Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: Bacterial genome helps define species and evolutionary relationships in aphids

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1654, 2009, Pages 187-196

  Jousselin, Emmanuelle ^a   Desdevises, Yves ^b   Coeur D'Acier, Armelle ^a  

^a MONTPELLIER SUPAGRO   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Aphids; Cospeciation; Endosymbiont; Phylogeny; Species delimitation

Indexed keywords

BACTERIAL DNA; DNA;

APHID; BACTERIUM; EVOLUTION; GENOME; PHYLOGENY; SPECIATION (BIOLOGY); SYMBIONT; TAXONOMY;

APHID; ARTICLE; BACTERIAL GENOME; BRACHYCAUDUS; BUCHNERA APHIDICOLA; CONTROLLED STUDY; MICROBIAL DIVERSITY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SPECIES COMPARISON; TAXONOMY;

APHIDIDAE; BACTERIA (MICROORGANISMS); BRACHYCAUDUS; BUCHNERA (PROTEOBACTERIA); BUCHNERA APHIDICOLA;

EID: 58149216507     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0679     Document Type: Article

References (67)

1. Achtman, M. & Wagner, M. 2008 Microbial diversity and the genetic nature of microbial species. Nat. Rev. Microbiol. 6, 431-440.
2. Anderson, B., Olivieri, I., Lourmas, M. & Stewart, B. A. 2004 Comparative population genetic structures and local adaptation of two mutualists. Evolution 58, 1730-1747.
3. Andreev, A. V. 2004 The subgeneric classification of Brachycaudus Van der Goot. In Aphids in a new millennium. Proc. of the 6th Int. Symp. on Aphids (ed. J. C. Simon, C. A. Dedryver, C. Rispe & M. Hulle), pp. 111-117. Rennes, France: INRA Editions.
4. Baumann, P. 2005 Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59, 155-189.
5. Baumann, L. & Baumann, P. 1994 Growth kinetics of the endosymbiont Buchnera aphidicola in the aphid Schizaphis graminum. Appl. Environ. Microbiol. 60, 3440-3443.
6. Bauman, P. & Bauman, L. 2005 Cospeciation between the primary endosymbionts ofmealybugs and their hosts. Curr. Microbiol. 50, 84-87.
7. Blackman, R. L. & Eastop, V. F. 2006. Aphids on the World's herbaceous plants and shrubs. London, UK: The Natural History Museum.
8. Buchner, P. 1965 Symbiosis in animals which suck plant juices. In Endosymbiosis of animals with plant microorganisms, pp. 210-432. New York, NY: Interscience.
9. Burger, H. C. 1975 Key to the European species of Brachycaudus, subgenus Acaudus (Homoptera: Aphidoidea) with redescriptions and note on B. persicae. Tijdschrift voor Entomol. 118, 99-116.
10. Clark, M. A., Moran, N. A., Bauman, P. & Wernegreen, J. J. 2000 Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54, 517-525.
11. Cocuzza, G., Cavalieri, V., Jousselin, E., Coeur d'acier, A. & Barbagallo, S. 2007 Morphological and molecular analysis of Brachycaudus, subgenus Appelia-complex (Rhynchota Aphididae). Redia XC, 33-49.
12. Cohan, F. M. 2002 What are bacterial species? Annu. Rev. Microbiol. 56, 457-487.
13. Coeur d'acier, A., Jousselin, E., Martin, J. F. & Rasplus, J. Y. 2007 Phylogeny of the genus Aphis Linnaeus, 1758 (Homoptera: Aphididae) inferred from mitochondrial DNA sequences. Mol. Phyl. Evol. 42, 598-611.
14. Coeur d'acier, A., Cocuzza, G., Jousselin, E., Cavalieri, V. & Barbagallo, S. 2008 Molecular phylogeny and systematics in the genus Brachycaudus (Homoptera: Aphididae): insights from a combined analysis of nuclear and mitochondrial genes. Zool. Script. 37, 175-193.
15. Criscione, C. D. & Blouin, M. S. 2007 Parasite phylogeographical congruencewith salmon host evolutionarily significant units: implications for salmon conservation. Mol. Ecol. 16, 993-1005.
16. Dettman, J. R., Jacobson, D. J. & Taylor, J. W. 2003 A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57, 2703-2720.
17. Douglas, A. E. 1998 Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43, 17-37.
18. Downie, D. A. & Gullan, P. J. 2005 Phylogenetic congruence of mealybugs and their primary endosymbionts. J. Evol. Biol. 18, 315-324.
19. Fahrenholz, H. 1913 Ectoparasiten und Abstammungslehre. Zool. Anz. 41, 371-374.
20. Fontaneto, D., Herniou, E. A., Boschetti, C., Caprioli, M., Melone, G., Ricci, C. & Barraclough, T. G. 2007 Independently evolving species in asexual bdelloid rotifers. Plos Biol. 5, 914-921.
21. Fontaneto, D., Boschetti, C. & Ricci, C. 2008 Cryptic diversification in ancient asexuals: evidence from the bdelloid rotifer Philodina flaviceps. J. Evol. Biol. 21, 580-587.
22. Gil, R., Sabater-Munoz, B., Perez-Brocal, V., Silva, F. J. & Latorre, A. 2006 Plasmids in the aphid endosymbiont Buchnera aphidicola with the smallest genomes. A puzzling evolutionary story. Gene 370, 17-25.
23. Gomez-Valero, L., Silva, F. J., Simon, J. C. & Latorre, A. 2007 Genome reduction of the aphid endosymbiont Buchnera aphidicola in a recent evolutionary time scale. Gene 389, 87-95.
24. Gruwell, M. E., Morse, G. E. & Normark, B. B. 2007 Phylogenetic congruence of armored scale insects (Hemiptera: Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes. Mol. Phyl. Evol. 44, 267-280.
25. Hafner, M. S., Sudman, P. D., Villablanca, F. X., Spradling, T. A., Demastes, J. W. & Nadler, S. A. 1994 Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087-1090.
26. Heie, O. E. 1967 Studies on fossil aphids (Homoptera: Aphidoidea). Spolia Zool. Musei Hauniensis 26, 1-273.
27. Heie, O. E. 1992 The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. IV. Family Aphididae: Part 1 of tribe Macrosiphini of subfamily Aphidinae. Leiden, The Netherlands: Brill, E. J.; New York, NY: Scandinavian Science Press Ltd.
28. Hosokawa, T., Kikuchi, Y., Nikoh, N. M. S. & Fukatsu, T. 2006 Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. Plos Biol. 4, 1841-1850.
29. Huelsenbeck, J. P. & Bull, J. J. 1996 A likelihood ratio test to detect conflicting phylogenetic signals. Syst. Biol. 45, 92-98.
30. Hughes, J., Kennedy, M., Johnson, K. P., Palma, R. L. & Page, R. D. M. 2007 Multiple cophylogenetic analyses reveal frequent cospeciation between pelecaniform birds and Pectinopygus lice. Syst. Biol. 56, 232-251.
31. Koga, R., Tsuchida, T. & Fukatsu, T. 2003 Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. B 270, 2543-2550.
32. Kumar, S., Tamura, K. & Nei, M. 2004 MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinf. 5, 150-163.
33. Latorre, A., Gil, R., Silva, F. J., Martinez-Torres, D. & Moya, A. 2003 Tempo and mode of genomic evolution in endosymbiotic bacteria of insects: the case of Buchnera aphidicola. Symbiosis 34, 301-316.
34. Le Gac, M., Hood, M. E., Fournier, E. & Giraud, T. 2007 Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61, 15-26.
35. Legendre, P., Desdevises, Y. & Bazin, E. 2002 A statistical test for host parasite coevolution. Syst. Biol. 51, 217-234.
36. Lerat, E., Daubin, V. & Moran, N. A. 2003 From gene trees to organismal phylogeny in prokaryotes: the case of the γ-proteobacteria. Plos Biol. 101, 101-109.
37. Lozier, J. D., Roderick, G. K. & Mills, N. J. 2007 Genetic evidence from mitochondrial, nuclear, and endosymbiont markers for the evolution of host plant associated species in the aphid genus Hyalopterus (Hemiptera: Aphididae). Evolution 61, 1353-1367.
38. Martinez-Torres, D., Buades, C., Latorre, A. & Moya, A. 2001 Molecular systematics of aphids and their primary endosymbionts. Mol. Phyl. Evol. 20, 437-449.
39. Marussich, W. A. & Machado, C. A. 2007 Host-specificity and coevolution among pollinating and nonpollinating New World fig wasps. Mol. Ecol. 16, 1925-1946.
40. McCoy, K. D., Boulinier, T. & Tirard, C. 2005 Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Mol. Ecol. 14, 2825-2838.
41. Monaghan, M. T., Balke, M., Gregory, T. R. & Vogler, A. P. 2005 DNA based species delineation in tropical beetles using mitochondrial and nuclear markers. Phil. Trans. R. Soc. B 360, 1925-1933.
42. Moran, N. A. 2001 The coevolution of bacterial endosymbionts and phloem-feeding insects. Ann. Miss. Bot. Gard. 88, 35-44.
43. Moran, N. A. & Degnan, P. H. 2006 Functional genomics of Buchnera and the ecology of aphid hosts. Mol. Ecol. 15, 1251-1261.
44. Moran, N. A., von Dohlen, C. D. & Baumann, P. 1995 Faster evolutionary rates in endosymbiotic bacteria than in cospeciating insect hosts. J. Mol. Evol. 41, 727-731.
45. Moran, N. A., Dunbar, H. E. & Wilcox, J. L. 2005a Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola. J. Bacteriol. 187, 4229-4237.
46. Moran, N. A., Tran, P. & Gerardo, N. M. 2005b Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl. Env. Microbiol. 71, 8802-8810.
47. Moya, A., Pereto, J., Gil, R. & Latorre, A. 2008 Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat. Rev. Gen. 9, 218-229.
48. Nieberding, C. M. & Olivieri, I. 2007 Parasites: proxies for host genealogy and ecology? Trends Ecol. Evol. 22, 156-165.
49. Nieberding, C., Morand, S., Libois, R. & Michaux, J. R. 2004 A parasite reveals cryptic phylogeographic history of its host. Proc. R. Soc. B 271, 2559-2568.
50. Page, R. D. M. 1991 Clocks, clades, and cospeciation: comparing rates of evolution and timing of cospeciation events in host-parasite assemblages. Syst. Zool. 40, 188-198.
51. Page, R. D. M. 1994 Parallel phylogenies: reconstructing the history of host-parasite assemblages. Cladistics 10, 155-173.
52. Page, R. D. M. 1996 Temporal congruence revisited: comparison of mitochondrial DNA sequence divergence in cospeciating pocket gophers and their chewing lice. Syst. Biol. 45, 151-167.
53. Perez-Brocal, V., Gil, R., Ramos, S., Lamelas, A., Postigo, M., Michelena, J. M., Silva, F. J., Moya, A. & Latorre, A. 2006 A small microbial genome: the end of a long symbiotic relationship? Science 314, 312-313.
54. Pons, J., Barraclough, T., Gomez-Zurita, J., Cardoso, A., Duran, D., Hazell, S., Kamoun, S., Sumlin, W. & Vogler, A. 2006 Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55, 595-609.
55. Rambaut, A. & Charleston, M. 2001. TREEEDIT: phylogenetic tree editor version 1. Oxford, UK: University of Oxford.
56. Remaudière, G. & Remaudière, M. 1997. Catalogue des Aphididae du monde - catalogue of the World's Aphididae [Homoptera, Aphidoidea]. Paris: Techniques et Pratiques.
57. Ruiz-Montoya, L., Munez-Farfan, J. & Dominguez, C. A. 2005 Changes in morphological traits of the cabbage aphid (Brevicoryne brassicae) associated with the use of different host plants. Ecol. Res. 20, 591-598.
58. Rutschmann, F. 2005 Bayesian molecular dating using PAML/ MULTIDIVTIME. A step-by-step manual, v. 1.4. See http://statgen.ncsu. edu/thorne/multidivtime.html.
59. Shaposhnikov, G. K. 1964 4. Suborder Aphidinea: aphids. In Bei Bienko's, keys to the insects of the European part of the USSR, vol. 1, pp. 489-616.
60. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. 2000 Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature 407, 81-86.
61. Sites, J. J. W. & Marshall, J. C. 2003 Delimiting species: a Renaissance issue in systematic biology. Trends Ecol. Evol. 18, 462-470.
62. Thorne, J. L. & Kishino, H. 2002 Divergence time and evolutionary rate estimation with multilocus data. Syst. Biol. 51, 689-702.
63. Vogler, A. P. & Monaghan, M. T. 2007 Recent advances in DNA taxonomy. J. Zool. Syst. Evol. Res. 45, 1-10.
64. von Dohlen, C. D. & Moran, N. A. 2000 Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation. Biol. J. Linn. Soc. 71, 689-717.
65. Wiens, J. J. & Penkrot, T. A. 2002 Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst. Biol. 51, 69-91.
66. Wilkinson, T. L., Fukatsu, T. & Ishikawa, H. 2003 Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Arth. Struct. Dev. 32, 241-245.
67. Wool, D. & Hales, D. 1997 Phenotypic plasticity in Australian cotton aphid (Homoptera: Aphididae) host plant effects on morphological variation. Ann. Entomol. Soc. Am. 90, 316-328.