The number of insect species transported to non-native regions is increasing, and, once established, these invasive insects have serious impacts on the environment and regional economies. Recent research highlights several cases of insect invasions facilitated by symbiotic microbes. Symbioses impact biological invasions, but few reviews have addressed the role of symbiotic microbes in insect invasions. Focusing on the insect–microbial symbiosis, we show the importance of microbial symbionts in determining the pest status of insects at insect–microbial levels, insect–plant–microbial levels, and other multispecific levels. Drawing on examples from different ecosystems, we review the key mechanisms and principles whereby facultative/mutualistic microbes affect insect invasions and coevolve with the invasive insects. We propose a conceptual framework for assessing the role of symbiotic microbes in insect invasions that promises improved risk analyses, spread and impact modeling, and management of invasive insects.

[Erratum, Closure]

An erratum has been published for this article:
The Role of Symbiotic Microbes in Insect Invasions

Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH. et al. 2013. Mountain pine beetles colonizing historical and naïve host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl. Environ. Microbiol. 79:3468–75 [Google Scholar]
  2. Adams AS, Jordan MS, Adams SM, Suen G, Goodwin LA. et al. 2011. Cellulose-degrading bacteria associated with the invasive woodwasp. Sirex noctilio. ISME J. 5:1323–31 [Google Scholar]
  3. Akbulut S, Stamps WT. 2012. Insect vectors of the pinewood nematode: a review of the biology and ecology of Monochamus species. For. Pathol. 42:89–99 [Google Scholar]
  4. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T. et al. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402–7 [Google Scholar]
  5. Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE. 2010. Microbial symbionts in insects influence down-regulation of defense genes in maize. PLOS ONE 5:e11339 [Google Scholar]
  6. Boucher DH, James S, Keeler KH. 1982. The ecology of mutualism. Annu. Rev. Ecol. Syst. 13:315–47 [Google Scholar]
  7. Bourtzis K, O'Neill S. 1998. Wolbachia infections and arthropod reproduction. BioScience 48:287–93 [Google Scholar]
  8. Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S. et al. 2003. Developmental origin and evolution of bacteriocytes in the aphid–Buchnera symbiosis. PLOS Biol 1:69–76 [Google Scholar]
  9. Bronstein JL. 2009. The evolution of facilitation and mutualism. J. Ecol. 97:1160–70 [Google Scholar]
  10. Calderón-Cortés N, Quesada M, Watanabe H, Cano-Camacho H, Oyama K. 2012. Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annu. Rev. Ecol. Evol. Syst. 43:45–71 [Google Scholar]
  11. Carrillo D, Duncan RE, Ploetz JN, Campbell AF, Ploetz RC. et al. 2014. Lateral transfer of a phytopathogenic symbiont among native and exotic ambrosia beetles. Plant Pathol 63:54–62 [Google Scholar]
  12. Casteel CL, Hansen AK, Walling LL, Paine TD. 2012. Manipulation of plant defense responses by the tomato psyllid (Bactericera cockerelli) and its associated endosymbiont. Candidatus Liberibacter psyllaurous. PLOS ONE 7:e35191 [Google Scholar]
  13. Cheng C. 2015. Ecological mediations of diverse microbial associates in a bark beetle Dendroctonus valens invasion in China PhD Dissertation 130 Institute of Zoology, Chinese Academy of Sciences, Beijing, China [Google Scholar]
  14. Cheng C, Zhou F, Lu M, Sun JH. 2015. Inducible pine rosin defense mediates interactions between an invasive insect–fungal complex and newly acquired sympatric fungal associates. Integr. Zool. 10:453–64 [Google Scholar]
  15. Cheng X-Y, Tian X-L, Wang Y-S, Lin R-M, Mao Z-C. et al. 2013. Metagenomics analysis of the pinewood nematode microbiome reveals a symbiotic relationship critical for xenobiotics degradation. Sci. Rep. 3:1869 [Google Scholar]
  16. Cruden DL, Markovetz AJ. 1987. Microbial ecology of the cockroach gut. Annu. Rev. Microbiol. 41:617–43 [Google Scholar]
  17. Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA. et al. 2003. Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299:386–88 [Google Scholar]
  18. De Fine Licht HH, Schiøtt M, Rogowska-Wrzesinska A, Nygaard S, Roepstorff P. et al. 2013. Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. PNAS 110:583–87 [Google Scholar]
  19. Desprez-Loustau M-L, Robin C, Buée M, Courtecuisse R, Garbaye J. et al. 2007. The fungal dimension of biological invasions. Trends Ecol. Evol. 22:472–80Excellent summary of fungal dimension of biological invasions. [Google Scholar]
  20. deWaard JR, Landry J-F, Schmidt BC, Derhousoff J, McLean JA. et al. 2009. In the dark in a large urban park: DNA barcodes illuminate cryptic and introduced moth species. Biodivers. Conserv. 18:3825–39 [Google Scholar]
  21. Dillon RJ, Dillon VM. 2004. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 49:71–92 [Google Scholar]
  22. Dillon RJ, Vennard CT, Buckling A, Charnley AK. 2005. Diversity of locust gut bacteria protects against pathogen invasion. Ecol. Lett. 8:1291–98 [Google Scholar]
  23. Dillon RJ, Vennard CT, Charnley AK. 2000. Pheromones: exploitation of gut bacteria in the locust. Nature 403:851 [Google Scholar]
  24. Douglas AE. 1989. Mycetocyte symbiosis in insects. Biol. Rev. 64:409–34 [Google Scholar]
  25. Douglas AE. 2009. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23:38–47 [Google Scholar]
  26. Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34 [Google Scholar]
  27. Douglas AE, Minto LB, Wilkinson TL. 2001. Quantifying nutrient production by the microbial symbionts in an aphid. J. Exp. Biol. 204:349–58 [Google Scholar]
  28. Ehrenfeld JG. 2010. Ecosystem consequences of biological invasions. Annu. Rev. Ecol. Evol. Syst. 41:59–80 [Google Scholar]
  29. Engelstädter J, Hurst GDD. 2009. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 40:127–49 [Google Scholar]
  30. Et-Touil A, Brasier CM, Bernier L. 1999. Localization of a pathogenicity gene in Ophiostoma novo-ulmi and evidence that it may be introgressed from O. ulmi. Mol. Plant-Microbe Interact. 12:6–15 [Google Scholar]
  31. Facon B, Hufbauer RA, Tayeh A, Loiseau A, Lombaert E. et al. 2011. Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr. Biol. 21:424–27 [Google Scholar]
  32. Fei S, Phillips J, Shouse M. 2014. Biogeomorphic impacts of invasive species. Annu. Rev. Ecol. Evol. Syst. 45:69–87 [Google Scholar]
  33. Feldhaar H. 2011. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 36:533–43 [Google Scholar]
  34. Feldhaar H, Straka J, Krischke M, Berthold K, Stoll S. et al. 2007. Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol. 5:48 [Google Scholar]
  35. Fraedrich SW, Harrington TC, Rabaglia RJ, Ulyshen MD, Mayfield AE. et al. 2008. A fungal symbiont of the redbay ambrosia beetle causes a lethal wilt in redbay and other Lauraceae in the southeastern United States. Plant Dis 92:215–24 [Google Scholar]
  36. Frago E, Dicke M, Godfray HCJ. 2012. Insect symbionts as hidden players in insect–plant interactions. Trends Ecol. Evol. 27:705–11 [Google Scholar]
  37. Goulson D. 2003. Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Evol. Syst. 34:1–26 [Google Scholar]
  38. Grarock K, Lindenmayer DB, Wood JT, Tidemann CR. 2013. Using invasion process theory to enhance the understanding and management of introduced species: a case study reconstructing the invasion sequence of the common myna (Acridotheres tristis). J. Environ. Manag. 129:398–409 [Google Scholar]
  39. Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D. et al. 2010. Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol. Ecol. 19:4365–78 [Google Scholar]
  40. Gurevitch J, Fox GA, Wardle GM, Inderjit Taub D. 2011. Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol. Lett. 14:407–18 [Google Scholar]
  41. Henry LM, Maiden MCJ, Ferrari J, Godfray HCJ. 2015. Insect life history and the evolution of bacterial mutualism. Ecol. Lett. 18:516–25 [Google Scholar]
  42. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE. et al. 2011. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–65A case study on the role of a bacterial symbiont in an invasive insect. [Google Scholar]
  43. Hiroki M, Kato Y, Kamito T, Miura K. 2002. Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften 89:167–70 [Google Scholar]
  44. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ. 2002. The causes and consequences of ant invasions. Annu. Rev. Ecol. Syst. 33:181–233 [Google Scholar]
  45. Holway DA, Suarez AV, Case TJ. 1998. Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–52 [Google Scholar]
  46. Hulcr J, Adams AS, Raffa K, Hofstetter RW, Klepzig KD. et al. 2010. Presence and diversity of Streptomyces in Dendroctonus and sympatric bark beetle galleries across North America. Microb. Ecol 61:759–68 [Google Scholar]
  47. Hulcr J, Dunn RR. 2011. The sudden emergence of pathogenicity in insect–fungus symbioses threatens naive forest ecosystems. Proc. R. Soc. B 278:2866–73Comprehensive summary of native and invasive insect–fungus symbioses in forestry ecosystems. [Google Scholar]
  48. Hulcr J, Rountree NR, Diamond SE, Stelinski LL, Fierer N. et al. 2012. Mycangia of ambrosia beetles host communities of bacteria. Microb. Ecol. 64:784–93 [Google Scholar]
  49. Humble LM, Allen EA. 2006. Forest biosecurity: alien invasive species and vectored organisms. Can. J. Plant Pathol. 28:S256–59 [Google Scholar]
  50. Hurst GDD, Hammarton TC, Bandi C, Majerus TMO, Bertrand D. et al. 1997. The diversity of inherited parasites of insects: The male-killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria. Genet. Res. 70:1–6 [Google Scholar]
  51. Jemal A, Hugh-Jones M. 1993. A review of the red imported fire ant (Solenopsis invicta Buren) and its impacts on plant, animal and human health. Prev. Vet. Med. 17:19–32 [Google Scholar]
  52. Jiu M, Zhou X-P, Tong L, Xu J, Yang X. et al. 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLOS ONE 2:e182 [Google Scholar]
  53. Joubert DA, Walker T, Carrington LB, De Bruyne JT, Kien DHT. et al. 2016. Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management. PLOS Pathog 12:e1005434 [Google Scholar]
  54. Kaltenpoth M, Gottler W, Herzner G, Strohm E. 2005. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15:475–79 [Google Scholar]
  55. Kendra PE, Montgomery WS, Niogret J, Epsky ND. 2013. An uncertain future for American Lauraceae: a lethal threat from redbay ambrosia beetle and laurel wilt disease. Am. J. Plant Sci. 4:727–38 [Google Scholar]
  56. Kolar C, Lodge DM. 2001. Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 16:199–204 [Google Scholar]
  57. Kostovcik M, Bateman C, Klarik M, Stelinski L, Jordal B, Hulcr J. 2015. The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing. ISME J 9:126–38Experimental evidence on ambrosia symbiosis from community pyrosequencing. [Google Scholar]
  58. Larkin DJ. 2012. Lengths and correlates of lag phases in upper-Midwest plant invasions. Biol. Invasions 14:827–38 [Google Scholar]
  59. Lee CE. 2002. Evolutionary genetics of invasive species. Trends Ecol. Evol. 17:386–91 [Google Scholar]
  60. Liebhold AM, Tobin PC. 2008. Population ecology of insect invasions and their management. Annu. Rev. Entomol. 53:387–408 [Google Scholar]
  61. Liu S-S, De Barro PJ, Xu J, Luan J-B, Zang L-S. et al. 2007. Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318:1769–72 [Google Scholar]
  62. Lockwood JL, Cassey P, Blackburn T. 2005. The role of propagule pressure in explaining species invasions. Trends Ecol. Evol. 20:223–28 [Google Scholar]
  63. Lou QZ, Lu M, Sun JH. 2014. Yeast diversity associated with invasive Dendroctonusvalens killing Pinus tabuliformis in China using culturing and molecular methods. Microb. Ecol. 68:397–415 [Google Scholar]
  64. Lu M, Wingfield MJ, Gillette NE, Mori SR, Sun JH. 2010. Complex interactions among host pines and fungi vectored by an invasive bark beetle. New Phytol 187:859–66The first evidence of symbiotic invasion of a beetle–fungus complex. [Google Scholar]
  65. Lu M, Wingfield MJ, Gillette NE, Sun JH. 2011. Do novel genotypes drive the success of an invasive bark beetle–fungus complex? Implications for potential reinvasion. Ecology 92:2013–19The first study on novel fungal genotypes driving the invasion success of a beetle–fungus complex. [Google Scholar]
  66. Lu M, Zhou XD, De Beer ZW, Wingfield MJ, Sun JH. 2009. Ophiostomatoid fungi associated with the invasive pine-infesting bark beetle, Dendroctonus valens, in China. Fungal Divers 38:133–45 [Google Scholar]
  67. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M. et al. 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10:689–710 [Google Scholar]
  68. Martínez AS, Fernández-Arhex V, Corley JC. 2006. Chemical information from the fungus Amylostereum areolatum and host-foraging behavioural in the parasitoid Ibalia leucospoides. Physiol. Entomol. 31:336–40 [Google Scholar]
  69. Martínez ÁT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S. et al. 2005. Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int. Microbiol. 8:195–204 [Google Scholar]
  70. McCutcheon JP, Moran NA. 2007. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. PNAS 104:19392–97 [Google Scholar]
  71. Mooney HA, Cleland EE. 2001. The evolutionary impact of invasive species. PNAS 98:5446–51 [Google Scholar]
  72. Morales-Jiménez J, Zúñiga G, Villa-Tanaca L, Hernández-Rodríguez C. 2009. Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonusvalens LeConte (Coleoptera: Curculionidae: Scolytinae). Microb. Ecol. 58:879–91 [Google Scholar]
  73. Morrien E, van der Putten WH. 2013. Soil microbial community structure of range-expanding plant species differs from co-occurring natives. J. Ecol. 101:1093–102 [Google Scholar]
  74. Mueller UG. 2012. Symbiont recruitment versus ant-symbiont co-evolution in the attine ant–microbe symbiosis. Curr. Opin. Microbiol. 15:269–77 [Google Scholar]
  75. Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A. et al. 2013. Defensive bacterome symbiont with a drastically reduced genome. Curr. Biol. 23:1478–84 [Google Scholar]
  76. Nakanishi K, Hoshino M, Nakai M, Kunimi Y. 2008. Novel RNA sequences associated with late male killing in Homona magnanima. Proc. R. Soc. B 275:1249–54 [Google Scholar]
  77. Ndlovu J, Richardson DM, Wilson JRU, Le Roux JJ. 2013. Co-invasion of South African ecosystems by an Australian legume and its rhizobial symbionts. J. Biogeogr. 40:1240–51 [Google Scholar]
  78. Negri I, Pellecchia M, Mazzoglio PJ, Patetta A, Alma A. 2006. Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX/XO sex-determination system. Proc. R. Soc. B 273:2409–22 [Google Scholar]
  79. Oh D-C, Poulsen M, Currie CR, Clardy J. 2009. Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat. Chem. Biol. 5:391–93 [Google Scholar]
  80. Ohkuma M, Noda S, Kudo T. 1999. Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl. Environ. Microbiol. 65:4926–34 [Google Scholar]
  81. Oliver KM, Moran NA, Hunter MS. 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. PNAS 102:12795–800 [Google Scholar]
  82. Oliver KM, Russell JA, Moran NA, Hunter MS. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. PNAS 100:1803–7 [Google Scholar]
  83. Paine TD, Raffa KF, Harrington TC. 1997. Interactions among Scolytid bark beetles, their associated fungi, and live host conifers. Annu. Rev. Entomol. 42:179–206 [Google Scholar]
  84. Piel J. 2002. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. PNAS 99:14002–7 [Google Scholar]
  85. Pieterse CMJ, Dicke M. 2007. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–69 [Google Scholar]
  86. Potrikus CJ, Breznak JA. 1981. Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. PNAS 78:4601–5 [Google Scholar]
  87. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC. et al. 2009. Mycorrhizal symbioses and plant invasions. Annu. Rev. Ecol. Evol. Syst. 40:699–715 [Google Scholar]
  88. Prior KM, Robinson JM, Meadley Dunphy SA, Frederickson ME. 2015. Mutualism between co-introduced species facilitates invasion and alters plant community structure. Proc. R. Soc. B 282:20142846 [Google Scholar]
  89. Richardson DM, Allsopp N, D'Antonio CM, Milton SJ, Rejmánek M. 2000. Plant invasions: the role of mutualism. Biol. Rev. 75:65–93 [Google Scholar]
  90. Richardson DM, Pyšek P. 2012. Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196:383–96 [Google Scholar]
  91. Rivera FN, González E, Gómez Z, López N, Hernández-Rodríguez C. et al. 2009. Gut-associated yeast in bark beetles of the genus Dendroctonus Erichson (Coleoptera: Curculionidae: Scolytinae). Biol. J. Linn. Soc. 98:325–42 [Google Scholar]
  92. Rodríguez-Echeverría S, Fajardo S, Ruiz-Díez B, Fernández-Pascual M. 2012. Differential effectiveness of novel and old legume–rhizobia mutualisms: implications for invasion by exotic legumes. Oecologia 170:253–61 [Google Scholar]
  93. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ. et al. 2009. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. PNAS 106:21236–41 [Google Scholar]
  94. Sabree ZL, Kambhampati S, Moran NA. 2009. Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. PNAS 106:19521–26 [Google Scholar]
  95. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J. et al. 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32:305–32 [Google Scholar]
  96. Sasaki T, Kawamura M, Ishikawa H. 1996. Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J. Insect Physiol. 42:125–29 [Google Scholar]
  97. Scarborough CL, Ferrari J, Godfray HCJ. 2005. Aphid protected from pathogen by endosymbiont. Science 310:1781 [Google Scholar]
  98. Scott JJ, Oh D-C, Yuceer MC, Klepzig KD, Clardy J. et al. 2008. Bacteria protection of beetle-fungus mutualism. Science 322:63 [Google Scholar]
  99. Shah MA, Reshi ZA, Khasa DP. 2009. Arbuscular mycorrhizas: drivers or passengers of alien plant invasion. Bot. Rev. 75:397–417 [Google Scholar]
  100. Shea K, Chesson P. 2002. Community ecology theory as a framework for biological invasions. Trends Ecol. Evol. 17:170–76 [Google Scholar]
  101. Simberloff D. 1997. Eradication. In. Stranger in Paradise: Impact and Management of Nonindigenous Species in Florida D Simberloff, DC Schmitz, TC Brown 221–28 Washington, DC: Island [Google Scholar]
  102. Simberloff D. 2009. The role of propagule pressure in biological invasions. Annu. Rev. Ecol. Evol. Syst. 40:81–102 [Google Scholar]
  103. Simberloff D, Von Holle B. 1999. Positive interactions of nonindigenous species: invasional meltdown?. Biol. Invasions 1:21–32 [Google Scholar]
  104. Six DL. 2013. The bark beetle holobiont: why microbes matter. J. Chem. Ecol. 39:989–1002 [Google Scholar]
  105. Slippers B, Hurley BP, Wingfield MJ. 2015. Sirex woodwasp: a model for evolving management paradigms of invasive forest pests. Annu. Rev. Entomol. 60:601–19 [Google Scholar]
  106. Snyder WE, Evans EW. 2006. Ecological effects of invasive arthropod generalist predators. Annu. Rev. Ecol. Evol. Syst. 37:95–122 [Google Scholar]
  107. Stouthamer R, Breeuwer JAJ, Hurst GDD. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53:71–102 [Google Scholar]
  108. Suarez AV, Tsutsui ND. 2008. The evolutionary consequences of biological invasions. Mol. Ecol. 17:351–60 [Google Scholar]
  109. Sun JH, Lu M, Gillette NE, Wingfield MJ. 2013. Red turpentine beetle: Innocuous native becomes invasive tree killer in China. Annu. Rev. Entomol. 58:293–311 [Google Scholar]
  110. Taerum SJ, Duong TA, de Beer ZW, Gillette N, Sun JH. et al. 2013. Large shift in symbiont assemblage in the invasive red turpentine beetle. PLOS ONE 8:e78126 [Google Scholar]
  111. Talbot PHB. 1977. The Sirex-Amylostereum-Pinus association. Annu. Rev. Phytopathol. 15:41–54 [Google Scholar]
  112. Thierry M, Becker N, Hajri A, Reynaud B, Lett J-M. et al. 2011. Symbiont diversity and non-random hybridization among indigenous (Ms) and invasive (B) biotypes of Bemisia tabaci. Mol. Ecol. 20:2172–87 [Google Scholar]
  113. Traveset A, Heleno R, Chamorro S, Vargas P, McMullen CK. et al. 2013. Invaders of pollination networks in the Galapagos Islands: emergence of novel communities. Proc. R. Soc. B 280:1–9 [Google Scholar]
  114. Traveset A, Richardson DM. 2014. Mutualistic interactions and biological invasions. Annu. Rev. Ecol. Evol. Syst. 45:89–113 [Google Scholar]
  115. Tschinkel WR. 2006. The Fire Ants Cambridge, MA: Harvard Univ. Press [Google Scholar]
  116. Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T. et al. 2010. Symbiotic bacterium modifies aphid body color. Science 330:1102–4 [Google Scholar]
  117. Vallet-Gely I, Lemaitre B, Boccard F. 2008. Bacterial strategies to overcome insect defences. Nat. Rev. Microbiol. 6:302–13 [Google Scholar]
  118. Vilcinskas A, Stoecker K, Schmidtberg H, Röhrich CR, Vogel H. 2013. Invasive harlequin ladybird carries biological weapons against native competitors. Science 340:862–63A case study on the role of a fungal symbiont in an invasive insect. [Google Scholar]
  119. Xu L, Lou Q, Cheng C, Lu M, Sun JH. 2015. Gut-associated bacteria of Dendroctonus valens and their involvement in verbenone production. Microb. Ecol. 70:1012–23 [Google Scholar]
  120. Xu L, Lu M, Sun JH. 2016. Invasive bark beetle-associated microbes degrade a host defensive monoterpene. Insect Sci 23:183–90 [Google Scholar]
  121. Wang B, Lu M, Cheng C, Salcedo C, Sun JH. 2013. Saccharide-mediated antagonistic effects of bark beetle fungal associates on larvae. Biol. Lett. 9:20120787 [Google Scholar]
  122. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH. et al. 2007. Metagenomic and functional analysis of hindgut microbial of a wood-feeding higher termite. Nature 450:560–69 [Google Scholar]
  123. Wilder SM, Holway DA, Suarez AV, LeBrun EG, Eubanks MD. 2011. Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasion. PNAS 108:20639–44 [Google Scholar]
  124. Zeh JA, Zeh DW. 2006. Male-killing Wolbachia in a live-bearing arthropod: brood abortion as a constraint on the spread of a selfish microbe. J. Invertebr. Pathol. 92:33–38 [Google Scholar]
  125. Zhang B, Edwards O, Kang L, Fuller S. 2014. A multi-genome analysis approach enables tracking of the invasive of a single Russian wheat aphid (Diuraphis noxia) clone throughout the New World. Mol. Ecol. 23:1940–51The first evidence of the role of a microbial symbiont in the spread of invasive insects. [Google Scholar]
  126. Zhao L, Lu M, Niu H, Fang G, Zhang S. et al. 2013. A native fungal symbiont facilitates the prevalence and development of an invasive pathogen-native vector symbiosis. Ecology 94:2817–26 [Google Scholar]
  127. Zhao L, Mota M, Vieira P, Butcher RA, Sun JH. 2014. Interspecific communication between pinewood nematode, its insect vector, and associated microbes. Trends Parasitol 30:299–308A comprehensive review of chemical communication between an invasive nematode, native vector beetle, and associated microbes. [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