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Inherited Microorganisms, Sex-Specific Virulence and Reproductive Parasitism

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Inherited Microorganisms, Sex-Specific Virulence and Reproductive Parasitism 88 Review TRENDS in Parasitology Vol.17 No.2 February 2001 sulfated polysaccharides is involved in host cell erythrocyte binding peptide from the gliding motility and infectivity of plasmodium infection. J. Biol. Chem. 274, 1267–1276 erythrocyte binding antigen, EBA-175, which sporozoites. Cell 90, 511–522 53 Muller, H.M. et al. (1993) Thrombospondin related blocks parasite multiplication and induces 59 Wengelnik, K. (1999) The A-domain and the anonymous protein (TRAP) of Plasmodium peptide-blocking antibodies. Infect. Immun. 66, thrombospondin-related motif of Plasmodium falciparum binds specifically to sulfated 4203–4207 falciparum TRAP are implicated in the invasion glycoconjugates and to HepG2 hepatoma cells 56 Hettmann, C. et al. (2000) A dibasic motif in the process of mosquito salivary glands. EMBO J. suggesting a role for this molecule in sporozoite tail of an apicomplexan myosin is an essential 18, 5195–5204 invasion of hepatocytes. EMBO J. 12, 2881–2889 determinant of plasma membrane localization. 60 Dessens, J.T. (1999) CTRP is essential for 54 Sim, B.K. et al. (1992) Localization of the 175- Mol. Biol. Cell 11, 1385–1400 mosquito infection by malaria ookinetes. kilodalton erythrocyte binding antigen in 57 Dobrowolski, J.M. et al. (1997) Participation of EMBO J. 18, 6221–6227 micronemes of Plasmodium falciparum myosin in gliding motility and host cell invasion by 61 Kappe, S. (1999) Conservation of a gliding motility merozoites. Mol. Biochem. Parasitol. 51, 157–159 Toxoplasma gondii. Mol. Microbiol. 26, 163–173 and cell invasion machinery in apicomplexan 55 Jakobsen, P.H. et al. (1998) Identification of an 58 Sultan, A.A. et al. (1997) TRAP is necessary for parasites. J. Cell Biol. 147, 937–944 Inherited microorganisms, sex-specific virulence and reproductive parasitism Claudio Bandi, Alison M. Dunn, Gregory D.D. Hurst and Thierry Rigaud Parasites show an amazing repertoire of adaptations, highlighted by complex development of mutualistic interactions. Vertically life cycles that allow both survival in the host and transmission among hosts. transmitted parasites and symbionts are, in most However, there is one heterogeneous group of microorganisms whose cases, microorganisms, either eukaryotic or adaptations are perhaps even more surprising: parthenogenesis induction, prokaryotic, referred to here as inherited feminization of genetic males, killing of male hosts and sperm-mediated microorganisms. sterilization of uninfected eggs. The common feature of these microorganisms is their mode of transmission: inheritance from mother to offspring. Here, we Evolutionary biology of inherited microorganisms present an introduction to hereditary symbiosis, focusing on microsporidia and The interaction between host and inherited bacteria that manipulate host reproduction in arthropods (reproductive microorganisms outlined above is a simplification of parasites). We also discuss the implications of one of these microorganisms, the way in which selection acts upon these agents. Wolbachia, for the control of arthropod pests and vectors and for the therapy of These microorganisms, being inherited, have filarial diseases. Finally, we discuss whether some parasites of vertebrates interests in common with their host – more precisely, might show sex-specific virulence. they are maternally inherited, and thus have interests in common with female hosts. The selective It is still held that natural selection will reduce the pressures on maternally inherited elements differ virulence of parasites to a state of peaceful from those on the genome of the host2. First, selection coexistence. The ecological and pathogenic conditions on inherited microorganisms should select directly leading to virulence reduction are not always easy to for beneficial effects towards the host sex responsible assess. The mode of transmission of parasites is for their transmission (i.e. in general, females)3. thought to be a key determinant in the evolution of Beneficial effects on males might follow indirectly, virulence1. For example, it is accepted that increased but are not a consequence of direct selection. In fact, virulence is favoured where parasite transmission is selection might favour microorganism strains that horizontal, where there is a high chance that a host is cause a reduction of the fitness of individuals not infected by several parasite strains, and where involved in their transmission (males or uninfected parasite virulence is associated with parasite females), if these effects are associated with an fecundity and with the likelihood of transmission. increase in the fitness of females bearing the However, where parasites are vertically transmitted infection. Thus, in addition to becoming benign or (from parent to offspring), the reproductive success of even beneficial to the hosts responsible for their host and parasite are more tightly interlinked, and transmission (infected females), selection on selection should favour more benign parasite strains. inherited microorganisms can favour the spread of Indeed, selection might also promote a positive phenotypes that are detrimental to those hosts not contribution of the inherited agent to the host. Thus, involved in their transmission (males or uninfected vertical transmission is also thought to promote the females)3–7. Indeed, maternal inheritance underlies http://parasites.trends.com 1471-4922/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-4758(00)01812-3 Review TRENDS in Parasitology Vol.17 No.2 February 2001 89 Fig. 1. Electron Parthenogenesis induction micrograph showing an The development of unfertilized eggs into females egg of the mosquito Culex pipiens harbouring (thelytokous parthenogenesis) would increase the numerous Wolbachia fitness of a maternally transmitted microorganism. bacteria (arrows). In In the early 1990s, it was first reported that mosquitoes and in other arthropods, various thelytokous parthenogenesis in certain species of strains of Wolbachia wasps could be cured by the administration of determine cytoplasmic antibiotics. This indicated the possible involvement of incompatibility (Fig. 3). some microorganism in parthenogenesis induction. Other reproductive manipulations Parthenogenesis in these and a range of other determined by Wolbachia Hymenoptera was subsequently shown to be are parthenogenesis, associated with infection with certain strains of feminization of genetic Wolbachia8. More recently, Wolbachia has also been males and death of male embryos. Abbreviations: shown to be associated with parthenogenesis in f, nuclei of follicular cells insects phylogenetically distant from the of the ovariole; n, oocyte Hymenoptera (Arakaki et al.; Vandekerchove et al., nucleus. Scale bar = ∗ 0.9 µm. Photograph by Abstracts) . In Hymenoptera, male progeny arise Luciano Sacchi and from (haploid) unfertilized eggs and females from Claudio Bandi. (diploid) zygotes that are the product of fertilization. Sex determination is based on ploidy. Wolbachia induces the production of all-female broods through the different forms of microorganism-induced doubling the chromosome constitution of unfertilized reproductive manipulations observed in arthropods. eggs, restoring diploidy, and thus producing female These manipulations frequently involve determining rather than male development15. Another possible a female-biased sex ratio: for maternally inherited case of parthenogenesis induction is seen in the mite microorganisms, males are dead ends. In some Leptotrombidium tsutsugamushi, where infection cases, all-female broods are produced by converting with the bacterium Orientia tsutsugamushi is the female host to a particular form of asexuality associated with female-biased sex ratios16. (thelytokous parthenogenesis)8,9; in other cases, Parthenogenesis-inducing Wolbachia are sexual reproduction is continued, but progeny that frequently fixed within the population, converting the would ordinarily develop as males instead develop sexual host species to an asexual one. In some of these as females (they are feminized)10. Apart from these species, the ability to reproduce sexually has been lost manipulations, certain inherited microorganisms over time. Although antibiotics give rise to the are relatively benign in females, but kill male larvae production of male progeny, these males are not or embryos, if this either facilitates their horizontal functional. In other species, the infection remains at a transmission, or if it enhances the survival of polymorphic equilibrium, with both uninfected and sisters of the dead male11–14. Finally, some infected individuals remaining. Polymorphism is inherited microorganisms cause cytoplasmic thought to be promoted by host factors that resist the Claudio Bandi incompatibility: through the sperm of infected males action or transmission of the bacterium15. Istituto di Patologia they sterilize those females that do not harbour Generale Veterinaria, 5–7 Feminizing microorganisms, sex determination and Università di Milano, them . Via Celoria 10, These different microbial manipulators of host genetic conflicts 20133 Milano, Italy. reproduction are known as reproductive parasites3. Parasitic feminization is induced by both bacterial e-mail: Reproductive parasites occur in various arthropod and protozoan microorganisms and has been reported [email protected] hosts (insects, mites, crustaceans) and have been in several crustaceans and in one insect10,17,18. These Alison M. Dunn assigned to different prokaryotic lineages,
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