Wolbachia endosymbiont responsible for cytoplasmic incompatibility in a terrestrial crustacean: effects in natural and foreign hosts

Wolbachia bacteria are vertically transmitted endosymbionts that disturb the reproduction of many arthropods thereby enhancing their spread in host populations. Wolbachia are often responsible for changes of sex ratios in terrestrial isopods, a result of the feminization of genotypic males. Here we found that the Wolbachia hosted by Cylisticus convexus (wCc) caused unidirectional cytoplasmic incompatibility (CI), an effect commonly found in insects. To understand the diversity of Wolbachia-induced effects in isopods, wCc were experimentally transferred in a novel isopod host, Armadillidium vulgare. wCc conserved the ability to induce CI. However, Wolbachia were not transmitted to the eggs, so the capacity to restore the compatibility in crosses involving two transinfected individuals was lost. The feminizing Wolbachia hosted by A. vulgare was unable to rescue CI induced by wCc. These results showed that Wolbachia in isopods did not evolved broadly to induce feminization, and that CI and the feminizing effect are probably due to different mechanisms. In addition, wCc reduces the mating capacity of infected C. convexus males, suggesting that the bacteria might alter reproductive behaviour. The maintenance of wCc in host populations is discussed.

[1]  T. Rigaud,et al.  Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice , 1995 .

[2]  R. Giordano,et al.  Mitotic Defects Associated with Cytoplasmic Incompatibility inDrosophila simulans , 1996 .

[3]  Ary A. Hoffmann,et al.  Cytoplasmic incompatibility in insects , 1997 .

[4]  D. Poinsot,et al.  Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships. , 1998, Genetics.

[5]  J. Werren,et al.  Induction of paternal genome loss by the paternal‐sex‐ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): A comparative study of early embryonic events , 1995, Molecular reproduction and development.

[6]  P. Juchault,et al.  Androgenic Hormone Specificity in Terrestrial Isopods (Oniscidea): Systematic Involvements , 1999 .

[7]  A. Imms Faune de France , 1946, Nature.

[8]  M. Wolfner,et al.  Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins. , 2000, Genetics.

[9]  K. Bourtzis,et al.  Wolbachia infections and arthropod reproduction , 1998 .

[10]  J. Werren,et al.  Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  J. Werren,et al.  The evolution of heritable symbionts , 1997 .

[12]  R. Giordano,et al.  16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Turelli EVOLUTION OF INCOMPATIBILITY‐INDUCING MICROBES AND THEIR HOSTS , 1994, Evolution; international journal of organic evolution.

[14]  F. Rousset,et al.  Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  D. Bouchon,et al.  New evidence for feminizing bacteria in terrestrial isopods : evolutionary implications , 1994 .

[16]  M. J. Hatcher,et al.  Population dynamics under parasitic sex ratio distortion. , 1999, Theoretical population biology.

[17]  M. Blaxter,et al.  Phylogeny of Wolbachia in filarial nematodes , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  H. Guzmán,et al.  Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart , 1994, Nature.

[19]  F. Rousset,et al.  Properties of Drosophila simulans strains experimentally infected by different clones of the bacterium Wolbachia , 1994, Heredity.

[20]  F. Rousset,et al.  Phylogeny and PCR–based classification of Wolbachia strains using wsp gene sequences , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  D. Bouchon,et al.  Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  J. Werren,et al.  Molecular identification of microorganisms associated with parthenogenesis , 1993, Nature.

[23]  S. West,et al.  Male–killing Wolbachia in two species of insect , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  J. Witteveldt,et al.  Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene , 1999, Insect molecular biology.

[25]  F. Vavre,et al.  Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. , 1999, Molecular biology and evolution.

[26]  R. Stouthamer,et al.  Cross-order transfer of Wolbachia from Muscidifurax uniraptor (Hymenoptera: Pteromalidae) to Drosophila simulans (Diptera: Drosophilidae) , 1999, Heredity.

[27]  F. Rousset,et al.  The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. , 1993, Journal of invertebrate pathology.

[28]  J. Moreau,et al.  Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity , 1999, Heredity.