Koehnke A, Telschow A, Werren JH, Hammerstein P. Life and death of an influential passenger: Wolbachia and the evolution of CI-modifiers by their hosts. PLoS One 4: e4425

Institute for Theoretical Biology, Humboldt-Universität zu Berlin, Berlin, Germany.
PLoS ONE (Impact Factor: 3.23). 02/2009; 4(2):e4425. DOI: 10.1371/journal.pone.0004425
Source: PubMed


Wolbachia are intracellular bacteria widely distributed among arthropods and nematodes. In many insect species these bacteria induce a cytoplasmic incompatibility (CI) between sperm of infected males and eggs of uninfected females. From an evolutionary point of view, CI is puzzling: In order to induce this modification-rescue system, Wolbachia affect sperm of infected males even though Wolbachia are only transmitted maternally. Phylogenetic studies of Wolbachia and hosts show that the bacteria rarely cospeciate with their hosts, indicating that infections are lost in host species. However, the mechanisms leading to Wolbachia loss are not well understood.
Using a population genetic model, we investigate the spread of host mutants that enhance or repress Wolbachia action by affecting either bacterial transmission or the level of CI. We show that host mutants that decrease CI-levels in males (e.g. by reducing Wolbachia-density during spermatogenesis) spread, even at cost to mutant males. Increase of these mutants can lead to loss of Wolbachia infections, either as a direct consequence of their increase or in a step-wise manner, and we derive analytically a threshold penetrance above which a mutation's spread leads to extinction of Wolbachia. Selection on host modifiers is sexually antagonistic in that, conversely, host mutants that enhance Wolbachia in females are favoured whereas suppressors are not.
Our results indicate that Wolbachia is likely to be lost from host populations on long evolutionary time scales due to reduction of CI levels in males. This can occur either by evolution of single host modifiers with large effects or through accumulation of several modifier alleles with small effects on Wolbachia action, even at cost to mutant males and even if infected hosts do not incur fecundity costs. This possibility is consistent with recent findings and may help to explain the apparent short evolutionary persistence times of Wolbachia in many host systems.

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Available from: Arnulf Koehncke
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    • "Nevertheless, the impressive host range of Wolbachia in arthropods suggests that such losses are frequently compensated by a recolonization of the population by Wolbachia (e.g. Koehncke et al., 2009). In any case, the colonization of uninfected hosts can be generated by the occurrence of horizontal transfers between or within host species. "
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    ABSTRACT: The Wolbachia are intracellular endosymbionts widely distributed among invertebrates. These primarily vertically transmitted α-proteobacteria have been intensively studied during the last decades due to their intriguing interactions with hosts, ranging from reproductive manipulations to mutualism. To optimize their vertical transmission from mother to offspring, the Wolbachia have developed fine-tuned strategies. However, the Wolbachia are not restricted to the female gonads and frequently exhibit wide intra-host distributions. This extensive colonization of somatic organs might be necessary for Wolbachia to develop their diverse extended phenotypes. From an endosymbiont's perspective, the within-host environment potentially presents different environmental constraints. Hence, the Wolbachia have to face different intracellular habitats, their host's immune system as well as other microorganisms co-occurring in the same host individual and sometimes even in the same cell. A means for the Wolbachia to protect themselves from these environmental constrains may be to live 'hidden' in vacuoles within host cells. In this review, we summarize the current knowledge regarding the extent of the Wolbachia pandemic and discuss the various environmental constraints these bacteria may have to face within their 'host ecosystem'. Finally, we identify new avenues for future research to better understand the complexity of Wolbachia's interactions with their intracellular environment.
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    • "Most of those phenomena have evolved as a consequence of vertical transmission of Wolbachia through the maternal line over evolutionary timescales. However, theory predicts that infections are lost eventually (Koehncke et al. 2009), and evidence exists that Wolbachia strains are transmitted horizontally between hosts on a frequent basis. Specifically , the lack of phylogenetic congruence between Wolbachia strains and arthropod hosts (O'Neill et al. 1992; Schilthuizen & Stouthamer 1997; Vavre et al. 1999; Baldo et al. 2008; Raychoudhury et al. 2009) has led to this conclusion. "
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    ABSTRACT: The endosymbiotic bacterium Wolbachia enhances its spread via vertical transmission by generating reproductive effects in its hosts, most notably cytoplasmic incompatibility (CI). Additionally, frequent interspecific horizontal transfer is evident from a lack of phylogenetic congruence between Wolbachia and its hosts. The mechanisms of this lateral transfer are largely unclear. To identify potential pathways of Wolbachia movements, we performed multilocus sequence typing of Wolbachia strains from bees (Anthophila). Using a host phylogeny and ecological data, we tested various models of horizontal endosymbiont transmission. In general, Wolbachia strains seem to be randomly distributed among bee hosts. Kleptoparasite-host associations among bees as well as other ecological links could not be supported as sole basis for the spread of Wolbachia. However, cophylogenetic analyses and divergence time estimations suggest that Wolbachia may persist within a host lineage over considerable timescales and that strictly vertical transmission and subsequent random loss of infections across lineages may have had a greater impact on Wolbachia strain distribution than previously estimated. Although general conclusions about Wolbachia movements among arthropod hosts cannot be made, we present a framework by which precise assumptions about shared evolutionary histories of Wolbachia and a host taxon can be modelled and tested. This article is protected by copyright. All rights reserved.
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    • "Altogether, both acquisition and loss are hallmarks of Wolbachia infection dynamics on evolutionary timescales (Frost et al. 2010). For a particular host species, infection patterns are thus cyclical over evolutionary time (Koehncke et al. 2009). First, Wolbachia would infect a species through horizontal transmission and spread through the new host by vertical transmission from generation to generation. "
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    ABSTRACT: Wolbachia are bacterial endosymbionts that manipulate the reproduction of their arthropod hosts. Although theory suggests that infections are frequently lost within host species due to the evolution of resistance, Wolbachia infect a huge number of species worldwide. This apparent paradox suggests that horizontal transmission between host species has been a key factor in shaping the global Wolbachia pandemic. Since Wolbachia infections are thus acquired and lost like any other infection, we use a standard epidemiological model to analyze Wolbachia horizontal transmission dynamics over evolutionary time. Conceptually modifying the model, we apply it not to transmission between individuals but between species. Since, on evolutionary timescales, infections spread frequently between closely related species and occasionally over large phylogenetic distances, we represent the set of host species as a small-world network which satisfies both requirements. Our model reproduces the effect of basic epidemiological parameters, which demonstrates the validity of our approach. We find that the ratio between transmission rate and recovery rate is crucial for determining the proportion of infected species(incidence) and that, in a given host network, the incidence may still be increasing over evolutionary time. Our results also point to the importance of occasional transmission over long phylogenetic distances for the observed high incidence levels of Wolbachia. In conclusion, we are able to explain why Wolbachia are so abundant among arthropods although selection for resistance within hosts often leads to infection loss. Furthermore, our unorthodox approach of using epidemiology in evolutionary time can be applied to all symbionts that use horizontal transmission to infect new hosts.
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