Effects of social immunity and unicoloniality on host-parasite interactions in invasive insect societies

Functional Ecology

Volumn 26, Issue 6, 2012, Pages 1300-1312

  Ugelvig, Line V ^a   Cremer, Sylvia ^a  

^a INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

Author keywords

Anti parasite defence; Evolution of increased competitive ability hypothesis; Founder effect; Genetic bottlenecks; Host parasite coevolution; Inbreeding; Invasion biology; Parasite adaptation; Parasite release; Social insects

Indexed keywords

ADAPTATION; ANTIPREDATOR DEFENSE; BIOLOGICAL CONTROL; COEVOLUTION; COLONY STRUCTURE; COMPETITIVE ABILITY; DISEASE TRANSMISSION; FOUNDER EFFECT; GENOTYPE; IMMUNITY; INBREEDING; INVASIVENESS; PEST CONTROL; POPULATION BOTTLENECK; QUEEN; SOCIAL BEHAVIOR; SOCIAL INSECT;

FORMICIDAE; HEXAPODA; ISOPTERA;

EID: 84869747133     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12013     Document Type: Article

References (177)

1. Allen, G., Seeman, O., Schmid-Hempel, P. & Buttermore, R. (2007) Low parasite loads accompany the invading population of the bumblebee, Bombus terrestris, in Tasmania. Insectes Sociaux, 54, 56-63.
2. Anderson, D. (1991) Kashmir bee virus - a relatively harmless virus of honeybee colonies. American Bee Journal, 131, 767-770.
3. Anderson, D.L. & Trueman, J.W.H. (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology, 24, 165-189.
4. Armitage, S.A.O. & Siva-Jothy, M.T. (2005) Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity, 94, 650-656.
5. Baer, B. & Schmid-Hempel, P. (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature, 397, 151-154.
6. Bailey, L. & Ball, B.V. (1991) Honey Bee Pathology. Academic Press, London, UK.
7. Bailey, L. & Gibbs, A.J. (1964) Acute infection of bees with paralysis virus. Journal of Insect Pathology, 6, 395-407.
8. Baracchi, D., Francese, S. & Turillazzi, S. (2011) Beyond the antipredatory defence: honey bee venom function as a component of social immunity. Toxicon, 58, 550-557.
9. Beatson, S.H. (1972) Pharaoh's ants as pathogen vectors in hospitals. The Lancet, 299, 425-427.
10. Beggs, J., Brockerhoff, E., Corley, J., Kenis, M., Masciocchi, M., Muller, F., Rome, Q. & Villemant, C. (2011) Ecological effects and management of invasive alien Vespidae. BioControl, 56, 505-526.
11. Blossey, B. & Notzold, R. (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83, 887-889.
12. Boecking, O. & Spivak, M. (1999) Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie, 30, 141-158.
13. Boomsma, J.J., Schmid-Hempel, P. & Hughes, W.O.H. (2005) Life histories and parasite pressure across the major groups of social insects. Insect Evolutionary Ecology: Proceedings of the Royal Entomological Society's 22nd Symposium (eds M.D.E. Fellowes, G.J. Holloway & J. Rolff), pp. 139-175. CABI publishing, Reading, UK.
14. Boot, W.J., van Baalen, M. & Sabelis, M.W. (1995) Why do Varroa mites invade worker brood cells of the honey bee despite lower reproductive success? Behavioral Ecology and Sociobiology, 36, 283-289.
15. Bos, N., Lefevre, T., Jensen, A.B. & d'Ettorre, P. (2012) Sick ants become unsociable. Journal of Evolutionary Biology, 25, 342-351.
16. Bouwma, A.M., Ahrens, M.E., DeHeer, C.J. & Shoemaker, D.D. (2006) Distribution and prevalence of Wolbachia in introduced populations of the fire ant Solenopsis invicta. Insect Molecular Biology, 15, 89-93.
17. Bowen-Walker, P.L., Martin, S.J. & Gunn, A. (1999) The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. Journal of Invertebrate Pathology, 73, 101-106.
18. Briano, J., Calcaterra, L. & Varone, L. (2012) Fire ants (Solenopsis spp.) and their natural enemies in southern South America. Psyche, 2012, 19.
19. Brown, W.L. (1968) An hypothesis concerning function of metapleural glands in ants. The American Naturalist, 102, 188-191.
20. Brown, M.J.F., Schmid-Hempel, R. & Schmid-Hempel, P. (2003) Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology, 72, 994-1002.
21. Bulet, P., Stocklin, R. & Menin, L. (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunological Reviews, 198, 169-184.
22. Buttermore, R.E. (1997) Observations of successful Bombus terrestris (L.) (Hymenoptera: Apidae) colonies in southern Tasmania. Australian Journal of Entomology, 36, 251-254.
23. Callcott, A.A. & Collins, H.L. (1996) Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918-1995. Florida Entomologist, 79, 240-251.
24. Calleri II, D.V., Reid, E.M., Rosengaus, R.B., Vargo, E.L. & Traniello, J.F.A. (2006) Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proceedings of the Royal Society of London. Series B, Biological Sciences, 273, 2633-2640.
25. Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F. & Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences of the United States of America, 108, 662-667.
26. Cerenius, L. & Soderhall, K. (2004) The prophenoloxidase-activating system in invertebrates. Immunological Reviews, 198, 116-126.
27. Cervo, R & Dani, F.R. (1996) Social parasitism and its evolution in Polistes. Natural History and Evolution of Paper-wasps (eds S. Turillazzi, M.J. West-Eberhard), pp. 98-112. Oxford University Press, Oxford.
28. Cervo, R., Zacchi, F. & Turillazzi, S. (2000) Polistes dominulus (Hymenoptera, Vespidae) invading North America: some hypotheses for its rapid spread. Insectes Sociaux, 47, 155-157.
29. Chapman, R.E. & Bourke, A.F.G. (2001) The influence of sociality on the conservation biology of social insects. Ecology Letters, 4, 650-662.
30. Chen, Y.P., Pettis, J.S., Evans, J.D., Kramer, M. & Feldlaufer, M.F. (2004) Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor. Apidologie, 35, 441-448.
31. Christe, P., Oppliger, A., Bancala, F., Castella, G. & Chapuisat, M. (2003) Evidence for collective medication in ants. Ecology Letters, 6, 19-22.
32. Colla, S.R., Otterstatter, M.C., Gegear, R.J. & Thomson, J.D. (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biological Conservation, 129, 461-467.
33. Cremer, S., Armitage, S.A.O. & Schmid-Hempel, P. (2007) Social immunity. Current Biology, 17, R693-R702.
34. Cremer, S., Ugelvig, L.V., Lommen, S.T.E., Petersen, K.S. & Pedersen, J.S. (2006) Attack of the invasive garden ant: aggression behaviour of Lasius neglectus (Hymenoptera: Formicidae) against native Lasius species in Spain. Myrmecologische Nachrichten, 9, 13-19.
35. Cremer, S., Ugelvig, L.V., Drijfhout, F.P., Schlick-Steiner, B.C., Steiner, F.M., Seifert, B., Hughes, D.P., Schulz, A., Petersen, K.S., Konrad, H., Stauffer, C., Kiran, K., Espadaler, X., d'Ettorre, P., Aktaç, N., Eilenberg, J., Jones, G.R., Nash, D.R., Pedersen, J.S. & Boomsma, J.J. (2008) The evolution of invasiveness in garden ants. PLoS ONE, 3, e3838.
36. Culliney, T.W. & Grace, J.K. (2000) Prospects for the biological control of subterranean termites (Isoptera: Rhinotermitidae), with special reference to Coptotermes formosanus. Bulletin of Entomological Research, 90, 9-21.
37. Di Prisco, G., Pennacchio, F., Caprio, E., Boncristiani Jr, H.F., Evans, J.D. & Chen, Y.P. (2011) Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. Journal of General Virology, 92, 151-155.
38. Diamond, J. (1997) Guns, Germs, and Steel: The Fates of Human Societies. W. W. Norton, New York City, USA.
39. Dong, Y., Taylor, H.E. & Dimopoulos, G. (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. Plos Biology, 4, 1137-1146.
40. Drees, B.M., Miller, R.W., Vinson, S.B. & Georgis, R. (1992) Susceptibility and behavioural response of red imported fire ant (Hymenoptera: Formicidae) to selected entomogenous nematodes (Rhabditida: Steinernematidae and Heterorhabditidae). Journal of Economic Entomology, 85, 365-370.
41. Dronnet, S., Chapuisat, M., Vargo, E.L., Lohou, C. & Bagneres, A.G. (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Molecular Ecology, 14, 1311-1320.
42. Durrer, S. & Schmid-Hempel, P. (1994) Shared use of flowers leads to horizontal pathogen transmission. Proceedings of the Royal Society of London. Series B, Biological Sciences, 258, 299-302.
43. Ebert, D. (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science, 265, 1084-1086.
44. Ellis, J.D., Hepburn, H.R., Ellis, A.M. & Elzen, P.J. (2003a) Social encapsulation of the small hive beetle (Aethina tumida Murray) by European honeybees (Apis mellifera L.). Insectes Sociaux, 50, 286-291.
45. Ellis, J.D., Hepburn, R., Delaplane, K.S., Neumann, P. & Elzen, P.J. (2003b) The effects of adult small hive beetles, Aethina tumida (Coleoptera: Nitidulidae), on nests and flight activity of Cape and European honey bees (Apis mellifera). Apidologie, 34, 399-408.
46. Elzen, P.J., Baxter, J.R., Westervelt, D., Randall, C., Delaplane, K.S., Cutts, L. & Wilson, W.T. (1999) Field control and biology studies of a new pest species, Aethina tumida Murray (Coleoptera, Nitidulidae), attacking European honey bees in the Western Hemisphere. Apidologie, 30, 361-366.
47. Elzen, P., Baxter, J., Neumann, P., Solbrig, A., Pirk, C., Hoffman, W. & Hepburn, R.H. (2000) Observations on the small hive beetle [Aethina tumida] in South Africa. American Bee Journal, 140, 304.
48. Epsky, N.D. & Capinera, J.L. (1988) Efficacy of the entomogenous nematode Steinernema feltiae against a subterranean termite, Reticulitermes tibialis (Isoptera, Rhinotermitidae). Journal of Economic Entomology, 81, 1313-1317.
49. Espadaler, X. & Bernal, V. (2003) Lasius neglectus a polygynous, sometimes invasive, ant. http://www.creaf.uab.es/xeg/lasius/, Ecology Unit and CREAF, Universitat Autònoma de Barcelona, Bellaterra.
50. Espadaler, X., Lebas, C., Wagenknecht, J. & Tragust, S. (2011) Laboulbenia formicarum (Ascomycota, Laboulbeniales), an exotic parasitic fungus, on an exotic ant in France. Vie et Milieu, 61, 41-44.
51. Evans, J.D. & Spivak, M. (2010) Socialized medicine: individual and communal disease barriers in honey bees. Journal of Invertebrate Pathology, 103, S62-S72.
52. Farenhorst, M., Mouatcho, J.C., Kikankie, C.K., Brooke, B.D., Hunt, R.H., Thomas, M.B., Koekemoer, L.L., Knols, B.G.J. & Coetzee, M. (2009) Fungal infection counters insecticide resistance in African malaria mosquitoes. Proceedings of the National Academy of Sciences of the United States of America, 106, 17443-17447.
53. Farish, D.J. (1972) Evolutionary implications of qualitative variation in grooming behavior of Hymenoptera (Insecta). Animal Behaviour, 20, 662-676.
54. Feener, D.J. (2000) Is the assembly of ant communities mediated by parasitoids? Oikos, 90, 79-88.
55. Fleury, F., Vavre, F., Ris, N., Fouillet, P. & Bouletreau, M. (2000) Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology, 121(Pt 5), 493-500.
56. Frentiu, F.D., Robinson, J., Young, P.R., McGraw, E.A. & O'Neill, S.L. (2010) Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS ONE, 5, e13398.
57. Gamboa, G.J., Noble, M.A., Thom, M.C., Togal, J.L., Srinivasan, R. & Murphy, B.D. (2004) The comparative biology of two sympatric paper wasps in Michigan, the native Polistes fuscatus and the invasive Polistes dominulus (Hymenoptera, Vespidae). Insectes Sociaux, 51, 153-157.
58. Genersch, E., Yue, C., Fries, I. & de Miranda, J.R. (2006) Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. Journal of Invertebrate Pathology, 91, 61-63.
59. Gerloff, C.U., Ottmer, B.K. & Schmid-Hempel, P. (2003) Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Functional Ecology, 17, 582-589.
60. Goulson, D., Lye, G.C. & Darvill, B. (2008) Decline and conservation of bumble bees. Annual Review of Entomology, 53, 191-208.
61. de Guzman, L.I., Rinderer, T.E. & Stelzer, J.A. (1997) DNA evidence of the origin of Varroa jacobsoni Oudemans in the Americas. Biochemical Genetics, 35, 327-335.
62. Halcroft, M., Spooner-Hart, R. & Neumann, P. (2011) Behavioral defense strategies of the stingless bee, Austroplebeia australis, against the small hive beetle, Aethina tumida. Insectes Sociaux, 58, 245-253.
63. Hamilton, C., Lejeune, B.T. & Rosengaus, R.B. (2011) Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus. Biology Letters, 7, 89-92.
64. Hart, A.G. & Ratnieks, F.L.W. (2001) Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes. Behavioral Ecology and Sociobiology, 49, 387-392.
65. Hart, A.G. & Ratnieks, F.L.W. (2002) Waste management in the leaf-cutting ant Atta colombica. Behavioral Ecology, 13, 224-231.
66. Hedges, L.M., Brownlie, J.C., O'Neill, S.L. & Johnson, K.N. (2008) Wolbachia and virus protection in insects. Science, 322, 702.
67. Heinze, J. & Walter, B. (2010) Moribund ants leave their nests to die in social isolation. Current Biology, 20, 249-252.
68. Helanterä, H., Strassmann, J.E., Carrillo, J. & Queller, D.C. (2009) Unicolonial ants: where do they come from, what are they and where are they going? Trends in Ecology & Evolution, 24, 341-349.
69. Hoffmann, D., Pettis, J.S. & Neumann, P. (2008) Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens). Insectes Sociaux, 55, 153-162.
70. Hölldobler, B. & Wilson, E.O. (1977) The number of queens: an important trait in ant evolution. Naturwissenschaften, 64, 8-15.
71. Holway, D.A., Suarez, A.V. & Case, T.J. (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science, 282, 949-952.
72. Holway, D.A., Lach, L., Suarez, A.V., Tsutsui, N.D. & Case, T.J. (2002) The causes and consequences of ant invasions. Annual Review of Ecology and Systematics, 33, 181-233.
73. Hughes, D.P. & Cremer, S. (2007) Plasticity in antiparasite behaviours and its suggested role in invasion biology. Animal Behaviour, 74, 1593-1599.
74. Hughes, W.O.H., Eilenberg, J. & Boomsma, J.J. (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proceedings of the Royal Society of London. Series B, Biological Sciences, 269, 1811-1819.
75. Hughes, D.P., Beani, L., Turillazzi, S. & Kathirithamby, J. (2003) Prevalence of the parasite Strepsiptera in Polistes as detected by dissection of immatures. Insectes Sociaux, 50, 62-68.
76. Human, K.G. & Gordon, D.M. (1999) Behavioral interactions of the invasive Argentine ant with native ant species. Insectes Sociaux, 46, 159-163.
77. Hunter, D.M., Milner, R.J., Scanlan, J.C. & Spurgin, P.A. (1999) Aerial treatment of the migratory locust, Locusta migratoria (L.) (Orthoptera: Acrididae) with Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) in Australia. Crop Protection, 18, 699-704.
78. Hurst, G.D.D., Jiggins, F.M., von der Schulenburg, J.H.G., Bertrand, D., West, S.A., Goriacheva II, Zakharov, I.A., Werren, J.H., Stouthamer, R. & Majerus, M.E.N. (1999) Male-killing Wolbachia in two species of insect. Proceedings of the Royal Society of London. Series B, Biological Sciences, 266, 735-740.
79. Husseneder, C., Simms, D.M., Aluko, G.K. & Delatte, J. (2010) Colony breeding system influences cuticular bacterial load of Formosan subterranean termite (Isoptera: Rhinotermitidae) workers. Environmental Entomology, 39, 1715-1723.
80. Kenis, M., Auger-Rozenberg, M.-A., Roques, A., Timms, L., Pere, C., Cock, M.J.W., Settele, J., Augustin, S. & Lopez-Vaamonde, C. (2009) Ecological effects of invasive alien insects. Biological Invasions, 11, 21-45.
81. Konrad, K., Vyleta, M.L., Theis, F.J., Stock, M., Tragust, S., Klatt, M., Drescher, V., Marr, C., Ugelvig, L.V. & Cremer, S. (2012) Social transfer of pathogenic fungus promotes active immunisation in ant colonies. Plos Biology, 10, e1001300.
82. Kronenberg, F. & Heller, H.C. (1982) Colonial thermoregulation in honey bees Apis mellifera. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 148, 65-76.
83. Kurtz, J. & Armitage, S.A.O. (2006) Alternative adaptive immunity in invertebrates. Trends in Immunology, 27, 493-496.
84. Lee, K.A. & Klasing, K.C. (2004) A role for immunology in invasion biology. Trends in Ecology & Evolution, 19, 523-529.
85. Leniaud, L., Pichon, A., Uva, P. & Bagneres, A.G. (2009) Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species. Bulletin of Entomological Research, 99, 1-10.
86. Liebert, A.E., Gamboa, G.J., Stamp, N.E., Curtis, T.R., Monnet, K.M., Turillazzi, S. & Starks, P.T. (2006) Genetics, behavior and ecology of a paper wasp invasion: Polistes dominulus in North America. Annales Zoologici Fennici, 43, 595-624.
87. Liersch, S. & Schmid-Hempel, P. (1998) Genetic variation within social insect colonies reduces parasite load. Proceedings of the Royal Society of London. Series B, Biological Sciences, 265, 221-225.
88. Lopez-Riquelme, G.O., Malo, E.A., Cruz-Lopez, L. & Fanjul-Moles, M.L. (2006) Antennal olfactory sensitivity in response to task-related odours of three castes of the ant Atta mexicana (Hymenoptera: Formicidae). Physiological Entomology, 31, 353-360.
89. Lowe, S., Browne, M., Boudjelas, S. & De Poorter, M. (2000) 100 of the World's Worst Invasive Alien Species: A selection from the Global Invasive Species Database, The Invasive Species Specialist Group (ISSG) of the World Conservation Union (IUCN), 12 pp.
90. Manfredini, F., Beani, L. & Grozinger, C.M. (2012) Examining the "evolution of increased competitive ability" hypothesis in response to co-evolved and general parasites in the invasive paper wasps Polistes dominulus. 5th Meeting of the European Sessions of the I.U.S.S.I. Montecatini Terme, Italy.
91. Martin, S.J. (1995) Ontogenesis of the mite Varroa jacobsoni Oud. in drone brood of the honeybee Apis mellifera L. under natural conditions. Experimental and Applied Acarology, 19, 199-210.
92. Martin, S.J., Highfield, A.C., Brettell, L., Villalobos, E.M., Budge, G.E., Powell, M., Nikaido, S. & Schroeder, D.C. (2012) Global honey bee viral landscape altered by a parasitic mite. Science, 336, 1304-1306.
93. Masterman, R.M., Ross, R.R., Mesce, K.M. & Spivak, M.S. (2001) Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). Journal of Comparative Physiology A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 187, 441-452.
94. Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York City, USA.
95. Meeus, I., Brown, M.J.F., De Graaf, D.C. & Smagghe, G. (2011) Effects of invasive parasites on bumble bee declines. Conservation Biology, 25, 662-671.
96. Milinski, M. (2006) The major histocompatibility complex, sexual selection, and mate choice. Annual Review of Ecology, Evolution, and Systematics, 37, 159-186.
97. Min, K.-T. & Benzer, S. (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proceedings of the National Academy of Sciences, 94, 10792-10796.
98. Mitchell, C.E. & Power, A.G. (2003) Release of invasive plants from fungal and viral pathogens. Nature, 421, 625-627.
99. Moller, H. (1996) Lessons for invasion theory from social insects. Biological Conservation, 78, 125-142.
100. Morrison, L.W. (2012) Biological control of Solenopsis fire ants by Pseudacteon parasitoids: theory and practice. Psyche, 2012, 11.
101. Neumann, P. & Elzen, P.J. (2004) The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): gaps in our knowledge of an invasive species. Apidologie, 35, 229-247.
102. Neumann, P., Pirk, C.W.W., Hepburn, H.R., Solbrig, A.J., Ratnieks, F.L.W., Elzen, P.J. & Baxter, J.R. (2001) Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.). Naturwissenschaften, 88, 214-216.
103. Oi, D.H. & Pereira, R.M. (1993) Ant behaviour and microbial pathogens (Hymenoptera: Formicidae). Florida Entomologist, 76, 63-74.
104. Oi, D.H., Pereira, R.M., Stimac, J.L. & Wood, L.A. (1994) Field applications of Beauveria bassiana for control of the red imported fire ant (Hymenoptera: Formicidae). Journal of Economic Entomology, 87, 623-630.
105. Oldroyd, B.P. (1999) Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trends in Ecology & Evolution, 14, 312-315.
106. O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. (1997) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, Oxford.
107. Orr, M.R., Seike, S.H., Benson, W.W. & Gilbert, L.E. (1995) Flies suppress fire ants. Nature, 373, 292-293.
108. Otterstatter, M.C. & Thomson, J.D. (2008) Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS ONE, 3, e2771.
109. Oudemans, A.C. (1904) On a new genus and species of parasitic acari. Notes from the Leyden Museum, 24, 216-222.
110. Paini, D.R. (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: a review. Austral Ecology, 29, 399-407.
111. Pal, S. & Wu, L.P. (2009) Lessons from the fly: pattern recognition in Drosophila melanogaster. Advances in Experimental Medicine and Biology, 653, 162-174.
112. Pamilo, P. & Crozier, R.H. (1997) Population biology of social insect conservation. Memoirs of the Museum of Victoria, 56, 411-419.
113. Pamilo, P., Gertsch, P., Thoren, P. & Seppa, P. (1997) Molecular population genetics of social insects. Annual Review of Ecology and Systematics, 28, 1-25.
114. Park, O.W., Pellett, F.C. & Paddock, F.B. (1939) Results of Iowa's 1937-1938 honeybee disease resistance program. American Bee Journal, 79, 577-582.
115. Passera, L. (1994) Characteristics of tramp species. Exotic Ants: Biology, Impact, and Control of Introduced Species (eds D.F. Williams), pp. 23-43. Westview Press, Boulder, Colorado.
116. Perdereau, E., Dedeine, F., Christidès, J.P., Dupont, S. & Bagnères, A.G. (2011) Competition between invasive and indigenous species: an insular case study of subterranean termites. Biological Invasions, 13, 1457-1470.
117. Pickett, K.M. & Wenzel, J.W. (2000) High productivity in haplometrotic colonies of the introduced paper wasp Polistes dominulus (Hymenoptera: Vespidae; Polistinae). Journal of the New York Entomological Society, 108, 314-325.
118. Pimentel, D., Lach, L., Zuniga, R. & Morrison, D. (2000) Environmental and economic costs of nonindigenous species in the United States. BioScience, 50, 53-65.
119. Plischuk, S., Martin-Hernandez, R., Prieto, L., Lucia, M., Botias, C., Meana, A., Abrahamovich, A.H., Lange, C.E. & Higes, M. (2009) South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera). Environmental Microbiology Reports, 1, 131-135.
120. Porter, S.D., Williams, D.F., Patterson, R.S. & Fowler, H.G. (1997) Intercontinental differences in the abundance of Solenopsis fire ants (Hymenoptera: Formicidae): escape from natural enemies? Environmental Entomology, 26, 373-384.
121. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25, 345-353.
122. Reuter, M., Pedersen, J.S. & Keller, L. (2005) Loss of Wolbachia infection during colonisation in the invasive Argentine ant Linepithema humile. Heredity, 94, 364-369.
123. Ribière, M., Ball, B. & Aubert, M. (2008) Natural history and geographical distribution of honey bee viruses. Virology and the Honey Bee (eds M. Aubert, B. Ball, I. Fries, R. Moritz, N. Milani & I. Bernadinelli), pp. 15-84. European Commission, Brussels.
124. Rosengaus, R.B., Guldin, M.R. & Traniello, J.F.A. (1998) Inhibitory effect of termite fecal pellets on fungal spore germination. Journal of Chemical Ecology, 24, 1697-1706.
125. Rosengaus, R.B., Maxmen, A.B., Coates, L.E. & Traniello, J.F.A. (1998) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behavioral Ecology and Sociobiology, 44, 125-134.
126. Rosenkranz, P., Aumeier, P. & Ziegelmann, B. (2010) Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, S96-S119.
127. Ross, K.G. (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Molecular Ecology, 10, 265-284.
128. Ross, K.G., Vargo, E.L. & Keller, L. (1996) Social evolution in a new environment: the case of introduced fire ants. Proceedings of the National Academy of Sciences of the United States of America, 93, 3021-3025.
129. Ross, K.G., Vargo, E.L., Keller, L. & Trager, J.C. (1993) Effect of a founder event on variation in the genetic sex-determining system of the fire ant Solenopsis invicta. Genetics, 135, 843-854.
130. Rothenbuhler, W.C. (1964a) Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood. Animal Behaviour, 12, 578-583.
131. Rothenbuhler, W.C. (1964b) Behaviour genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. American Zoology, 4, 111-123.
132. Rueppell, O., Hayworth, M.K. & Ross, N.P. (2010) Altruistic self-removal of health-compromised honey bee workers from their hive. Journal of Evolutionary Biology, 23, 1538-1546.
133. Ruiz-González, M.X., Bryden, J., Moret, Y., Reber-Funk, C., Schmid-Hempel, P. & Brown, M.J.F. (2012) Dynamic transmission, host quality and population structure in a multi-host parasite of bumble bees. Evolution, 66, 3053-3066.
134. Santillan-Galicia, M.T., Ball, B.V., Clark, S.J. & Alderson, P.G. (2010) Transmission of deformed wing virus and slow paralysis virus to adult bees (Apis mellifera L.) by Varroa destructor. Journal of Apicultural Research, 49, 141-148.
135. Schiff, N.M. & Sheppard, W.S. (1995) Genetic analysis of commercial honey bees (Hymenoptera: Apidae) from the Southeastern United States. Journal of Economic Entomology, 88, 1216-1220.
136. Schiff, N.M. & Sheppard, W.S. (1996) Genetic differentiation in the queen breeding population of the western United States. Apidologie, 27, 77-86.
137. Schmid-Hempel, P. (1998) Parasites in Social Insects. Princeton University Press, Princeton, NJ, USA.
138. Schrempf, A., Aron, S. & Heinze, J. (2006) Sex determination and inbreeding depression in an ant with regular sib-mating. Heredity, 97, 75-80.
139. Sebastien, A., Gruber, M.A.M. & Lester, P.J. (2012) Prevalence and genetic diversity of three bacterial endosymbionts (Wolbachia, Arsenophonus, and Rhizobiales) associated with the invasive yellow crazy ant (Anoplolepis gracilipes). Insectes Sociaux, 59, 33-40.
140. Seifert, B. (2000) Rapid range expansion in Lasius neglectus (Hymenoptera, Formicidae) - an Asian invader swamps Europe. Deutsche Entomologische Zeitschrift, 47, 173-179.
141. Shoemaker, D.D., Ross, K.G., Keller, L., Vargo, E.L. & Werren, J.H. (2000) Wolbachia infections in native and introduced populations of fire ants (Solenopsis spp.). Insect Molecular Biology, 9, 661-673.
142. Shoemaker, D.D., Ahrens, M., Sheill, L., Mescher, M., Keller, L. & Ross, K.G. (2003) Distribution and prevalence of Wolbachia infections in native populations of the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Environmental Entomology, 32, 1329-1336.
143. Simone-Finstrom, M. & Spivak, M. (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie, 41, 295-311.
144. Singh, R., Levitt, A.L., Rajotte, E.G., Holmes, E.C., Ostiguy, N., van Engelsdorp, D., Lipkin, W.I., dePamphilis, C.W., Toth, A.L. & Cox-Foster, D.L. (2010) RNA viruses in Hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis Hymenopteran species. PLoS ONE, 5, e14357.
145. Spiewok, S. & Neumann, P. (2006) Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida). Ecological Entomology, 31, 623-628.
146. Stafford, C.T. (1992) Fire ant allergy. Allergy Proceedings, 13, 11-16.
147. Stahlhut, J.K., Liebert, A.E., Starks, P.T., Dapporto, L. & Jaenike, J. (2006) Wolbachia in the invasive European paper wasp Polistes dominulus. Insectes Sociaux, 53, 269-273.
148. Stout, J.C. & Morales, C.L. (2009) Ecological impacts of invasive alien species on bees. Apidologie, 40, 388-409.
149. Sumana, A. & Starks, P.T. (2004) Grooming patterns in the primitively eusocial wasp Polistes dominulus. Ethology, 110, 825-833.
150. Thaxter, R. (1908) Contribution toward a monograph of the Laboulbeniaceae. Part II. Memoirs of the American Academy of Arts and Sciences, 13, 217-469.
151. Thomas, M.B. & Read, A.F. (2007) Can fungal biopesticides control malaria? Nature Reviews Microbiology, 5, 377-383.
152. Thomas, M.L., Payne-Makrisa, C.M., Suarez, A.V., Tsutsui, N.D. & Holway, D.A. (2006) When supercolonies collide: territorial aggression in an invasive and unicolonial social insect. Molecular Ecology, 15, 4303-4315.
153. Thomas, M.L., Payne-Makrisa, C.M., Suarez, A.V., Tsutsui, N.D. & Holway, D.A. (2007) Contact between supercolonies elevates aggression in Argentine ants. Insectes Sociaux, 54, 225-233.
154. Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature, 421, 628-630.
155. Traniello, J.F.A., Rosengaus, R.B. & Savoie, K. (2002) The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proceedings of the National Academy of Sciences of the United States of America, 99, 6838-6842.
156. Tsutsui, N.D., Suarez, A.V. & Grosberg, R.K. (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proceedings of the National Academy of Sciences of the United States of America, 100, 1078-1083.
157. Tsutsui, N.D., Suarez, A.V., Holway, D.A. & Case, T.J. (2000) Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences of the United States of America, 97, 5948-5953.
158. Ugelvig, L.V. & Cremer, S. (2007) Social prophylaxis: group interaction promotes collective immunity in ant colonies. Current Biology, 17, 1967-1971.
159. Ugelvig, L.V., Drijfhout, F.P., Kronauer, D.J.C., Boomsma, J.J., Pedersen, J.S. & Cremer, S. (2008) The introduction history of invasive garden ants in Europe: integrating genetic, chemical and behavioural approaches. BMC Biology, 6, 11.
160. Ugelvig, L.V., Kronauer, D.J.C., Schrempf, A., Heinze, J. & Cremer, S. (2010) Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proceedings of the Royal Society of London. Series B, Biological Sciences, 277, 2821-2828.
161. Uller, T. & Leimu, R. (2011) Founder events predict changes in genetic diversity during human-mediated range expansions. Global Change Biology, 17, 3478-3485.
162. Van Loon, A.J., Boomsma, J.J. & Andrasfalvy, A. (1990) A new polygynous Lasius spp. Hymenoptera Formicidae from Central Europe I. Description and general biology. Insectes Sociaux, 37, 348-362.
163. Vargo, E.L. & Husseneder, C. (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annual Review of Entomology, 54, 379-403.
164. Vargo, E.L., Husseneder, C. & Grace, J.K. (2003) Colony and population genetic structure of the Formosan subterranean termite, Coptotermes formosanus, in Japan. Molecular Ecology, 12, 2599-2608.
165. Vitikainen, E. & Sundstrom, L. (2011) Inbreeding and caste-specific variation in immune defence in the ant Formica exsecta. Behavioral Ecology and Sociobiology, 65, 899-907.
166. Watson, F.L., Püttmann-Holgado, R., Thomas, F., Lamar, D.L., Hughes, M., Kondo, M., Rebel, V.I. & Schmucker, D. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science, 309, 1874-1878.
167. Whitehorn, P.R., Tinsley, M.C., Brown, M.J.F., Darvill, B. & Goulson, D. (2011) Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proceedings of the Royal Society of London. Series B, Biological Sciences, 278, 1195-1202.
168. Wilder, S.M., Holway, D.A., Suarez, A.V., LeBrun, E.G. & Eubanks, M.D. (2011) Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasions. Proceedings of the National Academy of Sciences, 108, 20639-20644.
169. Williams, P.H. & Osborne, J.L. (2009) Bumblebee vulnerability and conservation world-wide. Apidologie, 40, 367-387.
170. Williams, D.F., Oi, D.H., Porter, S.D., Pereira, R.M. & Briano, J.A. (2003) Biological control of imported fire ants (Hymenoptera: Formicidae). American Entomologist, 49, 150-163.
171. Wilson, E.O. (1971) The Insect Societies. Harvard University Press, Cambridge, MA, USA.
172. Wilson-Rich, N. & Starks, P.T. (2010) The Polistes war: weak immune function in the invasive P. dominulus relative to the native P. fuscatus. Insectes Sociaux, 57, 47-52.
173. Wilson-Rich, N., Stuart, R.J. & Rosengaus, R.B. (2007) Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae. Journal of Invertebrate Pathology, 95, 17-25.
174. Wilson-Rich, N., Spivak, M., Fefferman, N.H. & Starks, P.T. (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annual Review of Entomology, 54, 405-423.
175. Xu, P., Shi, M. & Chen, X. (2009) Antimicrobial peptide evolution in the asiatic honey bee Apis cerana. PLoS ONE, 4, e4239.
176. Yang, X.L. & Cox-Foster, D.L. (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences of the United States of America, 102, 7470-7475.
177. Yang, C.-C., Yu, Y.-C., Valles, S.M., Oi, D.H., Chen, Y.-C., Shoemaker, D.W., Wu, W.-J. & Shih, C.-J. (2010) Loss of microbial (pathogen) infections associated with recent invasions of the red imported fire ant Solenopsis invicta. Biological Invasions, 12, 3307-3318.