Improving Sterile Insect Technique (SIT) for tsetse flies through research on their symbionts and pathogens

Journal of Invertebrate Pathology

Volumn 112, Issue SUPPL.1, 2013, Pages

  Abd Alla, Adly M M ^a   Bergoin, Max ^b   Parker, Andrew G ^a   Maniania, Nguya K ^c   Vlak, Just M ^d   Bourtzis, Kostas ^e,f   Boucias, Drion G ^g   Aksoy, Serap ^h  

^a INTERNATIONAL ATOMIC ENERGY AGENCY   (Austria)

^b CNRS   (France)

^c INTERNATIONAL CENTRE OF INSECT PHYSIOLOGY AND ECOLOGY ICIPE   (Kenya)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e University of Western Greece   (Greece)

^f BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^g UNIVERSITY OF FLORIDA   (United States)

^h YALE UNIVERSITY   (United States)

Author keywords

Glossinidae; Pathogens; Salivary gland hypertrophy virus; SIT; Symbionts; Tsetse

Indexed keywords

AFRICAN TRYPANOSOMIASIS; ANIMAL; BIOLOGICAL PEST CONTROL; FERTILITY; GLOSSINIDAE; HUMAN; METHODOLOGY; MICROBIOLOGY; REVIEW; SYMBIOSIS;

ANIMALS; FERTILITY; HUMANS; PEST CONTROL, BIOLOGICAL; SYMBIOSIS; TRYPANOSOMIASIS, AFRICAN; TSETSE FLIES;

ANIMALIA; BACTERIA (MICROORGANISMS); DIPTERA; FUNGI; GLOSSINA (GENUS); GLOSSINIDAE; HEXAPODA; TRYPANOSOMA;

EID: 84875806306     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2012.07.009     Document Type: Review

References (99)

1. Abd-Alla A., Bossin H., Cousserans F., Parker A., Bergoin M., Robinson A. Development of a non-destructive PCR method for detection of the salivary gland hypertrophy virus (SGHV) in tsetse flies. J. Virol. Methods 2007, 139:143-149.
2. Abd-Alla A.M.M., Cousserans F., Parker A.G., Jehle J.A., Parker N.J., Vlak J.M., Robinson A.S., Bergoin M. Genome analysis of a Glossina pallidipes salivary gland hypertrophy virus (GpSGHV) reveals a novel large double-stranded circular DNA virus. J. Virol. 2008, 82:4595-4611.
3. Abd-Alla A., Cousserans F., Parker A., Bergoin M., Chiraz J., Robinson A. Quantitative PCR analysis of the salivary gland hypertrophy virus (GpSGHV) in a laboratory colony of Glossina pallidipes. Virus Res. 2009, 139:48-53.
4. Abd-Alla A.M.M., Vlak J.M., Bergoin M., Maruniak J.E., Parker A.G., Burand J.P., Jehle J.A., Boucias D.G. Hytrosaviridae: a proposal for classification and nomenclature of a new insect virus family. Arch. Virol. 2009, 154:909-918.
5. Abd-Alla A.M.M., Boucias D.G., Bergoin M. Hytrosaviruses: structure and genomic properties. Insect Virology 2010, 103-121. Caister Academic Press, Norfolk. S. Asgari, K.N. Johnson (Eds.).
6. Abd-Alla A.M.M., Kariithi H., Parker A.G., Robinson A.S., Kiflom M., Bergoin M., Vreysen M.J.B. Dynamics of the salivary gland hypertrophy virus in laboratory colonies of Glossina pallidipes (Diptera: Glossinidae). Virus Res. 2010, 150:103-110.
7. Abd-Alla A.M.M., Parker A.G., Vreysen M.J.B., Bergoin M. Tsetse salivary gland hypertrophy virus: hope or hindrance for tsetse control?. PLoS Negl. Trop. Dis. 2011, 5:e1220.
8. Abd-Alla A.M.M., Salem T.Z., Parker A.G., Wang Y., Jehle J.A., Vreysen M.J.B., Boucias D. Universal primers for rapid detection of Hytrosaviruses. J. Virol. Methods 2011, 171:280-283.
9. Abd-Alla A.M., Adun H., Parker A.G., Vreysen M.J., Bergoin M. The antiviral drug valacyclovir successfully suppresses salivary gland hypertrophy virus (SGHV) in laboratory colonies of glossina pallidipes. PLoS. One 2012, 7:e38417.
10. Adams E.R., Hamilton P.B., Malele I.I., Gibson W.C. The identification, diversity and prevalence of trypanosomes in field caught tsetse in Tanzania using ITS-1 primers and fluorescent fragment length barcoding. Infect., Genet. Evolut. 2008, 8:439-444.
11. Adams E.R., Hamilton P.B., Rodrigues A.C., Malele I.I., Delespaux V., Teixeira M.M.G., Gibson W. New Trypanosoma (Duttonella) vivax genotypes from tsetse flies in East Africa. Parasitology 2010, 137:641-650.
12. Akman L., Yamashita A., Watanabe H., Oshima K., Shiba T., Hattori M., Aksoy S. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 2002, 32:402-407.
13. Akoda K., Van Den Abbeele J., Marcotty T., De Deken R., Sidibe I., van den Bossche P. Nutritional stress of adult female tsetse flies (Diptera: Glossinidae) affects the susceptibility of their offspring to trypanosomal infections. Acta Trop. 2009, 111:263-267.
14. Akoda K., van den Bossche P., Lyaruu E.A., De Deken R., Marcotty T., Coosemans M., Van Den Abbeele J. Maturation of a Trypanosoma Brucei infection to the infectious metacyclic stage is enhanced in nutritionaly stressed tsetse flies. J. Med. Entomol. 2009, 46:1446-1449.
15. Akoda K., van den Bossche P., Marcotty T., Kubi C., Coosemans M., Dedeken R., Van Den Abbeele J. Nutritional stress affects the tsetse fly's immune gene expression. Med. Vet. Entomol. 2009, 23:195-201.
16. Aksoy S. Tsetse - a haven for microorganisms. Parasitol. Today 2000, 16:114-118.
17. Aksoy S. Sleeping sickness elimination in sight: time to celebrate and reflect, but not relax. PLoS Negl. Trop. Dis. 2011, 5:1-3.
18. Aksoy S., Maudlin I., Dale C., Robinson A.S., O'Neill S.L. Prospects for control of African trypanosomiasis by tsetse vector manipulation. Trends Parasitol. 2001, 17:29-35.
19. Aksoy S., Weiss B., Attardo G. Paratransgenesis applied for control of tsetse transmitted sleeping sickness 8. Adv. Exp. Med. Biol. 2008, 627:35-48.
20. Aksoy S., Weiss B., Attardo G.M. Paratransgenesis applied for control of tsetse transmitted sleeping sickness. Transgenesis and the Management of Vector-Borne Disease (Advances in Experimental Medicine and Biology) 2008, 35-48. Springer Science-Business Media, LLC Landes Bioscience, New York, . S. Aksoy (Ed.).
21. Alam U., Medlok J., Brelsfoard C., Pais R., Lohs C., Balmand S., Carnogursky J., Heddi A., Takac P., Galvani A., Aksoy S. Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans. PLoS Pathog. 2012, 7:e1002415.
22. Arif B., Pavlik L. Insect cell culture: Virus replication and applications in biotechnology. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S138-S141.
23. Attardo G.M., Lohs C., Heddi A., Alam U.H., Yildirim S., Aksoy S. Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. J. Insect Physiol. 2008, 54:1-7.
24. Baker R.D., Maudlin I., Milligan P.J.M., Molyneux D.H., Welburn S.C. The possible role of Rickettsia-like organisms in trypanosomiasis epidemiology. Parasitology 1990, 100:209-217.
25. Balmand S., Lohs C., Aksoy S., Heddi A. Tissue distribution and transmission routes for the tsetse fly endosymbionts. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S116-S122.
26. Beard C.B., O'Neill S.L., Mason P., Mandelco L., Woese C.R., Tesh R.B., Richards F.F., Aksoy S. Genetic transformation and phylogeny of bacterial symbionts from tsetse 1. Insect Mol. Biol. 1993, 1:123-131.
27. Beard C.B., O'Neill S.L., Tesh R.B., Richards F.F., Aksoy S. Modification of arthropod vector competence via symbiotic bacteria. Parasitol. Today 1993, 9:180-183.
28. Beard C.B., Durvasula R.V., Richards F.F. Bacterial symbiosis in arthropods and the control of disease transmission. Emer. Infect. Dis. 1998, 4:581-591.
29. Bonomi A., Bassetti F., Gabrieli P., Beadell J., Falchetto M., Scolari F., Gomulski L.M., Regazzini E., Ouma J.O., Caccone A., Okedi L.M., Attardo G.M., Guglielmino C.R., Aksoy S., Malacrida A.R. Polyandry is a common event in wild populations of the tsetse fly Glossina fuscipes fuscipes and may impact population reduction measures. PLoS Negl. Trop Dis. 2011, 5:e1190.
30. Boucias D.G., Deng F., Hu Z., Garcia-Maruniak A., Lietze V.-U. Analysis of the structural proteins from the Musca domestica hytrosavirus with an emphasis on the major envelope protein. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S44-S52.
31. Bourtzis, K., 2008. Wolbachia-based technologies for insect pest population control. In: Aksoy, S. (Ed.), Transgenesis and the Management of Vector-Borne Disease (Advances in Experimental Medicine and Biology). Springer Science+Business Media. LLC 233 Springer Street, New York, New York 10013, USA, New York, pp. 104-113 <>. http://www.springer.com.
32. Bourtzis K., O'Neill S. Wolbachia infections and arthropod reproduction. Bioscience 1998, 48:287-293.
33. Budd L.T. DFID-funded tsetse and trypanosome research and development since 1980. Economic Analysis 2000, vol. 2. Natural Resources International Limited, Aylesford, UK.
34. Caljon G., De Vooght L., Abbeele J.V.D. Options for the delivery of anti-pathogen molecules in arthropod vectors. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S75-S82.
35. Calkins C.O., Webb J.C. A cage and support framework for behavioral tests of fruit flies in the field. Fla. Entomol. 1983, 66:514.
36. Chen X., Sond L., Aksoy S. Concordant evolution of a symbiont with its host insect species: Molecular phylogeny of Genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J. Mol. Evol. 1999, 48:49-58.
37. Cheng Q., Ruel T.D., Zhou W., Moloo S.K., Majiwa P., O'Neill S.L., Aksoy S. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Med. Vet. Entomol. 2000, 14:44-50.
38. De Vooght L., Caljon G., Coosemans M., Van Den Abbeele J. Functional analysis of the Twin-Arginine Translocation pathway in Sodalis glossinidius, a bacterial symbiont of the tsetse fly. Appl. Env. Microbiol. 2011, 77:1132-1134.
39. De Vooght L., Caljon G., Stijlemans S., Coosemans M., Van Den Abbeele J. Expression and extracellular release of a functional anti-trypanosome Nanobody in Sodalis glossinidius, a bacterial symbiont of the tsetse fly. Microb. Cell Fact. 2012, 11.
40. Doudoumis V., Tsiamis G., Wamwiri F., Brelsfoard C., Alam U., Aksoy E., Dalaperas S., Abd-Alla A., Ouma J., Takac P., Aksoy S., Bourtzis K. Detection and characterization of Wolbachia infections in laboratory and natural populations of different species of tsetse (genus Glossina). BMC Micobiology 2012, 12:1-13.
41. Doudoumis V., Alam U., Aksoy E., Abd-Alla A.M.M., Tsiamis G., Brelsfoard C., Aksoy S., Bourtzis K. Tsetse-Wolbachia symbiosis: Comes of age and has great potential for pest and disease control. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S94-S103.
42. Enyaru J.C., Ouma J.O., Malele I.I., Matovu E., Masiga D.K. Landmarks in the evolution of technologies for identifying trypanosomes in tsetse flies. Trends Parasitol. 2010, 26:388-394.
43. Farikou O., Njiokou F., Mbida J.A.M., Njitchouang G.R., Djeunga H.N., Asonganyi T., Simarro P.P., Cuny G., Geiger A. Tripartite interactions between tsetse flies, Sodalis glossinidius and trypanosomes - an epidemiological approach in two historical human african trypanosomiasis foci in Cameroon. Infect., Genet. Evol. 2010, 10:115-121.
44. Farikou O., Njiokou F., Simo G., Asonganyi T., Cuny G., Geiger A. Tsetse fly blood meal modification and trypanosome identification in two sleeping sickness foci in the forest of southern Cameroon. Acta Trop. 2010, 116:81-88.
45. Farikou O., Njiokou F., Cuny G., Geiger A. Microsatellite genotyping reveals diversity within populations of Sodalis glossinidius, the secondary symbiont of tsetse flies. Vet. Microbiol. 2011, 150:207-210.
46. Farikou O., Thevenon S., Njiokou F., Allal F., Cuny G., Geiger A. Genetic diversity and population structure of the secondary symbiont of tsetse flies, Sodalis glossinidius, in sleeping sickness foci in Camerooon. PLoS Negl. Trop. Dis. 2011, 5:e1281.
47. Garcia-Maruniak A., Maruniak J.E., Farmerie W., Boucias D.G. Sequence analysis of a non-classified, non-occluded DNA virus that causes salivary gland hypertrophy of Musca domestica, MdSGHV. Virology 2008, 377:184-196.
48. Garcia-Maruniak A., Abd-Alla A.M.M., Salem T.Z., Parker A.G., van Oers M.M., Maruniak J.E., Kim W., Burand J.P., Cousserans F., Robinson A.S., Vlak J.M., Bergoin M., Boucias D.G. Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. J. Gen. Virol. 2009, 90:334-346.
49. Geden C.J., Lietze V.U., Boucias D.G. Seasonal prevalence and transmission of salivary gland hypertrophy virus of house flies (Diptera: Muscidae). J. Med. Entomol. 2008, 45:42-51.
50. Geden C., Garcia-Maruniak A., Lietze V.U., Maruniak J., Boucias D.G. Impact of house fly salivary gland hyperthrophy virus (MdSGHV) on a heterologous host, Stomoxys calcitrans. J. Med. Entomol. 2011, 46:1128-1135.
51. Geden C.J., Steenberg T., Lietze V.-U., Boucias D.G. Salivary gland hyperthrophy virus of house flies in Denmark: prevalence, host range, and comparison with a Florida isolate. J. Vector. Ecol. 2011, 36:231-238.
52. Geiger A., Ravel S., Mateille T., Janelle J., Patrel D., Cuny G., Frutos R. Vector competence of Glossina palpalis gambiensis for Trypanosoma brucei s.l. and genetic diversity of the symbiont Sodalis glossinidius. Mol. Biol. Evol. 2007, 24:102-109.
53. Geiger A., Fardeau M.L., Grebaut P., Vatunga G., Josenando T., Herder S., Cuny G., Truc P., Ollivier B. First isolation of Enterobacter, Enterococcus, and Acinetobacter spp. as inhabitants of the tsetse fly (Glossina palpalis papalis) midgut. Infect., Genet. Evol. 2009, 9:1364-1370.
54. Geiger A., Fardeau M.L., Falsen E., Ollivier B., Cuny G. Serratia glossinae sp. nov., isolated from the midgut of the tsetse fly Glossina palpalis gambiensis. Int. J. Syst. Evol. Microbiol. 2010, 60:1261-1265.
55. Geiger A., Fardeau M.L., Njiokou F., Joseph M., Asonganyi T., Ollivier B., Cuny G. Bacterial diversity associated with populations of Glossina spp. from Cameroon and distribution within the Campo sleeping sickness focus. Microbial. Ecol. 2011, 62:632-643.
56. Hamilton P.B., Adams E.R., Malele I.I., Gibson W.C. A novel, high-throughput technique for species identification reveals a new species of tsetse-transmitted trypanosome related to the Trypanosoma brucei subgenus, Trypanozoon. Infect., Genet. Evol. 2008, 8:26-33.
57. Holmes P. Tsetse-transmitted trypanosomes-Their biology, disease impact and control. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S11-S14.
58. Ioannidis P., Dunning Hotopp J.C., Sapountzis P., Siozios S., Tsiamis G., Bordenstein S.R., Baldo L., Werren J.H., Bourtzis K. New criteria for selecting the origin of DNA replication in Wolbachia and closely related bacteria. BMC Genomics 2007, 8:182.
59. Jehle J.A., Abd-Alla A.M.M., Wang Y. Phylogeny and evolution of Hytrosaviridae. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S62-S67.
60. Kaiwa N., Hosokawa T., Kikuchi Y., Nikoh N., Meng X.Y., Kimura N., Ito M., Fukatsu T. Primary gut symbiont and secondary, Sodalis-allied symbiont of the Scutellerid stinkbug Cantao ocellatus 1. Appl. Environ. Microbiol. 2010, 76:3486-3494.
61. Kariithi H.M., Ince A.I., Boeren S., Vervoort J., Bergoin M., van Oers M.M., Abd-Alla A., Vlak J.M. Proteomic analysis of Glossina pallidipes Salivary Gland Hypertrophy Virus virions for immune intervention in tsetse fly colonies. J. Gen. Virol. 2010, 91:3065-3074.
62. Kariithi H.M., Ince I.A., Boeren S., Abd-Alla A.M.M., Parker A.G., Aksoy S., Vlak J.M., Oers M.M.v. The salivary secretome of the tsetse fly Glossina pallidipes (Diptera: Glossinidae) infected by salivary gland hypertrophy virus. PLoS Negl. Trop. Dis. 2011, 5:e1371.
63. Kariithi H.M., Ahmadi M., Parker A.G., Franz G., Ros V.I.D., Haq I., Elashry A.M., Vlak J.M., Bergoin M., Vreysen M.J.B., Abd-Alla A.M.M. Prevalence and genetic variation of salivary gland hypertrophy virus in wild populations of the tsetse fly Glossina pallidipes from southern and eastern Africa. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S123-S132.
64. Lietze V.U., Abd-Alla A.M.M., Vreysen M.J.B., Geden C.J., Boucias D.G. Salivary gland hypertrophy viruses: a novel group of insect pathogenic viruses. Annu. Rev. Entomol. 2010, 56:63-80.
65. Lietze V.U., Abd-Alla A.M., Boucias D.G. Two hytrosaviruses, MdSGHV and GpSGHV, induce distinct cytopathologies in their respective host insects. J. Invertebr. Pathol. 2011, 107:161-163.
66. Lietze V.U., Geden C.J., Doyle M.A., Boucias D.G. Disease dynamics and persistence of MdSGHV-infections in laboratory house fly (Musca domestica) populations. Appl. Environ. Microbiol. 2011, 78:311-317.
67. Lietze V.U., Salem T.Z., Prompiboon P., Boucias D.G. Tissue tropism of the Musca domestica salivary gland hypertrophy virus. Virus Res. 2011, 155:20-27.
68. Malele I.I., Kinung'hi S.M., Nyingilili H.S., Matemba L.E., Sahani J.K., Mlengeya T.D., Wambura M., Kibona S.N. Glossina dynamics in and around the sleeping sickness endemic Serengeti ecosystem of northwestern Tanzania. J. Vector. Ecol. 2007, 32:263-268.
69. Malele I., Nyingilili H., Msangi A. Factors defining the distribution limit of tsetse infestation and the implication for livestock sector in Tanzania. Afr. J. Agric. Res. 2011, 6:2341-2347.
70. Malele I.I., Magwisha H.B., Nyingilili H.B., Mamiro K.A., Rukambile E.J., Daffa J.W., Lyaruu E.A., Kapange L.A., Kasilagila G.K., Lwitiko N.K., Msami H.M., Kimbita E.N. Multiple Trypanosoma infections are common amongst Glossina species in the new farming areas of Rufiji district. Tanzania. Parasit. Vectors 2011, 4:217. (25 Ref.).
71. Malele I.I., Manangwa O., Nyingilili H.H., Kitwika W.A., Lyaruu E.A., Msangi A.R., Ouma J.O., Nkwangulila G., Abd-Alla A.M.M. Prevalence of SGHV among tsetse species of economic importance in Tanzania and their implication for SIT application. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S133-S137.
72. Maniania N.K., Ekesi S. The use of entomopathogenic fungi in the control of tsetse flies. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S83-S88.
73. Maudlin I., Welburn S.C., Mehlitz D. The relationship between rickettsia-like-organisms and trypanosome infections in natural populations of tsetse in Liberia 3. Trop. Med. Parasitol. 1990, 41:265-267.
74. McCutcheon J.P., Moran N.A. Extreme genome reduction in symbiotic bacteria 9. Nat. Rev. Microbiol. 2012, 10:13-26.
75. Muturi C.N., Ouma J.O., Malele I.I., Ngure R.M., Rutto J.J., Mithofer K.M., Enyaru J., Masiga D.K. Tracking the feeding patterns of tsetse flies (Glossina genus) by analysis of bloodmeals using mitochondrial cytochromes genes. PLoS One 2011, 6:1-6.
76. Nogge G. Sterility in tsetse flies (Glossina morsitans Westwood) caused by loss of symbionts. Experientia 1976, 32:995-996.
77. Novakova E., Hypsa V. A new Sodalis lineage from bloodsucking fly Craterina melbae (Diptera, Hippoboscoidea) originated independently of the tsetse flies symbiont Sodalis glossinidius 1. FEMS Microbiol. Lett. 2007, 269:131-135.
78. O'Neill S.L., Gooding R.H., Aksoy S. Phylogenetically distant symbiotic microorganisms reside in Glossina midgut and ovary tissues. Med. Vet. Entomol. 1993, 7:377-383.
79. Pais R., Lohs C., Wu Y., Wang J.W., Aksoy S. The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl. Environ. Microbiol. 2008, 74:5965-5974.
80. Prompiboon P., Lietze V.-U., Denton J.S.S., Geden C.J., Steenberg T., Boucias D.G. Musca domestica salivary gland hypertrophy virus, a globally distributed insect virus that infects and sterilizes female houseflies. Appl. Environ. Microbiol. 2010, 76:994-998.
81. Rio R.V., Hu Y., Aksoy S. Strategies of the home-team: symbioses exploited for vector-borne disease control. Trends Microbiol. 2004, 12:325-336.
82. Rio, R.V.M., Symula, R.E., Wang, J., Lohs, C., Wu, Y.N., Synder, A.K., Bjornson, R.D., Oshima, K., Biehl, B.S., Perna, N.T., Hattori, M., Aksoy, 2012. Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: Glossinidae) obligate symbiont Wigglesworthia. mBio vol. 3, p. e00240-11.
83. Saridaki A., Bourtzis K. Wolbachia-induced reproductive parasitism and applications. Entomol. Hellenica 2009, 18:3-16.
84. Saridaki A., Bourtzis K. Wolbachia: more than just a bug in insects' genitals. Curr. Opin. Microbiol. 2010, 13:67-72.
85. Sasanya J.J., Abd-Alla A.M.M., Parker A.G., Cannavan A. Analysis of the antiviral drugs acyclovir and valacyclovir-hydrochloride in tsetse flies (Glossina pallidipes) using LC-MSMS. J. Chromatogr. B Analyt. Technol. Biomed. Sci. 2010, 878:2384-2390.
86. Schneider D.I., Garschall K.I., Parker A.G., Abd-Alla A.M.M., Miller W.J. Global Wolbachia prevalence, titer fluctuations and their potential of causing cytoplasmic incompatibilities in tsetse flies and hybrids of Glossina morsitans subgroup species. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S104-S115.
87. Scolari F., Siciliano P., Gabrieli P., Gomulski L.M., Bonomi A., Gasperi G., Malacrida A.R. Safe and fit genetically modified insects for pest control: from lab to field applications. Genetica 2011, 139:41-52.
88. Serbus L.R., Casper-Lindley C., Landmann F., Sullivan W. The genetics and cell biology of Wolbachia-host interactions. Ann. Rev. Genet. 2008, 42:683-707.
89. Simarro P.P., Louis F.J., Jannin J. Sleeping sickness, forgotten illness: what are the consequences in the field?. Med. Trop. 2003, 63:231-235.
90. Snyder A.K., McMillen C.M., Wallenhorst P., Rio R.V. The phylogeny of Sodalis-like symbionts as reconstructed using surface-encoding loci. FEMS Microbiol. Lett. 2011, 317:143-151.
91. Vreysen M.J.B., Saleh K.M., Ali M.Y., Abdulla A.M., Zhu Z.-R., Juma K.G., Dyck V.A., Msangi A.R., Mkonyi P.A., Feldmann H.U. Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique. J. Econ. Entomol. 2000, 93:123-135.
92. Wang J., Brelsfoard C., Wu Y., Aksoy S. Intercommunity effects on microbiome and GpSGHV density regulation in tsetse flies. J. Invertebr. Pathol. 2013, 112(Suppl. 1):S32-S39.
93. Wang Y., Jehle J.A. Nudiviruses and other large, double-stranded circular DNA viruses if ubvertebrates: new insights on an old topic. J. Invertebr. Pathol. 2009, 101:187-193.
94. Wang Y., Burand J.P., Jehle J.A. Nudivirus genomics: diversity and classification. Virol. Sin. 2007, 22:128-136.
95. Wang Y., Bininda-Emonds O.R.P., Oers M.M.v., Vlak J.M., Jehle J.A. Nudiviruses give insights into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes. 2011, 42:444-456.
96. Weiss B.L., Wang J., Aksoy S. Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol. 2011, 9:e1000619.
97. Weiss B., Maltz M., Aksoy S. Obligate symbionts activate immune system development in the tsetse fly. J. Immunol. 2012.
98. Wernegreen J.J. Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Genet. 2002, 3:850-861.
99. Werren J.H., Baldo L., Clark M.E. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 2008, 6:741-751.