Cintia Akemi Oi

Conserved class of queen pheromones stops social insect workers from reproducing

Long Live the Queen Eusociality is often considered to have arisen, at least in part, due to the inclusive fitness that workers gain through helping their queen sister to raise her offspring. Van Oystaeyen et al. (p. 287; see the Perspective by Chapuisat) characterized the sterility-inducing queen pheromone across three distantly related eusocial hymenopterans (a wasp, a bumblebee, and a desert ant) and synthesized data across 69 other species. Queen pheromones appear to be remarkably conserved, which suggests that reproductive manipulation has ancient roots. Social insect queens use an ancient, evolutionarily conserved class of pheromones to prevent worker reproduction. [Also see Perspective by Chapuisat] A major evolutionary transition to eusociality with reproductive division of labor between queens and workers has arisen independently at least 10 times in the ants, bees, and wasps. Pheromones produced by queens are thought to play a key role in regulating this complex social system, but their evolutionary history remains unknown. Here, we identify the first sterility-inducing queen pheromones in a wasp, bumblebee, and desert ant and synthesize existing data on compounds that characterize female fecundity in 64 species of social insects. Our results show that queen pheromones are strikingly conserved across at least three independent origins of eusociality, with wasps, ants, and some bees all appearing to use nonvolatile, saturated hydrocarbons to advertise fecundity and/or suppress worker reproduction. These results suggest that queen pheromones evolved from conserved signals of solitary ancestors.

The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems

Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to remain sterile, are considered to play a key role in regulating the reproductive division of labor of insect societies. Although queen pheromones were long thought to be highly taxon-specific, recent studies have shown that structurally related long-chain hydrocarbons act as conserved queen signals across several independently evolved lineages of social insects. These results imply that social insect queen pheromones are very ancient and likely derived from an ancestral signalling system that was already present in their common solitary ancestors. Based on these new insights, we here review the literature and speculate on what signal precursors social insect queen pheromones may have evolved from. Furthermore, we provide compelling evidence that these pheromones should best be seen as honest signals of fertility as opposed to suppressive agents that chemically sterilize the workers against their own best interests.

Nectar-foraging behavior of Euglossine bees (Hymenoptera: Apidae) in urban areas

Euglossine bees have been described as long-distance pollinators because of their great flight capacities although flight capacity is not necessarily correlated to home range. Here we report the nectar-foraging behavior of two euglossine species (Euglossa cordata and Eulaema nigrita) in urban areas and the predictive power of wing wear as an age estimator of these bees, using mark-recapture techniques at Thevetia peruviana trees. A total of 870 bees were marked. Recapture rates were 33% (± 19.2) for E. cordata and 25% (± 2.5) for E. nigrita. Only 7 bees were sighted at a different site from where they were first captured. More than 75% of the individuals showed site-constancy at trees for at least 30 days. Wing wear accumulation rate was variable among individuals and it was a poor predictor of age for E. cordata. Our data show that euglossine bees may have small foraging ranges in urban areas, indicating that home ranges greatly differ from their flight capacity and homing ability.ZusammenfassungEuglossine Bienen (Prachtbienen) werden im allgemeinen als Weitdistanzbestäuber eingestuft, die grosse Sammelgebiete abdecken können. Sie sind dazu in der Lage aufgrund ihrer grossen Flugkapazität und dies obwohl Flugkapazität nicht notwendigerweise mit dem Heimatradius korreliert sein muss. In dieser Arbeit untersuchten wir das Nektarsammelverhalten von zwei Prachtbienenarten in Stadtgebieten, und wir bewerteten die Aussagekraft des Flügelabnutzungsgrads für die Altersabschätzung. Wir beschreiben zudem eine effiziente Methode zur Markierung dieser Bienen, die Etiketten leicht durch ihr intensives Putzverhalten verlieren können. Weibchen und Männchen von Euglossa cordata (nw = 596; nm = 53) und von Eulaema nigrita (nw = 106; nm = 115) (Tab. I) wurden markiert und später auf blühenden Bäumen der Art Thevetia peruviana (Apocynaceae) in einem Umkreis von 0,24–5,45 km im Stadtgebiet von São Carlos (SP, Brasilien) wiedergefangen. Die mittlere Wiederfangrate für Eg. cordata lag bei 33 % (± 19,2) und die für El. nigrita bei 25 % (± 2,5). Von den 213 wiedergefangenen Bienen wurden jedoch nur sieben an einem anderen Ort wiedergefangen als dem, an dem sie zuerst gefangen und markiert worden waren (Tab. II). Über 75 % der Bienen beider Arten zeigten ausserdem eine Ortskonstanz im Sammelverhalten an den Bäumen über mindestens 30 Tage hinweg. Bei Männchen war der Zeitraum allerdings kürzer als bei Weibchen (Abb. 3 und 4). Diese Ergebnisse weisen daraufhin, dass Prachtbienen bevorzugt über kurze Distanzen hinweg Nektar sammeln, dass sie ihre Sammelterritorien jedoch nach einiger Zeit wechseln können. Der Flügelabnutzungsgrad erwies sich als individuell stark variabel und schien bei Eg. cordata kein guter Altersindikator zu sein (Abb. 5). Unsere Daten zeigen, dass Euglossinen in Stadtgebieten aufgrund der Verteilung von Blüten relativ kleine Sammelgebiete haben können. Dies bedeutet, dass sich Heimatradien stark von den Faktoren Flugkapazität und Heimfindungsvermögen unterscheiden können.

Genetic differentiation of urban populations of Euglossa cordata from the state of São Paulo, Brazil

Males and females of Euglossa cordata collected inside flowers of Thevetia peruviana in urban areas of eleven cities of the state of São Paulo were analysed using allozymes and nine microsatellite loci. The analyses revealed that these populations have a high genetic diversity and are under genetic equilibrium, showing low population structuring and rare diploid males; consequently, high gene flow and effective population size (Ne) are inferred. These findings corroborate previous biological observations and phylogeographic evidence that report dispersion over long distances of Euglossini species in South America.

The origin and evolution of queen and fertility signals in Corbiculate bees.

BackgroundIn social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle have been shown to act as fertility signals. In addition, specific queen-characteristic hydrocarbons have been implicated as sterility-inducing queen signals in ants, wasps and bumblebees. In Corbiculate bees, however, the chemical nature of queen-characteristic and fertility-linked compounds appears to be more diverse than in ants and wasps. Moreover, it remains unknown how queen signals evolved across this group and how they might have been co-opted from fertility signals in solitary ancestors.ResultsHere, we perform a phylogenetic analysis of fertility-linked compounds across 16 species of solitary and eusocial bee species, comprising both literature data as well as new primary data from a key solitary outgroup species, the oil-collecting bee Centris analis, and the highly eusocial stingless bee Scaptotrigona depilis. Our results demonstrate the presence of fertility-linked compounds belonging to 12 different chemical classes. In addition, we find that some classes of compounds (linear and branched alkanes, alkenes, esters and fatty acids) were already present as fertility-linked signals in the solitary ancestors of Corbiculate bees, while others appear to be specific to certain species.ConclusionOverall, our results suggest that queen signals in Corbiculate bees are likely derived from ancestral fertility-linked compounds present in solitary bees that lacked reproductive castes. These original fertility-linked cues or signals could have been produced either as a by-product of ovarian activation or could have served other communicative purposes, such as in mate recognition or the regulation of egg-laying.

Conservation of Queen Pheromones Across Two Species of Vespine Wasps.

Social insects are known for their reproductive division of labor between queens and workers, whereby queens lay the majority of the colony’s eggs, and workers engage mostly in non-reproductive tasks. Queens produce pheromones that signal their presence and fertility to workers, which in turn generally remain sterile. Recently, it has been discovered that specific queen-characteristic cuticular hydrocarbons (CHCs) function as queen pheromones across multiple lineages of social insects. In the common wasp, Vespula vulgaris, several long-chain linear alkanes and 3-methylalkanes were shown to act as queen signals. Here, we describe similar bioassays with a related species of highly eusocial vespine wasp, the Saxon wasp, Dolichovespula saxonica. We show that a blend of queen-characteristic hydrocarbons that are structurally related to those of the common wasp inhibit worker reproduction, suggesting conservation of queen pheromones across social wasps. Overall, our results highlight the central importance of CHCs in chemical communication among social insects in general, and as conserved queen pheromones in these social wasps in particular.

Intraspecific worker parasitism in the common wasp, Vespula vulgaris

Insect societies display a remarkable level of cooperation, but their colonies also represent a valuable resource that can be taken advantage of by genetically unrelated individuals. Indeed, several recent studies have documented cases of intraspecific reproductive parasitism, whereby workers penetrate and lay eggs in unrelated colonies in order to have their brood raised by the host workers. Previously, it has been predicted that queenless colonies should be a prime target of such intraspecific worker parasitism, as in such colonies the parasite workers would be able to reproduce without interference from either the queen or other workers. So far, this prediction has been supported with data from the honeybee, but evidence from other social insect groups is currently lacking. Here we present the first such test in the common wasp, Vespula vulgaris. In particular, workers from queenright colonies left the natal nest at a higher rate than those from queenless colonies. However, contrary to our predictions, drifter workers targeted queenless and queenright colonies equally. Chemical data suggest that this lack of discrimination may be linked to recognition constraints and the lack of volatile signals that reliably indicate the presence or absence of the queen. In addition, in queenright colonies, drifters activated their ovaries at a rate that was ca. five times higher than the natal workers. Overall, our results suggest that also in wasps, workers can gain inclusive fitness by drifting to unrelated nests, even if the chances of successfully reproducing there may be very slim.

Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp

In insect societies, both queens and workers produce chemicals that reliably signal caste membership and reproductive status. The mechanisms that help to maintain the honesty of such queen and fertility signals, however, remain poorly studied. Here we test if queen signal honesty could be based on the shared endocrine control of queen fertility and the production of specific signals. In support of this “hormonal pleiotropy” hypothesis, we find that in the common wasp, application of methoprene (a juveline hormone analogue) caused workers to acquire a queen-like cuticular hydrocarbon profile, resulting in the overproduction of known queen pheromones as well as some compounds typically linked to worker fertility. By contrast, administration of precocene-I (a JH inhibitor) had a tendency to have the opposite effect. Furthermore, a clear gonadotropic effect of JH in queens was suggested by the fact that circulating levels of JH were ca. 2 orders of magnitude higher in queens than those in workers and virgin, non-egg-laying queens, even if methoprene or precocene treatment did not affect the ovary development of workers. Overall, these results suggest that queen signal honesty in this system is maintained by queen fertility and queen signal production being under shared endocrine control.