scholarly journals Conserved queen pheromones in bumblebees: a reply to Amsalem et al.

PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3332 ◽  
Author(s):  
Luke Holman ◽  
Jelle S. van Zweden ◽  
Ricardo C. Oliveira ◽  
Annette van Oystaeyen ◽  
Tom Wenseleers

In a recent study, Amsalem, Orlova & Grozinger (2015) performed experiments withBombus impatiensbumblebees to test the hypothesis that saturated cuticular hydrocarbons are evolutionarily conserved signals used to regulate reproductive division of labor in many Hymenopteran social insects. They concluded that the cuticular hydrocarbon pentacosane (C25), previously identified as a queen pheromone in a congeneric bumblebee, does not affect worker reproduction inB. impatiens. Here we discuss some shortcomings of Amsalem et al.’s study that make its conclusions unreliable. In particular, several confounding effects may have affected the results of both experimental manipulations in the study. Additionally, the study’s low sample sizes (mean n per treatment = 13.6, range: 4–23) give it low power, not 96–99% power as claimed, such that its conclusions may be false negatives. Inappropriate statistical tests were also used, and our reanalysis found that C25substantially reduced and delayed worker egg laying inB. impatiens. We review the evidence that cuticular hydrocarbons act as queen pheromones, and offer some recommendations for future queen pheromone experiments.

2016 ◽  
Author(s):  
Luke Holman ◽  
Jelle S van Zweden ◽  
Ricardo Caliari Oliveira ◽  
Annette van Oystaeyen ◽  
Tom Wenseleers

In a recent study, Amsalem et al. performed experiments with Bombus impatiens bumblebees to test the hypothesis that saturated cuticular hydrocarbons are evolutionarily conserved signals used to regulate reproductive division of labour in many Hymenopteran social insects. They concluded that the cuticular hydrocarbon pentacosane (C25), previously identified as a queen pheromone in a congeneric bumblebee, does not affect worker reproduction in B. impatiens. Here we identify some significant shortcomings of Amsalem et al.’s study that make its conclusions unreliable. In particular, inappropriate statistical tests were used, and a reanalysis of their dataset found that C25 substantially reduced and delayed worker egg laying in B. impatiens. Additionally, the study’s low sample sizes (mean n per treatment = 13.6, range: 4-23) give it low power, not 99% power as claimed, meaning that some its non-significant results may be false negatives. Additionally, several confounding effects may have affected the results of both experimental manipulations in the study


Author(s):  
Luke Holman ◽  
Jelle S van Zweden ◽  
Ricardo Caliari Oliveira ◽  
Annette van Oystaeyen ◽  
Tom Wenseleers

In a recent study, Amsalem et al. performed experiments with Bombus impatiens bumblebees to test the hypothesis that saturated cuticular hydrocarbons are evolutionarily conserved signals used to regulate reproductive division of labour in many Hymenopteran social insects. They concluded that the cuticular hydrocarbon pentacosane (C25), previously identified as a queen pheromone in a congeneric bumblebee, does not affect worker reproduction in B. impatiens. Here we identify some significant shortcomings of Amsalem et al.’s study that make its conclusions unreliable. In particular, inappropriate statistical tests were used, and a reanalysis of their dataset found that C25 substantially reduced and delayed worker egg laying in B. impatiens. Additionally, the study’s low sample sizes (mean n per treatment = 13.6, range: 4-23) give it low power, not 99% power as claimed, meaning that some its non-significant results may be false negatives. Additionally, several confounding effects may have affected the results of both experimental manipulations in the study


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Margarita Orlova ◽  
Etya Amsalem

AbstractQueen pheromones have long been studied as a major factor regulating reproductive division of labor in social insects. Hitherto, only a handful of queen pheromones were identified and their effects on workers have mostly been studied in isolation from the social context in which they operate. Our study examined the importance of behavioral and social context for the perception of queen semiochemicals by bumble bee workers. Our results indicate that a mature queen’s cuticular semiochemicals are capable of inhibiting worker reproduction only when accompanied by the queen’s visual presence and the offspring she produces, thus, when presented in realistic context. Queen’s chemistry, queen’s visual presence and presence of offspring all act to regulate worker reproduction, but none of these elements produces an inhibitory effect on its own. Our findings highlight the necessity to reconsider what constitutes a queen pheromone and suggest a new approach to the study of chemical ecology in social insects.


2021 ◽  
Author(s):  
Margarita Orlova ◽  
Etya Amsalem

Abstract Queen pheromones have long been studied as a major factor regulating reproductive division of labor in social insects. Hitherto, only a handful of queen pheromones were identified and their effects on workers have mostly been studied in isolation from the social context in which they operate. Our study examined the importance of behavioral and social context for the perception of queen semiochemicals by bumble bee workers. Our results indicate that a mature queen’s semiochemicals are capable of inhibiting worker reproduction only when accompanied by the queen’s visual presence and the offspring she produces, thus, when presented in realistic context. Queen’s chemistry, queen’s visual presence and presence of offspring all act in synergy to regulate worker reproduction, but none of these elements produces an inhibitory effect on its own. Our findings highlight the necessity to reconsider what constitutes a queen pheromone and suggest a new approach to the study of chemical ecology in social insects.


2015 ◽  
Vol 282 (1817) ◽  
pp. 20151800 ◽  
Author(s):  
Etya Amsalem ◽  
Margarita Orlova ◽  
Christina M. Grozinger

The regulation of reproductive division of labour is a key component in the evolution of social insects. Chemical signals are important mechanisms to regulate worker reproduction, either as queen-produced pheromones that coercively inhibit worker reproduction or as queen signals that honestly advertise her fecundity. A recent study suggested that a conserved class of hydrocarbons serve as queen pheromones across three independent origins of eusociality. In bumblebees ( Bombus terrestris ), pentacosane ( C 25) was suggested to serve as a queen pheromone. Here, we repeat these studies using a different species of bumblebee ( Bombus impatiens ) with a more controlled experimental design. Instead of dequeened colonies, we used same-aged, three-worker queenless groups comprising either experienced or naive workers (with/without adult exposure to queen pheromone). We quantified three hydrocarbons ( C 23, C 25 and C 27) on the cuticular surfaces of females and tested their effects on the two worker types. Our results indicate differences in responses of naive and experienced workers, genetic effects on worker reproduction, and general effects of hydrocarbons and duration of egg laying on ovary resorption rates. However, we found no evidence to support the theory that a conserved class of hydrocarbons serve as queen pheromones or queen signals in Bombus impatiens .


2021 ◽  
Author(s):  
Yuki Mitaka ◽  
Tadahide Fujita

Abstract Chemical communication underlies the sophisticated colony organization of social insects. In these insects, cuticular hydrocarbons (CHCs) play central roles in nestmate, task, and caste recognition, which contribute to maintenance of the social and reproductive division of labor. Queen-specific CHCs reflect queen fertility status and function as a queen recognition pheromone, triggering aggregation responses around the queens. However, there are only a few studies about the royal recognition mechanism in termites, and particularly, no study has reported about queen-specific CHCs in the species using asexual queen succession (AQS) system, in which the primary queen is replaced by neotenic queens produced parthenogenetically. In this study, we identified the CHC pheromone for neotenic queen recognition in the AQS termite species Reticulitermes speratus. Gas chromatography-mass spectrometry analyses revealed that the relative amount of n-pentacosane was disproportionately greater in the CHC profiles of queens than in the CHC profiles of kings, soldiers, and workers. Furthermore, we investigated the cuticular chemicals of the queen aggregate workers; bioassays demonstrated that n-pentacosane shows a worker arrestant activity in the presence of workers’ cuticular extract. These results suggest that R. speratus workers identify whether each individual is a neotenic queen by recognizing the relatively higher ratio of n-pentacosane in the conspecific CHC background. Moreover, they suggest that termites have evolved queen recognition behavior, independently of social hymenopterans.


2010 ◽  
Vol 277 (1701) ◽  
pp. 3793-3800 ◽  
Author(s):  
Luke Holman ◽  
Charlotte G. Jørgensen ◽  
John Nielsen ◽  
Patrizia d'Ettorre

The selective forces that shape and maintain eusocial societies are an enduring puzzle in evolutionary biology. Ordinarily sterile workers can usually reproduce given the right conditions, so the factors regulating reproductive division of labour may provide insight into why eusociality has persisted over evolutionary time. Queen-produced pheromones that affect worker reproduction have been implicated in diverse taxa, including ants, termites, wasps and possibly mole rats, but to date have only been definitively identified in the honeybee. Using the black garden ant Lasius niger , we isolate the first sterility-regulating ant queen pheromone. The pheromone is a cuticular hydrocarbon that comprises the majority of the chemical profile of queens and their eggs, and also affects worker behaviour, by reducing aggression towards objects bearing the pheromone. We further show that the pheromone elicits a strong response in worker antennae and that its production by queens is selectively reduced following an immune challenge. These results suggest that the pheromone has a central role in colony organization and support the hypothesis that worker sterility represents altruistic self-restraint in response to an honest quality signal.


2020 ◽  
Vol 16 (8) ◽  
pp. 20200348
Author(s):  
Ricardo Caliari Oliveira ◽  
Jonas Warson ◽  
David Sillam-Dussès ◽  
Beatriz Herrera-Malaver ◽  
Kevin Verstrepen ◽  
...  

The division of labour between reproductive queens and mostly sterile workers is among the defining characteristics of social insects. Queen-produced chemical signals advertising her presence and fertility status, i.e. queen pheromones, are normally used to assert the queen's reproductive dominance in the colony. Most queen pheromones identified to date are chemicals that stop the daughter workers from reproducing. Nevertheless, it has long been suggested that queen pheromones could also regulate reproduction in different ways. In some multiple-queen ants with obligately sterile workers, for example—such as fire ants and pharaoh ants—queen pheromones are thought to regulate reproduction by inhibiting the rearing of new sexuals. Here, we identify the first such queen pheromone in the pharaoh ant Monomorium pharaonis and demonstrate its mode of action via bioassays with the pure biosynthesized compound. In particular, we show that the monocyclic diterpene neocembrene, which in different Monomorium species is produced solely by fertile, egg-laying queens, strongly inhibits the rearing of new sexuals (queens and males) and also exerts a weakly attractive ‘queen retinue’ effect on the workers. This is the first time that a queen pheromone with such a dual function has been identified in a social insect species with obligately sterile workers.


Author(s):  
Sarah A Princen ◽  
Annette Van Oystaeyen ◽  
Clément Petit ◽  
Jelle S van Zweden ◽  
Tom Wenseleers

Abstract The evolutionary origin of queen pheromones (QPs), which regulate reproductive division of labor in insect societies, has been explained by two evolutionary scenarios: the sender-precursor hypothesis and the sensory exploitation hypothesis. These scenarios differ in terms of whether the signaling system was built on preadaptations on the part of either the sender queens or the receiver workers. While some social insect QPs—such as cuticular hydrocarbons—were likely derived from ancestral fertility cues and evolved according to the former theory, the honeybee’s queen mandibular pheromone (QMP) has been suggested to act directly on preexisting gene-regulatory networks linked with reproduction. This is evidenced by the fact that QMP has been shown to also inhibit ovary activation in fruit flies, thereby implying exploitation of conserved physiological pathways. To verify whether QMP has similar effects on more closely related eusocial species, we here tested for QMP cross-activity in the bumblebee Bombus terrestris. Interestingly, we found that the non-native QMP blend significantly inhibited egg laying in both worker and queen bumblebees and caused accompanying shifts in ovary activation. The native bumblebee QP pentacosane, by contrast, only inhibited the reproduction of the workers. Overall, these findings support the hypothesis that honeybee QMP likely evolved via a route of sensory exploitation. We argue that such exploitation could allow social insect queens to produce compounds that manipulate the workers to remain sterile, but that a major hurdle would be that the queens themselves would have to be immune to such compounds.


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