Beetle–Bacterial Symbioses: Endless Forms Most Functional

Literature Cited

1. 1. 

   Aanen DK, de Fine Licht HH, Debets AJM, Kerstes NAG, Hoekstra RF, Boomsma JJ. 2009. High symbiont relatedness stabilizes mutualistic cooperation in fungus-growing termites. Science 326:59561103–6
   [Google Scholar]
2. 2. 

   Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH et al. 2013. Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl. Environ. Microbiol. 79:113468–75
   [Google Scholar]
3. 3. 

   Alonso-Pernas P, Arias-Cordero E, Novoselov A, Ebert C, Rybak J et al. 2017. Bacterial community and PHB-accumulating bacteria associated with the wall and specialized niches of the hindgut of the forest cockchafer (Melolontha hippocastani). Front. Microbiol. 8:48716
   [Google Scholar]
4. 4. 

   Anbutsu H, Moriyama M, Nikoh N, Hosokawa T, Futahashi R et al. 2017. Small genome symbiont underlies cuticle hardness in beetles. PNAS 114:40E8382–91
   [Google Scholar]
5. 5. 

   Arce AN, Johnston PR, Smiseth PT, Rozen DE. 2012. Mechanisms and fitness effects of antibacterial defences in a carrion beetle. J. Evol. Biol. 25:5930–37
   [Google Scholar]
6. 6. 

   Ayayee P, Rosa C, Ferry JG, Felton G, Saunders M, Hoover K 2014. Gut microbes contribute to nitrogen provisioning in a wood-feeding cerambycid. Environ. Entomol. 43:4903–12
   [Google Scholar]
7. 7. 

   Ayayee PA, Larsen T, Rosa C, Felton GW, Ferry JG, Hoover K. 2016. Essential amino acid supplementation by gut microbes of a wood-feeding cerambycid. Environ. Entomol. 45:166–73
   [Google Scholar]
8. 8. 

   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 5:6e11339
   [Google Scholar]
9. 9. 

   Barraclough TG, Barclay MV, Vogler AP. 1998. Species richness: does flower power explain beetle-mania?. Curr. Biol. 8:23R843–45
   [Google Scholar]
10. 10. 

    Bar-Shmuel N, Behar A, Segoli M 2020. What do we know about biological nitrogen fixation in insects? Evidence and implications for the insect and the ecosystem. Insect Sci 27:3392–403
    [Google Scholar]
11. 11. 

    Bauer E, Kaltenpoth M, Salem H 2020. Minimal fermentative metabolism fuels extracellular symbiont in a leaf beetle. ISME J 14:3866–70
    [Google Scholar]
12. 12. 

    Becerra JX. 2007. The impact of herbivore-plant coevolution on plant community structure. PNAS 104:187483–88
    [Google Scholar]
13. 13. 

    Bennett GM, Moran NA. 2015. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. PNAS 112:3310169–76
    [Google Scholar]
14. 14. 

    Berasategui A, Axelsson K, Nordlander G, Schmidt A, Borg-Karlson A-K et al. 2016. The gut microbiota of the pine weevil is similar across Europe and resembles that of other conifer-feeding beetles. Mol. Ecol. 25:164014–31
    [Google Scholar]
15. 15. 

    Berasategui A, Moller AG, Weiss B, Beck CW, Bauchiero C et al. 2021. Symbiont genomic features and localization in the bean beetle, Callosobruchus maculatus. Appl. Environ. Microbiol. 87:12e0021221
    [Google Scholar]
16. 16. 

    Berasategui A, Salem H. 2020. Microbial determinants of folivory in insects. Cellular Dialogues in the Holobiont TG Bosch, M Hadfield 217–32 Boca Raton, FL: CRC Press
    [Google Scholar]
17. 17. 

    Berasategui A, Salem H, Paetz C, Santoro M, Gershenzon J et al. 2017. Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness. Mol. Ecol. 26:154099–110
    [Google Scholar]
18. 18. 

    Biedermann PHW, Vega FE. 2020. Ecology and evolution of insect-fungus mutualisms. Annu. Rev. Entomol. 65:431–55
    [Google Scholar]
19. 19. 

    Blackburn MB, Gundersen-Rindal DE, Weber DC, Martin PAW, Farrar RR 2008. Enteric bacteria of field-collected Colorado potato beetle larvae inhibit growth of the entomopathogens Photorhabdus temperata and Beauveria bassiana. Biol. Control 46:3434–41
    [Google Scholar]
20. 20. 

    Bright M, Bulgheresi S. 2010. A complex journey: transmission of microbial symbionts. Nat. Rev. Microbiol. 8:3218–30
    [Google Scholar]
21. 21. 

    Buchner P. 1965. Endosymbiosis of Animals with Plant Microorganisms Geneva: Interscience
22. 22. 

    Burton RA, Gidley MJ, Fincher GB. 2010. Heterogeneity in the chemistry, structure and function of plant cell walls. Nat. Chem. Biol. 6:10724–32
    [Google Scholar]
23. 23. 

    Busch A, Danchin EGJ, Pauchet Y. 2019. Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles. BMC Evol. Biol. 19:100
    [Google Scholar]
24. 24. 

    Ceja-Navarro JA, Karaoz U, Bill M, Hao Z, White RA et al. 2019. Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle. Nat. Microbiol. 4:5864–75
    [Google Scholar]
25. 25. 

    Ceja-Navarro JA, Nguyen NH, Karaoz U, Gross SR, Herman DJ et al. 2014. Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. ISME J 8:16–18
    [Google Scholar]
26. 26. 

    Ceja-Navarro JA, Vega FE, Karaoz U, Hao Z, Jenkins S et al. 2015. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 6:7618
    [Google Scholar]
27. 27. 

    Cheng C, Wickham JD, Chen L, Xu D, Lu M, Sun J. 2018. Bacterial microbiota protect an invasive bark beetle from a pine defensive compound. Microbiome 6:132
    [Google Scholar]
28. 28. 

    Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF et al. 2013. Herbivore exploits orally secreted bacteria to suppress plant defenses. PNAS 110:3915728–33
    [Google Scholar]
29. 29. 

    Chung SH, Scully ED, Peiffer M, Geib SM, Rosa C et al. 2017. Host plant species determines symbiotic bacterial community mediating suppression of plant defenses. Sci. Rep. 7:39690
    [Google Scholar]
30. 30. 

    Davis TS, Stewart JE, Mann A, Bradley C, Hofstetter RW 2019. Evidence for multiple ecological roles of Leptographium abietinum, a symbiotic fungus associated with the North American spruce beetle. Fungal Ecol 38:62–70
    [Google Scholar]
31. 31. 

    de Fine Licht HH, Biedermann PHW. 2012. Patterns of functional enzyme activity in fungus farming ambrosia beetles. Front. Zool. 9:13
    [Google Scholar]
32. 32. 

    Degenkolb T, Duering R-A, Vilcinskas A. 2011. Secondary metabolites released by the burying beetle Nicrophorus vespilloides: chemical analyses and possible ecological functions. J. Chem. Ecol. 37:7724–35
    [Google Scholar]
33. 33. 

    Després L, David J-P, Gallet C. 2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22:6298–307
    [Google Scholar]
34. 34. 

    Dose B, Niehs SP, Scherlach K, Florez LV, Kaltenpoth M, Hertweck C 2018. Unexpected bacterial origin of the antibiotic icosalide: two-tailed depsipeptide assembly in multifarious Burkholderia symbionts. ACS Chem. Biol. 13:92414–20
    [Google Scholar]
35. 35. 

    Douglas AE. 2009. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23:138–47
    [Google Scholar]
36. 36. 

    Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34
    [Google Scholar]
37. 37. 

    Duarte A, Welch M, Swannack C, Wagner J, Kilner RM. 2018. Strategies for managing rival bacterial communities: lessons from burying beetles. J. Anim. Ecol. 87:2414–27
    [Google Scholar]
38. 38. 

    Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 18:4586–608
    [Google Scholar]
39. 39. 

    Endara M-J, Coley PD, Ghabash G, Nicholls JA, Dexter KG et al. 2017. Coevolutionary arms race versus host defense chase in a tropical herbivore-plant system. PNAS 114:36E7499–505
    [Google Scholar]
40. 40. 

    Engl T, Eberl N, Gorse C, Krüger T, Schmidt THP et al. 2018. Ancient symbiosis confers desiccation resistance to stored grain pest beetles. Mol. Ecol. 27:82095–108
    [Google Scholar]
41. 41. 

    Engl T, Schmidt THP, Kanyile SN, Klebsch D. 2020. Metabolic cost of a nutritional symbiont manifests in delayed reproduction in a grain pest beetle. Insects 11:10717
    [Google Scholar]
42. 42. 

    Erb M, Reymond P. 2019. Molecular interactions between plants and insect herbivores. Annu. Rev. Plant Biol. 70:527–57
    [Google Scholar]
43. 43. 

    Farrell LD. 1998.. “ Inordinate fondness” explained: Why are there so many beetles?. Science 281:5376555–59
    [Google Scholar]
44. 44. 

    Flórez LV, Biedermann PHW, Engl T, Kaltenpoth M 2015. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat. Prod. Rep. 32:7904–36
    [Google Scholar]
45. 45. 

    Flórez LV, Kaltenpoth M. 2017. Symbiont dynamics and strain diversity in the defensive mutualism between Lagria beetles and Burkholderia. Environ. Microbiol. 19:93674–88
    [Google Scholar]
46. 46. 

    Flórez LV, Scherlach K, Gaube P, Ross C, Sitte E et al. 2017. Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism. Nat. Commun. 8:15172
    [Google Scholar]
47. 47. 

    Flórez LV, Scherlach K, Miller IJ, Rodrigues A, Kwan JC et al. 2018. An antifungal polyketide associated with horizontally acquired genes supports symbiont-mediated defense in Lagria villosa beetles. Nat. Commun. 9:15172
    [Google Scholar]
48. 48. 

    Gibson CM, Hunter MS. 2010. Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol. Lett. 13:2223–34
    [Google Scholar]
49. 49. 

    Guerreiro Filho O, Mazzafera P 2003. Caffeine and resistance of coffee to the berry borer Hypothenemus hampei (Coleoptera: Scolytidae). J. Agric. Food Chem. 51:246987–91
    [Google Scholar]
50. 50. 

    Hall CL, Wadsworth NK, Howard DR, Jennings EM, Farrell LD et al. 2011. Inhibition of microorganisms on a carrion breeding resource: the antimicrobial peptide activity of burying beetle (Coleoptera: Silphidae) oral and anal secretions. Environ. Entomol. 40:3669–78
    [Google Scholar]
51. 51. 

    Hammer TJ, Bowers MD. 2015. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179:11–14
    [Google Scholar]
52. 52. 

    Hammer TJ, Moran NA. 2019. Links between metamorphosis and symbiosis in holometabolous insects. Philos. Trans. R. Soc. Lond. B 374:178320190068
    [Google Scholar]
53. 53. 

    Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P. 1999. Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. PNAS 96:126814–19
    [Google Scholar]
54. 54. 

    Heise P, Liu Y, Degenkolb T, Vogel H, Schaberle TF, Vilcinskas A. 2019. Antibiotic-producing beneficial bacteria in the gut of the burying beetle Nicrophorus vespilloides. Front. Microbiol. 10:9185
    [Google Scholar]
55. 55. 

    Hirota B, Meng XY, Fukatsu T. 2020. Bacteriome-associated endosymbiotic bacteria of Nosodendron tree sap beetles (Coleoptera: Nosodendridae). Front. Microbiol. 11:18467
    [Google Scholar]
56. 56. 

    Hirota B, Okude G, Anbutsu H, Futahashi R, Moriyama M et al. 2017. A novel, extremely elongated, and endocellular bacterial symbiont supports cuticle formation of a grain pest beetle. mBio 8:57129
    [Google Scholar]
57. 57. 

    Hoang KL, Morran LT, Gerardo NM. 2019. Can a symbiont (also) be food?. Front. Microbiol. 10:3814
    [Google Scholar]
58. 58. 

    Hosokawa T, Hironaka M, Inadomi K, Mukai H, Nikoh N, Fukatsu T 2013. Diverse strategies for vertical symbiont transmission among subsocial stinkbugs. PLOS ONE 8:5634135
    [Google Scholar]
59. 59. 

    Huang Y-T, Skelton J, Hulcr J. 2019. Multiple evolutionary origins lead to diversity in the metabolic profiles of ambrosia fungi. Fungal Ecol 38:80–88
    [Google Scholar]
60. 60. 

    Hulcr J, Stelinski LL. 2017. The ambrosia symbiosis: from evolutionary ecology to practical management. Annu. Rev. Entomol. 62:285–303
    [Google Scholar]
61. 61. 

    Itoh H, Tago K, Hayatsu M, Kikuchi Y. 2018. Detoxifying symbiosis: microbe-mediated detoxification of phytotoxins and pesticides in insects. Nat. Prod. Rep. 35:5434–54
    [Google Scholar]
62. 62. 

    Janzen DH. 1977. Why fruits rot, seeds mold, and meat spoils. Am. Nat. 111:980691–713
    [Google Scholar]
63. 63. 

    Johnston PR, Rolff J. 2015. Host and symbiont jointly control gut microbiota during complete metamorphosis. PLOS Pathog 11:e1005246
    [Google Scholar]
64. 64. 

    Kabaluk T, Li-Leger E, Nam S. 2017. Metarhizium brunneum: an enzootic wireworm disease and evidence for its suppression by bacterial symbionts. J. Invertebr. Pathol. 150:82–87
    [Google Scholar]
65. 65. 

    Kaltenpoth M, Göttler W, Herzner G, Strohm E. 2005. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15:5475–79
    [Google Scholar]
66. 66. 

    Kaltenpoth M, Steiger S. 2014. Unearthing carrion beetles’ microbiome: characterization of bacterial and fungal hindgut communities across the Silphidae. Mol. Ecol. 23:61251–67
    [Google Scholar]
67. 67. 

    Keeling CI, Bohlmann J. 2006. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:4657–75
    [Google Scholar]
68. 68. 

    Kellner RLL. 2002. Molecular identification of an endosymbiotic bacterium associated with pederin biosynthesis in Paederus sabaeus (Coleoptera: Staphylinidae). Insect Biochem. Mol. Biol. 32:4389–95
    [Google Scholar]
69. 69. 

    Kellner RLL, Dettner K. 1996. Differential efficacy of toxic pederin in deterring potential arthropod predators of Paederus (Coleoptera: Staphylinidae) offspring. Oecologia 107:3293–300
    [Google Scholar]
70. 70. 

    Kiefer JST, Batsukh S, Bauer E, Hirota B, Weiss B et al. 2021. Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis. Commun. Biol. 4:554
    [Google Scholar]
71. 71. 

    Kikuchi Y, Hosokawa T, Nikoh N, Meng X-Y, Kamagata Y, Fukatsu T 2009. Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol 7:2
    [Google Scholar]
72. 72. 

    Kirsch R, Gramzow L, Theißen G, Siegfried BD, Ffrench-Constant RH et al. 2014. Horizontal gene transfer and functional diversification of plant cell wall degrading polygalacturonases: key events in the evolution of herbivory in beetles. Insect Biochem. Mol. Biol. 52:33–50
    [Google Scholar]
73. 73. 

    Klein A, Schrader L, Gil R, Manzano-Marín A, Flórez L et al. 2016. A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior. ISME J 10:2376–88
    [Google Scholar]
74. 74. 

    Kleinschmidt B, Kölsch G. 2011. Adopting bacteria in order to adapt to water—how reed beetles colonized the wetlands (Coleoptera, Chrysomelidae, Donaciinae). Insects 2:4540–54
    [Google Scholar]
75. 75. 

    Koga R, Meng X-Y, Tsuchida T, Fukatsu T. 2012. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. PNAS 109:20E1230–37
    [Google Scholar]
76. 76. 

    Kölsch G, Matz-Grund C, Pedersen BV. 2009. Ultrastructural and molecular characterization of endosymbionts of the reed beetle genus Macroplea (Chrysomelidae, Donaciinae), and proposal of “Candidatus Macropleicola appendiculatae” and “Candidatus Macropleicola muticae. .” Can. J. Microbiol. 55:111250–60
    [Google Scholar]
77. 77. 

    Kölsch G, Pedersen BV. 2008. Molecular phylogeny of reed beetles (Col., Chrysomelidae, Donaciinae): the signature of ecological specialization and geographical isolation. Mol. Phylogenet. Evol. 48:3936–52
    [Google Scholar]
78. 78. 

    Kölsch G, Pedersen BV. 2010. Can the tight co-speciation between reed beetles (Col., Chrysomelidae, Donaciinae) and their bacterial endosymbionts, which provide cocoon material, clarify the deeper phylogeny of the hosts?. Mol. Phylogenet. Evol. 54:3810–21
    [Google Scholar]
79. 79. 

    Kuriwada T, Hosokawa T, Kumano N, Shiromoto K, Haraguchi D, Fukatsu T. 2010. Biological role of Nardonella endosymbiont in its weevil host. PLOS ONE 5:10e13101
    [Google Scholar]
80. 80. 

    Lemoine MM, Engl T, Kaltenpoth M. 2020. Microbial symbionts expanding or constraining abiotic niche space in insects. Curr. Opin. Insect Sci. 39:14–20
    [Google Scholar]
81. 81. 

    Luan J, Sun X, Fei Z, Douglas AE 2018. Maternal inheritance of a single somatic animal cell displayed by the bacteriocyte in the whitefly Bemisia tabaci. Curr. Biol. 28:3459–65.e3
    [Google Scholar]
82. 82. 

    Maire J, Parisot N, Galvao Ferrarini M, Vallier A, Gillet B et al. 2020. Spatial and morphological reorganization of endosymbiosis during metamorphosis accommodates adult metabolic requirements in a weevil. PNAS 117:3219347–58
    [Google Scholar]
83. 83. 

    Maire J, Vincent-Monégat C, Masson F, Zaidman-Rémy A, Heddi A. 2018. An IMD-like pathway mediates both endosymbiont control and host immunity in the cereal weevil Sitophilus spp. Microbiome 6:6
    [Google Scholar]
84. 84. 

    Martinson VG. 2020. Rediscovering a forgotten system of symbiosis: historical perspective and future potential. Genes 11:91063
    [Google Scholar]
85. 85. 

    McCutcheon JP, Moran NA. 2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:113–26
    [Google Scholar]
86. 86. 

    McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD. 2009. Temporal lags and overlap in the diversification of weevils and flowering plants. PNAS 106:177083–88
    [Google Scholar]
87. 87. 

    McKenna DD, Shin S, Ahrens D, Balke M, Beza-Beza C et al. 2019. The evolution and genomic basis of beetle diversity. PNAS 116:4924729–37
    [Google Scholar]
88. 88. 

    Menezes C, Vollet-Neto A, Marsaioli AJ, Zampieri D, Fontoura IC et al. 2015. A Brazilian social bee must cultivate fungus to survive. Curr. Biol. 25:212851–55
    [Google Scholar]
89. 89. 

    Mithöfer A, Boland W. 2012. Plant defense against herbivores: chemical aspects. Annu. Rev. Plant Biol. 63:431–50
    [Google Scholar]
90. 90. 

    Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR. 2005. The evolution of agriculture in insects. Annu. Rev. Ecol. Evol. Syst. 36:563–95
    [Google Scholar]
91. 91. 

    Muhammad A, Habineza P, Ji TL, Hou YM, Shi ZH. 2019. Intestinal microbiota confer protection by priming the immune system of red palm weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae). Front. Physiol. 10:6294
    [Google Scholar]
92. 92. 

    Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A et al. 2013. Defensive bacteriome symbiont with a drastically reduced genome. Curr. Biol. 23:151478–84
    [Google Scholar]
93. 93. 

    Nathanson JA. 1984. Caffeine and related methylxanthines: possible naturally occurring pesticides. Science 226:4671184–87
    [Google Scholar]
94. 94. 

    Niehs SP, Kumpfmuller J, Dose B, Little RF, Ishida K et al. 2020. Insect-associated bacteria assemble the antifungal butenolide gladiofungin by non-canonical polyketide chain termination. Angew. Chem. Int. Ed. 59:23122–26
    [Google Scholar]
95. 95. 

    Noh MY, Muthukrishnan S, Kramer KJ, Arakane Y. 2016. Cuticle formation and pigmentation in beetles. Curr. Opin. Insect Sci. 17:1–9
    [Google Scholar]
96. 96. 

    Oakeson KF, Gil R, Clayton AL, Dunn DM, von Niederhausern AC et al. 2014. Genome degeneration and adaptation in a nascent stage of symbiosis. Genome Biol. Evol. 6:176–93
    [Google Scholar]
97. 97. 

    Piel J. 2002. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. PNAS 99:2214002–7
    [Google Scholar]
98. 98. 

    Piel J, Hofer I, Hui DQ 2004. Evidence for a symbiosis island involved in horizontal acquisition of pederin biosynthetic capabilities by the bacterial symbiont of Paederus fuscipes beetles. J. Bacteriol. 186:51280–86
    [Google Scholar]
99. 99. 

    Reis F, Kirsch R, Pauchet Y, Bauer E, Bilz LC et al. 2020. Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles. Nat. Commun. 11:2964
    [Google Scholar]
100. 100. 

     Rozen DE, Engelmoer DJP, Smiseth PT. 2008. Antimicrobial strategies in burying beetles breeding on carrion. PNAS 105:4617890–95
     [Google Scholar]
101. 101. 

     Salem H, Bauer E, Kirsch R, Berasategui A, Cripps M et al. 2017. Drastic genome reduction in an herbivore's pectinolytic symbiont. Cell 171:71520–31.e13
     [Google Scholar]
102. 102. 

     Salem H, Florez L, Gerardo N, Kaltenpoth M 2015. An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc. R. Soc. B 282: 1804.20142957
     [Google Scholar]
103. 103. 

     Salem H, Kirsch R, Pauchet Y, Berasategui A, Fukumori K et al. 2020. Symbiont digestive range reflects host plant breadth in herbivorous beetles. Curr. Biol. 30:152875–86.e4
     [Google Scholar]
104. 104. 

     Salem H, Onchuru TO, Bauer E, Kaltenpoth M. 2015. Symbiont transmission entails the risk of parasite infection. Biol. Lett. 11:1220150840
     [Google Scholar]
105. 105. 

     Scott JJ, Oh D-C, Yuceer MC, Klepzig KD, Clardy J, Currie CR 2008. Bacterial protection of beetle-fungus mutualism. Science 322:589863
     [Google Scholar]
106. 106. 

     Scott MP. 1998. The ecology and behavior of burying beetles. Annu. Rev. Entomol. 43:595–618
     [Google Scholar]
107. 107. 

     Scully ED, Geib SM, Carlson JE, Tien M, McKenna D, Hoover K. 2014. Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genom. 15:1096
     [Google Scholar]
108. 108. 

     Shukla SP, Beran F. 2020. Gut microbiota degrades toxic isothiocyanates in a flea beetle pest. Mol. Ecol. 29:234692–705
     [Google Scholar]
109. 109. 

     Shukla SP, Plata C, Reichelt M, Steiger S, Heckel DG et al. 2018. Microbiome-assisted carrion preservation aids larval development in a burying beetle. PNAS 115:4411274–79
     [Google Scholar]
110. 110. 

     Shukla SP, Vogel H, Heckel DG, Vilcinskas A, Kaltenpoth M. 2018. Burying beetles regulate the microbiome of carcasses and use it to transmit a core microbiota to their offspring. Mol. Ecol. 27:81980–91
     [Google Scholar]
111. 111. 

     Six D, Elser J. 2019. Extreme ecological stoichiometry of a bark beetle-fungus mutualism: stoichiometry of a symbiosis. Ecol. Entomol. 44:543–51
     [Google Scholar]
112. 112. 

     Skowronek M, Sajnaga E, Pleszczynska M, Kazimierczak W, Lis M, Wiater A 2020. Bacteria from the midgut of common cockchafer (Melolontha L.) larvae exhibiting antagonistic activity against bacterial symbionts of entomopathogenic nematodes: isolation and molecular identification. Int. J. Mol. Sci. 21:2580
     [Google Scholar]
113. 113. 

     Stammer H-J 1929. Die Symbiose der Lagriiden (Coleoptera). Z. Morphol. Ökol. Tiere 15:1–34
     [Google Scholar]
114. 114. 

     Stammer H-J. 1936. Studien an Symbiosen zwischen Käfern und Mikroorganismen. Z. Morphol. Ökol. Tiere 29:585–608
     [Google Scholar]
115. 115. 

     Sudakaran S, Kost C, Kaltenpoth M. 2017. Symbiont acquisition and replacement as a source of ecological innovation. Trends Microbiol 25:5375–90
     [Google Scholar]
116. 116. 

     Tianero MD, Balaich JN, Donia MS. 2019. Localized production of defence chemicals by intracellular symbionts of Haliclona sponges. Nat. Microbiol. 4:71149–59
     [Google Scholar]
117. 117. 

     Toju H, Tanabe AS, Notsu Y, Sota T, Fukatsu T. 2013. Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils. ISME J 7:71378–90
     [Google Scholar]
118. 118. 

     Uefuji H, Tatsumi Y, Morimoto M, Kaothien-Nakayama P, Ogita S, Sano H 2005. Caffeine production in tobacco plants by simultaneous expression of three coffee N-methyltrasferases and its potential as a pest repellant. Plant Mol. Biol. 59:2221–27
     [Google Scholar]
119. 119. 

     Vanderpool D, Bracewell RR, McCutcheon JP. 2018. Know your farmer: ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars. Mol. Ecol. 27:82077–94
     [Google Scholar]
120. 120. 

     Vigneron A, Masson F, Vallier A, Balmand S, Rey M et al. 2014. Insects recycle endosymbionts when the benefit is over. Curr. Biol. 24:192267–73
     [Google Scholar]
121. 121. 

     Vogel H, Shukla SP, Engl T, Weiss B, Fischer R et al. 2017. The digestive and defensive basis of carcass utilization by the burying beetle and its microbiota. Nat. Commun. 8:15186
     [Google Scholar]
122. 122. 

     Wang L, Feng Y, Tian J, Xiang M, Sun J et al. 2015. Farming of a defensive fungal mutualist by an attelabid weevil. ISME J 9:81793–801
     [Google Scholar]
123. 123. 

     Wang Y, Rozen DE. 2018. Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens. Ecol. Evol. 8:31646–54
     [Google Scholar]
124. 124. 

     Waterworth SC, Florez LV, Rees ER, Hertweck C, Kaltenpoth M, Kwan JC 2020. Horizontal gene transfer to a defensive symbiont with a reduced genome in a multipartite beetle microbiome. mBio 11:12851
     [Google Scholar]
125. 125. 

     Weiss B, Kaltenpoth M. 2016. Bacteriome-localized intracellular symbionts in pollen-feeding beetles of the genus Dasytes (Coleoptera, Dasytidae). Front. Microbiol. 7:7141
     [Google Scholar]
126. 126. 

     Zhang G, Browne P, Zhen G, Johnston A, Cadillo-Quiroz H, Franz N. 2017. Endosymbiont diversity and evolution across weevil tree of life. bioRxiv 171181. https://doi.org/10.1101/171181
     [Crossref]
127. 127. 

     Zhang S, Shu J, Xue H, Zhang W, Zhang Y et al. 2020. The gut microbiota in Camellia weevils are influenced by plant secondary metabolites and contribute to saponin degradation. mSystems 5:2e00692-19
     [Google Scholar]