The bacteria in the genus Wolbachia are cytoplasmically inherited symbionts of arthropods. Infection often causes profound changes in host reproduction, enhancing bacterial transmission and spread in a population. The reproductive alterations known to result from Wolbachia infection include cytoplasmic incompatibility (CI), parthenogenesis, feminization of genetic males, fecundity enhancement, male killing and, perhaps, lethality. Here, we report male killing in a third insect, the black £our beetle Tribolium madens, based on highly female-biased sex ratios of progeny from females infected with Wolbachia. The bias is cytoplasmic in nature as shown by repeated backcrossing of infected females with males of a naturally uninfected strain. Infection also lowers the egg hatch rates signi¢cantly to approximately half of those observed for uninfected females. Treatment of the host with antibiotics eliminated infection, reverted the sex ratio to unbiased levels and increased the percentage hatch. Typically Wolbachia infection is transmitted from mother to progeny, regardless of the sex of the progeny; however, infected T. madens males are never found. Virgin females are sterile, suggesting that the sex-ratio distortion in T. madens results from embryonic male killing rather than parthenogenesis. Based on DNA sequence data, the male-killing strain of Wolbachia in T. madens was indistinguishable from the CI-inducing Wolbachia in Tribolium confusum, a closely related beetle. Our ¢ndings suggest that host^symbiont interaction e¡ects may play an important role in the induction of Wolbachia reproductive phenotypes.
▪ Abstract Wolbachia bacteria are cytoplasmic endosymbionts with a wide range of effects on their hosts and are known to infect two major invertebrate groups, arthropods and nematodes. In arthropods Wolbachia alter host reproduction, causing unidirectional and bidirectional cytoplasmic incompatibility, parthenogenesis, feminization, and embryonic male killing. Wolbachia variation in reproductive effects is indicative of a high degree of evolutionary plasticity. As many as 75% of arthropods may be infected with Wolbachia, which in addition to affecting reproduction, can also directly affect host fitness by either increasing or decreasing survival and fecundity. We review the dynamics of embryonic male-killing, including effects on insect mating behavior, as well as the distribution and implication of Wolbachia infections in filarial nematodes. Arthropod host–Wolbachia phylogenies are not congruent, which is suggestive of horizontal transmission. The opposite has been shown in nematode-Wolbachia phylogenies, indicative of long-term association and vertical transmission. Multiple levels of parasitism within arthropods may promote horizontal transmission. Bacteriophage WO has recently been identified and is found in all Wolbachia-infected insect hosts so far examined. Extensive horizontal transmission of the phage occurs between different Wolbachia strains within a host as well as between Wolbachia in different hosts. The phage genome may carry genes important in determining both the effect of Wolbachia on arthropod host reproduction and host fitness and fecundity. The extensive horizontal transmission of the phage may explain the plasticity of Wolbachia's effect on arthropod hosts.
SUMMARYInfections with the rickettsial microorganism Wolbachia are cytoplasmically inherited and occur in a wide range of insect species and several other arthropods. Wolbachia infection often results in unidirectional cytoplasmic incompatibility (CI): crosses between infected males and uninfected females are incompatible and show a reduction of progeny or complete inviability. Unidirectional CI can also occur when males harbouring two incompatible Wolbachia strains are crossed with females infected with only one of the two strains. In the flour beetle Tribolium confusum, Wolbachia infections are of particular interest because of the severity of incompatibility. Typically, no progeny results from the incompatible cross, whereas only partial incompatibility is observed in most other hosts. Werren et al. (1995a) reported that Wolbachia infections in T. confusum consist of two bacterial strains belonging to distinct phylogenic groups, based on PCR amplification and sequence analysis of the bacterial cell division gene ftsZ. However, Fialho & Stevens (1996) showed that eight strains of T. confusum were infected with a single and common incompatibility type. Here we report analysis of the ftsZ gene by specific PCR amplification. Diagnostic restriction enzyme assays revealed no evidence of double infections in 11 geographic strains of T. confusum, including the strain examined by Werren et al. (1995a). Further, sequence analysis of the Wolbachia ftsZ gene and an internal transcribed spacer (ITS) region in two of these strains displayed no nucleotide variation or evidence of polymorphisms. Results suggest that T. confusum is infected with B-group Wolbachia only.
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