Wolbachia induces sexual isolation in Drosophila melanogaster and Drosophila simulans

Ialah Gazla, Maria Carmen Carracedo

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DOI: 10.4236/ojgen.2011.12005                

Abstract

Wolbachia are a group of intracellular bacteria, ma-ternally transmitted from infected females to their offspring, which affect a wide range of arthropods. Their presence is associated with Cytoplasmic Incompatibility (CI) in crosses between infected males and uninfected females and between populations carrying different strains of Wolbachia. The negative influence of Wolbachia a infection on progeny fitness in incompatible crosses can be considered a first step in the appearance of reproductive isolation between infected and uninfected individuals. In this work, we examined the possibility of assortative mating in response to Wolbachia infection, a response that evolved as an incipient mechanism of sexual isolation in the species D. melanogaster and D. simulans. We found that the females of each species could detect the presence of the bacterium in the other sex and chose to mate with males who had the same state of infection, whereas the males randomly attempted to mate with both infected and uninfected females. Thus, Wolbachia may act as an additive factor influencing sexual isolation in Drosophila populations and may play a role in speciation events.

Keywords

Wolbachia; Assortative Mating; Sexual Isolation; Speciation; Drosophila

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Dobzhansky, T. (1937) Genetics and the origins of species, Columbia University Press, New York.
[2]	Mayr, E. (1942) Systematic and the origin of species. Columbia University Press, New York.
[3]	Kawanishi, M. and Watanabe, T.K. (1981) Genes con-trolling courtship song and mating preference in Droso-phila melanogaster, D. simulans, and their hybrids. Evo-lution, 35, 1128-1133. doi:10.2307/2408126
[4]	Paterson, H.E.H. (1985) The recognition concept of spe-cies. In Species and speciation. In: Vrba, E.S., Ed., Transvaal Museum Monograph No. 4, Transvaal Mu-seum, Pretoria, 21-29.
[5]	O’Neill, S.L. and Karr, T.L. (1990) Bidirectional incom-patibility between conspecific populations of Drosophila simulans. Nature, 348, 178-180. doi:10.1038/348178a0
[6]	Bandi, C., Anderson, T.J.C., Genchi, C. and Blaxter, M. (1998) Phylogeny of Wolbachia in filarial nematodes. Proceedings of the Royal Society B: Biological Sciences, 265, 2407-2413. doi:10.1098/rspb.1998.0591
[7]	Werren, J.H. (1997) Biology of Wolbachia. Annual Review of Entomology, 42, 587-609. doi:10.1146/annurev.ento.42.1.587
[8]	Stouthamer, A.J., Breeuwer, A.J., Hurst, G.D.D., et al. (1999) Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annual Review of Microbiology, 53, 71-102. doi:10.1146/annurev.micro.53.1.71
[9]	Jeyaprakash, A. and Hoy, M.A. (2000) Long PCR im-proves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Molecular Biology, 9, 393-405. doi:10.1046/j.1365-2583.2000.00203.x
[10]	Dobson, S.L., Marsland, E.J. and Rattanadechakul, W. (2002) Mutualistic Wolbachia infection in Aedes albopitus: Accelerating cytoplasmic drive. Genetics, 160, 1087-1094.
[11]	McGraw, E.A. and O’Neill, S.L. (2003) Wolbachia pi-pientis: Intracellular infection and pathogenesis in Dro-sophila. Current Opinion in Microbiology, 7, 67-70. doi:10.1016/j.mib.2003.12.003
[12]	Floate, K.D., Kyei-Poku, G.K. and Coghlin, P.C. (2006) Overview and relevance of Wolbachia bacteria in bio-control research. Biocontrol Science and Technology, 16, 767-788. doi:10.1080/09583150600699606
[13]	Bourtzis, K., Braig, H.R. and Karr, T.L. (2003) Cytop-lasmic Incompatibility. In: Bourtzis, K. and Miller, T., Eds., Insect Symbiosis, CRC Press, Boca Raton, 217-246.
[14]	Hurst, G.D.D., Anbutsu, H., Kutsukake, M. and Fukatsu, T. (2003) Hidden from the host: Spiroplasma bacteria in-fecting Drosophila do not cause an immune response, but are suppressed by ectopic immune activation. Insect Mo-lecular Biology, 12, 93-97. doi:10.1046/j.1365-2583.2003.00380.x
[15]	Koivisto, R.K.K. and Braig, H.R. (2003) Microorganisms and parthenogenesis. Biological Journal of the Linnean Society, 79, 43-58. doi:10.1046/j.1095-8312.2003.00185.x
[16]	Rigaud, T. (1997) Inherited microorganisms and sex determination of arthropod hosts. In: O’Neill, S.L., Hoffmann, A.A. and Werren, J.H., Eds., Influential Pas-sengers: Inherited Microorganisms and Arthropod Re-production, Oxford University Press, Oxford, 81-101.
[17]	Werren, J.H. and O’Neill, S.L. (1997) The evolution of heritable symbionts. In: O’Neill, S.L., Hoffmann, A.A. and Werren, J.H., Eds., Influential Passengers: Inherited Microorganisms and Arthropod Reproduction, Oxford University Press, Oxford, 1-41.
[18]	Clancy, D.J. and Hoffmann, A.A. (1998) Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia infected Drosophila simulans. Entomologia Experimentalis et Applicata, 86, 13-24. doi:10.1046/j.1570-7458.1998.00261.x
[19]	Stevens, L. (1989) Environmental factors affecting re-productive incompatibility in flour beetles, genus Tribo-lium. Journal of Invertebrate Pathology, 53, 78-84. doi:10.1016/0022-2011(89)90076-1
[20]	Kyei-Poku, G.K., Floate, K.D., Benkel, B. and Goettel, M.S. (2003) Elimination of Wolbachia from Urolepis ru-fipes (Hymenoptera: Pteromalidae) with heat and antibiotic treatments: Implications for host reproduction. Biocontrol Science and Technology, 3, 341-354.
[21]	Aleksandrov, I.D., Aleksandrova, M.V., Goriacheva, I.I., Roshchina, N.V., Shaikevich, E.V. and Zakharov, I.A. (2007) Removing endosymbiotic Wolbachia specifically decreases lifespan of females and competitiveness in a laboratory strain of Drosophila melanogaster. Genetika, 43, 1372-1378.
[22]	Koukou, K., Pavlikaki, H., Kilias, G., Werren, J.H., et al. (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melano-gaster cage populations. Evolution: International Journal of Organic Evolution, 60, 87-96.
[23]	Breeuwer, J.A.J. and Werren, J.H. (1990) Microorgan-isms associated with chromosome destruction and re-productive isolation between two insect species. Nature, 346, 558-560. doi:10.1038/346558a0
[24]	Coyne, J.A. (1992) Genetics and speciation. Nature, 355, 511-515. doi:10.1038/355511a0
[25]	Werren, J.H. and Jaenike, J. (1995) Wolbachia and cy-toplasmic incompatibility in mycophagous Drosophila and their relatives. Heredity, 75, 320-326. doi:10.1038/hdy.1995.140
[26]	Vala, F., Egas, M., Breeuwer, J.A. and Sabelis, M.W. (2004) Wolbachia affects oviposition and mating beha-viour of its spider mite host. Journal of Evolutionary Bi-ology, 17, 692-700. doi:10.1046/j.1420-9101.2003.00679.x
[27]	Bordenstein, S.H., O Hara, F.P. and Werren, J.H. (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature, 409, 707-710. doi:10.1038/35055543
[28]	Turelli, M. and Hoffmann, A.A., (1991) Rapid spread of an inherited incompatibility factor in California Droso-phila. Nature, 353, 440-442. doi:10.1038/353440a0
[29]	Mercot, H., Llorente, B., Jacques, M., Atlan, A. and Montchamp-Moreau, C. (1995) Variability within the Seychelles cytoplasmic incompatibility system in Dro-sophila simulans. Genetics, 141, 1015-1023.
[30]	Hoffmann, A.A., Turelli, M. and Simmons, G.M. (1986) Unidirectional incompatibility between populations of Drosophila simulans. Evolution, 40, 692-701. doi:10.2307/2408456
[31]	Nigro, L. (I991) The effect of heteroplasmy on cytoplas-mic incompatibility in transplasmic lines of Drosophila simulans showing a complete replacement of the mito-chondrial DNA. Heredity, 66, 41-45. doi:10.1038/hdy.1991.5
[32]	Rousset, F. and Solignac, M. (1995) Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proceedings of the Na-tional Academy of Sciences of the USA, 92, 6389-6393. doi:10.1073/pnas.92.14.6389
[33]	Hoffmann, A.A., Clancy, D.J. and Duncan, J. (1996) Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity, 76, 18. doi:10.1038/hdy.1996.1
[34]	Charlat, S., Bonnavion, P. and Mer?ot, H. (2003) Wolba-chia segregation dynamics and levels of cytoplasmic in-compatibility in Drosophila sechellia. Heredity, 90, 157-161. doi:10.1038/sj.hdy.6800211
[35]	Hoffmann, A.A., Clancy, D.J. and Merton, E. (1994) Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics, 136, 993-999.
[36]	Reynolds, K. and Hoffmann, A.A. (2002) Male age, host effects and the weak expression or non expression of cy-toplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genetics Research, 80, 79-87. doi:10.1017/S0016672302005827
[37]	Reynolds, K., Thomson, L.J., Hoffmann, A.A., et al. (2003) The effects of host nuclear background and tem-perature on phenotypic effects of the virulent Wolbachia strain popcom in Drosophila melanogaster. Genetics, 164, 1027-1034.
[38]	Dean, M.D. (2006) A Wolbachia-associated fitness benefit depends on genetic background in Drosophila simulans. Proceedings of the Royal Society B: Biological Sciences, 273, 1415-1420. doi:10.1098/rspb.2005.3453
[39]	Yamada, R., Floate, K.D., Riegler, M. and O’Neill, S.L. (2007) Male development time influences strength of Wolbachia-induced cytoplasmic incompatibility expression in Drosophila melanogaster. Genetics, 106, 84-86.
[40]	Gomez Valero, L., Soriano Navarro, M., Pérez Brocal, V., Heddi, A., et al. (2004) Coexistence of Wolbachia with Buchnera aphidicola and a Secondary Symbiont in the Aphid Cinara cedri. The Journal of Bacteriology, 186, 6626-6633. doi:10.1128/JB.186.19.6626-6633.2004
[41]	Casares, P., Carracedo, M.C., San Miguel, E., Pi?eiro, R. and García-Florez, L. (1993) Male mating speed in Dro-sophila melanogaster: Differences in genetic architecture in relative performance according to female genotype. Behavior Genetics, 23, 349-358. doi:10.1007/BF01067436
[42]	Casares, P., Carracedo, M.C., Del Rio, B., Pi?eiro, R., García Flórez, L. and Barros, A.R. (1998) Disentangling the effects of mating propensity and mating choice in Drosophila. Evolution, 52, 126-133. doi:10.2307/2410927
[43]	Prouzan, A. (1976) Effects of age, rearing and mating experiences on frequency dependent sexual selection in Drosophila pseudoobscura. Evolution, 30, 130-145. doi:10.2307/2407680
[44]	Gazla, I.N. and Carracedo, M.C. (2009) Effect of intra-cellular Wolbachia on interspecific crosses between Drosophila melanogaster and Drosophila simulans. Ge-netics and Molecular Research, 8, 861-869. doi:10.4238/vol8-3gmr595
[45]	Weeks, AR., Turelli, M., Harcombe, W.R., Reynolds, K.T., et al. (2007) From parasite to mutualist: Rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biology, 5, 997-1005. doi:10.1371/journal.pbio.0050114
[46]	Peng, Y., John, E., Paul, J., et al. (2008) Wolbachia infec-tion alters olfactory-cued locomotion in Drosophila spp. Applied and Environmental Microbiology, 74, 3943-3948. doi:10.1128/AEM.02607-07