Advertisement

Ecology, Behavior and Evolution of Disease Resistance in Termites

  • Rebeca B. RosengausEmail author
  • James F.A. Traniello
  • Mark S. Bulmer
Chapter

Abstract

The nesting and feeding habits of termites create the risk of contact with microbial and invertebrate pathogens and parasites. Additionally, termite life history can result in cyclical decreases in nestmate genetic heterogeneity, increasing susceptibility to parasites, and sociality may elevate transmission rates of infection within colonies. Current research indicates that ecology and group living have selected for disease resistance in both basal and derived termite families, which have evolved diverse immune adaptations deployed sequentially or simultaneously at both individual and societal levels. These include inducible behavioral, biochemical, immunological and social mechanisms of infection control. Mortality from disease can be significant for reproductives, pseudergates and sterile castes, and influences colony fitness through impacts on colony size, demography, polymorphism, division of labor, communication, development, reproduction, colony foundation, and colony and population genetics. The hemimetabolic development, diplodiploid genetics, microbial symbioses and recalcitrant diets of termites present unique opportunities to model the effects of disease on immune function, including the adaptive design of immune molecules, life-history traits and social evolution. Comparisons can also be made between termite and hymenopteran immunocompetences, highlighting phylogenetic and ecological differences. We advocate a multidisciplinary approach to disease resistance in termites, focusing simultaneously on cellular and humoral immunity, antibiotic prophylaxis and social modes of infection control.

Keywords

Immune Protein Termite Species Fungal Conidium Innate Immune Gene Colony Foundation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Dr. Kenneth Grace for noting useful references and Brian Lejeune for help with formatting. This work was supported by an NSF CAREER Development grant (DEB-0447316) to RB Rosengaus and NSF IBN-9632134 and IBN-0116857 to JFA Traniello and JFA Traniello and RB Rosengaus, respectively.

References

  1. Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 125–148Google Scholar
  2. Adamo S, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus taxensis (formerly G. integer): trade-offs between immunity and reproduction. Anim Behav 62:417–425CrossRefGoogle Scholar
  3. Adams ES, Atkinson L, Bulmer MS (2007) Relatedness, recognition errors, and colony fusion in the termite Nasutitermes corniger. Behav Ecol Sociobiol 61:1195–1201CrossRefGoogle Scholar
  4. Bartz SH (1979) Evolution of eusociality in termites. Proc Natl Acad Sci U S A 76:5764–5768PubMedCrossRefGoogle Scholar
  5. Batra LR, Batra SWT (1966) Fungus-growing termites of tropical India and associated fungi. J Kans Entomol Soc 39:725–738Google Scholar
  6. Batra LR, Batra SWT (1979) Termite-fungus mutualism. In: Batra LR (ed) Insect-fungus symbiosis, nutrition, mutualisms, and commensalism. Wiley, New York, NY, pp 117–163Google Scholar
  7. Beattie A, Turnbull C, Hough T, Knox B (1986) Antibiotic production: a possible function for the metapleural gland of ants (Hymenoptera: Formicidae). Ann Entomol Soc Am 79:448–450Google Scholar
  8. Bignell DE, Eggleton P (2000) Termites in ecosystems. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 363–387Google Scholar
  9. Blackwell M, Rossi W (1986) Biogeography of fungal ectoparasites of termites. Mycotaxon 25:581–601Google Scholar
  10. Brossut R (1983) Allomonal secretions in cockroaches. J Chem Ecol 9:143–158CrossRefGoogle Scholar
  11. Brune A (2006) Symbiotic associations between termites and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E et al (eds) The Prokaryotes: symbiotic associations, biotechnology, applied microbiology, vol 1. Springer, New York, NY, pp 439–474Google Scholar
  12. Bulmer MS, Bachelet I, Raman R et al (2009) Targeting antimicrobial effector function in insect immunity as a pest control strategy. Proc Natl Acad Sci U S A 106:12652–12657PubMedCrossRefGoogle Scholar
  13. Bulmer MS, Crozier RH (2004) Duplication and diversifying selection among termite antifungal peptides. Mol Biol Evol 21:2256–2264PubMedCrossRefGoogle Scholar
  14. Bulmer MS, Crozier RH (2006) Variation in positive selection in termite GNBPs and Relish. Mol Biol Evol 23:317–326PubMedCrossRefGoogle Scholar
  15. Calleri DV, Reid E, Rosengaus RB et al (2006a) Inbreeding and disease resistance in a social insect: effects of genetic variation on immunocompetence in the termite Zootermopsis angusticollis. Proc R Soc Lond B 273:2633–2640CrossRefGoogle Scholar
  16. Calleri DV, Rosengaus RB, Traniello JFA (2005) Disease and colony foundation in the dampwood termite Zootermopsis angusticollis: the survival advantage of nestmate pairs. Naturwissenschaften 92:300–304PubMedCrossRefGoogle Scholar
  17. Calleri DV, Rosengaus RB, Traniello JFA (2006b) Disease and colony establishment in the dampwood termite Zootermopsis angusticollis: survival and fitness consequences of infection in primary reproductives. Insectes Soc 53:204–211CrossRefGoogle Scholar
  18. Calleri DV, Rosengaus RB, Traniello JFA (2007) Immunity and reproduction during colony foundation in the dampwood termite Zootermopsis angusticollis. Physiol Entomol 32:136–142CrossRefGoogle Scholar
  19. Calleri DV, Rosengaus RB, Traniello JFA (2010) Disease resistance in the drywood termite Incisitermes schwarzi (Isoptera: Kalotermitidae): does nesting ecology affect immunocompetence? J Insect Sci 10:Article 44Google Scholar
  20. Chen J, Henderson G, Grimm CC et al (1998a) Naphthalene in Formosan subterranean termite carton nests. J Agric Food Chem 46:2337–2339CrossRefGoogle Scholar
  21. Chen J, Henderson G, Grimms CC et al (1998b) Termites fumigate their nests with naphthalene. Nature 392:558–559CrossRefGoogle Scholar
  22. Choe D-H, Millar JG, Rust MK (2009) Chemical signals associated with life inhibit necrophoresis in Argentine ants. Proc Natl Acad Sci U S A 106:8251–8255PubMedCrossRefGoogle Scholar
  23. Chouvenc T, Su N-Y, Robert A (2009a) Susceptibility of seven termite species (Isoptera) to the pathogenic fungus Metarhizium anisopliae. Sociobiology 54:723–748Google Scholar
  24. Chouvenc T, Su N-Y, Robert A (2009b) Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. J Invertebr Pathol 101:130–136PubMedCrossRefGoogle Scholar
  25. Corby-Harris V, Pontaroli AC, Shimkets LJ et al (2007) Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl Environ Microbiol 73:3470–3479PubMedCrossRefGoogle Scholar
  26. Cremer S, Armitage S, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:R693–R702PubMedCrossRefGoogle Scholar
  27. Cremer S, Sixt M (2009) Analogies in the evolution of individual and social immunity. Philos Trans R Soc Lond B 364:129–142CrossRefGoogle Scholar
  28. Crosland MWJ, Traniello JFA (1997) Behavioral plasticity in division of labor in the lower termite Reticulitermes fukienensis. Naturwissenschaften 84:208–211CrossRefGoogle Scholar
  29. Cruse A (1998) Termite defences against microbial pathogens. PhD Thesis, Macquarie University, AustraliaGoogle Scholar
  30. Da Silva P, Jouvensal L, Lamberty M et al (2003) Solution structure of termicin, an antimicrobial peptide from the termite Pseudacanthotermes spiniger. Protein Sci 12:438–446PubMedCrossRefGoogle Scholar
  31. De Souza DJ, Van Vlaenderen J, Moret Y, Lenoir A (2008) Immune response affects ant trophallactic behaviour. J Insect Physiol 54:828–832PubMedCrossRefGoogle Scholar
  32. Dong Y, Taylor HE, Dimopoulos G (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4:e229PubMedCrossRefGoogle Scholar
  33. Dunn PE (1990) Humoral immunity in insects. BioScience 40:738–744CrossRefGoogle Scholar
  34. Eggleton P (2000) Global patterns of termite diversity. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 25–54Google Scholar
  35. Faulhaber LM, Karp RD (1992) A diphasic immune response against bacteria in the American cockroach. Immunology 75:378–381PubMedGoogle Scholar
  36. Fefferman NH, Traniello JFA (2009) Social insects as models in epidemiology: establishing the foundation for an interdisciplinary approach to disease and sociality. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, MA, pp 545–571Google Scholar
  37. Fefferman NH, Traniello JFA, Rosengaus RB, Calleri DV (2007) Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior and colony organization. Behav Ecol Sociobiol 61:565–577CrossRefGoogle Scholar
  38. Fei HX, Henderson G (2003) Comparative study of incipient colony development in the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera, Rhinotermitidae). Insectes Soc 50:226–233CrossRefGoogle Scholar
  39. Fellowes MDE, Kraaijeveld AR, Godfray HCJ (1998) Trade-offs constraining the evolution of Drosophila melanogaster defence against attack by the parasitoid Leptopilina boulardi. Proc R Soc Lond B 265:1553–1558CrossRefGoogle Scholar
  40. Fernández-Marín H, Zimmerman JK, Rehner SA, Wcislo WT (2006) Active use of the metapleural glands by ants in controlling fungal infection. Proc R Soc Lond B 273:1689–1695CrossRefGoogle Scholar
  41. Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643PubMedCrossRefGoogle Scholar
  42. Haine ER, Moret Y, Siva-Jothy M, Rolff J (2008a) Antimicrobial defense and persistent infection in insects. Science 322:1257–1259PubMedCrossRefGoogle Scholar
  43. Haine ER, Pollitt LC, Moret Y et al (2008b) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). J Insect Physiol 54:1090–1097PubMedCrossRefGoogle Scholar
  44. Hendee EC (1933) The association of the termites, Kalotermes minor, Reticulitermes hesperus, and Zootermopsis angusticollis with fungi. Univ Calif Publ Zool 39:111–134Google Scholar
  45. Hendee EC (1934) The association of termites and fungi. In: Kofoid CA (ed) Termites and termite control. Berkeley University, Berkeley, CA, pp 105–116Google Scholar
  46. Hughes DP, Pierce NE, Boomsma JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol 22:672–677CrossRefGoogle Scholar
  47. Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67:4399–4406PubMedCrossRefGoogle Scholar
  48. Inward D, Beccaloni G, Eggleton P (2007) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335PubMedCrossRefGoogle Scholar
  49. Jackson DE, Hart AG (2009) Does sanitation facilitate sociality? Anim Behav 77:e1–e5CrossRefGoogle Scholar
  50. Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216PubMedCrossRefGoogle Scholar
  51. Jiggins FM, Hurst GD (2003) The evolution of parasite recognition genes in the innate immune system: purifying selection on Drosophila melanogaster peptidoglycan recognition proteins. J Mol Evol 57:598–605PubMedCrossRefGoogle Scholar
  52. Jiggins FM, Kim KW (2005) The evolution of antifungal peptides in Drosophila. Genetics 171:1847–1859PubMedCrossRefGoogle Scholar
  53. Jiggins FM, Kim KW (2006) Contrasting evolutionary patterns in Drosophila immune receptors. J Mol Evol 63:769–780PubMedCrossRefGoogle Scholar
  54. John TJ, Samuel R (2000) Herd immunity and herd effect: new insights and definitions. Eur J Epidemiol 16:601–606PubMedCrossRefGoogle Scholar
  55. Karp RD, Duwel LE, Faulhaber LM, Harju MA (1994) Evolution of adaptive immunity: inducible responses in the American cockroach. Ann N Y Acad Sci 712(1):82–91PubMedCrossRefGoogle Scholar
  56. Karp RD, Duwel-Eby LE (1991) Adaptive immune responses in insects. In: Warr GW, Cohen N (eds) Phylogenesis of immune functions. CRC, Boca Raton, FL, pp 1–18Google Scholar
  57. Kirchner WH, Minkley N (2003) Nestmate discrimination in the harvester termite Hodotermes mossambicus. Insectes Soc 50:222–225CrossRefGoogle Scholar
  58. Kramm KR, West DF, Rockenbach PG (1982) Termite pathogens: transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes sp. termites. J Invertebr Pathol 40:1–6CrossRefGoogle Scholar
  59. Lamberty M, Zachary D, Lanot R et al (2001) Insect immunity – constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J Biol Chem 276:4085–4092PubMedCrossRefGoogle Scholar
  60. Le Guyader A, Rivault C, Chaperon J (1989) Microbial organisms carried by brown-banded cockroaches in relation to their spatial distribution in a hospital. Epidemiol Infect 102:485–492PubMedCrossRefGoogle Scholar
  61. Little TJ, O’Connor B, Colegrave N et al (2003) Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 13(6):489–492PubMedCrossRefGoogle Scholar
  62. Lo N, Engel MS, Cameron S et al (2007) Save Isoptera: A comment on Inward et al. Biol Lett 3:562–563PubMedCrossRefGoogle Scholar
  63. Logan JWM, Cowie RH, Wood TG (1990) Termite (Isoptera) control in agriculture and forestry by non-chemical methods: a review. Bull Entomol Res 80:309–330CrossRefGoogle Scholar
  64. Lutikova LI (1990) The influence of soil substrates from the Anacanthotermes ahngerianus Jac. termite-house on the development of entomopathogenic fungi. Mycol Phytopathol 24:520–528Google Scholar
  65. Maschwitz U (1974) Vergleichende Untersuchungen zur Funktion der Ameisenmetathorakaldrüse. Oecologia 16:303–310CrossRefGoogle Scholar
  66. Matsuura K (2001) Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus. Oikos 92:20–26CrossRefGoogle Scholar
  67. Matsuura K, Tamura T, Kobayashi N et al (2007) The antibacterial protein lysozyme identified as the termite egg recognition pheromone. PLoS ONE 2:e813. 10.137/journal.pone.0000813PubMedCrossRefGoogle Scholar
  68. Matsuura K, Vargo EL, Kawatsu K et al (2009a) Queen succession through asexual reproduction in termites. Science 323:1687PubMedCrossRefGoogle Scholar
  69. Matsuura K, Yashiro T, Shimizu K et al (2009b) Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme β-glucosidase. Curr Biol 19:1–7CrossRefGoogle Scholar
  70. Minkley N, Fujita A, Brune A, Kirchner WH (2006) Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insectes Soc 53:339–344CrossRefGoogle Scholar
  71. Miramontes O, DeSouza O (2008) Individual basis for collective behavior in the termite, Cornitermes cumulans. J Insect Sci 8:1–11PubMedCrossRefGoogle Scholar
  72. Moret Y (2006) Trans-generational immune priming: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc Biol Sci 273:1399–1405PubMedCrossRefGoogle Scholar
  73. Naug D, Camazine S (2002) The role of colony organization on pathogen transmission in social insects. J Theor Biol 215:427–439PubMedCrossRefGoogle Scholar
  74. Noirot C (1969) Glands and secretions. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press Inc, New York, NY, pp 89–123Google Scholar
  75. Ohkuma M, Noda S, Hongoh Y et al (2009) Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termite and the cockroach Cryptocercus. Proc R Soc Lond B 276:239–245CrossRefGoogle Scholar
  76. Owens IPF, Wilson K (1999) Immunocompetence: a neglected life history trait or conspicuous red herring? Trends Ecol Evol 14:170–172CrossRefGoogle Scholar
  77. Pasteels JM, Bordereau C (1998) Releaser pheromones in termites. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview Press, Boulder, CO, pp 193–215Google Scholar
  78. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3(3):e26PubMedCrossRefGoogle Scholar
  79. Pie MR, Rosengaus RB, Calleri DV, Traniello JFA (2005) Density and disease resistance in group-living insects: do eusocial species exhibit density-dependent prophylaxis? Ethol Ecol Evol 17:41–50CrossRefGoogle Scholar
  80. Pie MR, Rosengaus RB, Traniello JFA (2004) Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects. J Theor Biol 226(1):45–51PubMedCrossRefGoogle Scholar
  81. Polz MF, Harbison C, Cavanaugh CM (1999) Diversity and heterogeneity of epibiotic bacterial communities on the marine nematode Eubostrichus dianae. Appl Environ Microbiol 65:4271–4275PubMedGoogle Scholar
  82. Reeson AF, Wilson K, Gunn A et al (1998) Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density. Proc R Soc Lond B 265:1787–1791CrossRefGoogle Scholar
  83. Rheins LA, Karp RD (1985) Ontogeny of the invertebrate humoral immune response: studies on various developmental stages of the American cockroach (Periplaneta americana). Dev Comp Immunol 9:395–406PubMedCrossRefGoogle Scholar
  84. Rich S (1969) Quinones. In: Torgeson DC (ed) Fungicides: an advanced treatise, vol 2. Academic Press Inc, New York, NY, pp 647–648Google Scholar
  85. Rolff J, Siva-Jothy MT (2002) Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc Natl Acad Sci U S A 99:9916–9918PubMedCrossRefGoogle Scholar
  86. Roose-Amsaleg C, Brygoo Y, Harry M (2004) Ascomycete diversity in soil-feeding termite nests and soils from a tropical rainforest. Environ Microbiol 6:462–469PubMedCrossRefGoogle Scholar
  87. Rosengaus RB, Cornelisse T, Guschanski K, Traniello JFA (2007) Inducible immune proteins in the dampwood termite Zootermopsis angusticollis. Naturwissenschaften 94:25–33PubMedCrossRefGoogle Scholar
  88. Rosengaus RB, Guldin MR, Traniello JFA (1998a) Inhibitory effect of termite fecal pellets on fungal spore germination. J Chem Ecol 24:1697–1706CrossRefGoogle Scholar
  89. Rosengaus RB, Lefebvre ML, Carlock DM, Traniello JFA (2000a) Socially transmitted disease in adult reproductive pairs of the dampwood termite Zootermopsis angusticollis. Ethol Ecol Evol 12:419–433CrossRefGoogle Scholar
  90. Rosengaus RB, Lefebvre ML, Jordan C, Traniello JFA (1999a) Pathogen alarm behavior in a termite: A new form of communication in social insects. Naturwissenschaften 86:544–548PubMedCrossRefGoogle Scholar
  91. Rosengaus RB, Lefebvre ML, Traniello JFA (2000b) Inhibition of fungal spore germination by Nasutitermes: evidence for a possible antiseptic role of soldier defensive secretions. J Chem Ecol 26:21–39CrossRefGoogle Scholar
  92. Rosengaus RB, Maxmen AM, Coates LE, Traniello JFA (1998b) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav Ecol Sociobiol 44:125–134CrossRefGoogle Scholar
  93. Rosengaus RB, Moustakas JE, Calleri DV, Traniello JFA (2003) Nesting ecology and cuticular microbial loads in dampwood (Zootermopsis angusticollis) and drywood termites (Incisitermes minor, I. schwarzi, Cryptotermes cavifrons). J Insect Sci 3:31PubMedGoogle Scholar
  94. Rosengaus RB, Traniello JFA (1991) Biparental care in incipient colonies of the dampwood termite Zootermopsis angusticollis Hagen (Isoptera:Termopsidae). J Insect Behav 4:633–647CrossRefGoogle Scholar
  95. Rosengaus RB, Traniello JFA (1993a) Temporal polyethism in incipient colonies of the primitive termite Zootermopsis angusticollis: a single multi-age caste. J Insect Behav 6:237–252CrossRefGoogle Scholar
  96. Rosengaus RB, Traniello JFA (1993b) Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. Proc Natl Acad Sci U S A 90:6641–6645PubMedCrossRefGoogle Scholar
  97. Rosengaus RB, Traniello JFA (1997) Pathobiology and disease transmission in dampwood termites Zootermopsis angusticollis (Isoptera: Termopsidae) infected with the fungus Metarhizium anisopliae (Deuteromycotina:Hypomycetes). Sociobiology 30:185–195Google Scholar
  98. Rosengaus RB, Traniello JFA (2001) Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behav Ecol Sociobiol 50:546–556CrossRefGoogle Scholar
  99. Rosengaus RB, Traniello JFA, Chen T et al (1999b) Immunity in a social insect. Naturwissenschaften 86:588–591CrossRefGoogle Scholar
  100. Rosengaus RB, Traniello JFA, Lefebvre ML, Maxmen AB (2004) Fungistatic activity of the sternal gland secretion of the dampwood termite Zootermopsis angusticollis. Insectes Soc 51:1–6CrossRefGoogle Scholar
  101. Rowley AF, Powell A (2007) Invertebrate immune systems–specific, quasi-specific, or nonspecific? J Immunol 179:7209–7214PubMedGoogle Scholar
  102. Ryu JH, Kim SH, Lee HY et al (2008) Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319:777–782PubMedCrossRefGoogle Scholar
  103. Sackton TB, Lazzaro BP, Schlenke TA et al (2007) Dynamic evolution of the innate immune system in Drosophila. Nature Genetics 39:1461–1468PubMedCrossRefGoogle Scholar
  104. Sadd BM, Kleinlogel Y, Schmid-Hempel R, Schmid-Hempel P (2005) Trans-generational immune priming in a social insect. Biol Lett 1:386–388PubMedCrossRefGoogle Scholar
  105. Sadd BM, Schmid-Hempel P (2007) Facultative but persistent trans-generational immunity via the mother’s eggs in bumblebees. Curr Biol 17:1046–1047CrossRefGoogle Scholar
  106. Sands WL (1969) The association of termites and fungi. In: Krishna K, and Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, NY, pp 495–524Google Scholar
  107. Schlüns H, Crozier R (2009) Molecular and chemical immune defenses in ants (Hymenoptera: Formicidae). Myrmecol News 12:237–249Google Scholar
  108. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton, NJGoogle Scholar
  109. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366CrossRefGoogle Scholar
  110. Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551PubMedCrossRefGoogle Scholar
  111. Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32Google Scholar
  112. Sen R, Ishak HD, Estrada D et al (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci U S A 106:17805–17810PubMedCrossRefGoogle Scholar
  113. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11:217–321CrossRefGoogle Scholar
  114. Shellman-Reeve JS (1990) Dynamics of biparental care in the dampwood termite, Zootermopsis nevadensis (Hagen): Response to nitrogen availability. Behav Ecol Sociobiol 26:389–397CrossRefGoogle Scholar
  115. Shellman-Reeve JS (1997) Advantages of biparental care in the wood-dwelling termite, Zootermopsis nevadensis. Anim Behav 54:163–170PubMedCrossRefGoogle Scholar
  116. Siva-Jothy MT, Moret Y, Rolff J (2005) Insect immunity: an evolutionary ecology perspective. Adv Insect Physiol 32:1–48CrossRefGoogle Scholar
  117. Siva-Jothy MT, Tsubaki Y, Hooper R, Plaistow SJ (2001) Immune function in the face of chronic and acute parasite burdens. Physiol Entomol 26:1–6CrossRefGoogle Scholar
  118. Stow A, Briscoe D, Gillings M et al (2007) Antimicrobial defences increase with sociality in bees. Biol Lett 3:422–424PubMedCrossRefGoogle Scholar
  119. Stuart AM (1969) Social behavior and communication. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic, New York, NY, pp 193–232Google Scholar
  120. Söderhall K, Cerenius L (1998) Role of prophenoloxidase activating system in invertebrate immunity. Curr Opin Immunol 10:23–28PubMedCrossRefGoogle Scholar
  121. Thomas RJ (1987) Factors affecting the distribution and activity of fungi in the nests of Macrotermitinae (Isoptera). Soil Biol Biochem 19:343–349CrossRefGoogle Scholar
  122. Thompson GJ, Crozier YC, Crozier RH (2003) Isolation and characterization of a termite transferrin gene up-regulated on infection. Insect Mol Biol 12:1–7PubMedCrossRefGoogle Scholar
  123. Thorne BL (1997) Evolution of eusociality in termites. Annu Rev Ecol Syst 28:27–54CrossRefGoogle Scholar
  124. Thorne BL, Grimaldi DA, Krishna K (2000) Early fossil history of the termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 77–93Google Scholar
  125. Thorne BL, Traniello JFA (2003) Comparative social biology of basal taxa of ants and termites. Annu Rev Entomol 48:283–306PubMedCrossRefGoogle Scholar
  126. Thorne BL, Traniello JFA, Adams ES, Bulmer M (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies. Ethol Ecol Evol 11:149–169CrossRefGoogle Scholar
  127. Traniello JFA, Rosengaus RB, Savoie K (2002) The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc Natl Acad Sci U S A 99:6838–6842PubMedCrossRefGoogle Scholar
  128. Ugelvig LV, Cremer S (2007) Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr Biol 17:1967–1971PubMedCrossRefGoogle Scholar
  129. Viljakainen L, Evans JD, Hasselmann M et al (2009) Rapid evolution of immune proteins in social insects. Mol Biol Evol 26:1791–1801PubMedCrossRefGoogle Scholar
  130. Waller DA, LaFage JP (1987) Nutritional ecology of termites. In: Slansky F, Rodriguez JG (eds) Nutritional ecology of insects, mites and spiders. Wiley, New York, NY, pp 487–532Google Scholar
  131. Wang C, Powell JE, O’Connor BM (2002) Mites and nematodes associated with three subterranean termite species (Isoptera: Rhinotermitidae). Fla Entomol 85:499–506CrossRefGoogle Scholar
  132. Watson FL, Püttmann-Holgado R, Thomas F et al (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309:1874–1878PubMedCrossRefGoogle Scholar
  133. Wilson K, Cotter SC (2008) Density-dependent prophylaxis in insects. In: Ananthakrishnan TN, Whitman DW (eds) Insects and phenotypic plasticity: mechanisms and consequences. Science Publishers Inc, Plymouth, pp 137–176Google Scholar
  134. Wilson K, Reeson AF (1998) Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions. Ecol Entomol 23:100–101CrossRefGoogle Scholar
  135. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423PubMedCrossRefGoogle Scholar
  136. Wilson-Rich N, Stuart RJ, Rosengaus RB (2007) Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae. J Invertebr Pathol 95:17–25PubMedCrossRefGoogle Scholar
  137. Wood TG, Thomas RJ (1989) The mutualistic association between Macrotermitinae and Termitomyces. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic Press, San Diego, CA, pp 69–92CrossRefGoogle Scholar
  138. Yanagawa A, Shimizu S (2007) Resistance of the termite, Coptotermes formosanus Shiraki to Metarhizium anisopliae due to grooming. BioControl 52:75–85CrossRefGoogle Scholar
  139. Yanagawa A, Yokohari F, Shimizu S (2009) The role of antennae in removing entomopathogenic fungi from the cuticle of the termite, Coptotermes formosanus. J Insect Sci 9:6PubMedCrossRefGoogle Scholar
  140. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13:555–556PubMedGoogle Scholar
  141. Zhao C, Rickards RW, Trowell SC (2004) Antibiotics from Australian terrestrial invertebrates. Part 1: Antibacterial trinervitadienes from the termite Nasutitermes triodiae. Tetrahedron 60:10753–10759CrossRefGoogle Scholar
  142. Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22PubMedCrossRefGoogle Scholar

Copyright information

© Springer Netherlands 2010

Authors and Affiliations

  • Rebeca B. Rosengaus
    • 1
    Email author
  • James F.A. Traniello
    • 2
  • Mark S. Bulmer
    • 3
  1. 1.Department of BiologyNortheastern UniversityBostonUSA
  2. 2.Department of BiologyBoston UniversityBostonUSA
  3. 3.Department of Biological SciencesTowson UniversityTowsonUSA

Personalised recommendations