Wolbachia association with the tsetse fly, Glossina fuscipes fuscipes, reveals high levels of genetic diversity and complex evolutionary dynamics

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Symula, Rebecca E ^a,b   Alam, Uzma ^a   Brelsfoard, Corey ^a,c   Wu, Yineng ^a   Echodu, Richard ^a,d   Okedi, Loyce M ^e   Aksoy, Serap ^a   Caccone, Adalgisa ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d GULU UNIVERSITY   (Uganda)

^e National Livestock Resources Research Institute   (Uganda)

Author keywords

groEL; MLST; Population structure; Sequence diversity; Wolbachia

Indexed keywords

DNA; EVOLUTIONARY BIOLOGY; FLY; GENETIC VARIATION; HOST PREFERENCE; INFECTIOUS DISEASE; MICROBIAL COMMUNITY; POPULATION GENETICS; SIMULATION;

UGANDA;

ALPHAPROTEOBACTERIA; ARTHROPODA; GLOSSINA (GENUS); GLOSSINA FUSCIPES FUSCIPES; GLOSSINIDAE; WOLBACHIA; WOLBACHIA PIPIENTIS;

CHAPERONIN 60; MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; BACTERIAL GENE; FEMALE; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; GLOSSINIDAE; HAPLOTYPE; MICROBIOLOGY; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; POPULATION GENETICS; STATISTICAL MODEL; UGANDA; WOLBACHIA;

ANIMALS; CHAPERONIN 60; DNA, MITOCHONDRIAL; FEMALE; GENES, BACTERIAL; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; HAPLOTYPES; LIKELIHOOD FUNCTIONS; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; TSETSE FLIES; UGANDA; WOLBACHIA;

MLCS; MLOWN;

EID: 84873269624     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-31     Document Type: Article

References (53)

1. How many species are infected with Wolbachia?-A statistical analysis of current data. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH, FEMS Microbiol Lett 2008 281 215 220 (Pubitemid 351422951)
2. Discovery of a CI-inducing Wolbachia and its associated fitness costs in the biological control agent Aphytis melinus DeBach (Hymenoptera: Aphelinidae). Vasquez CJ, Stouthamer R, Jeong G, Morse JG, Biol Control 2011 58 192 198
3. Molecular detection and the phylogenetics of Wolbachia in Chinese spiders (Araneae). Wang Z-y, Deng C, Yun Y-l, Jian C, Peng Y, J Arachnol 2010 38 237 241
4. Taxonomic status of the intracellular bacterium Wolbachia pipientis. Lo N, Paraskevopoulos C, Bourtzis K, O'Neill SL, Werren JH, Bordenstein SR, Bandi C, Int J Syst Evol Microbiol 2007 57 654 657 (Pubitemid 46442146)
5. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MC, Tettelin H, Werren JH, Appl Environ Microbiol 2006 72 7098 7110 (Pubitemid 44748423)
6. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, O'Neill SL, PLoS Pathog 2009 5 1000368
7. Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. Kambris Z, Blagborough AM, Pinto SB, Blagrove MS, Godfray HC, Sinden RE, Sinkins SP, PLoS Pathog 2010 6 1001143
8. Wolbachia: master manipulators of invertebrate biology. Werren JH, Baldo L, Clark ME, Nat Rev Microbiol 2008 6 741 751
9. Cytoplasmic incompatibility and host population structure. Engelstadter J, Telschow A, Heredity (Edinb) 2009 103 196 207
10. Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations. Unckless RL, Boelio LM, Herren JK, Jaenike J, Proceedings of the Royal Society B: Biological Sciences 2009 276 2805 2811
11. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Turelli M, Hoffmann AA, McKechnie SW, Genetics 1992 132 713 723
12. Evolutionary history of a mosquito endosymbiont revealed through mitochondrial hitchhiking. Rasgon JL, Cornel AJ, Scott TW, Proceedings of the Royal Society B: Biological Sciences 2006 273 1603 1611 (Pubitemid 46931045)
13. On the evolution of cytoplasmic incompatibility in haplodiploid species. Egas M, Vala F, Breeuwer JA, Evolution 2002 56 1101 1109 (Pubitemid 34792107)
14. Stochastic spread of Wolbachia. Jansen VA, Turelli M, Godfray HC, Proc Biol Sci 2008 275 2769 2776
15. Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Nunes MD, Nolte V, Schlotterer C, Mol Biol Evol 2008 25 2493 2498
16. Rapid spread of an inherited incompatibility factor in California Drosophila. Turelli M, Hoffmann AA, Nature 1991 353 440 442 (Pubitemid 21912532)
17. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Mouton L, Henri H, Charif D, Bouletreau M, Vavre F, Biol Lett 2007 3 210 213 (Pubitemid 351878159)
18. Influence of aging on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Duron O, Fort P, Weill M, Heredity (Edinb) 2007 98 368 374 (Pubitemid 46801765)
19. The invasion and coexistence of competing Wolbachia strains. Keeling MJ, Jiggins FM, Read JM, Heredity (Edinb) 2003 91 382 388 (Pubitemid 37274425)
20. Wolbachia-induced unidirectional cytoplasmic incompatibility and the stability of infection polymorphism in parapatric host populations. Flor M, Hammerstein P, Telschow A, J Evol Biol 2007 20 696 706
21. Bidirectional cytoplasmic incompatibility and the stable coexistence of two Wolbachia strains in parapatric host populations. Telschow A, Yamamura N, Werren JH, J Theor Biol 2005 235 265 274 (Pubitemid 40603478)
22. Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Dutton TJ, Sinkins SP, Insect Mol Biol 2004 13 317 322 (Pubitemid 38791179)
23. Male-killing Wolbachia in drosophila: a temperature-sensitive trait with a threshold bacterial density. Hurst GD, Johnson AP, Schulenburg JH, Fuyama Y, Genetics 2000 156 699 709
24. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Cheng Q, Ruel TD, Zhou W, Moloo SK, Majiwa P, O'Neill SL, Aksoy S, Med Vet Entomol 2000 14 44 50 (Pubitemid 30186108)
25. Detection and characterization of Wolbachia infections in laboratory and natural populations of different species of tsetse flies (genus Glossina). Doudoumis V, Tsiamis G, Wamwiri F, Brelsfoard C, Alam U, Aksoy E, Dalaperas S, Abd-Alla A, Ouma J, Takac P, et al. BMC Microbiol 2012 12 3
26. Microfauna-host interactions: implications for trypanosome transmission dynamics in Glossina fuscipes fuscipes in Uganda. Alam UH, Chaz H, Symula RE, Brelsfoard C, Wu Y, Kruglov O, Okedi LM, Caccone A, Aksoy S, Appl Environ Microbiol 2012 78 4627 4637
27. Wolbachia Symbiont infections induce strong cytoplasmic incompatibility in the tsetse Fly Glossina morsitans. Alam U, Medlock J, Brelsfoard C, Pais R, Lohs C, Balmand S, Carnogursky J, Heddi A, Takac P, Galvani A, Aksoy S, PLoS Pathog 2011 7 1002415
28. High levels of genetic differentiation between Ugandan Glossina fuscipes fuscipes populations separated by Lake Kyoga. Abila PP, Slotman MA, Parmakelis A, Dion KB, Robinson AS, Muwanika VB, Enyaru JC, Okedi LM, Aksoy S, Caccone A, PLoS Negl Trop Dis 2008 2 242
29. Phylogeography and population structure of Glossina fuscipes fuscipes in Uganda: implications for control of tsetse. Beadell JS, Hyseni C, Abila PP, Azabo R, Enyaru JC, Ouma JO, Mohammed YO, Okedi LM, Aksoy S, Caccone A, PLoS Negl Trop Dis 2010 4 636
30. Temporal stability of Glossina fuscipes fuscipes populations in Uganda. Echodu R, Beadell JS, Okedi LM, Hyseni C, Aksoy S, Caccone A, Parasites and Vectors 2011 4
31. Widespread recombination throughout Wolbachia genomes. Baldo L, Bordenstein S, Wernegreen JJ, Werren JH, Mol Biol Evol 2006 23 437 449 (Pubitemid 43100057)
32. Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. Thompson JR, Marcelino LA, Polz MF, Nucleic Acids Res 2002 30 2083 2088 (Pubitemid 34537607)
33. Solutions for PCR, cloning and sequencing errors in population genetic analysis. Cummings SM, McMullan M, Joyce DA, van Oosterhout C, Conserv Genet 2010 11 1095 1097
34. GENECONV: A computer package for the statistical detection of gene conversion. Sawyer SA, Book GENECONV: A computer package for the statistical detection of gene conversion 181a 1999
35. mlstdbNet-distributed multi-locus sequence typing (MLST) databases. Jolley KA, Chan MS, Maiden MC, BMC Bioinforma 2004 5 86
36. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739
37. Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Casiraghi M, Bordenstein SR, Baldo L, Lo N, Beninati T, Wernegreen JJ, Werren JH, Bandi C, Microbiology 2005 151 4015 4022 (Pubitemid 41829981)
38. MacClade4: Analysis of phylogeny and character evolution. Maddison DRaMWP, Book MacClade4: Analysis of phylogeny and character evolution City: Sinauer Associates 408 2004
39. jModelTest: phylogenetic model averaging. Posada D, Mol Biol Evol 2008 25 1253 1256 (Pubitemid 351882013)
40. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Guindon S, Gascuel O, Syst Biol 2003 52 696 704 (Pubitemid 37365050)
41. Zwickl D, Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion The University of Texas at Austin, Section of Integrative Biology 2006
42. DNA sequence polymorphism analysis using DnaSP. Rozas J, Methods Mol Biol 2009 537 337 350
43. TCS: a computer program to estimate gene genealogies. Clement M, Posada D, Crandall KA, Mol Ecol 2000 9 1657 1659
44. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Excoffier L, Smouse PE, Quattro JM, Genetics 1992 131 479 491
45. Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, tephritidae). Arthofer W, Riegler M, Schneider D, Krammer M, Miller WJ, Stauffer C, Mol Ecol 2009 18 3816 3830
46. Variable infection frequency and high diversity of multiple strains of Wolbachia pipientis in Perkinsiella planthoppers. Hughes GL, Allsopp PG, Brumbley SM, Woolfit M, McGraw EA, O'Neill SL, Appl Environ Microb 2011 77 2165 2168
47. Atyame CM, Delsuc F, Pasteur N, Weill M, Duron O, Diversification of Wolbachia Endosymbiont in the Culex pipiens Mosquito Molecular Biology and Evolution 2011
48. Diversity and phylogeny of Wolbachia infecting Bactrocera dorsalis (Diptera: tephritidae) populations from China. Sun X, Cui L, Li Z, Environ Entomol 2007 36 1283 1289 (Pubitemid 350032815)
49. Molecular phylogenetics of tsetse flies (Diptera: Glossinidae) based on mitochondrial (COI, 16S, ND2) and nuclear ribosomal DNA sequences, with an emphasis on the palpalis group. Dyer NA, Lawton SP, Ravel S, Choi KS, Lehane MJ, Robinson AS, Okedi LM, Hall MJ, Solano P, Donnelly MJ, Mol Phylogenet Evol 2008 49 227 239
50. Cryptic diversity within the major trypanosomiasis vector Glossina fuscipes revealed by molecular markers. Dyer NA, Ravel S, Choi K-S, Darby AC, Causse S, Kapitano B, Hall MJR, Steen K, Lutumba P, Madinga J, et al. PLoS Negl Trop Dis 2011 5 1266
51. The distribution of Wolbachia in fig wasps: correlations with host phylogeny, ecology and population structure. Shoemaker DD, Machado CA, Molbo D, Werren JH, Windsor DM, Herre EA, Proc R Soc London, Ser B 2002 269 2257 2267 (Pubitemid 35341912)
52. Influence of host phylogeographic patterns and incomplete lineage sorting on within-species genetic variability in Wigglesworthia species, obligate symbionts of Tsetse flies. Symula RE, Marpuri I, Bjornson RD, Okedi L, Beadell J, Alam U, Aksoy S, Caccone A, Appl Environ Microb 2011 77 8400 8408
53. Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Russell JA, Goldman-Huertas B, Moreau CS, Baldo L, Stahlhut JK, Werren JH, Pierce NE, Evolution 2009 63 624 640