Queen pheromones modulate DNA methyltransferase activity in bee and ant workers.
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ABSTRACT:
SUBMITTER: Holman L
PROVIDER: S-EPMC4785935 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Several insect pheromones are multifunctional and have both releaser and primer effects. In honey bees (Apis mellifera), the queen mandibular pheromone (QMP) and e-beta-ocimene (eβ), emitted by young worker larvae, have such dual effects. There is increasing evidence that these multifunctional pheromones profoundly shape honey bee colony dynamics by influencing cooperative brood care, a fundamental aspect of eusocial insect behavior. Both QMP and eβ have been shown to affect worker physiology and behavior, but it has not yet been determined if these two key pheromones have interactive effects on hypopharyngeal gland (HPG) development, actively used in caring of larvae, and ovary activation, a component of worker reproductive physiology. Experimental results demonstrate that both QMP and eβ significantly suppress ovary activation compared to controls but that the larval pheromone is more effective than QMP. The underlying reproductive anatomy (total ovarioles) of workers influenced HPG development and ovary activation, so that worker bees with more ovarioles were less responsive to suppression of ovary activation by QMP. These bees were more likely to develop their HPG and have activated ovaries in the presence of eβ, providing additional links between nursing and reproductive physiology in support of the reproductive ground plan hypothesis.
| S-EPMC4220115 | biostudies-literature
Project description:Polygyny in social insects can greatly reduce within-nest genetic relatedness. In polygynous ant species, potential rival queens in colonies with multiple queens are often executed by other queens, workers, or both. The Argentine ant, Linepithema humile, native to South America, forms a "supercolony" that is composed of a large number of nests and is considered to contribute to the ant's invasion success. Currently, four mutually antagonistic supercolonies are contiguously distributed within a small area of Japan. Here, we analyzed the genetic structure and relatedness within and among the four supercolonies using microsatellite markers to clarify how L. humile maintains its supercoloniality. The results of AMOVA and BASP, the F ST values, and the existence of several private alleles indicated that the L. humile population in the Kobe area had a characteristic genetic structure. Within a given supercolony, there was significant genetic differentiation (F ST) among workers collected in May and those collected in September. The significant deviation from Hardy-Weinberg equilibrium increased, and the relatedness among workers significantly increased from May to September in all supercolonies. This result suggested that the supercolonies replaced old queens with new ones during the reproductive season, thus supporting the plausibility of queen execution. From the perspective of kin selection, workers collectively eliminate queens, thereby increasing their own inclusive fitness. Restricted gene flow among supercolonies, together with mating with sib and queen execution, could help to maintain the unique social structure of L. humile, the distribution of which is expanding worldwide.
| S-EPMC4588641 | biostudies-other
Project description: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.
| S-EPMC6453924 | biostudies-literature
Project description:We used RNA-se to compare gene expression patterns in workers of the bumble bee Bombus impatiens in response to the queen, the brood, both or none.
2022-02-13 | GSE196471 | GEO
Project description:BACKGROUND:The division of reproductive labor among group members in insect societies is regulated by "queen pheromones". However, it remains controversial whether these are manipulative, i.e., actively suppress worker reproduction, or honestly signal the fertility status of the queen to which workers react in their own interest by refraining from laying eggs. Manipulative queen control is thought to lead to an evolutionary arms race between queens and workers, resulting in complex queen bouquets that diverge strongly among different populations and species. In contrast, honest signals would evolve more slowly and might therefore differ less strongly within and among species. RESULTS:We aimed at determining the tempo of the evolution of queen signals in two ways. First, we investigated whether queens of Temnothorax ants are capable of controlling egg laying by workers of their own, closely, and distantly related species. Second, we compared the species- and caste-specific patterns of cuticular hydrocarbons, which are assumed to convey information on reproductive status. In mixed-species colonies, queens were not able to fully suppress egg-laying and male production by workers of unrelated species, while workers did not reproduce under the influence of a queen from their own species. Furthermore, the chemical profiles differed more strongly among queens of different species than among the respective workers. CONCLUSIONS:Our results suggest that cuticular hydrocarbons associated with fecundity are not fully conserved in evolution and evolve slightly faster than worker-specific components in the blend of cuticular hydrocarbons. While this higher rate of evolution might reflect an arms race between queens and workers, the observation that workers still respond to the presence of a queen from another species support the honest signal hypothesis. Future studies need to examine alternative explanations for a higher rate of evolution of queen-specific substances, such as an involvement of such compounds in mating.
| S-EPMC3060118 | biostudies-literature
Project description:Trait-mediated indirect interactions (TMII) can be as important as density-mediated indirect interactions. Here, we provide evidence for a novel trait-mediated cascade (where one TMII affects another TMII) and demonstrate that the mechanism consists of a predator eavesdropping on chemical signaling. Ants protect scale insects from predation by adult coccinellid beetles - the first TMII. However, parasitic phorid flies reduce ant foraging activity by 50% - the second TMII, providing a window of opportunity for female beetles to oviposit in high-quality microsites. Beetle larvae are protected from ant predation and benefit from living in patches with high scale densities. We demonstrate that female beetles can detect pheromones released by the ant when attacked by phorids, and that only females, and especially gravid females, are attracted to the ant pheromone. As ants reduce their movement when under attack by phorids, we conclude that phorids facilitate beetle oviposition, thus producing the TMII cascade.
| S-EPMC3488669 | biostudies-literature
Project description: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.
| S-EPMC5436554 | biostudies-literature
Project description:There are many differences in external morphology and internal physiology between the Apis mellifera queen bee and worker bee, some of which are relevant to beekeeping production. These include reproductive traits, body size, royal jelly secreting properties, and visual system development, among others. The identification of candidate genes that control the differentiation of these traits is critical for selective honeybee breeding programs. In this study, we compared the genomic methylation of queen bee and worker bee larvae at 3, 4, and 5 days of age by whole-genome bisulfite sequencing, and found that the basic characteristics of genomic methylation in queen and worker larvae were the same. There were approximately 49 million cytosines in the Apis larvae genome, of which about 90,000 were methylated. Methylated CpG sites accounted for 99% of the methylated cytosines, and methylation mainly occurred in exons. However, methylation levels of queen and worker larvae showed different trends with age: the methylation level of queen larvae varied with age in an inverted parabola, while the corresponding trend for worker larvae with resembled an exponential curve with a platform. The methylation level of queen larvae was higher than that of worker larvae at 3 days of age, lower than that of worker larvae at 4 days of age, and similar to that of worker larvae at 5 days old. The top 10 differentially methylated genes (DMGs) and 13 caste-specific methylated genes were listed, and correlations with caste determination were speculated. We additionally screened 38 DMGs between queen larvae and worker larvae involved in specific organ differentiation as well as reproduction, morphology, and vision differentiation during caste determination. These genes are potential molecular markers for selective breeding of A. mellifera to improve fecundity, royal jelly production, body size, and foraging, and represent candidate genes for investigating specialized functional segregation during the process of caste differentiation.
| S-EPMC7438783 | biostudies-literature
Project description: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.
| S-EPMC6599994 | biostudies-literature
Project description:Mating has profound effects on the physiology and behavior of female insects, and in honey bee (Apis mellifera) queens, these changes are permanent. Queens mate with multiple males during a brief period in their early adult lives, and shortly thereafter they initiate egg-laying. Furthermore, the pheromone profiles of mated queens differ from those of virgins, and these pheromones regulate many different aspects of worker behavior and colony organization. While it is clear that mating causes dramatic changes in queens, it is unclear if mating number has more subtle effects on queen physiology or queen-worker interactions; indeed, the effect of multiple matings on female insect physiology has not been broadly addressed. Because it is not possible to control the natural mating behavior of queens, we used instrumental insemination and compared queens inseminated with semen from either a single drone (single-drone inseminated, or SDI) or 10 drones (multi-drone inseminated, or MDI). We used observation hives to monitor attraction of workers to SDI or MDI queens in colonies, and cage studies to monitor the attraction of workers to virgin, SDI, and MDI queen mandibular gland extracts (the main source of queen pheromone). The chemical profiles of the mandibular glands of virgin, SDI, and MDI queens were characterized using GC-MS. Finally, we measured brain expression levels in SDI and MDI queens of a gene associated with phototaxis in worker honey bees (Amfor). Here, we demonstrate for the first time that insemination quantity significantly affects mandibular gland chemical profiles, queen-worker interactions, and brain gene expression. Further research will be necessary to elucidate the mechanistic bases for these effects: insemination volume, sperm and seminal protein quantity, and genetic diversity of the sperm may all be important factors contributing to this profound change in honey bee queen physiology, queen behavior, and social interactions in the colony.
| S-EPMC1989138 | biostudies-literature