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?

Molecular Phylogenetics and Evolution

Volumn 54, Issue 3, 2010, Pages 810-821

  Kölsch, Gregor ^a   Pedersen, Bo V ^b  

^a UNIVERSITY OF HAMBURG   (Germany)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

16S rRNA; Co speciation; Endosymbionts; Enterobacteriaceae; Insects; Mutation rate

Indexed keywords

BACTERIAL DNA; MITOCHONDRIAL DNA; RNA 16S;

ANIMAL; ARTICLE; BACTERIUM; BEETLE; BIOLOGICAL MODEL; CLASSIFICATION; DNA SEQUENCE; GENE; GENETICS; MICROBIOLOGY; MOLECULAR EVOLUTION; PHYLOGENY; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; SYMBIOSIS;

ANIMALS; BACTERIA; BEETLES; DNA, BACTERIAL; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENES, INSECT; GENETIC SPECIATION; MODELS, GENETIC; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS;

BACTERIA (MICROORGANISMS); CHRYSOMELIDAE; COLEOPTERA; DONACIINAE; ENTEROBACTERIACEAE; HEXAPODA;

EID: 76549114665     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2009.10.038     Document Type: Article

References (98)

1. Aanen D.K., Eggleton P., Rouland-Lefèvre C., Guldberg-Froeslev T., Rosendahl S., and Boomsma J.J. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc. Natl. Acad. Sci. USA 99 (2002) 14887-14892
2. Aksoy S., Chen X., and Hypsa V. Phylogeny and potential transmission routes of midgut-associated endosymbionts of tsetse (Diptera: Glossinidae). Insect Mol. Biol. 6 (1997) 183-190
3. Andersson S.G.E., and Kurland C.G. Reductive evolution of resident genomes. Trends Microbiol. 6 (1998) 263-268
4. Askevold I.S. Classification of Tertiary fossil Donaciinae of North America and their implications about evolution of Donaciinae (Coleoptera: Chrysomelidae). Can. J. Zool. 68 (1990) 2135-2145
5. Askevold I.S. Classification, reconstructed phylogeny, and geographic history of the New World members of Plateumaris Zhomson, 1859 (Coleoptera: Chrysomelidae: Donaciinae). Mem. Entomol. Soc. Canada 157 (1991) 1-175
6. Baumann P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59 (2005) 155-189
7. Baumann P., Baumann L., Lai C.-Y., and Rouhbakhsh D. Genetics, physiology, and the evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49 (1995) 55-94
8. Baumann P., Moran N., and Baumann L. Bacteriocyte-associated Endosymbionts of Insects. The Prokaryotes (2006), Springer, New York pp. 403-438
9. Billen J., and Buschinger A. Morphology and ultrastructure of a specialized bacterial pouch in the digestive tract of Tetraponera ants (Formicidae, Pseudomyrmecinae). Arthropod Struct. Dev. 29 (2000) 259-266
10. Böving A.G. Natural history of the larvae of Donaciinae. Int. Revue Ges. Hydrobiol.; Biol. Suppl. 3 (1910) 1-108
11. Buchner P. Tier und Pflanze in Symbiose (1930), Gebrüder Bornträger, Berlin
12. Buchner P. Endosymbiose der Tiere mit pflanzlichen Mikroorganismen (1953), Birkhäuser, Basel, Stuttgart
13. Cannone J.J., Subramanian S., Schnare M.N., Collett J.R., D'Souza L.M., Du Y., Feng B., Lin N., Madabusi L.V., Müller K.M., Pande N., Shang Z., Yu N., and Gutell R.R. The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinform. 3 (2002) 2
14. Chen S.H. Notes on Donaciine beetles. Sinensia 12 (1941) 1-17
15. Chen X., Li S., and Aksoy S. Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosmbiont, Wigglesworthia glossinidia. J. Mol. Evol. 48 (1999) 49-58
16. Clark M.A., Moran N.A., and Baumann P. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol. Biol. Evol. 16 (1999) 1586-1598
17. Clark M.A., Moran N.A., Baumann P., and Wernegreen J.J. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54 (2000) 517-525
18. Conord C., Despres L., Vallier A., Balmand S., Miquel C., Zundel S., Lemperiere G., and Heddi A. Long-term evolutionary stability of bacterial endosymbiosis in Curculionoidea: additional evidence of symbiont replacement in the Dryophthoridae family. Mol. Biol. Evol. 25 (2008) 859-868
19. Currie C.R., Wong B., Stuart A.E., Schultz T.R., Rehner S.A., Mueller U.G., Sung G.-H., Spatafora J.W., and Straus N.A. Ancient tripartite coevolution in the Attine ant-microbe symbiosis. Science 299 (2003) 386-388
20. Dale C., and Moran N.A. Molecular interactions between bacterial symbionts and their hosts. Cell 126 (2006) 453-465
21. de Vienne D.M., Giraud T., and Martin O.C. A congruence index for testing topological similarity between trees. Bioinformatics 23 (2007) 3119-3124
22. Degnan P.H., Lazarus A.B., Brock C.D., and Wernegreen J.J. Host-symbiont stability and fast evolutionary rates in an ant-bacterium association: cospeciation of Camponotus species and their endosymbionts, Candidatus Blochmannia. Syst. Biol. 53 (2004) 95-110
23. Dillon R.J., and Dillon V.M. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 49 (2004) 71-92
24. Douglas A.E. Mycetocyte symbiosis in insects. Biol. Rev. Camb. Phil. Soc. 64 (1989) 409-434
25. Douglas A.E. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43 (1998) 17-37
26. Douglas A.E., and Raven J.A. Genomes at the interface between bacteria and organelles. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 (2003) 5-17 (discussion 517-518)
27. Excoffier L., Laval G., and Schneider S. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinformatics Online 1 (2005) 47-50
28. Fukatsu T., and Nikoh N. Two intracellular symbiotic bacteria from the mulberry Psyllid Anomoneura mori (Insecta, Homoptera). Appl. Environ. Microbiol. 64 (1998) 3599-3606
29. Funk D.J., Wernegreen J.J., and Moran N.A. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics 157 (2001) 477-489
30. Gil R., Latorre A., and Moya A. Bacterial endosymbionts of insects: insights from comparative genomics. Environ. Microbiol. 6 (2004) 1109-1122
31. Gómez-Zurita, J., Hunt, T., Kopliku, F., Vogler, A.P., 2007. Recalibrated tree of leaf beetles (Chrysomelidae) indicates independent diversification of angiosperms and their insect herbivores. PLoS ONE 2 (4), e360. doi:10.1371/journal.pone.0000360.
32. Goettler W., Kaltenpoth M., Herzner G., and Strohm E. Morphology and ultrastructure of a bacteria cultivation organ: the antennal glands of female European beewolves, Philanthus triangulum (Hymenoptera, Crabronidae). Arthropod Struct. Dev. 36 (2007) 1-9
33. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 (1999) 95-98
34. Heddi A., Charles H., Khatchadourian C., Bonnot G., and Nardon P. Molecular characterization of the principal symbiotic bacteria of the weevil Sitophilus oryzae: a peculiar G + C content of an endocytobiotic DNA. J. Mol. Evol. 47 (1998) 52-61
35. Hirschler J. 4. Über leberartige Mitteldarmdrüsen und ihre embryonale Entwicklung bei Donacia (Coleoptera). Zool. Anz. 31 (1907) 766-770
36. Hirschler J. Die Embryonalentwicklung von Donacia crassipes L. Z. wiss. Zool. 92 (1909) 627-744
37. Hosokawa T., Kikuchi Y., Nikoh N., Shimada M., and Fukatsu T. Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol. 4 (2006) e337
38. Houk E.J., and Griffiths G.W. Intracellular symbiotes of the Homoptera. Annu. Rev. Entomol. 25 (1980) 161-187
39. Huelsenbeck J.P., and Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 (2001) 754-755
40. Kane M.D., and Pierce N.E. Diversity within diversity: molecular approaches to studying microbial interactions with insects. In: Schierwater B., Streit B., Wagner G.P., and DeSalle R. (Eds). Molecular Ecology and Evolution: Approaches and Applications (1994), Birkhauser Verlag, Basel 509-524
41. Kergoat G.J., Silvain J.-F., Buranapanichpan S., and Tuda M. When insects help to resolve plant phylogeny: evidence for a paraphyletic genus Acacia from the systematics and host-plant range of their seed-predators. Zool. Scr. 36 (2007) 143-152
42. Koch A. Insects and their endosymbionts. In: Henry S.M. (Ed). Symbiosis (1967), Academic Press, New York, London 1-106
43. Kölsch G., Matz-Grund C., and Pedersen B.V. 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 (2009) 1250-1260
44. Kölsch G., and Pedersen B.V. Molecular phylogeny of reed beetles (Col., Chrysomelidae, Donaciinae): the signature of ecological specialization and geographical isolation. Mol. Phylogen. Evol. 48 (2008) 936-952
45. Komaki K., and Ishikawa H. Intracellular bacterial symbionts of aphids possess many genomic copies per bacterium. J. Mol. Evol. 48 (1999) 717-722
46. Krell F.T., and Cranston P.S. Which side of the tree is more basal?. Syst. Entomol. 29 (2004) 279-281
47. Lai C.Y., Baumann L., and Baumann P. Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc. Natl. Acad. Sci. USA 91 (1994) 3819-3823
48. Lane D.J. 16S/23S rRNA sequencing. In: Stackebrandt E., and Goodfellow M. (Eds). Nucleic Acid Techniques in Bacterial Systematics (1991), John Wiley & Sons, Chichester New York Brisbane Toronto Singapore 115-175
49. Lefevre C., Charles H., Vallier A., Delobel B., Farrell B., and Heddi A. Endosymbiont phylogenesis in the Dryophthoridae weevils: evidence for bacterial replacement. Mol. Biol. Evol. 21 (2004) 965-973
50. Legendre, P., Anderson, M.J., 1998. DistPCoA. University of Montreal/University of Sydney.
51. Legendre P., Desdevises Y., and Bazin E. A statistical test for host-parasite coevolution. Syst. Biol. 51 (2002) 217-234
52. Lo N., Bandi C., Watanabe H., Nalepa C., and Beninati T. Evidence for cocladogenesis between diverse Dictyopteran lineages and their intracellular endosymbionts. Mol. Biol. Evol. 20 (2003) 907-913
53. López-Sánchez M.J., Neef A., Patiño-Navarrete R., Navarro L., Jiménez R., Latorre A., and Moya A. Blattabacteria, the endosymbionts of cockroaches, have small genome sizes and high genome copy numbers. Environ. Microbiol. 10 (2008) 3417-3422
54. Maekawa K., Park Y.C., and Lo N. Phylogeny of endosymbiont bacteria harbored by the woodroach Cryptocercus spp. (Cryptocercidae: Blattaria): molecular clock evidence for a late Cretaceous-early Tertiary split of Asian and American lineages. Mol. Phylogen. Evol. 36 (2005) 728-733
55. Martinez-Torres D., Buades C., Latorre A., and Moya A. Molecular systematics of aphids and their primary endosymbionts. Mol. Phylogen. Evol. 20 (2001) 437-449
56. Montllor C.B., Maxmen A., and Purcell A.H. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27 (2002) 189-195
57. Moran N.A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93 (1996) 2873-2878
58. Moran N.A., and Baumann P. Bacterial endosymbionts in animals. Curr. Opin. Microbiol. 3 (2000) 270-275
59. Moran N.A., and Wernegreen J.J. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15 (2000) 321-326
60. Moran N.A., Munson M.A., Baumann P., and Ishikawa H. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc. R. Soc. Lond. B 253 (1993) 167-171
61. Moran N.A., Dale C., Dunbar H., Smith W.A., and Ochman H. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ. Microbiol. 5 (2003) 116-126
62. Moran N.A., Plague G.R., Sandstrom J.P., and Wilcox J.L. A genomic perspective on nutrient provisioning by bacterial symbionts of insects. PNAS 100 (2003) 14543-14548
63. Moran N.A., Tran P., and Gerardo N.M. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl. Environ. Microbiol. 71 (2005) 8802-8810
64. Moya A., Pereto J., Gil R., and Latorre A. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat. Rev. Genet. 9 (2008) 218-229
65. Müller, K., 2002. GRate - relative rate tests for taxon groups using general DNA substitution models in PAUP*. Program distributed by the author, Bonn. Available from: .
66. Nardi J.B., Bee C.M., Miller L.A., Nguyen N.H., Suh S.-O., and Blackwell M. Communities of microbes that inhabit the changing hindgut landscape of a subsocial beetle. Arthropod Struct. Dev. 35 (2006) 57-68
67. Nelder M.P., Adler P.H., and Kachvoryan E.A. Do gut symbiotes reflect the endemism of their host black flies (Diptera: Simuliidae) in the Caucasus of Armenia?. J. Biogeogr. 32 (2005) 1333-1341
68. O'Neill S.L., Giordano R., Colbert A.M., Karr T.L., and Robertson H.M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. USA 89 (1992) 2699-2702
69. Ochman H., Elwyn S., and Moran N.A. Calibrating bacterial evolution. Proc. Natl. Acad. Sci. USA 96 (1999) 12638-12643
70. Oliver K.M., Russell J.A., Moran N.A., and Hunter M.S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. USA 100 (2003) 1803-1807
71. Peek A.S., Feldman R.A., Lutz R.A., and Vrijenhoek R.C. Cospeciation of chemoautotrophic bacteria and deep sea clams. Proc. Natl. Acad. Sci. USA 95 (1998) 9962-9966
72. Peterson J.K., and Schalk J.M. Internal bacteria in the Chrysomelidae. In: Jolivet P.H., Cox M.L., and Petitpierre E. (Eds). Novel Aspects of the Biology of Chrysomelidae (1994), Kluwer Academic Publisher, Dordrecht 393-405
73. Posada D., and Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
74. Ronquist F., and Huelsenbeck J.P. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
75. Russell J.A., Latorre A., Sabater-Munoz B., Moya A., and Moran N.A. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12 (2003) 1061-1075
76. Sauer C., Stackebrandt E., Gadau J., Hölldobler B., and Gross R. Systematic relationships and cospeciation of bacterial endosymbionts and their carpenter ant host species: proposal of the new taxon Candidatus Blochmannia gen. Nov. Int. J. Syst. Evol. Microbiol. 50 (2000) 1877-1886
77. Schröder D., Deppisch H., Obermayer M., Krohne G., Stackebrandt E., Hölldobler B., Goebel W., and Gross R. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol. Microbiol. 21 (1996) 479-489
78. Siddall M.E., Perkins S.L., and Desser S.S. Leech mycetome endosymbionts are a new lineage of alphaproteobacteria related to the Rhizobiaceae. Mol. Phylogen. Evol. 30 (2004) 178-186
79. Sota T., Bocak L., and Hayashi M. Molecular phylogeny and historical biogeography of the Holarctic wetland leaf beetle of the genus Plateumaris. Mol. Phylogen. Evol. 46 (2008) 183-192
80. Spaulding A., and von Dohlen C. Phylogenetic characterization and molecular evolution of bacterial endosymbionts in Psyllids (Hemiptera: Sternorrhyncha). Mol. Biol. Evol. 15 (1998) 1506-1513
81. Stammer H.-J. Neue Symbiosen bei Coleopteren. Verh. Dt. Zool. Ges. 1933 (1933) 150-155
82. Stammer H.-J. Studien an Symbiosen zwischen Käfern und Mikroorganismen. I. Die Symbiose der Donaciinen (Coleopt. Chrysomel.). Z. Morph. Ök. Tiere 29 (1935) 585-608
83. Stocsits R.R., Letsch H., Hertel J., Misof B., and Stadler P.F. Accurate and efficient reconstruction of deep phylogenies from structured RNAs. Nucl. Acids Res. 37 (2009) 6184-6193
84. Swofford D.L. PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods) (1998), Sinauer Ass., Sunderland, Massachusetts
85. Takiya D.M., Tran P.L., Dietrich C.H., and Moran N.A. Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol. Ecol. 15 (2006) 4175-4191
86. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
87. Thao M.L., and Baumann P. Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl. Environ. Microbiol. 70 (2004) 3401-3406
88. Thao M.L., Moran N.A., Abbot P., Brennan E.B., Burckhardt D.H., and Baumann P. Cospeciation of psyllids and their primary prokaryotic symbionts. Appl. Environ. Microbiol. 66 (2000) 2898-2905
89. Vinuesa P., Silva C., Werner D., and Martinez-Romero E. Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol. Phylogen. Evol. 34 (2005) 29-54
90. Weinert L.A., Tinsley M.C., Temperley M., and Jiggins F.M. Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. Biol. Lett. 3 (2007) 678-681
91. Wernegreen J.J. Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Gen. 3 (2002) 850-861
92. Wernegreen J.J., Degnan P.H., Lazarus A.B., Palacios C., and Bordenstein S.R. Genome evolution in an insect cell: distinct features of an ant-bacterial partnership. Biol. Bull. 204 (2003) 221-231
93. Wernegreen J.J., Lazarus A.B., and Degnan P.H. Small genome of Candidatus Blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle. Microbiology 148 (2002) 2551-2556
94. Wesenberg-Lund C. Biologie der Süsswasserinsekten (1943), Springer Verlag, Berlin
95. Whitfield J.B., and Kjer K.M. Ancient rapid radiations of insects: challenges for phylogenetic analysis. Annu. Rev. Entomol. 53 (2008) 449-472
96. Woolfit M., and Bromham L. Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol. Biol. Evol. 20 (2003) 1545-1555
97. Xia X., and Xie Z. DAMBE: data analysis in molecular biology and evolution. J. Hered. 92 (2001) 371-373
98. Zientz E., Dandekar T., and Gross R. Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol. Mol. Biol. Rev. 68 (2004) 745-770