Metamorphosis of a butterfly-associated bacterial community

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Hammer, Tobin J ^a,b   McMillan, W Owen ^b   Fierer, Noah ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ADULT; ANIMAL STRUCTURES; ARTICLE; BUTTERFLY; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DNA SEQUENCE; FEMALE; HELICONIUS ERATO; HIGH THROUGHPUT SEQUENCING; MALE; METAMORPHOSIS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROFLORA; NONHUMAN; REPRODUCTIVE BEHAVIOR; RNA GENE; RNA SEQUENCE; SYMBIOSIS; TAXONOMIC IDENTIFICATION;

ANIMALS; BIOLOGICAL EVOLUTION; BIOLOGICAL MARKERS; BUTTERFLIES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; METAMORPHOSIS, BIOLOGICAL; MICROBIOTA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

EID: 84899880796     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086995     Document Type: Article

References (80)

1. Boggs CL, Watt WB, Ehrlich PR (2003) Butterflies: ecology and evolution taking flight. The University of Chicago Press.
2. Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct. Ecol. 23, 38-47.
3. Brownlie JC, Johnson KN (2009) Symbiont-mediated protection in insect hosts. Trends Microbiol. 17, 348-354.
4. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 36, 533-543.
5. Engel P, Moran NA (2013) The gut microbiota of insects - diversity in structure and function. FEMS Microbiol. Rev. (doi:10.1111/1574-6976.12025).
6. Steinhaus EA (1941) A study of the bacteria associated with thirty species of insects. J. Bacteriol. 42, 757-790.
7. Kim JY, Lee J, Shin N-R, Yun J-H, Whon T-W, et al. (2013) Orbus sasakiae sp. nov., a bacterium isolated from the gut of the butterfly Sasakia charonda, and emended description of the genus Orbus. Int. J. Syst. Evol. Micr. 63, 1766-1770.
8. Tagami Y, Miura K (2004) Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Insect Mol. Biol. 13, 359-364. (Pubitemid 39048163)
9. Narita S, Nomura M, Kato Y, Fukatsu T (2006) Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications. Mol. Ecol. 15, 1095-1108.
10. Russell JA, Funaro CF, Giraldo YM, Goldman-Huertas B, Suh D, et al. (2012) A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review. PLoS ONE 7, e51027.
11. Kingsley V V. (1972) Persistence of Intestinal Bacteria in the Developmental Stages of the Monarch Butterfly (Danaus plexippus). J. Invertebr. Pathol. 20, 51-58.
12. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276, 734-740.
13. Broderick NA, Robinson CJ, McMahon MD, Holt J, Handelsman J, et al. (2009) Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biol. 7, 11.
14. Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J (2010) Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb. Ecol. 59, 199-211.
15. Lauzon C, McCombs S, Potter S, Peabody N (2009) Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the mediterranean fruit fly (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 102, 85-95.
16. Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl. Environ. Microb. 78, 2830-2840.
17. Vasanthakumar A, Handelsman J, Schloss PD, Bauer LS, Raffa KF (2008) Gut microbiota of an invasive subcortical beetle, Agrilus planipennis Fairmaire, across various life stages. Environ. Entomol. 37, 1344-1353.
18. Wong CNA, Ng P, Douglas AE (2011) Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ. Microbiol. 13, 1889-1900.
19. Brucker RM, Bordenstein SR (2012) The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66, 349-362.
20. Arias-Cordero E, Ping L, Reichwald K, Delb H, Platzer M, et al. (2012) Comparative evaluation of the gut microbiota associated with the below- and above-ground life stages (larvae and beetles) of the forest cockchafer, Melolontha hippocastani. PLoS ONE 7, e51557.
21. Colman DR, Toolson EC, Takacs-Vesbach CD (2012) Do diet and taxonomy influence insect gut bacterial communities? Mol. Ecol. 21, 5124-5137.
22. Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, et al. (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970-974.
23. 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. P. Natl. Acad. Sci. USA 106, 21236-21241.
24. Engler-Chaouat HS, Gilbert LE (2007) De novo synthesis vs. sequestration: negatively correlated metabolic traits and the evolution of host plant specialization in cyanogenic butterflies. J. Chem. Ecol. 33, 25-42. (Pubitemid 46011200)
25. Gilbert LE (1972) Pollen feeding and reproductive biology of Heliconius butterflies. P. Natl. Acad. Sci. USA 69, 1403-1407.
26. Brown KS (1981) The biology of Heliconius and related genera. Annu. Rev. Entomol. 26, 427-456.
27. The Heliconius Genome Consortium (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94-98.
28. Werren JH, Windsor D, Guo L (1995) Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. B 262, 197-204. (Pubitemid 26452508)
29. Muñoz AG, Baxter SW, Linares M, Jiggins CD (2011) Deep mitochondrial divergence within a Heliconius butterfly species is not explained by cryptic speciation or endosymbiotic bacteria. BMC Evol. Biol. 11, 358.
30. Xiang H, Wei G-F, Jia S, Miao X-X, Zhou Z, et al. (2006) Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can. J. Microbiol. 52, 1085-1092.
31. Belda E, Pedrola L, Peretó J, Martínez-Blanch JF, Montagud A, et al. (2011) Microbial diversity in the midguts of field and lab-reared populations of the European corn borer Ostrinia nubilalis. PLoS ONE 6, e21751.
32. Lehman RM, Lundgren JG, Petzke LM (2009) Bacterial communities associated with the digestive tract of the predatory ground beetle, Poecilus chalcites, and their modification by laboratory rearing and antibiotic treatment. Microb. Ecol. 57, 349-358.
33. Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A (2011) Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 7, e1002272.
34. Smiley J (1978) Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passiflora. Science 201, 745-747.
35. Walters JR, Stafford C, Hardcastle TJ, Jiggins CD (2012) Evaluating female remating rates in light of spermatophore degradation in Heliconius butterflies: pupal-mating monandry versus adult-mating polyandry. Ecol. Entomol. 37, 257-268.
36. Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. P. Natl. Acad. Sci. USA 105, 17994-17999.
37. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621-1624.
38. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336.
39. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461.
40. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, et al. (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618.
41. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microb. 73, 5261-5267. (Pubitemid 47326658)
42. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research 37, D141-D145.
43. Jones RT, Sanchez LG, Fierer N (2013) A cross-taxon analysis of insect-associated bacterial diversity. PLoS ONE 8, e61218.
44. Kuczynski J, Costello EK, Nemergut DR, Zaneveld J, Lauber CL, et al. (2010) Direct sequencing of the human microbiome readily reveals community differences. Genome Biology 11, 210.
45. R Core Team (2013) R: A language and environment for statistical computing. R Foundation Statistical Computing. (http://www.R-project.org).
46. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. (2013) vegan: Community Ecology Package. R package version 2.0-7. (http://CRAN.R- project.org/package = vegan).
47. Clarke KR, Gorley RN (2006) PRIMER v6. PRIMER-E, Plymouth, UK.
48. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84, 511-525. (Pubitemid 36893087)
49. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32-46.
50. Broderick NA, Raffa KF, Goodman RM, Handelsman J (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ. Microb. 70, 293-300. (Pubitemid 38090217)
51. Zaspel JM, Hoy MA (2008) Microbial diversity associated with the fruit-piercing and blood-feeding moth Calyptra thalictri (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 101, 1050-1055.
52. Brinkmann N, Martens R, Tebbe CC (2008) Origin and diversity of metabolically active gut bacteria from laboratory-bred larvae of Manduca sexta (Sphingidae, Lepidoptera, Insecta). Appl. Environ. Microb. 74, 7189-7196. (Pubitemid 352773570)
53. Martin JD, Mundt JO (1972) Enterococci in insects. Appl. Microbiol. 24, 575-580.
54. Fisher K, Phillips C (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiology 155, 1749-1757.
55. Bucher GE (1963) Survival of populations of Streptococcus faecalis Andrewes and Horder in the gut of Galleria mellonella (Linnaeus) during metamorphosis, and transmission of the bacteria to the filial generation of the host. J. Insect Pathol. 5, 336-343.
56. Kwong WK, Moran NA (2013) Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order 'Enterobacteriales' of the Gammaproteobacteria. Int. J. Syst. Evol. Micr. 63, 2008-2018.
57. Engel P, Kwong WK, Moran NA (2013) Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honey bee, Apis mellifera. Int. J. Syst. Evol. Micr. (doi:10.1099/ijs.0.049569-0).
58. Pinto-Tomás AA, Sittenfeld A, Uribe-Lorio L, Chavarria F, Mora M, et al. (2011) Comparison of midgut bacterial diversity in tropical caterpillars (Lepidoptera: Saturniidae) fed on different diets. Environ. Entomol. 40, 1111-1122.
59. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, et al. (2010) Acetic acid bacteria, newly emerging symbionts of insects. Appl. Environ. Microb. 76, 6963-6970.
60. Crotti E, Damiani C, Pajoro M, Gonella E, Rizzi A, et al. (2009) Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ. Microbiol. 11, 3252-3264.
61. Ryu J, Kim S-H, Lee H-Y, Bai J-Y, Nam Y-D, et al. (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319, 777-782. (Pubitemid 351225861)
62. Shin SC, Kim S-H, You H, Kim B, Kim AC, et al. (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334, 670-674.
63. Ridley E V, Wong AC-N, Westmiller S, Douglas AE (2012) Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS ONE 7, e36765.
64. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F (2007) Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol. Ecol. 59, 600-610. (Pubitemid 46376241)
65. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. P. Natl. Acad. Sci. USA, 109, 11002-11007.
66. Eberhard SH, Hikl AL, Boggs CL, Krenn HW (2009) Saliva or regurgitated nectar? What Heliconius butterflies (Lepidoptera: Nymphalidae) use for pollen feeding. Ann. Entomol. Soc. Am. 102, 1105-1108.
67. Sudakaran S, Salem H, Kost C, Kaltenpoth M (2012) Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol. Ecol. 21, 6134-6151.
68. Sabree ZL, Hansen AK, Moran NA (2012) Independent studies using deep sequencing resolve the same set of core bacterial species dominating gut communities of honey bees. PLoS ONE 7, e41250.
69. Nijhout HF, Williams CM (1974) Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. J. Exp. Biol. 61, 481-491.
70. Russell V, Dunn PE (1996) Antibacterial proteins in the midgut of Manduca sexta during metamorphosis. J. Insect Physiol. 42, 65-71. (Pubitemid 126686202)
71. Judy KJ, Gilbert LI (1969) Morphology of the alimentary canal during the metamorphosis of Hyalophora cecropia (Lepidoptera: Saturniidae). Ann. Entomol. Soc. Am. 62, 1438-1446.
72. Hakim RS, Baldwin K, Smagghe G (2010) Regulation of midgut growth, development, and metamorphosis. Annu. Rev. Entomol. 55, 593-608.
73. Lowe T, Garwood RJ, Simonsen TJ, Bradley RS, Withers PJ (2013) Metamorphosis revealed: time-lapse three-dimensional imaging inside a living chrysalis. J. R. Soc. Interface 10, 20130304.
74. Schultz JC, Lechowicz MJ (1986) Hostplant, larval age, and feeding behavior influence midgut pH in the gypsy moth (Lymantria dispar) . Oecologia 71, 133-137.
75. Appel HM, Maines LW (1995) The influence of host plant on gut conditions of gypsy moth (Lymantria dispar) caterpillars. J. Insect Physiol. 41, 241-246.
76. Kristensen NP (1999) Phylogeny of endopterygote insects, the most successful lineage of living organisms. Eur. J. Entomol. 96, 237-253.
77. Hennig W (1981) Insect phylogeny John Wiley & Sons.
78. Whiting MF (2003) Phylogeny of the holometabolous insects: the most successful group of terrestrial organisms. In: Assembling the Tree of Life (eds Cracraft J, Donoghue MJ), pp. 345-361. Oxford University Press.
79. Grimaldi D, Engel MS (2005) Evolution of the Insects Cambridge University Press.
80. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, et al. (2009) Bacterial community variation in human body habitats across space and time. Science 326, 1694-1697.