Male mating performance and cytoplasmic incompatibility in a wPip Wolbachia trans-infected line of Aedes albopictus (Stegomyia albopicta)

Medical and Veterinary Entomology

Volumn 27, Issue 4, 2013, Pages 377-386

  Moretti, R ^a   Calvitti, M ^a  

^a ENEA   (Italy)

Author keywords

Aedes albopictus (Stegomyia albopicta); Cytoplasmic incompatibility; Genetic control; Male competitiveness; Wolbachia pipientis

Indexed keywords

BACTERIUM; CYTOPLASMIC INCOMPATIBILITY; EGG; ENDOSYMBIONT; INFECTIVITY; MALE; MATING SUCCESS; MOSQUITO; PEST CONTROL; REPRODUCTIVE BIOLOGY; STERILITY;

AEDES ALBOPICTUS; ARTHROPODA; CULEX PIPIENS; CULICIDAE; DIPTERA; HEXAPODA; RICKETTSIACEAE; RICKETTSIALES; STEGOMYIA; WOLBACHIA; WOLBACHIA PIPIENTIS;

AEDES; AEDES ALBOPICTUS (STEGOMYIA ALBOPICTA); ANIMAL; ARTICLE; BIOLOGICAL PEST CONTROL; CYTOPLASMIC INCOMPATIBILITY; FEMALE; GENETIC REGULATION; MALE; MALE COMPETITIVENESS; METHODOLOGY; MICROBIOLOGY; MOSQUITO; PHYSIOLOGY; REPRODUCTION; SEXUAL BEHAVIOR; WOLBACHIA; WOLBACHIA PIPIENTIS;

AEDES ALBOPICTUS (STEGOMYIA ALBOPICTA); CYTOPLASMIC INCOMPATIBILITY; GENETIC CONTROL; MALE COMPETITIVENESS; WOLBACHIA PIPIENTIS;

AEDES; ANIMALS; FEMALE; MALE; MOSQUITO CONTROL; PEST CONTROL, BIOLOGICAL; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; WOLBACHIA;

EID: 84887154258     PISSN: 0269283X     EISSN: 13652915     Source Type: Journal    
DOI: 10.1111/j.1365-2915.2012.01061.x     Document Type: Article

References (62)

1. Alphey, L., Benedict, M., Bellini, R., Clark, G.G., Dame, D.A., Service, M.W. & Dobson, S.L. (2010) Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector-Borne and Zoonotic Diseases, 10, 295-311.
2. Andreasen, M.H. & Curtis, C.F. (2005) Optimal life stage for radiation sterilization of Anopheles males and their fitness for release. Medical and Veterinary Entomology, 19, 238-244.
3. Angelini, R., Finarelli, A.C., Angelini, P. et al. (2007) An outbreak of Chikungunya fever in the province of Ravenna, Italy. Eurosurveillance, 12, pii=3260.
4. Aultman, K.S., Beaty, B.J. & Walker, E.D. (2001) Genetically manipulated vectors of human disease: a practical overview. Trends in Parasitology, 17, 507-509.
5. Beaty, B.J. (2000) Genetic manipulation of vectors: a potential novel approach for control of vector-borne diseases. Proceedings of the National Academy of Sciences of the United States of America, 97, 10295-10297.
6. Bellini, R., Medici, A., Carrieri, M., Calvitti, M., Cirio, U. & Maini, S. (2002) Applicazione della tecnica del maschio sterile nella lotta contro Aedes albopictus in Italia: ottimizzazione delle fasi di allevamento massale e sessaggio. Atti XIX Congresso Italiano di Entomologia, 10-15 June 2002 Catania, Vol. 2, pp. 993-998. Litografia Tipografia Polaris, Sondrio.
7. Bellini, R., Calvitti, M., Medici, A., Carrieri, M., Celli, G. & Maini, S. (2007) Use of the sterile insect technique against Aedes albopictus in Italy: first results of a pilot trial. Area-Wide Control of Insect Pests: from Research to Field Implementation (ed. by M. J. B. Vreysen, A. S. Robinson & J. Hendrichs ), pp. 505-515. Springer, Dordrecht.
8. Bellini, R., Albieri, A., Balestrino, F. et al. (2010) Dispersal and survival of Aedes albopictus (Diptera: Culicidae) males in Italian urban areas and significance for sterile insect technique application. Journal of Medical Entomology, 47, 1082-1091.
9. Benedict, M.Q., Levine, R.S., Hawley, W.A. & Lounibos, L.P. (2007) Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector-Borne and Zoonotic Diseases, 7, 76-85.
10. Benjamin, S.N. & Bradshaw, W.E. (1994) Body size and flight activity effects on male reproductive success in the pitcher plant mosquito (Diptera: Culicidae). Annals of the Entomological Society of America, 83, 331-336.
11. Blagrove, M.S.C., Arias-Goeta, C., Failloux, A.-B. & Sinkins, S.P. (2012) Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proceedings of the National Academy of Sciences of the United States of America, 109, 255-260.
12. Boller, E.F., Russ, K., Vallo, V. & Bush, G.L. (1976) Incompatible races of the European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae) their origin and potential use in biological control. Entomologia Experimentalis et Applicata, 20, 237-247.
13. Boyer, S., Gilles, J., Merancienne, D., Lemperiere, G. & Fontenille, D. (2011) Sexual performance of male mosquito Aedes albopictus. Medical and Veterinary Entomology, 25, 454-459.
14. Boyer, S., Toty, C., Jacquet, M., Lemperiere, G. & Fontenille, D. (2012) Evidence of multiple inseminations in the field in Aedes albopictus. PLoS ONE, 7, e42040.
15. Brelsfoard, C.L. & Dobson, S.L. (2011) Wolbachia effects on host fitness and the influence of male ageing on cytoplasmic incompatibility in Aedes polynesiensis (Diptera: Culicidae). Journal of Medical Entomology, 48, 1008-1015.
16. Calvitti, M., Moretti, R., Porretta, D., Bellini, R. & Urbanelli, S. (2009) Effects on male fitness of removing Wolbachia infections from the mosquito Aedes albopictus. Medical and Veterinary Entomology, 23, 132-140.
17. Calvitti, M., Moretti, R., Lampazzi, E., Bellini, R. & Dobson, S.L. (2010) Characterization of a new Aedes albopictus (Diptera: Culicidae)-Wolbachia pipientis (Rickettsiales: Rickettsiaceae) symbiotic association generated by artificial transfer of the wPip strain from Culex pipiens (Diptera: Culicidae). Journal of Medical Entomology, 47, 179-187.
18. Chapman, T. (2009) Finding the right plugin: mosquitoes have the answer. PLoS Biology, 7, e1000273.
19. Dobson, S.L. (2003) Reversing Wolbachia-based population replacement. Trends in Parasitology, 19, 128-133.
20. Dobson, S.L. & Rattanadechakul, W. (2001) A novel technique for removing Wolbachia infections from Aedes albopictus. Journal of Medical Entomology, 38, 844-849.
21. Dobson, S.L., Fox, C.W. & Jiggins, F.M. (2002) The effect of Wolbachia-induced cytoplasmic incompatibility on host population size in natural and manipulated systems. Proceedings of the Royal Society of London, Series B, 269, 437-445.
22. Duron, O., Fort, P. & Weill, M. (2007) Influence of ageing on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Heredity, 98, 368-374.
23. Dyck, V.A., Hendrichs, J. & Robinson, A.S. (2005) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht.
24. Facchinelli, L., Valerio, L., Bond, J.G. et al. (2011) Development of a semi-field system for contained field trials with Aedes aegypti in southern Mexico. American Journal of Tropical Medicine and Hygiene, 85, 248-256.
25. Fried, M. (1971) Determination of sterile insect competitiveness. Journal of Economic Entomology, 64, 869-872.
26. Gibbons, R.V. (2010) Dengue conundrums. International Journal of Antimicrobial Agents, 365, 536-539.
27. Gould, F. & Schliekelman, P. (2004) Population genetics of autocidal control and strain replacement. Annual Reviews of Entomology, 49, 193-217.
28. Gratz, N.G. (2004) Critical review of the vector status of Aedes albopictus. Medical and Veterinary Entomology, 18, 215-227.
29. Gubler, D.J. (2002) The global emergence/resurgence of arboviral diseases as public health problems. Archives of Medical Research, 33, 330-342.
30. Gubler, D.J. (2004) The changing epidemiology of yellow fever and dengue, 1900 to 2003: full circle? Comparative Immunology, Microbiology and Infectious Diseases, 27, 319-330.
31. Hancock, P.A., Sinkins, S.P., Charles, H. & Godfray, J. (2011) Strategies for introducing Wolbachia to reduce transmission of mosquito-borne diseases. PLoS Neglected Tropical Diseases, 5, e1024.
32. Hansson, B. & Westerberg, L. (2002) On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology, 11, 2467-2474.
33. Helinski, M.E.H. & Knols, B.G.J. (2008) Mating competitiveness of male Anopheles arabiensis mosquitoes irradiated with a partially or fully sterilizing dose in small and large laboratory cages. Journal of Medical Entomology, 45, 698-705.
34. Helinski, M.E.H., Parker, A.G. & Knols, B.G.J. (2006) Radiation-induced sterility for pupal and adult stages of the malaria mosquito Anopheles arabiensis. Malaria Journal, 5, 41.
35. Hoffmann, A.A., Turelli, M. & Simmons, G.M. (1986) Unidirectional incompatibility between populations of Drosophila simulans. Evolution, 40, 692-701.
36. Hoffmann, A.A., Montgomery, B.L., Popovici, J. et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature, 476, 454-457.
37. Ioannidis, P. & Bourtzis, K. (2007) Insect symbionts and applications: the paradigm of cytoplasmic incompatibility-inducing Wolbachia. Entomological Research, 37, 125-138.
38. Jones, J.C. (1967) Spermatocysts in Aedes aegypti (Linnaeus). Biological Bulletin, 132, 23-33.
39. Jones, J.C. (1973) Are mosquitoes monogamous? Nature, 242, 343-344.
40. Kittayapong, P., Mongkalangoon, P., Baimai, V. & O'Neill, S.L. (2002) Host age effect and expression of cytoplasmic incompatibility in field populations of Wolbachia-superinfected Aedes albopictus. Heredity, 88, 270-274.
41. Knipling, E.F. (1955) Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology, 48, 459-462.
42. Krafsur, E. (1998) Sterile insect technique for suppressing and eradicating insect populations: 55 years and counting. Journal of Agricultural Entomology, 15, 303-317.
43. Lacroix, R., Delatte, H., Hue, T. & Reiter, P. (2009) Dispersal and survival of male and female Aedes albopictus (Diptera: Culicidae) on Réunion island. Journal of Medical Entomology, 46, 1117-1124.
44. La Ruche, G., Souarès, Y., Armengaud, A. et al. (2010) First two autochthonous dengue virus infections in metropolitan France. Eurosurveillance, 15, pii=19676.
45. Murphy, B., Jansen, C., Murray, J. & De Barro, P. (2010) Risk analysis on the Australian release of Aedes aegypti (L.) (Diptera: Culicidae) containing Wolbachia. CSIRO Report. http://eliminatedengue.com/LinkClick.aspx?fileticket=nMtZNaIayzw%3d&tabid=3911 [Accessed 16 October 2012].
46. Okanda, F.M., Dao, A., Njiru, B.N. et al. (2002) Behavioural determinants of gene flow in malaria vector populations: Anopheles gambiae males select large females as mates. Malaria Journal, 1, 10.
47. Poinsot, D., Bourtzis, K., Markakis, G., Savakis, C. & Mercot, H. (1998) Wolbachia transfer from Drosophila melanogaster to D. simulans: host effect and cytoplasmic incompatibility relationships. Genetics, 150, 227-237.
48. Ponlawat, A. & Harrington, L.C. (2007) Age and body size influence male sperm capacity of the dengue vector, Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology, 44, 422-426.
49. Ponlawat, A. & Harrington, L.C. (2009) Factors associated with male mating success of the dengue vector mosquito, Aedes aegypti. American Journal of Tropical Medicine and Hygiene, 80, 395-400.
50. Porretta, D., Bellini, R., Medici, A., Lampazzi, E., Calvitti, M. & Urbanelli, S. (2007) Evaluation of a strategy to restore genetic variability in mass-reared Aedes albopictus lines. 73rd Annual Meeting of the American Mosquito Control Association, 1-5 April 2007, Orlando, FL, p. 69.
51. Reed, D.H. & Frankham, R. (2003) Correlation between fitness and genetic diversity. Conservation Biology, 17, 230-237.
52. Robinson, A.S. (1998) Genetic control of insect pests. Biological and Biotechnological Control of Insect Pests (ed. by J. E. Rechcigl & N. A. Rechcigl ), pp. 141-169. Lewis Publishing, Boca Raton, FL.
53. Singh, K.R.P., Curtis, C.F. & Krishnamurthy, B.S. (1976) Partial loss of cytoplasmic incompatibility with age in males of Culex fatigans Wied. Annals of Tropical Medicine and Parasitology, 70, 463-466.
54. Sinkins, S.P. & Godfray, H.C.J. (2004) Use of Wolbachia to drive nuclear transgenes through insect populations. Proceedings of the Royal Society of London B, 271, 1421-1426.
55. Talbalaghi, A., Moutailler, S., Vazeille, M. & Failloux, A.-B. (2010) Are Aedes albopictus or other mosquito species from northern Italy competent to sustain new arboviral outbreaks? Medical and Veterinary Entomology, 24, 83-87.
56. Thomas, D.T., Donnelly, C.A., Wood, R.J. & Alphey, L.S. (2000) Insect population control using a dominant, repressible, lethal genetic system. Science, 287, 2474-2476.
57. Urbanelli, S., Bellini, R., Carrieri, M., Sallicandro, P. & Celli, G. (2000) Population structure of Aedes albopictus (Skuse): the mosquito which is colonizing Mediterranean countries. Heredity, 84, 331-337.
58. Walker, T., Johnson, P.H., Moreira, L.A. et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature, 476, 450-453.
59. Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6, 741-751.
60. Wise de Valdez, M.R., Nimmo, D., Betz, J., Gong, H.-F., James, A.A., Alphey, L. & Black, W.C. IV (2011) Genetic elimination of dengue vector mosquitoes. Proceedings of the National Academy of Sciences of the United States of America, 108, 4772-4775.
61. Wiwatanaratanabutr, I., Allan, S., Linthicum, K. & Kittayapong, P. (2010) Strain-specific differences in mating, oviposition, and host-seeking behaviour between Wolbachia-infected and uninfected Aedes albopictus. Journal of the American Mosquito Control Association, 26, 265-273.
62. Zabalou, S., Riegler, M., Theodorakopoulou, M., Stauffer, C. & Savakis, C. (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proceedings of the National Academy of Sciences of the United States of America, 101, 15042-15045.