Social insect colonies have evolved many collectively performed adaptations that reduce the impact of infectious disease and that are expected to maximize their fitness. This colony-level protection is termed social immunity, and it enhances the health and survival of the colony. In this review, we address how social immunity emerges from its mechanistic components to produce colony-level disease avoidance, resistance, and tolerance. To understand the evolutionary causes and consequences of social immunity, we highlight the need for studies that evaluate the effects of social immunity on colony fitness. We discuss the roles that host life history and ecology have on predicted eco-evolutionary dynamics, which differ among the social insect lineages. Throughout the review, we highlight current gaps in our knowledge and promising avenues for future research, which we hope will bring us closer to an integrated understanding of socio-eco-evo-immunology.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Akre RD, Garnett WB, MacDonald JF, Greene A, Landolt P. 1.  1976. Behavior and colony development of Vespula pensylvanica and V. atropilosa (Hymenoptera: Vespidae). J. Kans. Entomol. Soc. 49:63–84 [Google Scholar]
  2. Alexander RD. 2.  1974. The evolution of social behavior. Annu. Rev. Ecol. Syst. 5:325–83 [Google Scholar]
  3. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J. 3.  et al. 2003. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu. Rev. Ecol. Evol. Syst. 34:517–47 [Google Scholar]
  4. Andersen SB, Ferrari M, Evans HC, Elliot SL, Boomsma JJ, Hughes DP. 4.  2012. Disease dynamics in a specialized parasite of ant societies. PLOS ONE 7:e36352 [Google Scholar]
  5. Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL. 5.  et al. 2009. The life of a dead ant: the expression of an adaptive extended phenotype. Am. Nat. 174:424–33 [Google Scholar]
  6. Ansari MA, Vestergaard S, Tirry L, Moens M. 6.  2004. Selection of a highly virulent fungal isolate, Metarhizium anisopliae CLO 53, for controlling Hoplia philanthus. J. Invertebr. Pathol 85:89–96 [Google Scholar]
  7. Baer B, Armitage SA, Boomsma JJ. 7.  2006. Sperm storage induces an immunity cost in ants. Nature 441:872–75 [Google Scholar]
  8. Baracchi D, Cini A. 8.  2014. A socio-spatial combined approach confirms a highly compartmentalised structure in honeybees. Ethology 120:1167–76 [Google Scholar]
  9. Baracchi D, Fadda A, Turillazzi S. 9.  2012. Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J. Insect Physiol. 58:1589–96 [Google Scholar]
  10. Blanford S, Shi W, Christian R, Marden JH, Koekemoer LL. 10.  et al. 2011. Lethal and pre-lethal effects of a fungal biopesticide contribute to substantial and rapid control of malaria vectors. PLOS ONE 6:1–11 [Google Scholar]
  11. Boomsma JJ. 11.  2009. Lifetime monogamy and the evolution of eusociality. Philos. Trans. R. Soc. B 364:3191–207 [Google Scholar]
  12. Boomsma JJ, Beekman M, Cornwallis CK, Griffin AS, Holman L. 12.  et al. 2011. Only full-sibling families evolved eusociality. Nature 471:E4–5 [Google Scholar]
  13. Boomsma JJ, Gawne R. 13.  2017. Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation. Biol. Rev. Camb. Philos. Soc. In press. https://doi.org/10.1111/brv.12330
  14. Boomsma JJ, Jensen AB, Meyling NV, Eilenberg J. 14.  2014. Evolutionary interaction networks of insect pathogenic fungi. Annu. Rev. Entomol. 59:467–85 [Google Scholar]
  15. Boomsma JJ, Schmid-Hempel P, Hughes WOH. 15.  2005. Life histories and parasite pressure across the major groups of social insects. Insect Evolutionary Ecology MDE Fellowes, G Holloway, J Rolff 139–76 Wallingford, UK: CABI Publishing [Google Scholar]
  16. Boots M, Hudson PJ, Sasaki A. 16.  2004. Large shifts in pathogen virulence relate to host population structure. Science 303:842–44 [Google Scholar]
  17. Boots M, Sasaki A. 17.  1999. “Small worlds” and the evolution of virulence: infection occurs locally and at a distance. Proc. R. Soc. B 266:1933–38 [Google Scholar]
  18. Bos N, Lefèvre T, Jensen AB, D'Ettorre P. 18.  2012. Sick ants become unsociable. J. Evol. Biol. 25:342–51 [Google Scholar]
  19. Boughton RK, Joop G, Armitage SAO. 19.  2011. Outdoor immunology: methodological considerations for ecologists. Funct. Ecol. 25:81–100 [Google Scholar]
  20. Bourke AFG. 20.  2011. Principles of Social Evolution Oxford, UK: Oxford Univ. Press
  21. Bourke AFG, Franks NR. 21.  1995. Social Evolution in Ants Princeton, NJ: Princeton Univ. Press
  22. Brown MJF, Loosli R, Schmid-Hempel P. 22.  2000. Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–27 [Google Scholar]
  23. Brütsch T, Felden A, Reber A, Chapuisat M. 23.  2014. Ant queens (Hymenoptera: Formicidae) are attracted to fungal pathogens during the initial stage of colony founding. Myrmecol. News 20:71–76 [Google Scholar]
  24. Brütsch T, Jaffuel G, Vallat A, Turlings TCJ, Chapuisat M. 24.  2017. Wood ants produce a potent antimicrobial agent by applying formic acid on tree-collected resin. Ecol. Evol. 7:2249–54 [Google Scholar]
  25. Buechel D, Schmid-Hempel P. 25.  2016. Colony pace: a life-history trait affecting social insect epidemiology. Proc. R. Soc. B 283:20151919 [Google Scholar]
  26. Calleri DV, Rosengaus RB, Traniello JFA. 26.  2006. Disease and colony establishment in the dampwood termite Zootermopsis angusticollis: survival and fitness consequences of infection in primary reproductives. Insectes Soc 53:204–11 [Google Scholar]
  27. Chak STC, Duffy JE, Hultgren KM, Dustin R. 27.  2017. Evolutionary transitions towards eusociality in snapping shrimps. Nat. Ecol. Evol. 1:1–26 [Google Scholar]
  28. Chapuisat M, Oppliger A, Magliano P, Christe P. 28.  2007. Wood ants use resin to protect themselves against pathogens. Proc. R. Soc. B 274:2013–17 [Google Scholar]
  29. Charbonneau D, Dornhaus A. 29.  2015. Workers “specialized” on inactivity: behavioral consistency of inactive workers and their role in task allocation. Behav. Ecol. Sociobiol. 69:1459–72 [Google Scholar]
  30. Chouvenc T, Efstathion CA, Elliott ML, Su N. 30.  2013. Extended disease resistance emerging from the faecal nest of a subterranean termite. Proc. R. Soc. B 280:20131885 [Google Scholar]
  31. Chouvenc T, Su N-Y. 31.  2012. When subterranean termites challenge the rules of fungal epizootics. PLOS ONE 7:e34484 [Google Scholar]
  32. Cotter SC, Kilner RM. 32.  2010. Personal immunity versus social immunity. Behav. Ecol. 21:663–68 [Google Scholar]
  33. Cremer S, Armitage SAO, Schmid-Hempel P. 33.  2007. Social immunity. Curr. Biol. 17:R693–702 [Google Scholar]
  34. Cremer S, Sixt M. 34.  2009. Analogies in the evolution of individual and social immunity. Philos. Trans. R. Soc. B 364:129–42 [Google Scholar]
  35. Cremer S, Ugelvig LV, Drijfhout FP, Schlick-Steiner BC, Steiner FM. 35.  et al. 2008. The evolution of invasiveness in garden ants. PLOS ONE 3:e3838 [Google Scholar]
  36. Csata E, Czekes Z, Eros K, Német E, Hughes M. 36.  et al. 2013. Comprehensive survey of Romanian myrmecoparasitic fungi: new species, biology and distribution. North-West. J. Zool. 9:23–29 [Google Scholar]
  37. Curtis VA. 37.  2014. Infection-avoidance behaviour in humans and other animals. Trends Immunol 35:457–64 [Google Scholar]
  38. de Bekker C, Quevillon LE, Smith PB, Fleming KR, Ghosh D. 38.  et al. 2014. Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evol. Biol. 14:166 [Google Scholar]
  39. Diez L, Lejeune P, Detrain C. 39.  2014. Keep the nest clean: survival advantages of corpse removal in ants. Biol. Lett. 10:20140306 [Google Scholar]
  40. Diez L, Moquet L, Detrain C. 40.  2013. Post-mortem changes in chemical profile and their influence on corpse removal in ants. J. Chem. Ecol. 39:1424–32 [Google Scholar]
  41. Drum NH, Rothenbuhler WC. 41.  1983. Non-stinging aggressive responses of worker honeybees to hivemates, intruder bees and bees affected with chronic bee paralysis. J. Apic. Res. 22:256–60 [Google Scholar]
  42. Durrer S, Schmid-Hempel P. 42.  1994. Shared use of flowers leads to horizontal pathogen transmission. Proc. R. Soc. B 258:299–302 [Google Scholar]
  43. Espadaler X, Santamaria S. 43.  2012. Ecto- and endoparasitic fungi on ants from the Holarctic region. Psyche 2012:168478 [Google Scholar]
  44. Evans HC. 44.  1974. Natural control of arthropods, with special reference to ants (Formicidae), by fungi in the tropical high forest of Ghana. J. Appl. Ecol. 11:37–49 [Google Scholar]
  45. Evans HC, Elliot SL, Hughes DP. 45.  2011. Hidden diversity behind the zombie-ant fungus Ophiocordyceps unilateralis: four new species described from carpenter ants in Minas Gerais, Brazil. PLOS ONE 6:1–9 [Google Scholar]
  46. Evans JD, Spivak M. 46.  2010. Socialized medicine: individual and communal disease barriers in honey bees. J. Invertebr. Pathol. 103:S62–72 [Google Scholar]
  47. Ewald PW. 47.  2004. Evolution of virulence. Infect. Dis. Clin. North Am. 18:1–15 [Google Scholar]
  48. Farji-Brener AG, Elizalde L, Fernández-Marín H, Amador-Vargas S. 48.  2016. Social life and sanitary risks: Evolutionary and current ecological conditions determine waste management in leaf-cutting ants. Proc. R. Soc. B 283:20160625 [Google Scholar]
  49. Fernández-Marín H, Zimmerman JK, Nash DR, Boomsma JJ, Wcislo WT. 49.  2009. Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc. R. Soc. B 276:2263–69 [Google Scholar]
  50. Fernández-Marín H, Zimmerman JK, Rehner SA, Wcislo WT. 50.  2006. Active use of the metapleural glands by ants in controlling fungal infection. Proc. R. Soc. B 273:1689–95 [Google Scholar]
  51. Fox LR. 51.  1988. Diffuse coevolution within complex communities. Ecology 69:906–7 [Google Scholar]
  52. Free J. 52.  1958. The drifting of honey-bees. J. Agric. Sci. 51:294–306 [Google Scholar]
  53. Freeland WJ. 53.  1976. Pathogens and the evolution of primate sociality. Biotropica 8:12–24 [Google Scholar]
  54. Freitak D, Schmidtberg H, Dickel F, Lochnit G, Vogel H, Vilcinskas A. 54.  2014. The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5:547–54 [Google Scholar]
  55. Gandon S. 55.  2004. Evolution of multihost parasites. Evolution 58:455–69 [Google Scholar]
  56. Giehr J, Grasse AV, Cremer S, Heinze J, Schrempf A. 56.  2017. Ant queens increase their reproductive efforts after pathogen infection. R. Soc. Open Sci. 4:170547 [Google Scholar]
  57. Gordon DM. 57.  1989. Dynamics of task switching in harvester ants. Anim. Behav. 38:194–204 [Google Scholar]
  58. Gordon DM. 58.  2013. The rewards of restraint in the collective regulation of foraging by harvester ant colonies. Nature 498:91–93 [Google Scholar]
  59. Gordon DM. 59.  2016. From division of labor to the collective behavior of social insects. Behav. Ecol. Sociobiol. 70:1101–8 [Google Scholar]
  60. Gracia ES, de Bekker C, Russell J, Manlove K, Hanks E. 60.  2014. Within the fortress: a specialized parasite of ants is not evicted. bioRxiv 002501 https://doi.org/10.1101/002501
  61. Graham AL, Allen JE, Read AF. 61.  2005. Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Evol. Syst. 36:373–97 [Google Scholar]
  62. Graystock P, Hughes WOH. 62.  2011. Disease resistance in a weaver ant, Polyrhachis dives, and the role of antibiotic-producing glands. Behav. Ecol. Sociobiol. 65:2319–27 [Google Scholar]
  63. Greene MJ, Gordon DM. 63.  2003. Social insects: cuticular hydrocarbons inform task decisions. Nature 423:32 [Google Scholar]
  64. Hamilton WD. 64.  1987. Kinship, recognition, disease, and intelligence: constraints of social evolution. Animal Societies: Theories and Facts Y Ito, J Brown, J Kikkawa 81–102 Tokyo: Jpn. Sci. Soc. Press [Google Scholar]
  65. Hefetz A, Blum MS. 65.  1978. Biosynthesis of formic acid by the poison glands of formicine ants. Biochim. Biophys. Acta 543:484–96 [Google Scholar]
  66. Heinze J, Walter B. 66.  2010. Moribund ants leave their nests to die in social isolation. Curr. Biol. 20:249–52 [Google Scholar]
  67. Helanterä H. 67.  2016. An organismal perspective on the evolution of insect societies. Front. Ecol. Evol. 4:1–12 [Google Scholar]
  68. Hernández López J, Riessberger-Gallé U, Crailsheim K, Schuehly W. 68.  2017. Cuticular hydrocarbon cues of immune-challenged workers elicit immune activation in honey bee queens. Mol. Ecol. 38:42–49 [Google Scholar]
  69. Hughes DP, Araújo J, Loreto R, Quevillon L, de Bekker C, Evans HC. 69.  2016. From so simple a beginning: the evolution of behavioral manipulation by fungi. Adv. Genet. 94:1–33 [Google Scholar]
  70. Hughes WOH, Bot ANM, Boomsma JJ. 70.  2010. Caste-specific expression of genetic variation in the size of antibiotic-producing glands of leaf-cutting ants. Proc. R. Soc. B 277:609–15 [Google Scholar]
  71. Hughes WOH, Eilenberg J, Boomsma JJ. 71.  2002. Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc. R. Soc. B 269:1811–19 [Google Scholar]
  72. Hughes WOH, Petersen KS, Ugelvig LV, Pedersen D, Thomsen L. 72.  et al. 2004. Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. BMC Evol. Biol. 4:45 [Google Scholar]
  73. Hughes WOH, Thomsen L, Eilenberg J, Boomsma JJ. 73.  2004. Diversity of entomopathogenic fungi near leaf-cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J. Invertebr. Pathol. 85:46–53 [Google Scholar]
  74. Iwao K, Rausher MD. 74.  1997. Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. Am. Nat. 149:316–35 [Google Scholar]
  75. Joop G, Roth O, Schmid-Hempel P, Kurtz J. 75.  2014. Experimental evolution of external immune defences in the red flour beetle. J. Evol. Biol. 27:1562–71 [Google Scholar]
  76. Keller L. 76.  1998. Queen lifespan and colony characteristics in ants and termites. Insectes Soc 45:235–46 [Google Scholar]
  77. Keller S, Kessler P, Schweizer C. 77.  2003. Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metarhizium anisopliae. BioControl 48:307–19 [Google Scholar]
  78. Koch H, Brown MJF, Stevenson PC. 78.  2017. The role of disease in bee foraging ecology. Curr. Opin. Insect Sci. 21:60–67 [Google Scholar]
  79. Konrad M, Grasse AV, Tragust S, Cremer S. 79.  2014. Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Proc. R. Soc. B 282:20141976 [Google Scholar]
  80. Konrad M, Pull CD, Seif K, Metzler S, Grasse AV, Cremer S. 80.  Ants express risk-adjusted sanitary care. bioRxiv 170365 https://doi.org/10.1101/170365
  81. Konrad M, Vyleta ML, Theis FJ, Stock M, Tragust S. 81.  et al. 2012. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLOS Biol 10:e1001300 [Google Scholar]
  82. Lach L, Parr C, Abbott K. 82.  2010. Ant Ecology Oxford, UK: Oxford Univ. Press
  83. LeBoeuf AC, Waridel P, Brent CS, Gonçalves AN, Menin L. 83.  et al. 2016. Oral transfer of chemical cues, growth proteins and hormones in social insects. eLife 5:e20375 [Google Scholar]
  84. Leclerc JB, Detrain C. 84.  2017. Loss of attraction for social cues leads to fungal-infected Myrmica rubra ants withdrawing from the nest. Anim. Behav. 129:133–41 [Google Scholar]
  85. Leggett HC, Buckling A, Long GH, Boots M. 85.  2013. Generalism and the evolution of parasite virulence. Trends Ecol. Evol. 28:592–96 [Google Scholar]
  86. Lenoir A, D'Ettorre P, Errard C, Hefetz A. 86.  2001. Chemical ecology and social parasitism in ants. Annu. Rev. Entomol. 46:573–99 [Google Scholar]
  87. Leonhardt SD, Menzel F, Nehring V, Schmitt T. 87.  2016. Ecology and evolution of communication in social insects. Cell 164:1277–87 [Google Scholar]
  88. Lipsitch M, Nowak MA, Ebert D, May RM. 88.  1995. The population dynamics of vertically and horizontally transmitted parasites. Proc. R. Soc. B 260:321–27 [Google Scholar]
  89. Loreto RG, Elliot SL, Freitas MLR, Pereira TM, Hughes DP. 89.  2014. Long-term disease dynamics for a specialized parasite of ant societies: a field study. PLOS ONE 9:e103516 [Google Scholar]
  90. Loreto RG, Hughes DP. 90.  2016. Disease dynamics in ants: a critical review of the ecological relevance of using generalist fungi to study infections in insect societies. Adv. Genet. 94:287–306 [Google Scholar]
  91. Małagocka J, Jensen AB, Eilenberg J. 91.  2017. Pandora formicae, a specialist ant pathogenic fungus: new insights into biology and taxonomy. J. Invertebr. Pathol. 143:108–14 [Google Scholar]
  92. Marikovsky PI. 92.  1962. On some features of behavior of the ants Formica rufa L. infected with fungous disease. Insect Soc 2:173–79 [Google Scholar]
  93. Masri L, Cremer S. 93.  2014. Individual and social immunisation in insects. Trends Immunol 35:471–82 [Google Scholar]
  94. Medzhitov R, Schneider DS, Soares MP. 94.  2012. Disease tolerance as a defense strategy. Science 335:936–41 [Google Scholar]
  95. Mersch DP, Crespi A, Keller L. 95.  2013. Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340:1090–93 [Google Scholar]
  96. Meunier J. 96.  2015. Social immunity and the evolution of group living in insects. Philos. Trans. R. Soc. B 370:20140102 [Google Scholar]
  97. Meyling NV, Eilenberg J. 97.  2007. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol. Control. 43:145–55 [Google Scholar]
  98. Moret Y, Schmid-Hempel P. 98.  2001. Immune defence in bumble-bee offspring. Nature 414:506 [Google Scholar]
  99. Natsopoulou ME, McMahon DP, Paxton RJ. 99.  2016. Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee. Behav. Ecol. Sociobiol. 70:1019–31 [Google Scholar]
  100. Naug D, Camazine S. 100.  2002. The role of colony organization on pathogen transmission in social insects. J. Theor. Biol. 215:427–39 [Google Scholar]
  101. Okuno M, Tsuji K, Sato H, Fujisaki K. 101.  2011. Plasticity of grooming behavior against entomopathogenic fungus Metarhizium anisopliae in the ant Lasius japonicus. J. Ethol. 30:23–27 [Google Scholar]
  102. Oliveira RC, Oi CA, Vollet-Neto A, Wenseleers T. 102.  2016. Intraspecific worker parasitism in the common wasp. Vespula vulgaris. Anim. Behav. 113:79–85 [Google Scholar]
  103. Ortiz-Urquiza A, Keyhani NO. 103.  2016. Molecular genetics of Beauveria bassiana infection of insects. Adv. Genet. 94:165–249 [Google Scholar]
  104. Pinter-Wollman N, Wollman R, Guetz A, Holmes S, Gordon DM. 104.  2011. The effect of individual variation on the structure and function of interaction networks in harvester ants. J. R. Soc. Interface 8:1562–73 [Google Scholar]
  105. Poinar GO, Thomas GM. 105.  1984. A fossil entomogenous fungus from Dominican amber. Experientia 40:578–79 [Google Scholar]
  106. Pontieri L, Vojvodic S, Graham R, Pedersen JS, Linksvayer TA. 106.  2014. Ant colonies prefer infected over uninfected nest sites. PLOS ONE 9:e111961 [Google Scholar]
  107. Pull CD, Ugelvig LV, Wiesenhofer F, Tragust S, Schmitt T. 107.  et al. 2017. Destructive disinfection of infected brood prevents systemic disease spread in ant colonies. bioRxiv 116657 https://doi.org/10.1101/116657
  108. Purcell J, Chapuisat M. 108.  2012. The influence of social structure on brood survival and development in a socially polymorphic ant: insights from a cross-fostering experiment. J. Evol. Biol. 25:2288–97 [Google Scholar]
  109. Qiu H-L, Lu L-H, Shi Q-X, Tu C-C, Lin T, He Y-R. 109.  2015. Differential necrophoric behaviour of the ant Solenopsis invicta towards fungal-infected corpses of workers and pupae. Bull. Entomol. Res. 105:607–14 [Google Scholar]
  110. Queller DC, Strassmann JE. 110.  2003. Eusociality. Curr. Biol. 13:R861–63 [Google Scholar]
  111. Queller DC, Strassmann JE. 111.  2009. Beyond society: the evolution of organismality. Philos. Trans. R. Soc. B 364:3143–55 [Google Scholar]
  112. Råberg L, Sim D, Read AF. 112.  2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812–14 [Google Scholar]
  113. Ravichandran KS. 113.  2010. Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums. J. Exp. Med. 207:1807–17 [Google Scholar]
  114. Reber A, Chapuisat M. 114.  2012. Diversity, prevalence and virulence of fungal entomopathogens in colonies of the ant Formica selysi. Insectes Soc 59:231–39 [Google Scholar]
  115. Reber A, Purcell J, Buechel SD, Buri P, Chapuisat M. 115.  2011. The expression and impact of antifungal grooming in ants. J. Evol. Biol. 24:954–64 [Google Scholar]
  116. Richard F-J, Aubert A, Grozinger C. 116.  2008. Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 6:50 [Google Scholar]
  117. Richard F-J, Holt HL, Grozinger CM. 117.  2012. Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genom 13:558 [Google Scholar]
  118. Rigaud T, Perrot-Minnot MJ, Brown MJ. 118.  2010. Parasite and host assemblages: Embracing the reality will improve our knowledge of parasite transmission and virulence. Proc. Biol. Sci. 277:3693–702 [Google Scholar]
  119. Roberts DW, St. Leger RJ. 119.  2004. Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Adv. Appl. Microbiol. 54:1–70 [Google Scholar]
  120. Robie AA, Seagraves KM, Egnor SER, Branson K. 120.  2017. Machine vision methods for analyzing social interactions. J. Exp. Biol. 220:25–34 [Google Scholar]
  121. Rosengaus R, Jordan C, Lefebvre M, Traniello J. 121.  1999. Pathogen alarm behavior in a termite: a new form of communication in social insects. Naturwissenschaften 86:544–48 [Google Scholar]
  122. Rosengaus RB, Maxmen AB, Coates LE, Traniello JFA. 122.  1998. Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav. Ecol. Sociobiol. 44:125–34 [Google Scholar]
  123. Rosengaus RB, Traniello JFA, Bulmer MS. 123.  2011. Ecology, behavior and evolution of disease resistance in termites. Biology of Termites: A Modern Synthesis DE Bignell, Y Roisin, N Lo 165–91 New York: Springer [Google Scholar]
  124. Roth O, Joop G, Eggert H, Hilbert J, Daniel J. 124.  et al. 2010. Paternally derived immune priming for offspring in the red flour beetle. Tribolium castaneum. J. Anim. Ecol. 79:403–13 [Google Scholar]
  125. Ru O, Hayworth MK, Ross NP. 125.  2010. Altruistic self-removal of health-compromised honey bee workers from their hive. J. Evol. Biol. 23:1538–46 [Google Scholar]
  126. Sadd BM, Kleinlogel Y, Schmid-Hempel R, Schmid-Hempel P. 126.  2005. Trans-generational immune priming in a social insect. Biol. Lett. 1:386–88 [Google Scholar]
  127. Sah P, Méndez JD, Bansal S. 127.  2017. Disease implications of animal social organization and network structure - a quantitative analysis. bioRxiv 106633 https://doi.org/10.1101/106633
  128. Salathé M, Jones JH. 128.  2010. Dynamics and control of diseases in networks with community structure. PLOS Comput. Biol. 6:e1000736 [Google Scholar]
  129. Scharf I, Modlmeier AP, Beros S, Foitzik S. 129.  2012. Ant societies buffer individual-level effects of parasite infections. Am. Nat. 180:671–83 [Google Scholar]
  130. Schmid-Hempel P. 130.  1998. Parasites in Social Insects Princeton, NJ: Princeton Univ. Press
  131. Schmid-Hempel P. 131.  2001. On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–58 [Google Scholar]
  132. Schmid-Hempel P. 132.  2011. Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics New York: Oxford Univ. Press
  133. Schmid-Hempel P. 133.  2017. Parasites and their social hosts. Trends Parasitol 33:24–76 [Google Scholar]
  134. Schmid-Hempel P, Schmid-Hempel R. 134.  1993. Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects. Behav. Ecol. Sociobiol. 33:319–27 [Google Scholar]
  135. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N. 135.  et al. 2010. RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLOS ONE 5:12e14357 [Google Scholar]
  136. Soares MP, Teixeira L, Moita LF. 136.  2017. Disease tolerance and immunity in host protection against infection. Nat. Rev. Immunol. 17:83–96 [Google Scholar]
  137. Spivak M, Masterman R, Ross R, Mesce KA. 137.  2003. Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J. Neurobiol. 55:341–54 [Google Scholar]
  138. Spivak M, Reuter GS. 138.  2001. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32:555–65 [Google Scholar]
  139. Stroeymeyt N, Casillas-Pérez B, Cremer S. 139.  2014. Organisational immunity in social insects. Curr. Opin. Insect Sci. 5:1–15 [Google Scholar]
  140. Suarez AV, Holway DA, Case TJ. 140.  2001. Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. PNAS 98:1095–100 [Google Scholar]
  141. Sun Q, Zhou X. 141.  2013. Corpse management in social insects. Int. J. Biol. Sci. 9:313–21 [Google Scholar]
  142. Toju H, Yamamichi M, Guimarães PR Jr., Olesen JM, Mougi A. 142.  et al. 2017. Synthesis at the metacommunity level. Nat. Ecol. Evol. 1:1–11 [Google Scholar]
  143. Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S. 143.  2013. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Curr. Biol. 23:76–82 [Google Scholar]
  144. Tragust S, Ugelvig LV, Chapuisat M, Heinze J, Cremer S. 144.  2013. Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies. BMC Evol. Biol. 13:225 [Google Scholar]
  145. Tranter C, LeFevre L, Evison SEF, Hughes WOH. 145.  2015. Threat detection: contextual recognition and response to parasites by ants. Behav. Ecol. 26:396–405 [Google Scholar]
  146. Trible W, Chang N-C, Matthews BJ, McKenzie SK, Olivos-Cisneros L. 146.  et al. 2017. orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. bioRxiv 112532 https://doi.org/10.1101/112532
  147. Ugelvig LV, Cremer S. 147.  2007. Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr. Biol. 17:1967–71 [Google Scholar]
  148. Ugelvig LV, Cremer S. 148.  2012. Effects of social immunity and unicoloniality on host-parasite interactions in invasive insect societies. Funct. Ecol. 26:1300–12 [Google Scholar]
  149. Ugelvig LV, Kronauer DJC, Schrempf A, Heinze J, Cremer S. 149.  2010. Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc. R. Soc. B 277:2821–28 [Google Scholar]
  150. Ulrich Y, Sadd BM, Schmid-Hempel P. 150.  2011. Strain filtering and transmission of a mixed infection in a social insect. J. Evol. Biol. 24:354–62 [Google Scholar]
  151. Visscher PK. 151.  1983. The honey bee way of death: necrophoric behaviour in Apis mellifera colonies. Anim. Behav. 31:1070–76 [Google Scholar]
  152. Waddington KD, Rothenbuhler WC. 152.  1976. Behaviour associated with hairless-black syndrome of adult honeybees. J. Apic. Res. 15:35–41 [Google Scholar]
  153. Wagner D, Gordon DM. 153.  1999. Colony age, neighborhood density and reproductive potential in harvester ants. Oecologia 119:175–82 [Google Scholar]
  154. Walker TN, Hughes WOH. 154.  2009. Adaptive social immunity in leaf-cutting ants. Biol. Lett. 5:446–48 [Google Scholar]
  155. West SA, Griffin AS, Gardner A. 155.  2007. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20:415–32 [Google Scholar]
  156. Westhus C, Ugelvig LV, Tourdot E, Heinze J, Doums C, Cremer S. 156.  2014. Increased grooming after repeated brood care provides sanitary benefits in a clonal ant. Behav. Ecol. Sociobiol. 68:1701–10 [Google Scholar]
  157. Wheeler WM. 157.  1911. The ant-colony as an organism. J. Morphol. 22:307–25 [Google Scholar]
  158. Wilson EO. 158.  1971. The Insect Societies Cambridge, MA: Belknap Press
  159. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT. 159.  2009. Genetic, individual, and group facilitation of disease resistance in insect societies. Annu. Rev. Entomol. 54:405–23 [Google Scholar]
  160. Wilson-Rich N, Stuart RJ, Rosengaus RB. 160.  2007. Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae.. J. Invertebr. Pathol. 95:17–25 [Google Scholar]
  161. Yanagawa A, Fujiwara-Tsujii N, Akino T, Yoshimura T, Yanagawa T, Shimizu S. 161.  2011. Behavioral changes in the termite, Coptotermes formosanus (Isoptera), inoculated with six fungal isolates. J. Invertebr. Pathol. 107:100–6 [Google Scholar]
  162. Yanagawa A, Shimizu S. 162.  2007. Resistance of the termite, Coptotermesformosanus Shiraki, to Metarhizium anisopliae due to grooming. BioControl 52:75–85 [Google Scholar]
  163. Yek SH, Nash DR, Jensen AB, Boomsma JJ. 163.  2012. Regulation and specificity of antifungal metapleural gland secretion in leaf-cutting ants. Proc. R. Soc. B 279:4215–22 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error