Naturally occurring single and double infection with Wolbachia strains in the butterfly Eurema hecabe: Transmission efficiencies and population density dynamics of each Wolbachia strain

FEMS Microbiology Ecology

Volumn 61, Issue 2, 2007, Pages 235-245

  Narita, Satoko ^b   Nomura, Masashi ^b   Kageyama, Daisuke ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b CHIBA UNIVERSITY   (Japan)

Author keywords

Double infection; Eurema hecabe; Feminization; Quantitative PCR; Vertical transmission efficiency; Wolbachia

Indexed keywords

BACTERIAL DISEASE; BACTERIUM; BUTTERFLY; CYTOPLASMIC INCOMPATIBILITY; DISEASE TRANSMISSION; FEMINIZATION; HOST-PATHOGEN INTERACTION; INFECTIVITY; POLYMERASE CHAIN REACTION; POPULATION DENSITY; SEX REVERSAL; VERTICAL TRANSMISSION;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BUTTERFLY; EMBRYO; FAT BODY; FEMALE; FEMINIZATION; LEG; MALE; MALPIGHIAN TUBULE; MIDGUT; MOTHER; NONHUMAN; OVARY; POPULATION DENSITY; PRIORITY JOURNAL; PROGENY; TESTIS; VERTICAL TRANSMISSION; WOLBACHIA;

ANIMALS; BUTTERFLIES; COLONY COUNT, MICROBIAL; DISEASE TRANSMISSION, VERTICAL; EMBRYONIC DEVELOPMENT; FEMALE; LARVA; MALE; MORTALITY; PUPA; SEX RATIO; WOLBACHIA;

ALPHAPROTEOBACTERIA; ARTHROPODA; EUREMA HECABE; WOLBACHIA;

EID: 34447504706     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2007.00333.x     Document Type: Article

References (42)

1. Bordenstein S Werren JH (2000) Do Wolbachia influence fecundity in Nasonia vitripennis? Heredity 84 : 54 62.
2. Bourtzis K Miller TA, eds (2003) Insect Symbiosis. CRC Press, Boca Raton, FL.
3. Bourtzis K Miller TA, eds (2005) Insect Symbiosis. CRC Press, Boca Raton, FL.
4. Bourtzis K, Dobson SL, Braig HR O'Neill SL (1998) Rescuing Wolbachia have been overlooked. Nature 391 : 852 853.
5. Dobson S, Marsland E Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160 : 1087 1094.
6. Dutton TJ Sinkins SP (2004) Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect Mol Biol 13 : 317 322.
7. Dworkin MM, Falkow S, Rosenberg E, Schleifer KH Stackebrandt E, eds (2006) Prokaryotes: A Handbook on the Biology of Bacteria: Symbiotic Associations, Biotechnology, Applied Microbiology, 3rd edn, pp. 959. Springer-Verlag, Berlin.
8. Fry A Rand D (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56 : 1976 1981.
9. Giordano R, O'Neill SL Robertson H (1995) Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics 140 : 1307 1317.
10. Hacombe W Hoffmann AA (2004) Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. J Invert Pathol 87 : 45 50.
11. Hiroki M, Kato Y, Kamito T Miura K (2002) Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften 89 : 167 170.
12. Hiroki M, Tagami Y, Miura K Kato Y (2004) Multiple infection with Wolbachia inducing different reproductive manipulations in the butterfly Eurema hecabe. Proc R Soc Lond B 271 : 1751 1755.
13. Hiroki M, Ishii Y Kato Y (2005) Variation in the prevalence of cytoplasmic incompatibility-inducing Wolbachia in the butterfly Eurema hecabe across the Japanese archipelago. Evol Ecol Res 7 : 931 942.
14. Hoffmann A Turelli M (1988) Unidirectional incompatibility in Drosophila simulans: geographic variation and fitness effects. Genetics 119 : 435 444.
15. Ijichi N, Kondo N, Matsumoto R, Shimada M, Ishikawa H Fukatsu T (2002) Internal spatiotemporal population dynamics of infection with three Wolbachia strains in the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Appl Environ Microbiol 68 : 4074 4080.
16. Jamnongluk W, Kittayapong P, Baimai V O'Neill SL (2002) Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species. Curr Microbiol 45 : 255 260.
17. Jiggins FM, Randerson JP, Hurst GD Majerus ME (2002) How can sex ratio distorters reach extreme prevalence? Male-killing Wolbachia are not suppressed and have near-perfect vertical transmission efficiency in Acraea encedon. Evolution 56 : 2290 2295.
18. Johanowicz D Hoy M (1999) Wolbachia infection dynamics in experimental laboratory populations of Metaseiulus occidentalis. Entomol Exp Appl 93 : 259 268.
19. Kageyama D Traut W (2004) Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc R Soc Lond B 271 : 251 258.
20. Kittayapong P, Baisley KJ, Sharpe RG, Baimai V O'Neill SL (2002) Maternal transmission efficiency of Wolbachia superinfections in Aedes albopictus populations in Thailand. Am J Trop Med Hyg 66 : 103 107.
21. Kondo N, Ijichi N, Shimada M Fukatsu T (2002) Prevailing triple infection with Wolbachia in Callosobruchus chinensis (Coleoptera: Bruchidae). Mol Ecol 11 : 167 180.
22. Kondo N, Shimada M Fukatsu T (2005) Infection density of Wolbachia endosymbionts affected by co-infection and host genotype. Biol Lett 1 : 488 491.
23. McCullagh P Nelder JA (1989) Generalized Linear Models, 2nd edn. Chapman and Hall, London.
24. Montllor CB, Maxmen A Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27 : 189 195.
25. Mouton L, Henri H, Bouletreau M Vavre F (2003) Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol Ecol 12 : 3459 3465.
26. Mouton L, Dedeine F, Henri H, Bouletreau M, Profizi N Vavre F (2004) Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics 168 : 181 189.
27. Narita S, Kageyama D, Nomura M Fukatsu T (2007) Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl Environ Microbiol, in press.
28. Narita S, Nomura M, Kato Y Fukatsu T (2006) Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications. Mol Ecol 15 : 1095 1108.
29. Nyholm SV McFall-Ngai MJ (2004) The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2 : 632 642.
30. Oliver KM, Russell JA, Moran NA Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100 : 1803 1807.
31. Oliver KM, Moran NA Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102 : 12795 12800.
32. O'Neill SL, Hoffmann AA Werren JH, eds (1997) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, New York.
33. Perrot-Minnot MJ, Guo LR Werren JH (1996) Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effect on compatibility. Genetics 143 : 961 972.
34. Poinsot D, Charlat S Mercot H (2003) On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. BioEssays 25 : 259 265.
35. R Development Core Team (2005) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL.
36. Rousset F Solignac M (1995) Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci USA 92 : 6389 6393.
37. Rousset F, Braig HR O'Neill SL (1999) A stable triple Wolbachia infection in Drosophila with nearly additive incompatibility effects. Heredity 82 : 620 627.
38. Sinkins SP, Braig HR O'Neill SL (1995) Wolbachia pipientis: bacterial density and unidirectional cytoplasmic incompatibility between infected populations of Aedes albopictus. Exp Parasitol 81 : 284 291.
39. Traut W Marec F (1996) Sex chromomatin in Lepidoptera. Q Rev Biol 71 : 239 256.
40. Tsuchida T, Koga R Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303 : 1989.
41. Vavre F, Girin C Bouletreau M (1999) Phylogenetic status of fecundity-enhancing Wolbachia that does not induce thelytoky in Trichogramma. Insect Mol Biol 8 : 67 72.
42. Zhou W, Rousset F O'Neill S (1998) Phylogeny and PCR based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond B 265 : 509 515.