted 16 November 2005.     

Reproductive division of labor, dominance, and ecdysteroid levels in hemolymph and ovary of the bumble bee Bombus terrestris

To determine whether ecdysteroids are associated with reproductive division of labor in Bombus terrestris, we measured their levels in hemolymph and ovaries of queens and workers. Queens heading colonies had large active ovaries with high ecdysteroid content, whereas virgin gynes and mated queens before and after diapause had undeveloped ovaries with low ecdysteroid content. The hemolymph ecdysteroid titer was rather variable, but in a pooled analysis of mated queens before and after diapause versus colony-heading queens, ecdysteroid titers were higher in the latter group. In workers, agonistic behavior, ovarian activity, ovarian ecdysteroid content, and hemolymph ecdysteroid titers were positively correlated, and were lowest when a queen was present. In queenless workers, ecdysteroid levels were elevated in dominant workers, and were also influenced by the presence of brood and by group demography; hormone levels were higher in bees kept in larger groups. These findings are consistent with the premise that in B. terrestris the ovary is the primary site of ecdysteroid synthesis, and they show that ecdysteroids levels vary with the social environment.     

Advertised quality,caste and food availability influence the survival cost of juvenile hormone in paper wasps

Life-history trade-offs are often hormonally mediated. Here, we provide a comparative perspective on the endocrine basis of life-history trade-offs by examining the invertebrate hormone juvenile hormone (JH). JH is often associated with benefits, including increased dominance and reproductive success. We tested whether JH reduced survival of Polistes dominulus wasps and whether this survival cost was influenced by factors such as advertised quality, food availability, caste and body size. Overall, JH reduced individual survival. Among fed and unfed queens, JH reduced survival in a dose-dependent manner. Among workers, JH had a stronger effect on survival of fed workers than unfed workers. Unfed workers died quickly and body size was the best predictor of survival. Surprisingly, queens and workers treated with JH survived longer when they had signals advertising high quality than when they had signals advertising low quality. The relationship between advertised quality and ability to withstand high levels of JH suggests that there are differential physiological costs associated with ornament elaboration that could play a role in maintaining signal accuracy over evolutionary time. Overall, the convergence of endocrine-mediated costs across diverse systems suggests that endocrine-mediated trade-offs may be an adaptive way to optimize resource allocation rather than a non-adaptive constraint specific to a particular hormone.     

Endocrine changes in maturing primary queens of Zootermopsis angusticollis

Termite queens are highly specialized for reproduction, but little is known about the endocrine mechanisms regulating this ability. We studied changes in the endocrinology and ovarian maturation in primary reproductive females of the dampwood termite Zootermopsis angusticollis following their release from inhibitory stimuli produced by mature queens. Winged alates were removed from their natal nest, manually dewinged, then paired in an isolated nest with a reproductive male. Development was tracked by monitoring ovarian development, in vitro rates of juvenile hormone (JH) production by corpora allata, and hemolymph titers of JH and ecdysteroids. The production rate and titer of JH were positively correlated with each other but negatively correlated with ecdysteroid titer. Four days after disinhibition, JH release and titer decreased while ecdysteroid titer increased. The new levels persisted until day 30, after which JH increased and ecdysteroids decreased. Fully mature queens had the highest rates of JH production, the lowest ecdysteroid titers, and the greatest number of functional ovarioles. The results support the hypothesis that JH plays a dual role in termite queens depending on their stage of development; an elevated JH titer in immature alates may maintain reproductive inhibition, but an elevated JH titer in mature queens may stimulate ovarian activity. The decline in JH production and the elevation in ecdysteroid titer correspond to a period of physiological reorganization and activation. The specific function of ecdysteroids is unknown but they may help to modulate the activity of the corpora allata.     

The effect of juvenile hormone on temporal polyethism in the paper wasp Polistes dominulus

Juvenile hormone (JH) has an important role in the behavior of eusocial Hymenoptera. Previous work has shown that JH influences aggression and dominance behavior in primitive eusocial insects that lack discrete queen and worker castes (e.g. Bombus bees and Polistes wasps). In contrast, JH is one of the factors that mediates temporal polyethism among workers in advanced eusocial insects that have reproductive castes (e.g. Apis bees and Polybiawasps). Therefore, initial observations suggest that JH may have different roles in primitive and advanced eusocial taxa. Here, we use detailed behavioral observations of marked individuals to test whether JH influences temporal polyethism in the primitive eusocial wasp Polistes dominulus. First, we show that workers in P. dominulus have an age-related division of labor, as workers switch from nest work to foraging as they mature. Then, we show that application of JH accelerates the onset of foraging behavior.Workers treated with JH start foraging at a younger age than control workers. Therefore, JH mediates temporal polyethism in the primitively eusocial insect Polistes dominulus. Received 23 April 2008; revised 6 August 2008; accepted 11 August 2008     

Morphology and reproductive behaviour of intercastes in the ponerine antPachycondyla obscuricornis

Summary Queens are usually the functional reproductives inPachycondyla obscuricornis, but none were found in one colony collected near Brasilia. In this colony, three adults differed morphologically from workers; although wingless, their thorax was more or less like that of winged queens (scutum and scutellum distinct; metanotum larger than that of workers). Another 11 such individuals were found by opening cocoons. We consider that these are intercastes (sensu Peeters, 1991). Two adult intercastes were mated and laid eggs. In contrast, all the workers were virgin, but some laid distinct trophic eggs which were fed to the two reproductives. Following experimental removal of the intercastes, dominance interactions began among the workers, and reproductive eggs were then laid. Intercastes with a reproductive function have not been reported previously in the Ponerinae. They are distinct from ergatoid queens (permanently wingless reproductive caste) or gamergates (mated egglaying workers).     

Stress resistance and longevity are not directly linked to levels of enzymatic antioxidants in the ponerine ant Harpegnathos saltator

Background

The molecular mechanisms of variations in individual longevity are not well understood, even though longevity can be increased substantially by means of diverse experimental manipulations. One of the factors supposed to be involved in the increase of longevity is a higher stress resistance. To test this hypothesis in a natural system, eusocial insects such as bees or ants are ideally suited. In contrast to most other eusocial insects, ponerine ants show a peculiar life history that comprises the possibility to switch during adult life from a normal worker to a reproductive gamergate, therewith increasing their life expectancy significantly.

Results

We show that increased resistance against major stressors, such as reactive oxygen species and infection accompanies the switch from a life-history trait with normal lifespan to one with a longer life expectancy. A short period of social isolation was sufficient to enhance stress resistance of workers from the ponerine ant species Harpegnathos saltator significantly. All ant groups with increased stress resistances (reproducing gamergates and socially isolated workers) have lower catalase activities and glutathione levels than normal workers. Therewith, these ants resemble the characteristics of the youngest ants in the colony.

Conclusions

Social insects with their specific life history including a switch from normal workers to reproducing gamergates during adult life are well suited for ageing research. The regulation of stress resistance in gamergates seemed to be modified compared to foraging workers in an economic way. Interestingly, a switch towards more stress resistant animals can also be induced by a brief period of social isolation, which may already be associated with a shift to a reproductive trajectory. In Harpegnathos saltator, stress resistances are differently and potentially more economically regulated in reproductive individuals, highlighting the significance of reproduction for an increase in longevity in social insects. As already shown for other organisms with a long lifespan, this trait is not directly coupled to higher levels of enzymatic and non-enzymatic antioxidants.     

Seasonal cycle of colony structure in the Ponerine ant Pachycondyla chinensis in western Japan (Hymenoptera, Formicidae)

Investigation of reproductive strategies of ants in the subfamily Ponerinae is important for understanding of the evolution of social structure and of the significance of caste dimorphisms. The biology of species with mated and egg-laying workers (gamergates) has been studied for many species, however, little attention has been paid to species that reproduce via alate queens only. We investigated the seasonal cycle of changes in the colony structure of Pachycondyla chinensis reproduced by alate queens in western Japan, and found the following novel biological characteristics of this species. P. chinensis showed a remarkable caste dimorphism in ovariole numbers: workers had no ovaries while queens had 18 to 36 ovarioles in their ovaries. The nesting system seemed to be polydomous: 266 of 400 nests collected were queenless. The number of queenless nests increased during the reproductive season. Among the 134 queenright nests, 38 had several mated-queens without significant differences in ovary activation and the remaining 96 nests were monogynous. During winter to early spring, most nests were polygynous. After alate production, most of the old queens seemed to die or be expelled and replaced by new queens. Virgin dealated queens were often found and they seemed to have laid eggs. Received 3 August 2007; revised 19 December 2007; accepted 20 December 2007     

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.     

Endocrine mediated phenotypic plasticity: Condition-dependent effects of juvenile hormone on dominance and fertility of wasp queens

There has been increasing interest in the mechanisms that mediate behavioral and physiological plasticity across individuals with similar genotypes. Some of the most dramatic plasticity is found within and between social insect castes. For example, Polistes wasp queens can nest alone, dominate a group of cooperative queens, or act as worker-like subordinates who rarely reproduce. Previous work suggests that condition-dependent endocrine responses may play a role in plasticity between castes in the hymenoptera. Here, we test whether condition-dependent endocrine responses influence plasticity within castes in the wasp Polistes dominulus. We experimentally manipulate juvenile hormone (JH) titers in nest-founding queens and assess whether JH mediates variation in behavior and physiology. JH generally increased dominance and fertility of queens, but JH's effects were not uniform across individuals. JH had a stronger effect on the dominance and fertility of large individuals and individuals with facial patterns advertising high quality than on the dominance and fertility of small individuals and those advertising low quality. These results demonstrate that JH has condition-dependent effects. As such, they clarify how JH can mediate different behaviors in well nourished queens and poorly nourished workers. Many Polistes queens nest cooperatively with other queens, so condition-dependent hormonal responses provide a mechanism for queens to adaptively allocate energy based on their probability of successfully becoming the dominant queen. Research on the endocrine basis of plasticity often focuses on variation in endocrine titers alone. However, differential endocrine responses are likely to be a widespread mechanism mediating behavioral and physiological plasticity.     

Fecundity and the Behavioural Profile of Reproductive Workers in the Queenless Ant, Pachycondyla (= Ophthalmopone) berthoudi

Morphologically specialized queens are absent in Pachycondyla (=  Ophthalmopone ) berthoudi (ant subfamily Ponerinae). Instead, several of the workers mate and reproduce (gamergates). Gamergate proportion in nests commonly varies between nests and different times of the year. Individual fecundity of gamergates varies according to the number of these individuals in a nest, and we examined their behaviour in relation to fecundity in nests with different proportions of gamergates. In nests with high proportions of gamergates, they exhibited a diversity of behaviours inside the nest and in some cases could not be distinguished behaviourally from sterile workers. The fecundity of these gamergates was low and variable. In nests with low proportions, gamergates were relatively more fecund, and did not participate in colony labour. The behavioural profile of gamergates is therefore linked to their reproductive physiology, which is influenced by the number of mated individuals in the nest.     

Juvenile hormone in adult eusocial hymenoptera: Gonadotropin and behavioral pacemaker

Studies on the role of juvenile hormone (JH) in adult social Hymenoptera have focused on the regulation of two fundamental aspects of colony organization: reproductive division of labor between queens and workers and age-related division of labor among workers. JH acts as a gonadotropin in the primitively eusocial wasp and bumble bee species studied, and may also play this role in the advanced eusocial fire ants. However, there is no evidence that JH acts as a traditional gonadotropin in the advanced eusocial honey bee or in the few other ant species that have recently begun to be studied. The role of JH in age-related division of labor has been most thoroughly examined in honey bees. Results of these studies demonstrate that JH acts as a “behavioral pacemaker,” influencing how fast a worker grows up and makes the transition from nest activities to foraging. Hypotheses concerning the evolutionary relationship between the two functions of JH in adult eusocial Hymenoptera are discussed. Arch. Insect Biochem. Physiol. 35:559–583, 1997. © 1997 Wiley-Liss, Inc.     

Behavioral and Physiological Aspects of Reproductive Control in a Diacamma Species from Malaysia (Formicidae,Ponerinae)

The reproductive system of a Diacamma species from Malaysia is described. Intact colonies have no queens. Instead one mated worker (gamergate) reproduces. Only a few workers (2%) have weakly developed ovaries. Newly emerged workers possess thoracic appendages, called gemmae, but only one worker retains them, mates and becomes a gamergate. All other individuals are mutilated mostly by already mutilated workers. After the gamergate has been removed this mutilation-behavior continues for at least 24 h. After three days no more mutilation occurs. Groups of workers without gamergate start to fight about one week after the gamergate was removed and one worker reaches the alpha-position and becomes the sole egg layer. When workers emerge in already established groups they are not mutilated. Workers, which were isolated one week earlier than the rest of the group, and thus already escaped inhibition by the gamergate, had a higher chance to obtain the alpha-position. To test factors that might influence worker-dominance, juvenile hormone titer was measured. Juvenile hormone was not detectable in gamergates and alpha-workers but the amounts of juvenile hormone in non-reproductive workers increased with age. This is discussed with regard to the situation found in honeybees.     

Competition over workers: fertility signalling in wingless queens of <Emphasis Type="Italic">Hypoponera opacior</Emphasis>

The ant Hypoponera opacior exhibits alternative reproductive morphs associated with distinct sexual behaviours. Wingless, worker-like gynes mate in fall in their mother nest. Subsequently, these polygynous nests divide and wingless queens disperse on foot accompanied by workers, which help during nest foundation. Local resource competition amongst wingless queens was indicated by male-biased sex ratios. Queens compete over access to workers, and this competition manifests in dominance interactions. We colour-marked queens and workers to study this behaviour. Marked queens were treated aggressively and frequently killed by nestmates, whilst similarly labelled workers were readopted. We hypothesise that mated wingless queens—although they resemble workers in external morphology—differ chemically and that fertile queens with divergent odours are not tolerated. Thereby, sterile H. opacior workers avoid the risk to raise offsprings of unrelated queens. However, when nests split, workers should base their decision which queen to follow not only on relatedness, but also on queen fertility. Cuticular hydrocarbon profiles of queens could serve as an honest signal for workers. Indeed, gas chromatography showed that hydrocarbon composition differs between workers and mated queens and is linked to ovary development in queens. Workers and unmated queens exhibit complex profiles of short-chained hydrocarbons, whilst fertile queens carry few, long-chained alkenes and branched alkanes. Furthermore, ovary length was correlated to the relative amounts of characteristic hydrocarbons of queens. The chemical profile was also associated with eye size—an unalterable trait in adult insects—suggesting that larval nutrition and consequently body size affects adult ovary development.     

Population and colony structure and morphometrics in the queen dimorphic harvester ant, <Emphasis Type="Italic">Pogonomyrmex pima</Emphasis>

The North American seed-harvester ant Pogonomyrmex (Ephebomyrmex) pima displays a dimorphism that consists of winged (alate) and wingless (intermorph) queens; both types of queens are fully reproductive. Microsatellite allele frequencies and a mitochondrial phylogeny demonstrate (1) alate and intermorph queens represent an intraspecific wing polymorphism, and (2) an absence of assortative mating and inbreeding by males. Surveys at our field site in southcentral Arizona, USA, demonstrated that only one type of queen (intermorph or dealate) occurred in each colony, including those excavated during the season in which reproductive sexuals were present. Colony structure appeared to vary by queen type as most intermorph colonies contained multiple mated queens. Alternatively, dealate queen colonies rarely contained a mated queen. Our inability to find mated dealate queens in these colonies probably resulted from difficulty in excavating the entire colony and reproductive queen, especially given that these colonies were only excavated over one day. A morphometric analysis demonstrated that intermorph queens are intermediate in size to that of workers and alate queens, but that intermorph queens retain all of the specialized anatomical features of alate queens (except for wings). Some colonies had queens that foraged and performed nest maintenance activities, and these queens sometimes accounted for a significant portion of colony foraging trips. Dissections revealed that these queens were uninseminated; some of these queens produced males in the laboratory. Received 24 October 2006; revised 1 December 2006; accepted 8 December 2006.     

Hormonal correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi

In colonies of the queenless ant Streblognathus peetersi, dominance interactions produce a reproductive hierarchy in which one individual, the alpha, is capable of producing offspring while her subordinates remain infertile. Based on differences between behaviour and cuticular hydrocarbon profiles, the subordinates can be further divided into high and low ranking workers. Although it had been shown previously that alphas treated with a juvenile hormone analog lose their reproductive status, little was known of the endocrinological basis of dominance in this species. To elucidate the underlying endocrinology of these three ranks, we measured the individual in vitro rate of juvenile hormone (JH) production of excised corpora allata, and the ecdysteroid titer of pooled hemolymph samples. Production of JH was highest in low-ranking workers, intermediate in high rankers, and almost undetectable in alphas. Ecdysteroid titers were low for low rankers, but were more than twice as high for both high rankers and alphas. The results support the hypothesis that JH suppresses ovarian function in these queenless ants, and suggest that ecdysteroids may be responsible for stimulating vitellogenin production. The possible role of these hormones as behavioural modulators is also discussed. An erratum to this article can be found at     

Worker policing limits the number of reproductives in a ponerine ant

Reproductive division of labour is an essential feature of insect sociality, but the regulation of sterility among colony members remains incompletely understood. Ant workers and queens are morphologically divergent and workers are only capable of producing males in a colony, although they usually do not do so. Worker policing is one mechanism proposed for their infertility and it can be expressed as either aggressive inhibition of ovarian activity among workers or destruction of worker-laid eggs. A few studies have shown that workers with developed ovaries are preferentially attacked by nest-mates, but adequate demonstration of worker policing also requires evidence that these attacks result in the suppression of ovarian activity or death. We investigated worker policing in the ponerine ant Harpegnathos saltator in which workers are able to mate and replace the founding queen. Five colonies were each divided into two groups, one of which consisted exclusively of infertile workers. Some individuals in the orphaned groups began laying eggs during the three-week separation and upon reunification these were vigorously attacked by infertile workers of the other groups. The ovarian activity of these new egg layers became inhibited, as revealed by subsequent dissection of marked individuals. Worker policing in H. saltator appears to function primarily in preventing an excess of reproductive workers.