Open Access Research

© 2010 Maisonnasse et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Research New insights into honey bee (Apis mellifera) pheromone communication. Is the queen mandibular pheromone alone in colony regulation? Abstract Background: In social insects, the queen is essential to the functioning and homeostasis of the colony. This influence has been demonstrated to be mediated through pheromone communication. However, the only social insect for which any queen pheromone has been identified is the honey bee (Apis mellifera) with its well-known queen mandibular pheromone (QMP). Although pleiotropic effects on colony regulation are accredited to the QMP, this pheromone does not trigger the full behavioral and physiological response observed in the presence of the queen, suggesting the presence of additional compounds. We tested the hypothesis of a pheromone redundancy in honey bee queens by comparing the influence of queens with and without mandibular glands on worker behavior and physiology. Results: Demandibulated queens had no detectable (E)-9-oxodec-2-enoic acid (9-ODA), the major compound in QMP, yet they controlled worker behavior (cell construction and queen retinue) and physiology (ovary inhibition) as efficiently as intact queens. Conclusions: We demonstrated that the queen uses other pheromones as powerful as QMP to control the colony. It follows that queens appear to have multiple active compounds with similar functions in the colony (pheromone redundancy). Our findings support two hypotheses in the biology of social insects: (1) that multiple semiochemicals with synonymous meaning exist in the honey bee, (2) that this extensive semiochemical vocabulary exists because it confers an evolutionary advantage to the colony. Background A remarkable trait of social insect colonies is the assemblage of individuals into a coherent social unit. Members of the society exhibit an organization mainly controlled by a complex pheromonal language [1]. Behavioral evidence for division of reproduction and labor in the colony indicates the importance of pheromones in both queen-worker and worker-worker interactions, including mediating the regulation of task allocation [2]. In the case of honey bees, coordination of the different tasks is partly mediated by chemical signals [2]. In social insects phero

[1]  E. Plettner,et al.  A scientific note on E-β-ocimene, a new volatile primer pheromone that inhibits worker ovary development in honey bees , 2009, Apidologie.

[2]  Sarah D. Kocher,et al.  Queen reproductive state modulates pheromone production and queen-worker interactions in honeybees. , 2009, Behavioral ecology : official journal of the International Society for Behavioral Ecology.

[3]  J. Heinze,et al.  Honest and dishonest communication in social Hymenoptera , 2009, Journal of Experimental Biology.

[4]  Sarah D. Kocher,et al.  Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera) , 2008, BMC Genomics.

[5]  C. Grozinger,et al.  Pheromonal regulation of starvation resistance in honey bee workers (Apis mellifera) , 2008, Naturwissenschaften.

[6]  R. Moritz,et al.  The role of the queen mandibular gland pheromone in honeybees (Apis mellifera): honest signal or suppressive agent? , 2008, Behavioral Ecology and Sociobiology.

[7]  Henry S. Pollock,et al.  Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies , 2008, Proceedings of the National Academy of Sciences.

[8]  A. Mercer,et al.  Queen Pheromone Blocks Aversive Learning in Young Worker Bees , 2007, Science.

[9]  C. Pirk,et al.  Pheromonal dominance and the selection of a socially parasitic honeybee worker lineage (Apis mellifera capensis Esch.) , 2007, Journal of evolutionary biology.

[10]  R. E. Page,et al.  The Gene vitellogenin Has Multiple Coordinating Effects on Social Organization , 2007, PLoS biology.

[11]  S. Härtel,et al.  Social parasitism by honeybee workers (Apis mellifera capensis Esch.): evidence for pheromonal resistance to host queen’s signals , 2006, Behavioral Ecology and Sociobiology.

[12]  G. DeGrandi-Hoffman,et al.  Volatile compounds emitted by live European honey bee (Apis mellifera L.) queens. , 2006, Journal of insect physiology.

[13]  Mark L. Winston,et al.  Pheromone Communication in the Honeybee (Apis mellifera L.) , 2005, Journal of Chemical Ecology.

[14]  C. Keeling,et al.  A scientific note on the aliphatic esters in queen honey bees , 2005 .

[15]  R. Boulay,et al.  Queen–signal modulation of worker pheromonal composition in honeybees , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[16]  Mark L. Winston,et al.  The effect of queen pheromones on worker honey bee ovary development , 2003, Naturwissenschaften.

[17]  M. Winston,et al.  New components of the honey bee (Apis mellifera L.) queen retinue pheromone , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[18]  F. Ratnieks,et al.  Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing , 2002, Nature.

[19]  R. Moritz,et al.  The ontogenetic pattern of mandibular gland components in queenless worker bees (Apis mellifera capensis Esch.). , 2001, Journal of insect physiology.

[20]  V. Soroker,et al.  Dufour's gland secretion of the queen honeybee (Apis mellifera): an egg discriminator pheromone or a queen signal? , 2001, Behavioral Ecology and Sociobiology.

[21]  M. Winston,et al.  Queen and pheromonal factors influencing comb construction by simulated honey bee (Apis mellifera L.) swarms , 2001, Insectes Sociaux.

[22]  H. Hepburn,et al.  Modes of worker reproduction, reproductive dominance and brood cell construction in queenless honeybee (Apis mellifera L.) colonies , 2000 .

[23]  R. Currie,et al.  Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.) , 2000 .

[24]  R. Crewe,et al.  The Releaser Effects of the Tergal Gland Secretion of Queen Honeybees (Apis mellifera) , 1999, Journal of Insect Behavior.

[25]  Y. Le Conte,et al.  Effect of Aliphatic Esters on Ovary Development of Queenless Bees (Apis mellifera L.) , 1998, Naturwissenschaften.

[26]  G. Robinson,et al.  Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers. , 1998, Journal of insect physiology.

[27]  M. Winston,et al.  Species- and Caste-Determined Mandibular Gland Signals in Honeybees (Apis) , 1997, Journal of Chemical Ecology.

[28]  M. Winston,et al.  Mandibular gland components of european and africanized honey bee queens (Apis mellifera L.) , 1996, Journal of Chemical Ecology.

[29]  L. Keller,et al.  The role of queen pheromones in social insects: queen control or queen signal? , 1993, Animal Behaviour.

[30]  M. Winston,et al.  Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone , 1991, Behavioral Ecology and Sociobiology.

[31]  M. Winston,et al.  The role of queen mandibular pheromone and colony congestion in honey bee (Apis mellifera L.) reproductive swarming (Hymenoptera: Apidae) , 1991, Journal of Insect Behavior.

[32]  H. Hepburn,et al.  The queen in relation to wax secretion and comb building in honeybees , 1991, Journal of Comparative Physiology A.

[33]  M. Winston,et al.  Semiochemicals of the honeybee queen mandibular glands , 1990, Journal of Chemical Ecology.

[34]  M. Winston,et al.  The influence of queen mandibular pheromones on worker attraction to swarm clusters and inhibition of queen rearing in the honey bee (Apis mellifera L.) , 1989, Insectes Sociaux.

[35]  N. Koeniger The biology of the honey bee , 1988, Insectes Sociaux.

[36]  M. Winston,et al.  Semiochemical basis of the retinue response to queen honey bees , 1988, Nature.

[37]  H. Velthuis,et al.  OVARIAN DEVELOPMENT IN APIS MELLIFERA WORKER BEES , 1970 .

[38]  H. Velthuis Queen substances from the abdomen of the honey bee queen , 1970, Zeitschrift für vergleichende Physiologie.

[39]  N. Gary Mandibular Gland Extirpation in Living Queen and Worker Honey Bees (Apis mellifera) , 1961 .

[40]  G. Robinson,et al.  Endocrine Influences on the Organization of Insect Societies , 2009 .

[41]  Abraham Hefetz,et al.  Primer pheromones in social hymenoptera. , 2008, Annual review of entomology.

[42]  M. Winston,et al.  Variation in worker response to honey bee (Apis mellifera L.) queen mandibular pheromone (Hymenoptera: Apidae) , 2005, Journal of Insect Behavior.

[43]  Andrew B. Barron,et al.  Measuring the cost of worker reproduction in honeybees: work tempo in an "anarchic" line , 2004 .

[44]  R. Crewe,et al.  Honeybee queen tergal gland secretion affects ovarian development in caged workers , 1999 .

[45]  K. Naumann Grooming behaviors and the translocation of queen mandibular gland pheromone on worker honey bees (Apis mellifera L) , 1991 .

[46]  J. V. Es,et al.  Some Functional Aspects of the Mandibular Glands of the Queen Honeybee , 1964 .