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Luke Holman - One of the best experts on this subject based on the ideXlab platform.
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comparative transcriptomics of social insect Queen Pheromones
Nature Communications, 2019Co-Authors: Luke Holman, Kalevi Trontti, Alexander S MikheyevAbstract:Queen Pheromones are chemical signals that mediate reproductive division of labor in eusocial animals. Remarkably, Queen Pheromones are composed of identical or chemically similar compounds in some ants, wasps and bees, even though these taxa diverged >150MYA and evolved Queens and workers independently. Here, we measure the transcriptomic consequences of experimental exposure to Queen Pheromones in workers from two ant and two bee species (genera: Lasius, Apis, Bombus), and test whether they are similar across species. Queen pheromone exposure affected transcription and splicing at many loci. Many genes responded consistently in multiple species, and the set of pheromone-sensitive genes was enriched for functions relating to lipid biosynthesis and transport, olfaction, production of cuticle, oogenesis, and histone (de)acetylation. Pheromone-sensitive genes tend to be evolutionarily ancient, positively selected, peripheral in the gene coexpression network, hypomethylated, and caste-specific in their expression. Our results reveal how Queen Pheromones achieve their effects, and suggest that ants and bees use similar genetic modules to achieve reproductive division of labor. Queen Pheromones are used by eusocial insects to regulate all aspects of colony life. Here, Holman et al. compare the effects of Queen pheromone on gene expression and splicing in four eusocial insect species, giving insight into the mechanism and evolution of division of reproductive labour.
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Comparative transcriptomics of social insect Queen Pheromones
Nature Publishing Group, 2019Co-Authors: Luke Holman, Kalevi Trontti, Heikki Helanterä, Alexander S MikheyevAbstract:Queen Pheromones are used by eusocial insects to regulate all aspects of colony life. Here, Holman et al. compare the effects of Queen pheromone on gene expression and splicing in four eusocial insect species, giving insight into the mechanism and evolution of division of reproductive labour
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conserved Queen Pheromones in bumblebees a reply to amsalem et al
PeerJ, 2017Co-Authors: Luke Holman, Jelle S Van Zweden, Ricardo Caliari Oliveira, Annette Van Oystaeyen, Tom WenseleersAbstract:In a recent study, Amsalem, Orlova & Grozinger (2015) performed experiments with Bombus impatiens bumblebees 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 in B. 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 C25 substantially reduced and delayed worker egg laying in B. impatiens. We review the evidence that cuticular hydrocarbons act as Queen Pheromones, and offer some recommendations for future Queen pheromone experiments.
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Highly specific responses to Queen pheromone in three Lasius ant species
Behavioral Ecology and Sociobiology, 2016Co-Authors: Luke Holman, Brian Hanley, Jocelyn G MillarAbstract:Queen Pheromones mediate the reproductive division of labor in social insect colonies and provide novel opportunities for investigating the evolution of animal communication. Previous work found that Queens in the ant genus Lasius produce several 3-methylalkanes in greater relative amounts than workers do. At least one of these (3-MeC_31) is a Queen pheromone that regulates worker sterility in two Lasius species, although there are indications that other 3-methylalkanes might also function as Queen Pheromones. Here, we presented workers from three Lasius species with four different 3-methylalkanes, and measured the effect on worker ovary development. In all three species, only 3-MeC_31 showed clear evidence of inhibiting worker fecundity. Our results suggest that worker ants can discriminate homologous hydrocarbons that differ in chain length and only treat specific homologs as Queen Pheromones. These results provide insight into the conflicting selective pressures on cuticular hydrocarbons arising from their multiple roles in signaling and adaptation to the abiotic environment.
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Queen Pheromones modulate DNA methyltransferase activity in bee and ant workers
The Royal Society, 2015Co-Authors: Luke Holman, Kalevi Trontti, Heikki HelanteräAbstract:DNA methylation is emerging as an important regulator of polyphenism in the social insects. Research has concentrated on differences in methylation between Queens and workers, though we hypothesized that methylation is involved in mediating other flexible phenotypes, including pheromone-dependent changes in worker behaviour and physiology. Here, we find that exposure to Queen pheromone affects the expression of two DNA methyltransferase genes in Apis mellifera honeybees and in two species of Lasius ants, but not in Bombus terrestris bumblebees. These results suggest that Queen Pheromones influence the worker methylome, pointing to a novel proximate mechanism for these key social signals.
Jelle S Van Zweden - One of the best experts on this subject based on the ideXlab platform.
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honeybees possess a structurally diverse and functionally redundant set of Queen Pheromones
Proceedings of The Royal Society B: Biological Sciences, 2019Co-Authors: Sarah A Princen, Jelle S Van Zweden, Ricardo Caliari Oliveira, Jocelyn G Millar, Ulrich R Ernst, Tom WenseleersAbstract:Queen Pheromones, which signal the presence of a fertile Queen and induce workers to remain sterile, play a key role in regulating reproductive division of labour in insect societies. In the honeybee, volatiles produced by the Queen's mandibular glands have been argued to act as the primary sterility-inducing Pheromones. This contrasts with evidence from other groups of social insects, where specific Queen-characteristic hydrocarbons present on the cuticle act as conserved Queen signals. This led us to hypothesize that honeybee Queens might also employ cuticular Pheromones to stop workers from reproducing. Here, we support this hypothesis with the results of bioassays with synthetic blends of Queen-characteristic alkenes, esters and carboxylic acids. We show that all these compound classes suppress worker ovary development, and that one of the blends of esters that we used was as effective as the Queen mandibular pheromone (QMP) mix. Furthermore, we demonstrate that the two main QMP compounds 9-ODA and 9-HDA tested individually were as effective as the blend of all four major QMP compounds, suggesting considerable signal redundancy. Possible adaptive reasons for the observed complexity of the honeybee Queen signal mix are discussed.
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do primitively eusocial wasps use Queen Pheromones to regulate reproduction a case study of the paper wasp polistes satan
Frontiers in Ecology and Evolution, 2019Co-Authors: Ricardo Caliari Oliveira, Jelle S Van Zweden, Fabio S Nascimento, Jocelyn G Millar, Sidnei Mateus, Tom WenseleersAbstract:In several highly eusocial insect species with morphologically distinct castes, Queen-characteristic cuticular hydrocarbons (CHCs) have been shown to act as Queen signals that suppress the reproduction of nestmate workers. However, it is not known whether such Queen Pheromones might also play a role in regulating reproductive division of labour in primitively eusocial insects that lack morphologically defined castes. Here, we experimentally tested whether a blend of CHCs which occurred in higher concentrations in the dominant breeding female act as a Queen pheromone, and inhibit reproduction by subordinate females in the primitively eusocial paper wasp Polistes satan. In contrast to earlier findings with highly eusocial species, our results show that although specific compounds were enhanced in dominant, reproductively active females, a blend of five of these compounds did not inhibit development of the ovaries of female nestmates. Instead, the dominant female had to be physically present to prevent subordinate females from reproducing. Our results are in line with earlier evidence suggesting that fertility-linked compounds in primitively eusocial wasps act only as cues and help to regulate reproduction when used in conjunction with aggressive dominance behaviour, meaning the physical presence of the dominant female. Alternatively, our results support the hypothesis that Queen Pheromones in highly eusocial insects were co-opted from fertility cues that were already present in primitively eusocial ancestors, even when initially, such compounds were merely produced as by-products of ovarian activation, without actually serving to signal reproductive status.
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conserved Queen Pheromones in bumblebees a reply to amsalem et al
PeerJ, 2017Co-Authors: Luke Holman, Jelle S Van Zweden, Ricardo Caliari Oliveira, Annette Van Oystaeyen, Tom WenseleersAbstract:In a recent study, Amsalem, Orlova & Grozinger (2015) performed experiments with Bombus impatiens bumblebees 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 in B. 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 C25 substantially reduced and delayed worker egg laying in B. impatiens. We review the evidence that cuticular hydrocarbons act as Queen Pheromones, and offer some recommendations for future Queen pheromone experiments.
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Conservation of Queen Pheromones Across Two Species of Vespine Wasps.
Journal of chemical ecology, 2016Co-Authors: Jocelyn G Millar, Jelle S Van Zweden, Tom WenseleersAbstract: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.
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biological activity of the enantiomers of 3 methylhentriacontane a Queen pheromone of the ant lasius niger
The Journal of Experimental Biology, 2016Co-Authors: Marine Motais De Narbonne, Jelle S Van Zweden, Tom Wenseleers, Jocelyn G Millar, Jan E Bello, Patrizia DettorreAbstract:Queen Pheromones are essential for regulation of the reproductive division of labor in eusocial insect species. Although only the Queen is able to lay fertilized eggs and produce females, in some cases workers may develop their ovaries and lay male-destined eggs, thus reducing the overall colony efficiency. As long as the Queen is healthy, it is usually in the workers' collective interest to work for the colony and remain sterile. Queens signal their fertility via Pheromones, which may have a primer effect, affecting the physiology of workers, or a releaser effect, influencing worker behavior. The Queen pheromone of the ant Lasius niger was among the first Queen Pheromones of social insects to be identified. Its major component is 3-methylhentriacontane (3-MeC31), which is present in relatively large amounts on the Queen's cuticle and on her eggs. 3-MeC31 regulates worker reproduction by inhibiting ovarian development. Most monomethyl-branched hydrocarbons can exist in two stereoisomeric forms. The correct stereochemistry is fundamental to the activity of most bioactive molecules, but this has rarely been investigated for methyl-branched hydrocarbons. Here, we tested the bioactivity of the (S)- and (R)-enantiomers of 3-MeC31, and found that whereas both enantiomers were effective in suppressing worker ovarian development, (S)-3-MeC31 appeared to be more effective at suppressing aggressive behavior by workers. This suggests that the natural pheromone may be a mixture of the two enantiomers. The enantiomeric ratio produced by Queens remains unknown because of the small amounts of the compound available from each Queen.
Patrizia Dettorre - One of the best experts on this subject based on the ideXlab platform.
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biological activity of the enantiomers of 3 methylhentriacontane a Queen pheromone of the ant lasius niger
The Journal of Experimental Biology, 2016Co-Authors: Marine Motais De Narbonne, Jelle S Van Zweden, Tom Wenseleers, Jocelyn G Millar, Jan E Bello, Patrizia DettorreAbstract:Queen Pheromones are essential for regulation of the reproductive division of labor in eusocial insect species. Although only the Queen is able to lay fertilized eggs and produce females, in some cases workers may develop their ovaries and lay male-destined eggs, thus reducing the overall colony efficiency. As long as the Queen is healthy, it is usually in the workers' collective interest to work for the colony and remain sterile. Queens signal their fertility via Pheromones, which may have a primer effect, affecting the physiology of workers, or a releaser effect, influencing worker behavior. The Queen pheromone of the ant Lasius niger was among the first Queen Pheromones of social insects to be identified. Its major component is 3-methylhentriacontane (3-MeC31), which is present in relatively large amounts on the Queen's cuticle and on her eggs. 3-MeC31 regulates worker reproduction by inhibiting ovarian development. Most monomethyl-branched hydrocarbons can exist in two stereoisomeric forms. The correct stereochemistry is fundamental to the activity of most bioactive molecules, but this has rarely been investigated for methyl-branched hydrocarbons. Here, we tested the bioactivity of the (S)- and (R)-enantiomers of 3-MeC31, and found that whereas both enantiomers were effective in suppressing worker ovarian development, (S)-3-MeC31 appeared to be more effective at suppressing aggressive behavior by workers. This suggests that the natural pheromone may be a mixture of the two enantiomers. The enantiomeric ratio produced by Queens remains unknown because of the small amounts of the compound available from each Queen.
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conserved class of Queen Pheromones stops social insect worker reproduction
2014Co-Authors: Caliari R Oliveira, Jelle S Van Zweden, Annette Van Oystaeyen, Luke Holman, Johan Billen, Carmen Romero, Patrizia Dettorre, Mohammadreza Khalesi, Felix Wackers, Jocelyn G MillarAbstract:20 - Reproductive division of labour and the evolution of Queen Pheromones, Oral Presentation
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conserved class of Queen Pheromones stops social insect workers from reproducing
Science, 2014Co-Authors: Annette Van Oystaeyen, Jelle S Van Zweden, Ricardo Caliari Oliveira, Luke Holman, Johan Billen, Carmen Romero, Patrizia Dettorre, Mohammadreza Khalesi, Felix L Wackers, Jocelyn G MillarAbstract: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.
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the evolution of Queen Pheromones in the ant genus lasius
Journal of Evolutionary Biology, 2013Co-Authors: Luke Holman, Patrizia Dettorre, Robert LanfearAbstract:Queen Pheromones are among the most important chemical messages regulating insect societies yet they remain largely undiscovered, hindering research into interesting proximate and ultimate questions. Identifying Queen Pheromones in multiple species would give new insight into the selective pressures and evolutionary constraints acting on these ubiquitous signals. Here, we present experimental and comparative evidence that 3-methylalkanes, hydrocarbons present on the Queen's cuticle, are a Queen pheromone throughout the ant genus Lasius. Interspecific variation in the chemical profile is consistent with 3-methylalkanes evolving more slowly than other types of hydrocarbons, perhaps due to differential selection or evolutionary constraints. We argue that the sensory ecology of the worker response imposes strong stabilizing selection on Queen Pheromones relative to other hydrocarbons. 3-Methylalkanes are also strongly physiologically and genetically coupled with fecundity in at least one Lasius species, which may translate into evolutionary constraints. Our results highlight how honest signalling could minimize evolutionary conflict over reproduction, promoting the evolution and maintenance of eusociality.
Jocelyn G Millar - One of the best experts on this subject based on the ideXlab platform.
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honeybees possess a structurally diverse and functionally redundant set of Queen Pheromones
Proceedings of The Royal Society B: Biological Sciences, 2019Co-Authors: Sarah A Princen, Jelle S Van Zweden, Ricardo Caliari Oliveira, Jocelyn G Millar, Ulrich R Ernst, Tom WenseleersAbstract:Queen Pheromones, which signal the presence of a fertile Queen and induce workers to remain sterile, play a key role in regulating reproductive division of labour in insect societies. In the honeybee, volatiles produced by the Queen's mandibular glands have been argued to act as the primary sterility-inducing Pheromones. This contrasts with evidence from other groups of social insects, where specific Queen-characteristic hydrocarbons present on the cuticle act as conserved Queen signals. This led us to hypothesize that honeybee Queens might also employ cuticular Pheromones to stop workers from reproducing. Here, we support this hypothesis with the results of bioassays with synthetic blends of Queen-characteristic alkenes, esters and carboxylic acids. We show that all these compound classes suppress worker ovary development, and that one of the blends of esters that we used was as effective as the Queen mandibular pheromone (QMP) mix. Furthermore, we demonstrate that the two main QMP compounds 9-ODA and 9-HDA tested individually were as effective as the blend of all four major QMP compounds, suggesting considerable signal redundancy. Possible adaptive reasons for the observed complexity of the honeybee Queen signal mix are discussed.
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do primitively eusocial wasps use Queen Pheromones to regulate reproduction a case study of the paper wasp polistes satan
Frontiers in Ecology and Evolution, 2019Co-Authors: Ricardo Caliari Oliveira, Jelle S Van Zweden, Fabio S Nascimento, Jocelyn G Millar, Sidnei Mateus, Tom WenseleersAbstract:In several highly eusocial insect species with morphologically distinct castes, Queen-characteristic cuticular hydrocarbons (CHCs) have been shown to act as Queen signals that suppress the reproduction of nestmate workers. However, it is not known whether such Queen Pheromones might also play a role in regulating reproductive division of labour in primitively eusocial insects that lack morphologically defined castes. Here, we experimentally tested whether a blend of CHCs which occurred in higher concentrations in the dominant breeding female act as a Queen pheromone, and inhibit reproduction by subordinate females in the primitively eusocial paper wasp Polistes satan. In contrast to earlier findings with highly eusocial species, our results show that although specific compounds were enhanced in dominant, reproductively active females, a blend of five of these compounds did not inhibit development of the ovaries of female nestmates. Instead, the dominant female had to be physically present to prevent subordinate females from reproducing. Our results are in line with earlier evidence suggesting that fertility-linked compounds in primitively eusocial wasps act only as cues and help to regulate reproduction when used in conjunction with aggressive dominance behaviour, meaning the physical presence of the dominant female. Alternatively, our results support the hypothesis that Queen Pheromones in highly eusocial insects were co-opted from fertility cues that were already present in primitively eusocial ancestors, even when initially, such compounds were merely produced as by-products of ovarian activation, without actually serving to signal reproductive status.
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Conservation of Queen Pheromones Across Two Species of Vespine Wasps.
Journal of chemical ecology, 2016Co-Authors: Jocelyn G Millar, Jelle S Van Zweden, Tom WenseleersAbstract: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.
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biological activity of the enantiomers of 3 methylhentriacontane a Queen pheromone of the ant lasius niger
The Journal of Experimental Biology, 2016Co-Authors: Marine Motais De Narbonne, Jelle S Van Zweden, Tom Wenseleers, Jocelyn G Millar, Jan E Bello, Patrizia DettorreAbstract:Queen Pheromones are essential for regulation of the reproductive division of labor in eusocial insect species. Although only the Queen is able to lay fertilized eggs and produce females, in some cases workers may develop their ovaries and lay male-destined eggs, thus reducing the overall colony efficiency. As long as the Queen is healthy, it is usually in the workers' collective interest to work for the colony and remain sterile. Queens signal their fertility via Pheromones, which may have a primer effect, affecting the physiology of workers, or a releaser effect, influencing worker behavior. The Queen pheromone of the ant Lasius niger was among the first Queen Pheromones of social insects to be identified. Its major component is 3-methylhentriacontane (3-MeC31), which is present in relatively large amounts on the Queen's cuticle and on her eggs. 3-MeC31 regulates worker reproduction by inhibiting ovarian development. Most monomethyl-branched hydrocarbons can exist in two stereoisomeric forms. The correct stereochemistry is fundamental to the activity of most bioactive molecules, but this has rarely been investigated for methyl-branched hydrocarbons. Here, we tested the bioactivity of the (S)- and (R)-enantiomers of 3-MeC31, and found that whereas both enantiomers were effective in suppressing worker ovarian development, (S)-3-MeC31 appeared to be more effective at suppressing aggressive behavior by workers. This suggests that the natural pheromone may be a mixture of the two enantiomers. The enantiomeric ratio produced by Queens remains unknown because of the small amounts of the compound available from each Queen.
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Highly specific responses to Queen pheromone in three Lasius ant species
Behavioral Ecology and Sociobiology, 2016Co-Authors: Luke Holman, Brian Hanley, Jocelyn G MillarAbstract:Queen Pheromones mediate the reproductive division of labor in social insect colonies and provide novel opportunities for investigating the evolution of animal communication. Previous work found that Queens in the ant genus Lasius produce several 3-methylalkanes in greater relative amounts than workers do. At least one of these (3-MeC_31) is a Queen pheromone that regulates worker sterility in two Lasius species, although there are indications that other 3-methylalkanes might also function as Queen Pheromones. Here, we presented workers from three Lasius species with four different 3-methylalkanes, and measured the effect on worker ovary development. In all three species, only 3-MeC_31 showed clear evidence of inhibiting worker fecundity. Our results suggest that worker ants can discriminate homologous hydrocarbons that differ in chain length and only treat specific homologs as Queen Pheromones. These results provide insight into the conflicting selective pressures on cuticular hydrocarbons arising from their multiple roles in signaling and adaptation to the abiotic environment.
Holman Luke - One of the best experts on this subject based on the ideXlab platform.
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Comparative transcriptomics of social insect Queen Pheromones
'Springer Science and Business Media LLC', 2019Co-Authors: Holman Luke, Helanterä Heikki, Trontti Kalevi, Mikheyev, Alexander S.Abstract:Queen Pheromones are chemical signals that mediate reproductive division of labor in eusocial animals. Remarkably, Queen Pheromones are composed of identical or chemically similar compounds in some ants, wasps and bees, even though these taxa diverged >150MYA and evolved Queens and workers independently. Here, we measure the transcriptomic consequences of experimental exposure to Queen Pheromones in workers from two ant and two bee species (genera: Lasius, Apis, Bombus), and test whether they are similar across species. Queen pheromone exposure affected transcription and splicing at many loci. Many genes responded consistently in multiple species, and the set of pheromone-sensitive genes was enriched for functions relating to lipid biosynthesis and transport, olfaction, production of cuticle, oogenesis, and histone (de)acetylation. Pheromone-sensitive genes tend to be evolutionarily ancient, positively selected, peripheral in the gene coexpression network, hypomethylated, and caste-specific in their expression. Our results reveal how Queen Pheromones achieve their effects, and suggest that ants and bees use similar genetic modules to achieve reproductive division of labor
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Comparative transcriptomics of social insect Queen Pheromones
'Springer Science and Business Media LLC', 2019Co-Authors: Holman Luke, Helanterä Heikki, Trontti Kalevi, Mikheyev, Alexander S.Abstract:Queen Pheromones are chemical signals that mediate reproductive division of labor in eusocial animals. Remarkably, Queen Pheromones are composed of identical or chemically similar compounds in some ants, wasps and bees, even though these taxa diverged > 150MYA and evolved Queens and workers independently. Here, we measure the transcriptomic consequences of experimental exposure to Queen Pheromones in workers from two ant and two bee species (genera: Lasius, Apis, Bombus), and test whether they are similar across species. Queen pheromone exposure affected transcription and splicing at many loci. Many genes responded consistently in multiple species, and the set of pheromone-sensitive genes was enriched for functions relating to lipid biosynthesis and transport, olfaction, production of cuticle, oogenesis, and histone (de)acetylation. Pheromone-sensitive genes tend to be evolutionarily ancient, positively selected, peripheral in the gene coexpression network, hypomethylated, and caste-specific in their expression. Our results reveal how Queen Pheromones achieve their effects, and suggest that ants and bees use similar genetic modules to achieve reproductive division of labor.Peer reviewe
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Comparative transcriptomics of social insect Queen Pheromones
'Springer Science and Business Media LLC', 2019Co-Authors: Holman Luke, Helanterä Heikki, Trontti Kalevi, Mikheyev AlexanderAbstract:Queen Pheromones are chemical signals that mediate reproductive division of labor in eusocial animals. Remarkably, Queen Pheromones are composed of identical or chemically similar compounds in some ants, wasps and bees, even though these taxa diverged > 150MYA and evolved Queens and workers independently. Here, we measure the transcriptomic consequences of experimental exposure to Queen Pheromones in workers from two ant and two bee species (genera: Lasius, Apis, Bombus), and test whether they are similar across species. Queen pheromone exposure affected transcription and splicing at many loci. Many genes responded consistently in multiple species, and the set of pheromone-sensitive genes was enriched for functions relating to lipid biosynthesis and transport, olfaction, production of cuticle, oogenesis, and histone (de)acetylation. Pheromone-sensitive genes tend to be evolutionarily ancient, positively selected, peripheral in the gene coexpression network, hypomethylated, and caste-specific in their expression. Our results reveal how Queen Pheromones achieve their effects, and suggest that ants and bees use similar genetic modules to achieve reproductive division of labor.This work received funding from the Research School of Biology at Australian National University to LH; a Discovery Project (DP170100772) to LH and ASM; the Kone Foundation to HH; the Academy of Finland to HH (135970, 127390), and the Center of Excellence in Biological Interactions (284666)
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Queen Pheromones and reproductive division of labor: a meta-analysis
'Oxford University Press (OUP)', 2018Co-Authors: Holman LukeAbstract:Our understanding of chemical communication between social insect Queens and workers has advanced rapidly in recent years. Several studies have identified chemicals produced by Queens and other fertile females that apparently induce sterility in other colony members. However, other experiments produced nonsignificant results, leading some to argue either that earlier reports were mistaken, or that some Queen Pheromones only work in specific contexts. Here, I review the experimental evidence using meta-analysis, and show that there is near-universal support for the hypothesis that fertility-related chemicals cause sterility regardless of context; studies finding otherwise can be explained most parsimoniously as false negatives. Additionally, Queen pheromone experiments that were not performed blind recorded much stronger effect sizes, suggesting bias. I conclude by highlighting several outstanding questions in the field, and by offering recommendations for future studies
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Conserved Queen Pheromones in bumblebees: A reply to Amsalem et al
'PeerJ', 2017Co-Authors: Holman Luke, Caliari Oliveira Ricardo, Van Oystaeyen Annette, Van Zweden Jelle, Wenseleers TomAbstract:In a recent study, Amsalem, Orlova & Grozinger (2015) performed experiments with Bombus impatiens bumblebees 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 in B. 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 C25 substantially reduced and delayed worker egg laying in B. impatiens. We review the evidence that cuticular hydrocarbons act as Queen Pheromones, and offer some recommendations for future Queen pheromone experiments.status: publishe
