Genetics, Vol. 178, 2145-2160, April 2008, Copyright © 2008
doi:10.1534/genetics.107.086488

Multiple Rescue Factors Within a Wolbachia Strain

Sofia Zabalou^*,, Angeliki Apostolaki^*,, Savvas Pattas, Zoe Veneti^*, Charalampos Paraskevopoulos, Ioannis Livadaras^*, George Markakis, Terry Brissac, Hervé Merçot^,** and Kostas Bourtzis^*,,1

^* Institute of Molecular Biology and Biotechnology, FORTH, Vassilika Vouton, Heraklion 71110, Crete, Greece, Technological Educational Institute of Crete, Heraklion 71110, Crete, Greece, UMR 7138, Equipe Génétique & Evolution, CNRS-Université Paris 6, 75252 Paris Cedex 05, France, Department of Environmental and Natural Resources Management, University of Ioannina, Agrinio 30100, Greece and ^** Institute Jacques Monod, UMR 7592, CNRS-Universités Paris 6&7, 75251 Paris Cedex 05, France

¹ Corresponding author: Department of Environmental and Natural Resources Management, University of loannina, 30100 Agrinio, Greece.
E-mail: kbourtz{at}uoi.gr

Wolbachia-induced cytoplasmic incompatibility (CI) is expressed when infected males are crossed with either uninfected females or females infected with Wolbachia of different CI specificity. In diploid insects, CI results in embryonic mortality, apparently due to the the loss of the paternal set of chromosomes, usually during the first mitotic division. The molecular basis of CI has not been determined yet; however, several lines of evidence suggest that Wolbachia exhibits two distinct sex-dependent functions: in males, Wolbachia somehow "imprints" the paternal chromosomes during spermatogenesis (mod function), whereas in females, the presence of the same Wolbachia strain(s) is able to restore embryonic viability (resc function). On the basis of the ability of Wolbachia to induce the modification and/or rescue functions in a given host, each bacterial strain can be classified as belonging in one of the four following categories: mod⁺ resc⁺, mod^– resc⁺, mod^– resc^–, and mod⁺ resc^–. A so-called "suicide" mod⁺ resc^– strain has not been found in nature yet. Here, a combination of embryonic cytoplasmic injections and introgression experiments was used to transfer nine evolutionary, distantly related Wolbachia strains (wYak, wTei, wSan, wRi, wMel, wHa, wAu, wNo, and wMa) into the same host background, that of Drosophila simulans (STCP strain), a highly permissive host for CI expression. We initially characterized the modification and rescue properties of the Wolbachia strains wYak, wTei, and wSan, naturally present in the yakuba complex, upon their transfer into D. simulans. Confocal microscopy and multilocus sequencing typing (MLST) analysis were also employed for the evaluation of the CI properties. We also tested the compatibility relationships of wYak, wTei, and wSan with all other Wolbachia infections. So far, the cytoplasmic incompatibility properties of different Wolbachia variants are explained assuming a single pair of modification and rescue factors specific to each variant. This study shows that a given Wolbachia variant can possess multiple rescue determinants corresponding to different CI systems. In addition, our results: (a) suggest that wTei appears to behave in D. simulans as a suicide mod⁺ resc^– strain, (b) unravel unique CI properties, and (c) provide a framework to understand the diversity and the evolution of new CI-compatibility types.

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