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1.  Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus) 
BMC Genomics  2014;15:75.
In social groups, dominant individuals may socially inhibit reproduction of subordinates using aggressive interactions or, in the case of highly eusocial insects, pheromonal communication. It has been hypothesized these two modes of reproductive inhibition utilize conserved pathways. Here, we use a comparative framework to investigate the chemical and genomic underpinnings of reproductive dominance in the primitively eusocial wasp Polistes metricus. Our goals were to first characterize transcriptomic and chemical correlates of reproductive dominance and second, to test whether dominance-associated mechanisms in paper wasps overlapped with aggression or pheromone-related gene expression patterns in other species. To explore whether conserved molecular pathways relate to dominance, we compared wasp transcriptomic data to previous studies of gene expression associated with pheromonal communication and queen-worker differences in honey bees, and aggressive behavior in bees, Drosophila, and mice.
By examining dominant and subordinate females from queen and worker castes in early and late season colonies, we found that cuticular hydrocarbon profiles and genome-wide patterns of brain gene expression were primarily associated with season/social environment rather than dominance status. In contrast, gene expression patterns in the ovaries were associated primarily with caste and ovary activation. Comparative analyses suggest genes identified as differentially expressed in wasp brains are not related to queen pheromonal communication or caste in bees, but were significantly more likely to be associated with aggression in other insects (bees, flies), and even a mammal (mice).
This study provides the first comprehensive chemical and molecular analysis of reproductive dominance in paper wasps. We found little evidence for a chemical basis for reproductive dominance in P. metricus, and our transcriptomic analyses suggest that different pathways regulate dominance in paper wasps and pheromone response in bees. Furthermore, there was a substantial impact of season/social environment on gene expression patterns, indicating the important role of external cues in shaping the molecular processes regulating behavior. Interestingly, genes associated with dominance in wasps were also associated with aggressive behavior in bees, solitary insects and mammals. Thus, genes involved in social regulation of reproduction in Polistes may have conserved functions associated with aggression in insects and other taxa.
PMCID: PMC3922164  PMID: 24472515
Wasps; Social behavior; Genomics; Aggression; Pheromones; Chemical communication
2.  Inclusive fitness theory and eusociality 
Abbot, Patrick | Abe, Jun | Alcock, John | Alizon, Samuel | Alpedrinha, Joao A. C. | Andersson, Malte | Andre, Jean-Baptiste | van Baalen, Minus | Balloux, Francois | Balshine, Sigal | Barton, Nick | Beukeboom, Leo W. | Biernaskie, Jay M. | Bilde, Trine | Borgia, Gerald | Breed, Michael | Brown, Sam | Bshary, Redouan | Buckling, Angus | Burley, Nancy T. | Burton-Chellew, Max N. | Cant, Michael A. | Chapuisat, Michel | Charnov, Eric L. | Clutton-Brock, Tim | Cockburn, Andrew | Cole, Blaine J. | Colegrave, Nick | Cosmides, Leda | Couzin, Iain D. | Coyne, Jerry A. | Creel, Scott | Crespi, Bernard | Curry, Robert L. | Dall, Sasha R. X. | Day, Troy | Dickinson, Janis L. | Dugatkin, Lee Alan | El Mouden, Claire | Emlen, Stephen T. | Evans, Jay | Ferriere, Regis | Field, Jeremy | Foitzik, Susanne | Foster, Kevin | Foster, William A. | Fox, Charles W. | Gadau, Juergen | Gandon, Sylvain | Gardner, Andy | Gardner, Michael G. | Getty, Thomas | Goodisman, Michael A. D. | Grafen, Alan | Grosberg, Rick | Grozinger, Christina M. | Gouyon, Pierre-Henri | Gwynne, Darryl | Harvey, Paul H. | Hatchwell, Ben J. | Heinze, Jürgen | Helantera, Heikki | Helms, Ken R. | Hill, Kim | Jiricny, Natalie | Johnstone, Rufus A. | Kacelnik, Alex | Kiers, E. Toby | Kokko, Hanna | Komdeur, Jan | Korb, Judith | Kronauer, Daniel | Kümmerli, Rolf | Lehmann, Laurent | Linksvayer, Timothy A. | Lion, Sébastien | Lyon, Bruce | Marshall, James A. R. | McElreath, Richard | Michalakis, Yannis | Michod, Richard E. | Mock, Douglas | Monnin, Thibaud | Montgomerie, Robert | Moore, Allen J. | Mueller, Ulrich G. | Noë, Ronald | Okasha, Samir | Pamilo, Pekka | Parker, Geoff A. | Pedersen, Jes S. | Pen, Ido | Pfennig, David | Queller, David C. | Rankin, Daniel J. | Reece, Sarah E. | Reeve, Hudson K. | Reuter, Max | Roberts, Gilbert | Robson, Simon K. A. | Roze, Denis | Rousset, Francois | Rueppell, Olav | Sachs, Joel L. | Santorelli, Lorenzo | Schmid-Hempel, Paul | Schwarz, Michael P. | Scott-Phillips, Tom | Shellmann-Sherman, Janet | Sherman, Paul W. | Shuker, David M. | Smith, Jeff | Spagna, Joseph C. | Strassmann, Beverly | Suarez, Andrew V. | Sundström, Liselotte | Taborsky, Michael | Taylor, Peter | Thompson, Graham | Tooby, John | Tsutsui, Neil D. | Tsuji, Kazuki | Turillazzi, Stefano | Úbeda, Francisco | Vargo, Edward L. | Voelkl, Bernard | Wenseleers, Tom | West, Stuart A. | West-Eberhard, Mary Jane | Westneat, David F. | Wiernasz, Diane C. | Wild, Geoff | Wrangham, Richard | Young, Andrew J. | Zeh, David W. | Zeh, Jeanne A. | Zink, Andrew
Nature  2011;471(7339):10.1038/nature09831.
PMCID: PMC3836173  PMID: 21430721
3.  Chronic parasitization by Nosema microsporidia causes global expression changes in core nutritional, metabolic and behavioral pathways in honey bee workers (Apis mellifera) 
BMC Genomics  2013;14(1):799.
Chronic infections can profoundly affect the physiology, behavior, fitness and longevity of individuals, and may alter the organization and demography of social groups. Nosema apis and Nosema ceranae are two microsporidian parasites which chronically infect the digestive tract of honey bees (Apis mellifera). These parasites, in addition to other stressors, have been linked to increased mortality of individual workers and colony losses in this key pollinator species. Physiologically, Nosema infection damages midgut tissue, is energetically expensive and alters expression of immune genes in worker honey bees. Infection also accelerates worker transition from nursing to foraging behavior (termed behavioral maturation). Here, using microarrays, we characterized global gene expression patterns in adult worker honey bee midgut and fat body tissue in response to Nosema infection.
Our results indicate that N. apis infection in young workers (1 and 2 days old) disrupts midgut development. At 2 and 7 days post-infection in the fat body tissue, N. apis drives metabolic changes consistent with energetic costs of infection. A final experiment characterizing gene expression in the fat bodies of 14 day old workers parasitized with N. apis and N. ceranae demonstrated that Nosema co-infection specifically alters conserved nutritional, metabolic and hormonal pathways, including the insulin signaling pathway, which is also linked to behavioral maturation in workers. Interestingly, in all experiments, Nosema infection did not appear to significantly regulate overall expression of canonical immune response genes, but infection did alter expression of acute immune response genes identified in a previous study. Comparative analyses suggest that changes in nutritional/metabolic processes precede changes in behavioral maturation and immune processes.
These genome-wide studies of expression patterns can help us disentangle the direct and indirect effects of chronic infection, and understand the molecular pathways that regulate disease symptoms.
Electronic supplementary material
The online version of this article (doi:10.1186/1471-2164-14-799) contains supplementary material, which is available to authorized users.
PMCID: PMC4046765  PMID: 24245482
Nosema; Honey bee; Behavioral maturation; Insulin signaling pathway; Innate immunity; Chronic parasite; Nutrition; Genomics; Stress
4.  Chemical Profiles of Two Pheromone Glands Are Differentially Regulated by Distinct Mating Factors in Honey Bee Queens (Apis mellifera L.) 
PLoS ONE  2013;8(11):e78637.
Pheromones mediate social interactions among individuals in a wide variety of species, from yeast to mammals. In social insects such as honey bees, pheromone communication systems can be extraordinarily complex and serve to coordinate behaviors among many individuals. One of the primary mediators of social behavior and organization in honey bee colonies is queen pheromone, which is produced by multiple glands. The types and quantities of chemicals produced differ significantly between virgin and mated queens, and recent studies have suggested that, in newly mated queens, insemination volume or quantity can affect pheromone production. Here, we examine the long-term impact of different factors involved during queen insemination on the chemical composition of the mandibular and Dufour's glands, two of the major sources of queen pheromone. Our results demonstrate that carbon dioxide (an anesthetic used in instrumental insemination), physical manipulation of genital tract (presumably mimicking the act of copulation), insemination substance (saline vs. semen), and insemination volume (1 vs. 8 µl) all have long-term effects on mandibular gland chemical profiles. In contrast, Dufour's gland chemical profiles were changed only upon insemination and were not influenced by exposure to carbon dioxide, manipulation, insemination substance or volume. These results suggest that the chemical contents of these two glands are regulated by different neuro-physiological mechanisms. Furthermore, workers responded differently to the different mandibular gland extracts in a choice assay. Although these studies must be validated in naturally mated queens of varying mating quality, our results suggest that while the chemical composition of Dufour's gland is associated with mating status, that of the mandibular glands is associated with both mating status and insemination success. Thus, the queen appears to be signaling both status and reproductive quality to the workers, which may impact worker behavior and physiology as well as social organization and productivity of the colony.
PMCID: PMC3827242  PMID: 24236028
5.  Sociogenomics of Cooperation and Conflict during Colony Founding in the Fire Ant Solenopsis invicta 
PLoS Genetics  2013;9(8):e1003633.
One of the fundamental questions in biology is how cooperative and altruistic behaviors evolved. The majority of studies seeking to identify the genes regulating these behaviors have been performed in systems where behavioral and physiological differences are relatively fixed, such as in the honey bee. During colony founding in the monogyne (one queen per colony) social form of the fire ant Solenopsis invicta, newly-mated queens may start new colonies either individually (haplometrosis) or in groups (pleometrosis). However, only one queen (the “winner”) in pleometrotic associations survives and takes the lead of the young colony while the others (the “losers”) are executed. Thus, colony founding in fire ants provides an excellent system in which to examine the genes underpinning cooperative behavior and how the social environment shapes the expression of these genes. We developed a new whole genome microarray platform for S. invicta to characterize the gene expression patterns associated with colony founding behavior. First, we compared haplometrotic queens, pleometrotic winners and pleometrotic losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social ranks of the two cofoundresses. Haplometrotic and pleometrotic queens differed in the expression of genes involved in stress response, aging, immunity, reproduction and lipid biosynthesis. Smaller sets of genes were differentially expressed between winners and losers. In the second experiment, switching social rank had a much greater impact on gene expression patterns than the initial/final rank. Expression differences for several candidate genes involved in key biological processes were confirmed using qRT-PCR. Our findings indicate that, in S. invicta, social environment plays a major role in the determination of the patterns of gene expression, while the queen's physiological state is secondary. These results highlight the powerful influence of social environment on regulation of the genomic state, physiology and ultimately, social behavior of animals.
Author Summary
The characterization of the genomic basis for complex behaviors is one of the major goals of biological research. The genomic state of an individual results from the interplay between its internal condition (the “nature”) and the external environment (the “nurture”), which may include the social environment. Colony founding in the fire ant Solenopsis invicta is a complex process that serves as a useful model for investigating how the interplay between genes and social environment shapes social behavior. Unrelated, newly mated S. invicta queens may start a new colony as a group, but ultimately only one queen will survive and gain full reproductive dominance. By uncovering the genetic basis for founding behavior in fire ants we therefore provide useful insights into how cooperative behavior evolved in a context that might be considered primitively eusocial, because newly mated queens in a founding association are morphologically, physiologically and genetically very similar and display no evident division of labor. Our results suggest that social environment (founding singly or in pairs, switching dominance rank vs. maintaining rank) is a much greater driver of gene expression changes than social rank itself, suggesting that social environment, and not reproductive state, is a key regulator of gene expression, physiology and ultimately, behavior.
PMCID: PMC3738511  PMID: 23950725
6.  cGMP modulates responses to queen mandibular pheromone in worker honey bees 
Responses to social cues, such as pheromones, can be modified by genotype, physiology, or environmental context. Honey bee queens produce a pheromone (queen mandibular pheromone; QMP) which regulates aspects of worker bee behavior and physiology. Forager bees are less responsive to QMP than young bees engaged in brood care, suggesting that physiological changes associated with behavioral maturation modulate response to this pheromone. Since 3′, 5′-cyclic guanosine monophosphate (cGMP) is a major regulator of behavioral maturation in workers, we examined its role in modulating worker responses to QMP. Treatment with a cGMP analog resulted in significant reductions in both behavioral and physiological responses to QMP in young caged workers. Treatment significantly reduced attraction to QMP and inhibited the QMP-mediated increase in vitellogenin RNA levels in the fat bodies of worker bees. Genome-wide analysis of brain gene expression patterns demonstrated that cGMP has a larger effect on expression levels than QMP, and that QMP has specific effects in the presence of cGMP, suggesting that some responses to QMP may be dependent on an individual bees' physiological state. Our data suggest that cGMP-mediated processes play a role in modulating responses to QMP in honey bees at the behavioral, physiological, and molecular levels.
PMCID: PMC3705726  PMID: 21626397
behavioral genetics; neuroethology; honey bees; pheromone; communication
7.  Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera) 
BMC Genomics  2012;13:558.
Social insects, such as honey bees, use molecular, physiological and behavioral responses to combat pathogens and parasites. The honey bee genome contains all of the canonical insect immune response pathways, and several studies have demonstrated that pathogens can activate expression of immune effectors. Honey bees also use behavioral responses, termed social immunity, to collectively defend their hives from pathogens and parasites. These responses include hygienic behavior (where workers remove diseased brood) and allo-grooming (where workers remove ectoparasites from nestmates). We have previously demonstrated that immunostimulation causes changes in the cuticular hydrocarbon profiles of workers, which results in altered worker-worker social interactions. Thus, cuticular hydrocarbons may enable workers to identify sick nestmates, and adjust their behavior in response. Here, we test the specificity of behavioral, chemical and genomic responses to immunostimulation by challenging workers with a panel of different immune stimulants (saline, Sephadex beads and Gram-negative bacteria E. coli).
While only bacteria-injected bees elicited altered behavioral responses from healthy nestmates compared to controls, all treatments resulted in significant changes in cuticular hydrocarbon profiles. Immunostimulation caused significant changes in expression of hundreds of genes, the majority of which have not been identified as members of the canonical immune response pathways. Furthermore, several new candidate genes that may play a role in cuticular hydrocarbon biosynthesis were identified. Effects of immune challenge expression of several genes involved in immune response, cuticular hydrocarbon biosynthesis, and the Notch signaling pathway were confirmed using quantitative real-time PCR. Finally, we identified common genes regulated by pathogen challenge in honey bees and other insects.
These results demonstrate that honey bee genomic responses to immunostimulation are substantially broader than the previously identified canonical immune response pathways, and may mediate the behavioral changes associated with social immunity by orchestrating changes in chemical signaling. These studies lay the groundwork for future research into the genomic responses of honey bees to native honey bee parasites and pathogens.
PMCID: PMC3483235  PMID: 23072398
Honey bees; Immunity; Genomics; Social behavior; Social immunity; Chemical ecology; Cuticular hydrocarbons; Nestmate recognition
8.  Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera 
BMC Genomics  2010;11:602.
The ectoparasitic mite Varroa destructor has emerged as the primary pest of domestic honey bees (Apis mellifera). Here we present an initial survey of the V. destructor genome carried out to advance our understanding of Varroa biology and to identify new avenues for mite control. This sequence survey provides immediate resources for molecular and population-genetic analyses of Varroa-Apis interactions and defines the challenges ahead for a comprehensive Varroa genome project.
The genome size was estimated by flow cytometry to be 565 Mbp, larger than most sequenced insects but modest relative to some other Acari. Genomic DNA pooled from ~1,000 mites was sequenced to 4.3× coverage with 454 pyrosequencing. The 2.4 Gbp of sequencing reads were assembled into 184,094 contigs with an N50 of 2,262 bp, totaling 294 Mbp of sequence after filtering. Genic sequences with homology to other eukaryotic genomes were identified on 13,031 of these contigs, totaling 31.3 Mbp. Alignment of protein sequence blocks conserved among V. destructor and four other arthropod genomes indicated a higher level of sequence divergence within this mite lineage relative to the tick Ixodes scapularis. A number of microbes potentially associated with V. destructor were identified in the sequence survey, including ~300 Kbp of sequence deriving from one or more bacterial species of the Actinomycetales. The presence of this bacterium was confirmed in individual mites by PCR assay, but varied significantly by age and sex of mites. Fragments of a novel virus related to the Baculoviridae were also identified in the survey. The rate of single nucleotide polymorphisms (SNPs) in the pooled mites was estimated to be 6.2 × 10-5per bp, a low rate consistent with the historical demography and life history of the species.
This survey has provided general tools for the research community and novel directions for investigating the biology and control of Varroa mites. Ongoing development of Varroa genomic resources will be a boon for comparative genomics of under-represented arthropods, and will further enhance the honey bee and its associated pathogens as a model system for studying host-pathogen interactions.
PMCID: PMC3091747  PMID: 20973996
9.  Queen reproductive state modulates pheromone production and queen-worker interactions in honeybees 
Behavioral Ecology  2009;20(5):1007-1014.
The mandibular glands of queen honeybees produce a pheromone that modulates many aspects of worker honeybee physiology and behavior and is critical for colony social organization. The exact chemical blend produced by the queen differs between virgin and mated, laying queens. Here, we investigate the role of mating and reproductive state on queen pheromone production and worker responses. Virgin queens, naturally mated queens, and queens instrumentally inseminated with either semen or saline were collected 2 days after mating or insemination. Naturally mated queens had the most activated ovaries and the most distinct chemical profile in their mandibular glands. Instrumentally inseminated queens were intermediate between virgins and naturally mated queens for both ovary activation and chemical profiles. There were no significant differences between semen- and saline-inseminated queens. Workers were preferentially attracted to the mandibular gland extracts from queens with significantly more activated ovaries. These studies suggest that the queen pheromone blend is modulated by the reproductive status of the queens, and workers can detect these subtle differences and are more responsive to queens with higher reproductive potential. Furthermore, it appears as if insemination substance does not strongly affect physiological characteristics of honeybee queens 2 days after insemination, suggesting that the insemination process or volume is responsible for stimulating these early postmating changes in honeybee queens.
PMCID: PMC2744121  PMID: 22476212
behavior; caste; chemical communication; pheromone; reproduction; social insect
10.  The transcription factor Krüppel homolog 1 is linked to hormone mediated social organization in bees 
Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Honey bee and bumble bee colonies consist of a single reproductive queen and facultatively sterile workers. The queens' influences on the workers are mediated largely via inhibition of juvenile hormone titers, which affect division of labor in honey bees and worker reproduction in bumble bees. Studies in honey bees identified a transcription factor, Krüppel-homolog 1 (Kr-h1), whose expression in worker brains is significantly downregulated in the presence of a queen or queen pheromone and higher in forager bees, making this gene an ideal candidate for examining the evolutionary conservation of socially regulated pathways in Hymenoptera.
In contrast to honey bees, bumble bees foragers do not have higher Kr-h1 levels relative to nurses: in one of three colonies levels were similar in nurses and foragers, and in two colonies levels were higher in nurses. Similarly to honey bees, brain Kr-h1 levels were significantly downregulated in the presence versus absence of a queen. Furthermore, in small queenless groups, Kr-h1 levels were downregulated in subordinate workers with undeveloped ovaries relative to dominant individuals with active ovaries. Brain Kr-h1 levels were upregulated by juvenile hormone treatment relative to a vehicle control. Finally, phylogenetic analysis indicates that KR-H1 orthologs are presence across insect orders. Though this protein is highly conserved between honey bees and bumble bees, there are significant differences between orthologs of insects from different orders.
Our results suggest that Kr-h1 is associated with juvenile hormone mediated regulation of reproduction in bumble bees. The expression of this transcription factor is inhibited by the queen and associated with endocrine mediated regulation of social organization in two species of bees. Thus, KR-H1 may transcriptionally regulate a conserved genetic module that is part of a pathway that has been co-opted to function in social behavior, and adjusts the behavior of workers to their social environmental context.
PMCID: PMC2876159  PMID: 20429952
11.  Individual Variation in Pheromone Response Correlates with Reproductive Traits and Brain Gene Expression in Worker Honey Bees 
PLoS ONE  2010;5(2):e9116.
Variation in individual behavior within social groups can affect the fitness of the group as well as the individual, and can be caused by a combination of genetic and environmental factors. However, the molecular factors associated with individual variation in social behavior remain relatively unexplored. We used honey bees (Apis mellifera) as a model to examine differences in socially-regulated behavior among individual workers, and used transcriptional profiling to determine if specific gene expression patterns are associated with these individual differences. In honey bees, the reproductive queen produces a pheromonal signal that regulates many aspects of worker behavior and physiology and maintains colony organization.
Methodology/Principal Findings
Here, we demonstrate that there is substantial natural variation in individual worker attraction to queen pheromone (QMP). Furthermore, worker attraction is negatively correlated with ovariole number—a trait associated with reproductive potential in workers. We identified transcriptional differences in the adult brain associated with individual worker attraction to QMP, and identified hundreds of transcripts that are organized into statistically-correlated gene networks and associated with this response.
Our studies demonstrate that there is substantial variation in worker attraction to QMP among individuals, and that this variation is linked with specific differences in physiology and brain gene expression patterns. This variation in individual response thresholds may reveal underlying variation in queen-worker reproductive conflict, and may mediate colony function and productivity by creating variation in individual task performance.
PMCID: PMC2817734  PMID: 20161742
12.  Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera) 
BMC Genomics  2008;9:232.
The molecular mechanisms underlying the post-mating behavioral and physiological transitions undergone by females have not been explored in great detail. Honey bees represent an excellent model system in which to address these questions because they exhibit a range of "mating states," with two extremes (virgins and egg-laying, mated queens) that differ dramatically in their behavior, pheromone profiles, and physiology. We used an incompletely-mated mating-state to understand the molecular processes that underlie the transition from a virgin to a mated, egg-laying queen. We used same-aged virgins, queens that mated once but did not initiate egg-laying, and queens that mated once and initiated egg-laying.
Differences in the behavior and physiology among groups correlated with the underlying variance observed in the top 50 predictive genes in the brains and the ovaries. These changes were correlated with either a behaviorally-associated pattern or a physiologically-associated pattern. Overall, these results suggest that the brains and the ovaries of queens are uncoupled or follow different timescales; the initiation of mating triggers immediate changes in the ovaries, while changes in the brain may require additional stimuli or take a longer time to complete. Comparison of our results to previous studies of post-mating changes in Drosophila melanogaster identified common biological processes affected by mating, including stress response and alternative-splicing pathways. Comparison with microarray data sets related to worker behavior revealed no obvious correlation between genes regulated by mating and genes regulated by behavior/physiology in workers.
Studying the underlying molecular mechanisms of post-mating changes in honey bee queens will not only give us insight into how molecular mechanisms regulate physiological and behavioral changes, but they may also lead to important insights into the evolution of social behavior. Post-mating changes in gene regulation in the brains and ovaries of honey bee queens appear to be triggered by different stimuli and may occur on different timescales, potentially allowing changes in the brains and the ovaries to be uncoupled.
PMCID: PMC2413142  PMID: 18489784
13.  Effects of Insemination Quantity on Honey Bee Queen Physiology 
PLoS ONE  2007;2(10):e980.
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.
PMCID: PMC1989138  PMID: 17912357

Results 1-13 (13)