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Review of Treatment Methods to Remove Wolbachia Bacteria from Arthropods

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Review of Treatment Methods to Remove Wolbachia Bacteria from Arthropods Review of treatment methods to remove Wolbachia bacteria from arthropods Y.-Y. Li, K. D. Floate, P. G. Fields & B.- P. Pang Symbiosis ISSN 0334-5114 Volume 62 Number 1 Symbiosis (2014) 62:1-15 DOI 10.1007/s13199-014-0267-1 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Symbiosis (2014) 62:1–15 DOI 10.1007/s13199-014-0267-1 Review of treatment methods to remove Wolbachia bacteria from arthropods Y. - Y. L i & K. D. Floate & P.G. Fields & B.-P.Pang Received: 17 October 2013 /Accepted: 15 January 2014 /Published online: 30 January 2014 # Springer Science+Business Media Dordrecht 2014 Abstract Wo l b a c h i a are intracellular bacteria that infect nu- 1 Introduction merous and diverse arthropod species including economic pests of crops and disease vectors affecting livestock and Wo l b a c h i a bacteria (α-Proteobacteria) are arguably the most humans. Research on these symbionts has identified profound successful symbionts of arthropods worldwide. They report- effects of Wo l b a c h i a on their hosts with possible application in edly infect 17 to 76 % of diverse taxa that include members of pest control. Such research often requires methods to cure Class Insecta (insects), Class Arachnida (mites, scorpions, infections. To facilitate future research on these bacteria, we spiders), Class Malacostraca (amphipods, isopods) and Class reviewed the Wo l b a c h i a literature to summarize results of 110 Maxillopoda (barnacles) (Baldo et al. 2007; Bouchon et al. studies spanning 62 taxa that report on treatment methods and 1998; Cordaux et al. 2012; Duron et al. 2008; Floate et al. outcomes. Application of tetracycline in diet is the most 2006; Hilgenboecker et al. 2008; Jeyaprakash and Hoy 2000; common method and is typically successful. Rifampicin is Rowley et al. 2004; Werren et al. 1995;ZugandHammerstein secondarily used, and may be successful when tetracycline is 2012). In some insect orders, the prevalence of infections not. Elevated temperatures can be used to eliminate infections, among species may approach 100 %; e.g., lice (Anoplura, but is not often used. Rearing hosts under crowded conditions Mallophaga) (Kyei-Poku et al. 2005). Infections also occur or starvation has been shown to reduce Wo l b a c h i a titre which in filarial nematodes (Nematoda: Class Secernentea), includ- affects maternal transmission. Application of treatment ing the causative agents for river blindness and elephantiasis methods has a number of considerations with possible impli- (Taylor et al. 2005). Given the importance of their hosts as cations for the interpretation of data. This review is intended to economic pests of crops, or as vectors of diseases affecting alert the reader to treatment options and potential non-target humans and animals, a tremendous amount of resources has effects. been directed towards research on Wo l b a c h i a – host interac- tions (Fig. 1). Keywords Wo l b a c h i a . Elimination . Antibiotics . The success of these bacteria reflects their ability to ma- Temperature nipulate the reproductive biology of their host to enhance the spread of infections across generations. Wo l b a c h i a are mainly transmitted from infected mothers to their offspring via egg cytoplasm (Hoffmann and Turelli 1988). Thus, manipulations Y.<Y. L i : B.<P. Pang (*) typically confer a competitive advantage to infected females College of Agriculture, Inner Mongolia Agricultural University, over their uninfected sisters. One type of manipulation is Hohhot, Inner Mongolia, China cytoplasmic incompatibility (CI), which occurs when unin- e-mail: [email protected] fected females mate with Wolbachia-infected males. Y.<Y. L i : K. D. Floate Depending upon the host species, CI can cause egg mortality, Lethbridge Research Centre, Agriculture and Agri-Food Canada, the death of female embryos, or the development of eggs into Lethbridge, AB, Canada males that would otherwise develop into females. A second type of manipulation is the induction of parthenogenesis, P. G. Fields Cereal Research Centre, Agriculture and Agri-Food Canada, whereby unfertilized eggs develop into females. A third type Winnipeg, MB, Canada is feminization, which causes genetic males to develop into Author's personal copy 2 Y.-Y. Li et al. Fig. 1 Reported in 2-year increments, three metrics document the grow- ‘Floate’, but provide data through 2012. c ‘Google’ values (n=12 559) ing research emphasis on Wolbachia. a ‘Floate’ reports values (n=704) derive from Google Scholar (http://scholar.google.ca/) and report the from Floate et al. (2006). These identify original research articles located number of ‘results’ obtained using ‘Wo l b a c h i a’ as the search term for using database searches of CAB Abstracts, Biological Abstracts, and ‘articles (excluding patents and legal documents)’. Google Scholar values PubMed with ‘Wolbachia’ as the search term and subsequently vetted include original research articles, but also books, abstracts, theses and by KDF for content. Data for 2005 (n=100) is excluded. b ‘Scopus’ other items obtained from sources in addition to scientific journals. Prior values (n=1 667) derive from the Scopus database (http://www.scopus. to 1981, total values for Floate, Scopus and Google are 40, 13 and 146, com/) and identify the number of ‘articles’ that include ‘Wolbachia’ in the respectively abstract, title or keywords. They generally correspond with those for functional females. A fourth type is male-killing, in which experimental research on Wo l b a c h i a to relatively few taxa. In Wo l b a c h i a cause the death of male embryos. These manipula- a survey of 510 papers published prior to 2006 that report on tions and other effects of Wo l b a c h i a on their hosts have been Wo l b a c h i a – arthropod associations, 58 % were restricted to the subject of numerous reviews (e.g., Floate et al. 2006; taxa in four insect families: Drosophilidae (25.5), Culicidae Werren 1997; Werren et al. 2008;White2011;Engelstädter (19.4), Trichogrammatidae (8.2), Pteromalidae (5.1) (Floate and Hurst 2009;Feldhaar2011). et al. 2006). Within these families, research was limited to a The effects of Wo l b a c h i a are elegantly demonstrated by handful of genera and particularly species characterized by the treating hosts to manipulate infections and then comparing ease of laboratory culture, short generation times, high fecun- the reproductive fitness of treated versus untreated hosts. In dity, and which easily were treated with antibiotics. Several one study, antibiotic treatments were used to reduce titre levels hundred additional research articles since then have been of parthenogenesis-inducing Wolbachia in colonies of the published on Wo l b a c h i a (Fig. 1), but relatively few of them parasitoid wasp Muscidifurax uniraptor (Hymenoptera: report experimental manipulations. Pteromalidae). Whereas untreated (infected) colonies pro- Even when successful methods have been identified to duced only female progeny, colonies with decreasing levels remove Wolbachia from its host, the outcome is far from of Wolbachia produced increasingly higher proportions of certain. It has been our experience that when treatments do male progeny (Zchori-Fein et al. 2000). In a second study, work, they require continuous application to the host during antibiotic treatments were used to remove infections of CI- egg-to-adult development for two or more generations (Floate inducing Wo l b a c h i a from colonies of the confused flour bee- and Coghlin 2010; Kyei-Poku et al. 2003; Yamada et al. tle, Tribolium confusum (Coleoptera: Tenebrionidae). 2007). Thus, we were intrigued by reports that infections Subsequent crosses of uninfected females to infected males could be easily removed from T. confusum. Stevens (1989) produced no offspring, whereas all other crosses produced removed Wo l b a c h i a with 100 % success by rearing immature normal numbers of offspring (Wade and Stevens 1985). hosts for 22 days at 37 °C. Wade and Stevens (1985)removed These and similar studies (e.g., Breeuwer and Werren 1990; infections in 20 days by rearing adults on flour treated with Min and Benzer 1997; Otsuka and Takaoka 1997;Wadeand 1.25 mg tetracycline/g flour. Despite considerable effort in our Stevens 1985) emphasize the importance of being able to own lab, however, we have been unable to repeat these results experimentally cure infections to document the consequences (Y. Li, unpubl. research, see Table 1). Otsuka and Takaoka of Wo l b a c h i a infection to host reproduction and biology. (1997) cured infections of Wo l b a c h i a in the mosquito Aedes Despite its importance in clarifying Wo l b a c h i a – host rela- albopictus (Diptera: Culicidae) by exposing first-instar larvae tionships, challenges in curing infections have restricted to tetracycline (5.0 mg/ml water) for 24 h. Using this same Author's personal copy Methods to remove Wolbachia 3 Ta b l e 1 Studies reporting on the use of antibiotics to treat infections of Wolbachia in arthropods Taxa (common namea) Antibiotic added to diet Duration (outcome) Reference Class Arachnida Acarina (chiggers, mites, ticks) Tetranychidae (spider mites) Bryobia praetiosa Tetracycline (1.5 mg/ml) 4 days (curedb) (Weeks and Breeuwer 2001) Panonychus mori Tetracycline (1 mg/ml) 1 generation (cured) (Hong et al.
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