Symbiont diversity and non-random hybridization among indigenous (Ms) and invasive (B) biotypes of Bemisia tabaci

Molecular Ecology

Volumn 20, Issue 10, 2011, Pages 2172-2187

  Thierry, M ^a   Becker, N ^b   Hajri, A ^a   Reynaud, B ^a   Lett, J M ^a   Delatte, H ^a  

^a UNIVERSITÉ DE LA RÉUNION   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Bemisia tabaci; biotypes; hybridization; microsatellites; mitochondrial DNA; secondary symbionts

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CLASSIFICATION; ENTEROBACTERIACEAE; GENETICS; HEMIPTERA; HYBRIDIZATION; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; RICKETTSIA; SYMBIOSIS; WOLBACHIA;

ANIMALS; DNA, MITOCHONDRIAL; ENTEROBACTERIACEAE; HEMIPTERA; HYBRIDIZATION, GENETIC; MICROSATELLITE REPEATS; PHYLOGENY; RICKETTSIA; SYMBIOSIS; WOLBACHIA;

ALEYRODIDAE; ARSENOPHONUS; BEMISIA TABACI; CANDIDATUS CARDINIUM; CANDIDATUS FRITSCHEA; CANDIDATUS PORTIERA ALEYRODIDARUM; HEMIPTERA; RICKETTSIA; WOLBACHIA;

EID: 79955572790     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05087.x     Document Type: Article

References (71)

1. Arnold J, (1993) Cytonuclear disequilibria in hybrid zones. Annual Review of Ecology and Systematics, 24, 521-553.
2. Asmussen MA, Basten CJ, (1996) Constraints and normalized measures for cytonuclear disequilibria. Heredity, 76, 207-214. (Pubitemid 126733272)
3. Barton NH, Hewitt GM, (1989) Adaptation, speciation and hybrid zones. Nature, 341, 497-503.
4. Basten CJ, Asmussen MA, (1997) The exact test for cytonuclear disequilibria. Genetics, 146, 1165-1171. (Pubitemid 27290997)
5. Bird J, Maramorosch K, (1978) Virus and virus diseases associated with whiteflies. Advances in Virus Research, 22, 55-110.
6. Braig HR, Zhou WG, Dobson SL, et al., (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Journal of Bacteriology, 180, 2373-2378. (Pubitemid 28217350)
7. Brown JK, Frohlich DR, Rosell RC, (1995) The sweet-potato or silverleaf whiteflies-biotypes of bemisia-tabaci or a species complex. Annual Review of Entomology, 40, 511-534.
8. Calvert LA, Cuervo M, Arroyave JA, Constantino LM, Bellotti A, Frohlich D, (2001) Morphological and mitochondrial DNA marker analyses of whiteflies (Homoptera: Aleyrodidae) colonizing cassava and beans in Colombia. Annals of the Entomological Society of America, 94, 512-519. (Pubitemid 33734111)
9. Carlsson J, (2008) Effects of microsatellite null alleles on assignment testing. Journal of Heredity, 99, 616-623.
10. Chiel E, Gottlieb Y, Zchori-Fein E, et al. (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bulletin of Entomological Research, 97, 407-413. (Pubitemid 47106577)
11. Chiel E, Zchori-Fein E, Inbar M, et al. (2009) Almost there: transmission routes of bacterial symbionts between trophic levels. PLoS ONE, 4, e4767.
12. Claridge MF, Dawah HA, Wilson MR, (1997) Species in insect herbivores and parasitoids-sibling species, host races and biotypes. In: Species, The Units of Biodiversity (eds, Claridge MF, Dawah HA, Wilson MR,). Chapman & Hall, London, pp. 247-272.
13. Clerget-Froidevaux MS, Seugnet I, Demeneix BA, (2004) Thyroid status co-regulates thyroid hormone receptor and co-modulator genes specifically in the hypothalamus. FEBS Letters, 569, 341-345. (Pubitemid 38844642)
14. Cruzan MB, Arnold ML, (1999) Consequences of cytonuclear epistasis and assortative mating for the genetic structure of hybrid populations. Heredity, 82, 36-45. (Pubitemid 29087448)
15. Dalmon A, Halkett F, Granier M, Delatte H, Peterschmitt M, (2008) Genetic structure of the invasive pest Bemisia tabaci: evidence of limited but persistent genetic differentiation in glasshouse populations. Heredity, 100, 316-325. (Pubitemid 351282132)
16. De Barro PJ, (2005) Genetic structure of the whitefly Bemisia tabaci in the Asia-Pacific region revealed using microsatellite markers. Molecular Ecology, 14, 3695-3718.
17. De Barro PJ, Driver F, Trueman JW, Curran J, (2000) Phylogenetic relationships of world populations of Bemisia tabaci (Gennadius) using ribosomal ITS1. Molecular Phylogenetics and Evolution, 16, 29-36. (Pubitemid 30466874)
18. De Barro PJ, Liu SS, Boykin LM, Dinsdale AB, (2011) Bemisia tabaci: a statement of species status. Annual Reviw of Entomology, 56, 1-19.
19. Delatte H, Reynaud B, Granier M, et al. (2005) A new silverleaf-inducing biotype Ms of Bemisia tabaci (Hemiptera: Aleyrodidae) indigenous to the islands of the south-west Indian Ocean. Bulletin of Entomological Research, 95, 29-35. (Pubitemid 40252967)
20. Delatte H, David P, Granier M, et al. (2006) Microsatellites reveal extensive geographical, ecological and genetic contacts between invasive and indigenous whitefly biotypes in an insular environment. Genetics Research, 87, 109-124. (Pubitemid 43744805)
21. Delatte H, Lett JM, Lefeuvre P, Reynaud B, Peterschmitt M, (2007) An insular environment before and after TYLCV introduction. In: Tomato Yellow Leaf Curl Virus Disease, Management, Molecular Biology, Breeding for Resistance (ed., Czosnek H,). Springer, Dordrecht, The Netherlands, pp. 13-23.
22. Delatte H, Duyck PF, Triboire A, et al. (2009) Bioecology of the invasive B biotype compared to the indigenous Ms biotype of Bemisia tabaci in La Réunion. Biological Invasions, 11, 1059-1070.
23. Delatte H, Holota H, Warren BH, et al., (2011) Genetic diversity, geographical range and origin of Bemisia tabaci biotype Ms. Bulletin of Entomological Research, in press.
24. Dinsdale A, Cook L, Riginos C, Buckley YM, Barro PD, (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America, 103, 196-208.
25. Dobzhansky T, (1970) Genetics of the Evolutionary Process, pp. 1-505. Columbia University Press, New York.
26. Duron O, Bouchon D, Boutin S, et al. (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biology, 6, 27.
27. Engelstadter J, Hurst GDD, (2009) The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology Evolution and Systematics, 40, 127-149.
28. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620. (Pubitemid 40886055)
29. Everett KDE, Hornung LJ, Andersen AA, (1999) Rapid detection of the chlamydiaceae and other families in the order chlamydiales: three PCR tests. Journal of Clinical Microbiology, 37, 575-580. (Pubitemid 29091267)
30. Everett KD, Thao M, Horn M, Dyszynski GE, Baumann P, (2005) Novel chlamydiae in whiteflies and scale insects: endosymbionts 'Candidatus Fritschea bemisiae' strain Falk and 'Candidatus Fritschea eriococci' strain Elm. International Journal of Systematic and Evolutionary Microbiology, 55, 1581-1587. (Pubitemid 41015607)
31. Excoffier L, Laval G, Schneider S, (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
32. Feldhaar H, Gross R, (2009) Insects as hosts for mutualistic bacteria. International Journal of Medical Microbiology, 299, 1-8.
33. Frohlich DR, Torres-Jerez I, Bedford ID, Markham PG, Brown JK, (1999) A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial DNA markers. Molecular Ecology, 8, 1683-1691. (Pubitemid 29514708)
34. Ghanim M, Kontsedalov S, (2009) Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Management Science, 65, 939-942.
35. Gottlieb Y, Ghanim M, Chiel E, et al., (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Applied and Environmental Microbiology, 72, 3646-3652. (Pubitemid 43728021)
36. Gottlieb Y, Ghanim M, Gueguen G, et al. (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB Journal, 22, 2591-2599. (Pubitemid 351948676)
37. Gottlieb Y, Zchori-Fein E, Mozes-Daube N, et al. (2010) The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. Journal of Virology, 84, 9310-9317.
38. Gueguen G, Vavre F, Gnankine O, et al. (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Molecular Ecology, 19, 4365-4376.
39. Guindon S, Lethiec F, Duroux P, Gascuel O, (2005) PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Research, 33, W557-W559. (Pubitemid 44529983)
40. Haine ER, (2008) Symbiont-mediated protection. Proceedings of the Royal Society B: Biological Sciences, 275, 353-361.
41. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH, (2008) How many species are infected with Wolbachia?-A statistical analysis of current data. FEMS Microbiology Letters, 281, 215-220. (Pubitemid 351422951)
42. Hunter MS, Perlman SJ, Kelly SE, (2003) A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proceedings of the Royal Society B: Biological Sciences, 270, 2185-2190. (Pubitemid 37289886)
43. Jarne P, Lagoda PJL, (1996) Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution, 11, 424-429. (Pubitemid 126394588)
44. Jombart T, (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405. (Pubitemid 351737150)
45. Jones D, (2003) Plant viruses transmitted by whiteflies. European Journal of Plant Pathology, 109, 195-219. (Pubitemid 36405500)
46. Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M, Ghanim M, (2008) The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science, 64, 789-792. (Pubitemid 352009564)
47. Moran NA, Dunbar HE, (2006) Sexual acquisition of beneficial symbionts in aphids. Proceedings of the National Academy of Sciences, USA, 103, 12803-12806. (Pubitemid 44298642)
48. Oliveira MRV, Henneberry TJ, Anderson P, (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Protection, 20, 709-723. (Pubitemid 33146095)
49. Oliver KM, Degnan PH, Burke GR, Moran NA, (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology, 55, 247-266.
50. Perring TM, (2001) The Bemisia tabaci species complex. Crop Protection, 20, 725-737. (Pubitemid 33146096)
51. Peterschmitt M, Granier M, Mekdoud R, et al. (1999) First report of tomato yellow leaf curl virus in Réunion Island. Plant Disease, 83, 303.
52. Posada D, (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Research, 34, W700-W703. (Pubitemid 44529861)
53. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. (Pubitemid 30397141)
54. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
55. Rousset F, (2008) GENEPOP '007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources, 8, 103-106. (Pubitemid 350231212)
56. Sandstrom JP, Russell JA, White JP, Moran NA, (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Molecular Ecology, 10, 217-228. (Pubitemid 32097542)
57. Scarborough CL, Ferrari J, Godfray HCJ, (2005) Aphid protected from pathogen by endosymbiont. Science, 310, 1781.
58. Skaljac M, Zanic K, Ban SG, Kontsedalov S, Ghanim M, (2010) Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiology, 10, 142.
59. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599. (Pubitemid 47236692)
60. Thao ML, Baumann P, (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Applied and Environmental Microbiology, 70, 3401-3406. (Pubitemid 38745884)
61. Thao ML, Baumann L, Hess JM, et al. (2003) Phylogenetic evidence for two new insect-associated chlamydia of the family Simkaniaceae. Current Microbiology, 47, 46-50. (Pubitemid 36918040)
62. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680. (Pubitemid 24354800)
63. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538. (Pubitemid 39147523)
64. Varma A, Malathi VG, (2003) Emerging geminivirus problems: a serious threat to crop production. Annals of Applied Biology, 142, 145-164. (Pubitemid 36658678)
65. Vorburger C, Gehrer L, Rodriguez P, (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biological Letters, 6, 109-111.
66. Weeks AR, Robert V, Richard S, (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proceedings of the Royal Society B: Biological Sciences, Biology, 270, 1857-1865. (Pubitemid 37082884)
67. Weir BS, Cockerham CC, (1984) Estimating F-Statistics for the analysis of population structure. Evolution, 38, 1358-1370. (Pubitemid 16277759)
68. Xu J, De Barro PJ, Liu SS, (2010) Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bulletin of Entomological Research, 100, 359-366.
69. Zchori-Fein E, Gottlieb Y, Kelly SE, et al. (2001) A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proceedings of the National Academy of Sciences, USA, 98, 12555-12560. (Pubitemid 33019984)
70. Zchori-Fein E, Brown JK, (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Annals of the Entomological Society of America, 95, 711-718. (Pubitemid 36225389)
71. Zchori-Fein E, Perlman SJ, Kelly SE, Katzir N, Hunter MS, (2004) Characterization of a 'Bacteroidetes' symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of 'Candidatus Cardinium hertigii'. International Journal of Systematic and Evolutionnary Microbiology, 54, 961-968. (Pubitemid 38771803)