Fertility signalling and reproductive skew in queenless ants (original) (raw)
Related papers
Animal Behaviour
In social groups, competition often gives rise to conflicts, which are regulated through a variety of mechanisms. In several social insect species, the conflict for male production that takes place between workers after queen loss, is regulated through the establishment of a reproductive hierarchy. A recent study of Neoponera apicalis showed that workers differ in their fertility levels in the presence of the queen and proposed that such idiosyncratic differences might influence access to the top of the hierarchy after queen loss. In this study, we therefore sought to characterize the influence of the initial heterogeneity in ovarian development and its chemical
Regulation of reproduction in a queenless ant: aggression, pheromones and reduction in conflict
Proceedings. Biological sciences / The Royal Society, 2002
In the monogynous queenless ant Diacamma ceylonense, the future reproductive (future gamergate) is very aggressive towards infertile workers during the first days of her adult life. Overt aggression disappears at about three weeks, when the future gamergate begins to lay male-destined eggs and is ready to mate. Over the same period, her cuticular hydrocarbon profile alters, changing from a chemical signature similar to that of a sterile worker towards that of a gamergate. In nature, these behavioural and chemical changes will coincide with a reduction in conflict within the nest: faced with a virgin future gamergate, infertile workers have an interest in producing male-destined eggs; however, once the gamergate produces female eggs, they have an interest in rearing her offspring. This demonstration of a shift from physical inhibition to chemical signalling is interpreted in terms of sociogenetic theory, the role of cuticular hydrocarbons as an indicator of fertility in insects and t...
Cuticular hydrocarbons correlated with reproductive status in a queenless ant
Proceedings of The Royal Society B: Biological Sciences, 1999
Reproductive division of labour is regulated behaviourally in social insects lacking morphologically specialized castes. The directional nature of dominance interactions shows that recognition occurs, but little is known about its basis. In the queenless ant Dinoponera quadriceps, the top worker in the hierarchy (`alpha') mates and produces o¡spring in each colony, while other workers remain virgin. Dominant ants frequently rub one antenna of subordinates against their own cuticle, and alpha and infertile nest-mates consistently di¡er in their relative proportions of the cuticular hydrocarbon 9-hentriacontene (9-C 31 ). The second-ranking`beta' occasionally lays unfertilized eggs and we show that she has less 9-C 31 than the alpha but more than infertile workers. To investigate further the link between 9-C 31 and ovarian activity, we experimentally removed alpha workers (n 11 individuals) and used solid-phase microextraction (SPME) with gas chromatography to measure changes in 9-C 31 on live beta workers which attained alpha status. The proportion of 9-C 31 on the replacement alpha increased signi¢cantly after six weeks, in parallel with her gain in fecundity. We discuss whether 9-C 31 provides honest information about egglaying ability, enabling ants to recognize the di¡erent classes of nest-mates involved in reproductive con£icts. Such fertility cues could reliably underpin the antagonistic interactions occurring in insect societies.
Fertility Signaling and Partitioning of Reproduction in the Ant Neoponera apicalis
Journal of Chemical Ecology, 2015
All individuals in social insect colonies benefit from being informed about the presence and fertility state of reproducers. This allows the established reproductive individuals to maintain their reproductive monopoly without the need for physical control, and the non-reproductive individuals to make appropriate reproductive choices. Here, we studied whether fertility signaling is responsible for the partitioning of reproduction in the ant Neoponera apicalis. This species forms small colonies from one single-mated queen, with workers establishing reproductive hierarchies when hopelessly queenless. Previous studies identified putative fertility signals, particularly the hydrocarbon 13-methylpentacosane (13-MeC 25 ), and have shown that precise status discrimination based on these signals could be involved in the regulation of reproductive activities. Here, we extend these findings and reveal that all individuals, be they queens or workers, differ in their cuticular hydrocarbon profile according to fertility state. Proportions of 13-MeC 25 were a strong predictor of an individual's ovarian activity, and could, thus, advertise the established reproducer(s) in both queenright and queenless conditions. Furthermore, this compound might play a key role in the establishment of the reproductive hierarchy, since workers with low fertility at the onset of hierarchy formation already have relatively high amounts of 13-MeC 25 . Dyadic encounters showed that individuals with experimentally increased amounts of 13-MeC 25 triggered less agonistic interactions from top rankers, in accord with them Badvertisingĥ igher status. Thus, these bioassays supported the use of 13-MeC 25 by competing ants. This simple recognition system potentially allows permanent regulation of partitioning of reproduction in this species.
Cuticular hydrocarbons provide reliable cues of fertility in the ant Gnamptogenys striatula
2006
Abstract In ca. 150 species of queenless ants, a specialized queen caste is rare or absent, and mated workers take over the role of the queen in some or all of the colonies. Previously, it has been shown that reproduction in queenless ants is regulated by a combination of dominance behavior and chemical fertility signaling. It is unknown, however, whether chemical signals alone can sufficiently regulate reproduction.
Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size
Behavioral Ecology and Sociobiology, 2007
Models based on the kin selection theory predict that in social hymenopterans, queens may favor a lower investment in the production of sexuals than workers. However, in perennial colonies, this conflict may be tuned down by colony-level selection because of the trade off between colony survival and reproductive allocation. In this study, we present a survey of sexual production in colonies of Aphaenogaster senilis, a common species of ant in the Iberian Peninsula. Similar to most species that reproduce by fission, males were found in large excess compared to gynes (172:1). Sexuals were more likely to be found in queenless than in queenright (QR) field colonies. However, we also found a few gynes and numerous males in very large QR colonies. We compared these data with those available in the literature for A. rudis, a congeneric species from North America that has independent colony founding. The sex ratio in this species was only five males for each female, and sexuals were mostly found in QR nests, irrespective of colony size. We confirmed queen inhibition of sexual production in A. senilis in laboratory experiments and provide evidence that this inhibition is mediated by a nonvolatile pheromone. To seek the potential source of such a queen pheromone, we analyzed the secretions of two conspicuous exocrine glands, the Dufour's and postpharyngeal glands (DG and PPG, respectively) in both queens and workers. Both secretions were composed of hydrocarbons, but that of DG also contained small quantities of tetradecanal and hexadecanal. The hydrocarbon profile of the DG and PPG showed notable caste specificity suggesting a role in caste-related behavior. The PPG secretions also differed between colonies suggesting its role in colonylevel recognition. We suggest that in A. senilis, there are two modes of colony fission: First, in very large colonies, gynes are produced, probably because of the dilution of the queen pheromone, and consequently one or more gynes leave the mother colony with workers and brood to found a new nest. This is beneficial at the colony level because it avoids the production of costly sexuals in small colonies. However, because the queen and workers have different optima for sexual production, we hypothesize that queens tend to overproduce the pheromone to delay their production. This in turn may drive workers to leave the mother colony during nest relocation and to produce sexuals once they are away from the queen's influence, creating a second mode of colony fission.
Hormonal correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi
Journal of Comparative …, 2006
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.
Division of reproductive labor in insect societies is often based on worker self-restraint and both queen and worker policing. Workers of many hitherto studied wasps, bees and ants do not lay eggs in the presence of a queen. However, it is presently unclear how far these observations in a few select clades can be generalized. We investigated if and how queens maintain a reproductive monopoly in colonies of the elongate twig ant, Pseudomyrmex gracilis, a member of the previously unstudied ant subfamily Pseudomyrmecinae. Colonies are usually headed by a single, singly mated queen (monogyny, monandry). Workers therefore would be more closely related to males produced by other workers (r=0.375) than to the sons of queens (r= 0.25). Nevertheless, workers appear to refrain from laying male-destined eggs in the presence of the queen. In queenless conditions, workers form dominance hierarchies by antennal boxing, and only one or a few high-ranking individuals readily begin to lay eggs. When returned into a queenright colony, egg-laying workers are immediately bitten, stung and expelled or killed by other workers. While the composition of cuticular hydrocarbons clearly differed between castes, it less clearly reflected worker ovarian development. An association with worker ovarian development that would allow workers to monitor the reproductive status of nestmates could only be tentatively postulated for certain substances. Our study broadens our knowledge about reproductive conflict in social Hymenoptera and shows that worker sterility in the presence of a queen is more common in monogynous, monandrous ants than expected from relatedness alone.
Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant
Behavioral Ecology, 1999
In insect societies lacking morphologically specialized breeders and helpers, reproduction is often restricted to behaviorally dominant individuals. Such societies occur in about 100 species of ants that have secondarily lost the queen caste. All females, who are morphologically workers, can potentially mate and lay eggs but only a few do so, and we demonstrate in Dinoponera quadriceps that this is regulated by a dominance hierarchy. Six types of agonistic interactions allowed the ranking of 5-10 workers in the hierarchy (n ϭ 15 colonies). In particular, alpha and beta had characteristic behavioral profiles and were easily recognized. Only alpha mated, and workers ranking beta to delta sometimes produced unfertilized, male-destined eggs. Natural replacements (n ϭ 19) and experimental removals (n ϭ 15) of alpha demonstrated that beta was the individual most likely to replace alpha, although gamma and more rarely delta sometimes did, and we discuss the conflict that occurs among high-ranking individuals over who should replace alpha. After such replacements, the new alpha behaved more aggressively than the overthrown alpha. Newly emerged workers tended to reach high ranks and displaced older high-ranking individuals down the hierarchy. Lowranking subordinates often prevented high-ranking individuals from replacing alpha by biting and holding their appendages (worker policing), which is consistent with the pattern of relatedness associated with monogyny and monandry in D. quadriceps. We investigated the relative importance of chemical communication and dominance interactions to regulate reproduction. Alpha, beta, and sterile workers have different signatures of cuticular hydrocarbons, and these may provide honest information which underpins worker policing by low-ranking individuals.
PLOS ONE
In insect societies, chemical communication plays an important role in colony reproduction and individual social status. Many studies have indicated that cuticular hydrocarbons (CHCs) are the main chemical compounds encoding reproductive status. However, these studies have largely focused on queenless or monogynous species whose workers are capable of egg laying and have mainly explored the mechanisms underlying queen-worker or worker-worker reproductive conflicts. Less is known about what occurs in highly polygynous ant species with permanently sterile workers. Here, we used the Argentine ant as a model to examine the role of CHCs in communicating reproductive information in such insect societies. The Argentine ant is unicolonial, highly polygynous, and polydomous. We identified several CHCs whose presence and levels were correlated with queen age, reproductive status, and fertility. Our results also provide new insights into queen executions in the Argentine ant, a distinctive feature displayed by this species in its introduced range. Each spring, just before new sexuals appear, workers eliminate up to 90% of the mated queens in their colonies. We discovered that queens that survived execution had different CHC profiles from queens present before and during execution. More specifically, levels of some CHCs were higher in the survivors, suggesting that workers could eliminate queens based on their chemical profiles. In addition, queen CHC profiles differed based on season and species range (native vs. introduced). Overall, the results of this study provide new evidence that CHCs serve as queen signals and do more than just regulate worker reproduction.