Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers

BackgroundImmune response pathways have been relatively well-conserved across animal species, with similar systems in both mammals and invertebrates. Interestingly, honey bees have substantially reduced numbers of genes associated with immune function compared with solitary insect species. However, social species such as honey bees provide an excellent environment for pathogen or parasite transmission with controlled environmental conditions in the hive, high population densities, and frequent interactions. This suggests that honey bees may have developed complementary mechanisms, such as behavioral modifications, to deal with disease.ResultsHere, we demonstrate that activation of the immune system in honey bees (using bacterial lipopolysaccharides as a non-replicative pathogen) alters the social responses of healthy nestmates toward the treated individuals. Furthermore, treated individuals expressed significant differences in overall cuticular hydrocarbon profiles compared with controls. Finally, coating healthy individuals with extracts containing cuticular hydrocarbons of immunostimulated individuals significantly increased the agonistic responses of nestmates.ConclusionSince cuticular hydrocarbons play a critical role in nestmate recognition and other social interactions in a wide variety of insect species, modulation of such chemical profiles by the activation of the immune system could play a crucial role in the social regulation of pathogen dissemination within the colony.

[1]  Yongliang Fan,et al.  Hydrocarbon synthesis by enzymatically dissociated oenocytes of the abdominal integument of the German Cockroach, Blattella germanica , 2003, Naturwissenschaften.

[2]  D. Liang,et al.  “You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile , 2000, Naturwissenschaften.

[3]  B. Ball,et al.  The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni , 1988 .

[4]  R. Reyment Compositional data analysis , 1989 .

[5]  Gene E Robinson,et al.  Pheromone-mediated gene expression in the honey bee brain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  K. Magor,et al.  Evolution of effectors and receptors of innate immunity. , 2001, Developmental and comparative immunology.

[7]  N. Tsutsui,et al.  The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (Linepithema humile) , 2007, Insectes Sociaux.

[8]  G. Robinson Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonall regulated response thresholds , 1987, Journal of Comparative Physiology A.

[9]  J. Hoffmann,et al.  The immune response of Drosophila , 2003, Nature.

[10]  Y. P. Chen,et al.  Immune pathways and defence mechanisms in honey bees Apis mellifera , 2006, Insect molecular biology.

[11]  J. Traniello,et al.  Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects. , 2004, Journal of theoretical biology.

[12]  A. Aubert Invertebrate studies and the evolution of comparative psychoneuroimmunology , 2007, Brain, Behavior, and Immunity.

[13]  M. Breed,et al.  Kin discrimination by worker honey bees in genetically mixed groups. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Boomsma,et al.  Trade-offs in group living: transmission and disease resistance in leaf-cutting ants , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  Thomas D. Seeley,et al.  Fever in honeybee colonies , 2000, Naturwissenschaften.

[16]  R. Cardé,et al.  Novel and Highly Specific Transport of a Volatile Sex Pheromone by Hemolymph Lipophorin in Moths , 1998, Naturwissenschaften.

[17]  M. Spivak,et al.  The relationship between hygienic behavior and suppression of mite reproduction as honey bee (Apis mellifera) mechanisms of resistance to Varroa destructor , 2006 .

[18]  Young-Joon Kim,et al.  Overview of innate immunity in Drosophila. , 2005, Journal of biochemistry and molecular biology.

[19]  M. Spivak,et al.  Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior , 2001 .

[20]  N. Perrimon,et al.  Sequential activation of signaling pathways during innate immune responses in Drosophila. , 2002, Developmental cell.

[21]  William J. Bell,et al.  Chemical Ecology of Insects , 1985, Springer US.

[22]  A. Aubert,et al.  Social management of LPS-induced inflammation in Formica polyctena ants , 2008, Brain, Behavior, and Immunity.

[23]  P. Schmid-Hempel,et al.  Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects , 1993, Behavioral Ecology and Sociobiology.

[24]  M. Breed Nestmate recognition in honey bees , 1983, Animal Behaviour.

[25]  R. V. Vander Meer,et al.  Nestmate Recognition in Ants , 2019, Pheromone Communication in Social Insects.

[26]  G. Robinson,et al.  Gene Expression Profiles in the Brain Predict Behavior in Individual Honey Bees , 2003, Science.

[27]  S. Martin The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach , 2001 .

[28]  S. Tauszig,et al.  LPS-induced immune response in Drosophila , 2000, Journal of endotoxin research.

[29]  Xiaolong Yang,et al.  Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[30]  M. Breed,et al.  Comb wax effects on the ontogeny of honey bee nestmate recognition , 1998, Animal Behaviour.

[31]  Roger A. Morse,et al.  Honey Bee Pests, Predators and Diseases , 1990 .

[32]  R. Dantzer Innate immunity at the forefront of psychoneuroimmunology , 2004, Brain, Behavior, and Immunity.

[33]  W. Getz,et al.  Honey bee kin recognition: learning self and nestmate phenotypes , 1986, Animal Behaviour.

[34]  P. Parker,et al.  Parasites reduce attractiveness and reproductive success in male grain beetles , 2000, Animal Behaviour.

[35]  L. Bailey Honey Bee Pathology , 1981 .

[36]  K. Waddington,et al.  Behaviour Associated with Hairless-Black Syndrome of Adult Honeybees , 1976 .

[37]  Der-I Wang,et al.  The Division of Labor and Queen Attendance Behavior of Nosema-Infected Worker Honey Bees , 1970 .

[38]  E. Vargo,et al.  Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis , 2006, Proceedings of the Royal Society B: Biological Sciences.

[39]  F. Ferro,et al.  Cytokines and the Brain , 2004, International journal of immunopathology and pharmacology.

[40]  V. Pawlowsky-Glahn,et al.  on Compositional Data Analysis , 2007 .

[41]  P. Schmid-Hempel,et al.  Social Immunity , 2007, Current Biology.

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

[43]  S. Turillazzi,et al.  Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. , 2005, Chemical senses.

[44]  Michael Poulsen,et al.  Specificity in Chemical Profiles of Workers, Brood and Mutualistic Fungi in Atta, Acromyrmex, and Sericomyrmex Fungus-growing Ants , 2007, Journal of Chemical Ecology.

[45]  P. Schmid-Hempel,et al.  In vivo dynamics of an immune response in the bumble bee Bombus terrestris. , 2004, Journal of invertebrate pathology.

[46]  G. J. Blomquist,et al.  Ecological, behavioral, and biochemical aspects of insect hydrocarbons. , 2005, Annual review of entomology.

[47]  B. Ball,et al.  The incidence and world distribution of honey bee viruses , 1996 .

[48]  T. L. Singer Roles of Hydrocarbons in the Recognition Systems of Insects , 1998 .

[49]  S. Turillazzi,et al.  Polistes biglumis bimaculatus epicuticular hydrocarbons and nestmate recognition (Hymenoptera, Vespidae) , 1997, Insectes Sociaux.

[50]  J. Traniello,et al.  The development of immunity in a social insect: Evidence for the group facilitation of disease resistance , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[51]  T. Seeley,et al.  Parasites, Pathogens, and Polyandry in Honey Bees , 1998, The American Naturalist.

[52]  C. Brooke Worth,et al.  The Insect Societies , 1973 .

[53]  P. Schmid-Hempel,et al.  Exploitation of cold temperature as defence against parasitoids in bumblebees , 1993, Nature.

[54]  Dhruba Naug,et al.  Experimentally induced change in infectious period affects transmission dynamics in a social group , 2007, Proceedings of the Royal Society B: Biological Sciences.

[55]  U. Mueller,et al.  Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens , 2006, Biology Letters.

[56]  Jay D. Evans,et al.  Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. , 2006, Journal of invertebrate pathology.

[57]  F. Ratnieks,et al.  Learning and discrimination of individual cuticular hydrocarbons by honeybees (Apis mellifera). , 2005, Chemical senses.

[58]  H. H. Laidlaw Instrumental Insemination of Honeybee Queens: Its Origin and Development , 1987 .

[59]  T. Seeley,et al.  Parasites, Pathogens, and Polyandry in Social Hymenoptera , 1988, The American Naturalist.

[60]  G. Robinson,et al.  Endocrine modulation of a pheromone-responsive gene in the honey bee brain , 2007, Journal of Comparative Physiology A.

[61]  A. Hefetz,et al.  Food influence on colonial recognition and chemical signature between nestmates in the fungus-growing ant Acromyrmex subterraneus subterraneus , 2004, CHEMOECOLOGY.

[62]  A. Aubert,et al.  Sickness and behaviour in animals: a motivational perspective , 1999, Neuroscience & Biobehavioral Reviews.

[63]  J. Traniello,et al.  Pathogen Alarm Behavior in a Termite: A New Form of Communication in Social Insects , 1999, Naturwissenschaften.

[64]  Y. Ip,et al.  A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. , 1996, Genes & development.

[65]  Y. Le Conte,et al.  Modifications of the cuticular hydrocarbon profile of Apis mellifera worker bees in the presence of the ectoparasitic mite Varroa jacobsoni in brood cells , 2001, Parasitology.

[66]  J. Evans Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease. , 2006, Journal of invertebrate pathology.

[67]  Nina H. Fefferman,et al.  Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior, and colony organization , 2007, Behavioral Ecology and Sociobiology.

[68]  B. Hart Behavioral adaptations to pathogens and parasites: Five strategies , 1990, Neuroscience & Biobehavioral Reviews.

[69]  G. D. Waller Honey Bee Pests, Predators, and Diseases , 1979 .

[70]  M. Breed,et al.  The Chemical Basis for Nestmate Recognition and Mate Discrimination in Social Insects , 1995 .

[71]  A. Aubert,et al.  Cytokines and Immune-Related Behaviors , 2008 .

[72]  T. Ganz,et al.  Innate immunity: from plants to humans. , 2000, Immunology today.

[73]  M. Rantala,et al.  Do pheromones reveal male immunocompetence? , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  Scott Camazine,et al.  The role of colony organization on pathogen transmission in social insects. , 2002, Journal of theoretical biology.