Genetic, individual, and group facilitation of disease resistance in insect societies.

In this review, we provide a current reference on disease resistance in insect societies. We start with the genetics of immunity in the context of behavioral and physiological processes and scale up levels of biological organization until we reach populations. A significant component of this review focuses on Apis mellifera and its role as a model system for studies on social immunity. We additionally review the models that have been applied to disease transmission in social insects and elucidate areas for future study in the field of social immunity.

[1]  P. Starks,et al.  The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). , 2008, Journal of insect physiology.

[2]  R. Dallai,et al.  Circulating hemocytes from larvae of the paper wasp Polistes dominulus (Hymenoptera, Vespidae). , 2008, Tissue & cell.

[3]  M. Chapuisat,et al.  Prophylaxis with resin in wood ants , 2008, Animal Behaviour.

[4]  A. Soares,et al.  In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. , 2008, Journal of invertebrate pathology.

[5]  P. Schmid-Hempel,et al.  Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees , 2007, Current Biology.

[6]  D. Hughes,et al.  Plasticity in antiparasite behaviours and its suggested role in invasion biology , 2007, Animal Behaviour.

[7]  C. Tirard,et al.  Phenotypic plasticity of immune defence linked with foraging activity in the ant Cataglyphis velox , 2007, Journal of evolutionary biology.

[8]  M. Winston,et al.  Genome‐wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera) , 2007, Molecular ecology.

[9]  M. Gillings,et al.  Antimicrobial defences increase with sociality in bees , 2007, Biology Letters.

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

[11]  Robin J Stuart,et al.  Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae. , 2007, Journal of invertebrate pathology.

[12]  Haobo Jiang,et al.  Regulation of phenoloxidase activity by high- and low-molecular-weight inhibitors from the larval hemolymph of Manduca sexta. , 2007, Insect biochemistry and molecular biology.

[13]  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.

[14]  T. Seeley,et al.  Queen promiscuity lowers disease within honeybee colonies , 2007, Proceedings of the Royal Society B: Biological Sciences.

[15]  Jeffrey W. Harris.  Bees with Varroa Sensitive Hygiene preferentially remove mite infested pupae aged ≤ five days post capping , 2007 .

[16]  Leonard J Foster,et al.  Quantitative Comparison of Caste Differences in Honeybee Hemolymph*S , 2006, Molecular & Cellular Proteomics.

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

[18]  J. Traniello,et al.  Inducible immune proteins in the dampwood termite Zootermopsis angusticollis , 2006, Naturwissenschaften.

[19]  H. Arathi,et al.  Inefficient task partitioning among nonhygienic honeybees, Apis mellifera L., and implications for disease transmission , 2006, Animal Behaviour.

[20]  E. Mallon,et al.  An immune response in the bumblebee, Bombus terrestris leads to increased food consumption , 2006, BMC Physiology.

[21]  M. Brehélin,et al.  Insect haemocytes: what type of cell is that? , 2006, Journal of insect physiology.

[22]  Mark J. F. Brown,et al.  Males vs workers: testing the assumptions of the haploid susceptibility hypothesis in bumblebees , 2006, Behavioral Ecology and Sociobiology.

[23]  M. Gardner,et al.  Transmission mode and distribution of parasites among groups of the social lizard Egernia stokesii , 2006, Parasitology Research.

[24]  Eamonn B. Mallon,et al.  Insect psychoneuroimmunology: Immune response reduces learning in protein starved bumblebees (Bombus terrestris) , 2006, Brain, Behavior, and Immunity.

[25]  P. Starks,et al.  Honey bee workers as mobile insulating units , 2005, Insectes Sociaux.

[26]  J. Boomsma,et al.  Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection , 2005, Insectes Sociaux.

[27]  M. Beekman,et al.  The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera , 2005, Journal of Comparative Physiology A.

[28]  M. Spivak,et al.  A multifactorial study of the resistance of honeybees Apis mellifera to the mite Varroa destructor over one year in Mexico , 2005 .

[29]  A. Sumana,et al.  Diploid males and their triploid offspring in the paper wasp Polistes dominulus , 2005, Biology Letters.

[30]  Z. Simões,et al.  Molecular characterization of a cDNA encoding prophenoloxidase and its expression in Apis mellifera. , 2005, Insect biochemistry and molecular biology.

[31]  A. Sumana,et al.  Grooming Patterns in the Primitively Eusocial Wasp Polistes dominulus , 2004 .

[32]  P. Parker,et al.  EFFECTS OF HOST SOCIALITY ON ECTOPARASITE POPULATION BIOLOGY , 2004, The Journal of parasitology.

[33]  P. Starks,et al.  Triploid females and diploid males: underreported phenomena in Polistes wasps? , 2004, Insectes Sociaux.

[34]  J. Boomsma,et al.  GENETIC DIVERSITY AND DISEASE RESISTANCE IN LEAF-CUTTING ANT SOCIETIES , 2004, Evolution; international journal of organic evolution.

[35]  S. Beshers,et al.  The role of male disease susceptibility in the evolution of haplodiploid insect societies † , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  L. Cerenius,et al.  The prophenoloxidase‐activating system in invertebrates , 2004, Immunological reviews.

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

[38]  L. Kruuk,et al.  Costs of resistance: genetic correlations and potential trade‐offs in an insect immune System , 2003, Journal of evolutionary biology.

[39]  Stefan Fuchs,et al.  Hot bees in empty broodnest cells: heating from within , 2003, Journal of Experimental Biology.

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

[41]  P. Schmid-Hempel,et al.  Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris , 2003 .

[42]  M. Spivak,et al.  Differences in olfactory sensitivity and behavioral responses among honey bees bred for hygienic behavior , 2003, Behavioral Ecology and Sociobiology.

[43]  M. Spivak,et al.  Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. , 2003, Journal of neurobiology.

[44]  E. Mallon,et al.  SPECIFIC VERSUS NONSPECIFIC IMMUNE DEFENSE IN THE BUMBLEBEE, BOMBUS TERRESTRIS L. , 2003, Evolution; international journal of organic evolution.

[45]  P. Starks.  Selection for uniformity: xenophobia and invasion success , 2003 .

[46]  P. Schmid-Hempel,et al.  Bumblebee workers from different sire groups vary in susceptibility to parasite infection , 2003 .

[47]  D. Tarpy.  Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  B. Oldroyd,et al.  Seven suggestive quantitative trait loci influence hygienic behavior of honey bees , 2002, Naturwissenschaften.

[49]  M. Strand,et al.  Insect hemocytes and their role in immunity. , 2002, Insect biochemistry and molecular biology.

[50]  Jürgen Tautz,et al.  Hot spots in the bee hive , 2002, Naturwissenschaften.

[51]  G. Otero-Colina,et al.  Varroa destructor (Acari: Varroidae) infestation in queen, worker, and drone brood of Apis mellifera (Hymenoptera: Apidae) , 2002, The Canadian Entomologist.

[52]  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.

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

[54]  L. Keller,et al.  Evolution of supercolonies: The Argentine ants of southern Europe , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[55]  S. Simpson,et al.  Coping with crowds: Density-dependent disease resistance in desert locusts , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[56]  B. Lemaître,et al.  Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[57]  R. Arlettaz,et al.  The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis) , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  P. Schmid-Hempel,et al.  UNEXPECTED CONSEQUENCES OF POLYANDRY FOR PARASITISM AND FITNESS IN THE BUMBLEBEE, BOMBUS TERRESTRIS , 2001, Evolution; international journal of organic evolution.

[59]  M. Spivak,et al.  Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.) , 2001, Journal of Comparative Physiology A.

[60]  H. Arathi,et al.  Influence of colony genotypic composition on the performance of hygienic behaviour in the honeybee, Apis mellifera L. , 2001, Animal Behaviour.

[61]  J. Šimúth,et al.  Isolation of a peptide fraction from honeybee royal jelly as a potential antifoulbrood factor , 2001 .

[62]  M. Spivak,et al.  Varroa destructor Infestation in Untreated Honey Bee (Hymenoptera: Apidae) Colonies Selected for Hygienic Behavior , 2001, Journal of economic entomology.

[63]  L. Otvos,et al.  Antibacterial peptides isolated from insects. , 2000, Journal of peptide science : an official publication of the European Peptide Society.

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

[65]  H. Arathi,et al.  Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. , 2000 .

[66]  D. Gilley,et al.  Heat Shielding: A Novel Method of Colonial Thermoregulation in Honey Bees , 1999, Naturwissenschaften.

[67]  Holway,et al.  Animal behavior: an essential component of invasion biology. , 1999, Trends in ecology & evolution.

[68]  R. Crozier,et al.  Ployandry versus polygyny versus parasites , 1999 .

[69]  A. Maxmen,et al.  Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae) , 1998, Behavioral Ecology and Sociobiology.

[70]  P. Schmid-Hempel.  Parasites in Social Insects , 1998 .

[71]  P. Schmid-Hempel,et al.  Genetic variation within social insect colonies reduces parasite load , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[72]  P. Schmid-Hempel,et al.  Colony performance and immunocompetence of a social insect, Bombus terrestris, in poor and variable environments , 1998 .

[73]  P. Starks,et al.  ‘Male-stuffing’ in wasp societies , 1997, Nature.

[74]  H. Moller.  Lessons for invasion theory from social insects , 1996 .

[75]  Ian A. Cameron,et al.  Why We Get Sick: the New Science of Darwinian Medicine , 1995 .

[76]  P. Schmid-Hempel,et al.  Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[77]  U. Müller,et al.  Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. , 1995, Journal of neurobiology.

[78]  M. Hammer.  An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees , 1993, Nature.

[79]  F. Ratnieks,et al.  Division of honey bee drones during swarming , 1993, Animal Behaviour.

[80]  R. Dudley,et al.  PARASITE DETERRENCE AND THE ENERGETIC COSTS OF SLAPPING IN HOWLER MONKEYS, ALOUATTA PALLIATA , 1990 .

[81]  E. Sober,et al.  Reviving the superorganism. , 1989, Journal of theoretical biology.

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

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

[84]  R. Moritz.  A Reevaluation of the Two-Locus Model for Hygienic Behavior in Honeybees (Apis mellifera L.) , 1988 .

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

[86]  M. Nasr,et al.  Response of foster Asian honeybee (Apis cerana Fabr.) colonies to the brood of European honeybee (Apis mellifera L.) infested with parasitic mite, Varroa jacobsoni oudemans , 1987 .

[87]  B. Cole.  Multiple mating and the evolution of social behavior in the hymenoptera , 1983, Behavioral Ecology and Sociobiology.

[88]  R. Menzel,et al.  The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybeeApis mellifera , 1982, Journal of comparative physiology.

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

[90]  P. Gunby.  Fever, Its Biology, Evolution, and Function , 1980 .

[91]  B. Heinrich.  Mechanisms of Body-Temperature Regulation in Honeybees, Apis Mellifera: I. Regulation of Head Temperature , 1980 .

[92]  H. Bernheim,et al.  Fever in the lizard Dipsosaurus dorsalis , 1974, Nature.

[93]  R. Matthews.  The Insects: Structure and Function , 1971 .

[94]  S. Sakagami,et al.  Worker brood survival in honeybees , 1968, Researches on Population Ecology.

[95]  Ronald M. Jones,et al.  Behaviour genetics of nest cleaning in honey bees. II. Responses of two inbred lines to various amounts of cyanide-killed brood , 1964 .

[96]  W. C. Rothenbuhler.  Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood ☆ , 1964 .

[97]  W. C. Rothenbuhler.  BEHAVIOR GENETICS OF NEST CLEANING IN HONEY BEES. IV. RESPONSES OF F1 AND BACKCROSS GENERATIONS TO DISEASE-KILLED BLOOD. , 1964, American zoologist.

[98]  E. Holst,et al.  The Mechanism of Colony Resistance to American Foulbrood , 1942 .

[99]  O. W. Park.  Testing for Resistance to American Foulbrood in Honeybees , 1937 .

[100]  M. Strand.  2 – INSECT HEMOCYTES AND THEIR ROLE IN IMMUNITY , 2008 .

[101]  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 .

[102]  S. Turillazzi,et al.  Genetics, behavior and ecology of a paper wasp invasion : Polistes dominulus in North America , 2006 .

[103]  The Honeybee Genome Sequencing Consortium,et al.  Erratum: Insights into social insects from the genome of the honeybee Apis mellifera , 2006, Nature.

[104]  P. Starks,et al.  Heat shielding: a task for youngsters , 2005 .

[105]  J. Klaudiny,et al.  Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. , 2005, Insect biochemistry and molecular biology.

[106]  B. H. Smith,et al.  Brood Odor Discrimination Abilities in Hygienic Honey Bees (Apis mellifera L.) Using Proboscis Extension Reflex Conditioning , 2004, Journal of Insect Behavior.

[107]  H. Tabunoki,et al.  Purification and cDNA cloning of a novel antibacterial peptide with a cysteine-stabilized alphabeta motif from the longicorn beetle, Acalolepta luxuriosa. , 2004, Developmental and Comparative Immunology.

[108]  M. Rantala,et al.  Individual variation in immune function in the ant Formica exsecta; effects of the nest, body size and sex , 2004, Evolutionary Ecology.

[109]  D. Sumpter,et al.  The dynamics of virus epidemics in Varroa -infested honey bee colonies , 2004 .

[110]  H. Tabunoki,et al.  Purification and cDNA cloning of a novel antibacterial peptide with a cysteine-stabilized αβ motif from the longicorn beetle, Acalolepta luxuriosa , 2004 .

[111]  M. Chapuisat,et al.  Evidence for collective medication in ants , 2003 .

[112]  J. Fewell,et al.  Models of division of labor in social insects. , 2001, Annual review of entomology.

[113]  M. C. Marcucci,et al.  Propolis: recent advances in chemistry and plant origin , 2000 .

[114]  W. Wickler.  Editorial ‐ Wolfgang Wickler , 2000 .

[115]  O. Boecking,et al.  Behavioral defenses of honey bees against Varroa jacobsoni Oud. , 1999 .

[116]  Guy Theraulaz,et al.  Role and variability of response thresholds in the regulation of division of labor in insect societies , 1999 .

[117]  P. Schmid-Hempel,et al.  Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee , 1999, Nature.

[118]  M. Spivak,et al.  Performance of hygienic honey bee colonies in a commercial apiary , 1998 .

[119]  M. Spivak,et al.  Hygienic behaviour of honey bees and its application for control of brood diseases and varroa: Part II. Studies on hygienic behaviour since the Rothenbuhler era , 1998 .

[120]  M. Spivak,et al.  Hygienic behaviour of honey bees and its application for control of brood diseases and varroa Part I. Hygienic behaviour and resistance to American foulbrood , 1998 .

[121]  David Francis,et al.  IBRA 49th Annual General Meeting Cardiff University, 3 October 1998 , 1998 .

[122]  M. Spivak.  Honey bee hygienic behavior and defense against Varroa jacobsoni , 1996 .

[123]  M. Hammer,et al.  Learning and memory in the honeybee. , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[124]  G. Robinson.  Regulation of division of labor in insect societies. , 1992, Annual review of entomology.

[125]  Ying-shin Peng,et al.  The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans , 1987 .

[126]  W. Conner,et al.  Endotoxin-induced behavioural fever in the Madagascar cockroach, Gromphadorhina portentosa , 1984 .

[127]  P. Visscher.  Adaptations of honey bees (Apis mellifera) to problems of nest hygiene. , 1980 .

[128]  G. Holton.  Sociobiology: the new synthesis? , 1977, Newsletter on science, technology & human values.

[129]  J. Alcock.  Animal Behavior: An Evolutionary Approach , 1975 .

[130]  W. C. Rothenbuhler,et al.  Behaviour Genetics of Nest Cleaning in Honeybees. VI. Interactions of Age and Genotype of Bees, and Nectar Flow , 1971 .

[131]  W. C. Rothenbuhler,et al.  Behaviour Genetics of Nest Cleaning in Honeybees V. Effect of Previous Experience and Composition of Mixed Colonies on Response to Disease-Killed Brood , 1967 .

[132]  Victor C. Thompson.  Behaviour Genetics of Nest Cleaning in Honeybees. III. Effect of Age of Bees of a Resistant Line on Their Response to Disease-Killed Brood , 1964 .