MEEGID 1944 No. of Pages 12, Model 5G 8 May 2014 Infection, Genetics and Evolution xxx (2014) xxx–xxx 1 Contents lists available at ScienceDirect Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid 6 7 3 Mosquito and sand fly gregarines of the genus Ascogregarina and 4 Psychodiella (Apicomplexa: Eugregarinorida, Aseptatorina) – Overview 5 of their taxonomy, life cycle, host specificity and pathogenicity a,⇑ b 8 Q1 Lucie Lantova , Petr Volf 9 a Institute of Histology and Embryology, 1st Faculty of Medicine, Charles University in Prague, Albertov 4, 128 00 Prague 2, Czech Republic 10 b Department of Parasitology, Faculty of Science, Charles University in Prague, Vinicna 7, 128 44 Prague 2, Czech Republic 11 12 article info abstract 2714 15 Article history: Mosquitoes and sand flies are important blood-sucking vectors of human diseases such as malaria or 28 16 Received 30 January 2014 leishmaniasis. Nevertheless, these insects also carry their own parasites, such as gregarines; these mon- 29 17 Received in revised form 16 April 2014 oxenous pathogens are found exclusively in invertebrates, and some of them have been considered useful 30 18 Accepted 24 April 2014 in biological control. Mosquito and sand fly gregarines originally belonging to a single genus Ascogrega- 31 19 Available online xxxx rina were recently divided into two genera, Ascogregarina comprising parasites of mosquitoes, bat flies, 32 hump-backed flies and fleas and Psychodiella parasitizing sand flies. Currently, nine mosquito Ascogrega- 33 20 Keywords: rina and five Psychodiella species are described. These gregarines go through an extraordinarily interest- 34 21 Ascogregarina ing life cycle; the mosquito and sand fly larvae become infected by oocysts, the development continues 35 22 Psychodiella 23 Coevolution transtadially through the larval and pupal stages to adults and is followed by transmission to the off- 36 24 Host specificity spring by genus specific mechanisms. In adult mosquitoes, ascogregarines develop in the Malpighian 37 25 Pathogenicity tubules, and oocysts are defecated, while in the sand flies, the gregarines are located in the body cavity, 38 26 their oocysts are injected into the accessory glands of females and released during oviposition. These life 39 history differences are strongly supported by phylogenetical study of SSU rDNA proving disparate posi- 40 tion of Ascogregarina and Psychodiella gregarines. This work reviews the current knowledge about Asco- 41 gregarina and Psychodiella gregarines parasitizing mosquitoes and sand flies, respectively. It gives a 42 comprehensive insight into their taxonomy, life cycle, host specificity and pathogenicity, showing a very 43 close relationship of gregarines with their hosts, which suggests a long and strong parasite-host 44 coevolution. 45 Ó 2014 Published by Elsevier B.V. 46 47 48 49 50 1. Introduction et al., 2004), microsporidia (reviewed by Andreadis, 2007), bacteria 63 (reviewed by Minard et al., 2013) and viruses (reviewed by Becnel 64 51 Mosquitoes (Diptera: Culicidae) and sand flies (Diptera: and White, 2007). Similarly, sand flies suffer from the presence of a 65 52 Psychodidae) are blood-sucking insects and important vectors of wide range of pathogens (reviewed by Warburg et al., 1991) such 66 53 human pathogens. Apart from a number of pathogenic viruses, as mites (e.g., Lewis and Macfarlane, 1981), nematodes (e.g., 67 54 mosquitoes transmit Plasmodium (Apicomplexa: Haemosporida) Secundio et al., 2002), protists (e.g., McConnell and Correa, 1964), 68 55 and Filarioidea (Nematoda: Spirurida), while sand flies are the vec- fungi (e.g., Akhoundi et al., 2012), microsporidia (e.g., Matos 69 56 tors of Leishmania (Euglenozoa: Trypanosomatida) and Bartonella et al., 2006), bacteria (e.g., Gouveia et al., 2008) and viruses (e.g., 70 57 (Proteobacteria). As pointed out by Warburg (1991), the life cycle Warburg and Pimenta, 1995). 71 58 of these insects comprising water and terrestrial larval stages, Mosquitoes and sand flies also serve as hosts of gregarines 72 59 respectively, can facilitate growth and persistence of various (Apicomplexa) of the genus Ascogregarina (Ward, Levine and Craig, 73 60 entomopathogens. In mosquitoes, these include mites (e.g., 1982) and Psychodiella Votypka, Lantova and Volf, 2009, respec- 74 61 Kirkhoff et al., 2013), nematodes (reviewed by Petersen, 1980), tively. Phylum Apicomplexa encompasses very important human 75 62 protists (reviewed by Clark, 1980), fungi (reviewed by Scholte pathogens such as Cryptosporidium, Toxoplasma or Plasmodium, 76 while gregarines are parasites exclusively of invertebrates. This 77 might give the impression that they would not be of much 78 ⇑ Corresponding author. Tel.: +420 224968118; fax: +420 224919899. importance to humans; however, especially the neogregarines are 79 E-mail addresses: [email protected] (L. Lantova), [email protected] (P. Volf). http://dx.doi.org/10.1016/j.meegid.2014.04.021 1567-1348/Ó 2014 Published by Elsevier B.V. Please cite this article in press as: Lantova, L., Volf, P. Mosquito and sand fly gregarines of the genus Ascogregarina and Psychodiella (Apicomplexa: Eugre- garinorida, Aseptatorina) – Overview of their taxonomy, life cycle, host specificity and pathogenicity. Infect. Genet. Evol. (2014), http://dx.doi.org/10.1016/ j.meegid.2014.04.021 MEEGID 1944 No. of Pages 12, Model 5G 8 May 2014 2 L. Lantova, P. Volf / Infection, Genetics and Evolution xxx (2014) xxx–xxx 80 generally considered useful in biological control of insect pests. Fur- included in a single genus Ascogregarina. The type species of this 110 81 thermore, sand fly gregarines are known to seriously harm labora- genus is Ascogregarina culicis (Ross, 1898), originally described as 111 82 tory-reared colonies; therefore, they negatively affect the research Gregarina culicidis (Ross, 1895)orGregarina culicis (Ross, 1898) 112 83 on vector-borne infections. and later renamed as Lankesteria culicis (Wenyon, 1911). The first 113 84 Even though Ascogregarina and Psychodiella are affecting impor- described sand fly gregarine was originally named Monocystis mac- 114 85 tant vectors of human diseases, they have not been given the atten- kiei by Shortt and Swaminath (1927) or Lankesteria phlebotomi 115 86 tion they deserve, and information available about them is mackiei by Missiroli (1932). Grasse (1953) proposed a new name 116 87 currently insufficient. This applies particularly for the sand fly gre- Ascocystis for gregarines of the genus Lankesteria parasitizing 117 88 garines. Before 2010, there had been only three described species insects, and he renamed La. culicis as Ascocystis culicis. Similarly, 118 89 of Psychodiella, the host specificity and pathogenicity of these par- Ormieres (1965) and Tuzet and Rioux (1966) renamed La. ph. mac- 119 90 asites had only been evaluated experimentally in a single study, kiei as Ascocystis mackiei, and later Scorza and Carnevali (1981) 120 91 and closer descriptions of the life cycle and fine structure had been brought morphological evidence placing sand fly gregarines of 121 92 available only about one species. the genus Monocystis into the genus Ascocystis. Levine (1977) and 122 93 This work brings a comprehensive overview of all the described Ormieres (1965) accepted Ascocystis from Grasse (1953) for para- 123 94 species of Ascogregarina and Psychodiella from mosquitoes and sites of Diptera and restricted Lankesteria to parasites of ascidians. 124 95 sand flies, including their taxonomy, life cycle, pathogenicity and However, the name Ascocystis is a synonym for Ascocystis Bather, 125 96 host specificity features. It brings evidence that both species of 1889 used for fossil crinoid echinoderm; therefore, Ward et al. 126 97 these parasites have a very close relationship with their hosts, sug- (1982) established a new name Ascogregarina for the gregarines 127 98 gesting a long coevolution. from Diptera formerly known as Ascocystis. 128 Votypka et al. (2009) pointed out several features that distin- 129 99 2. Taxonomy guish gregarines of the genus Ascogregarina parasitizing mosqui- 130 toes from the ones found in sand flies. Representatives of these 131 100 Members of the genus Ascogregarina (syn. Monocystis von Stein, two groups have different hosts (Culicidae versus Psychodidae), 132 101 1848, Lankesteria Mingazzini, 1891 and Ascocystis Grasse, 1953) and their life cycles differ considerably (for details see Sections 3 133 102 and Psychodiella are aseptate eugregarines (Eugregarinorida: Asep- and 4, Figs. 1 and 2). In adult mosquitoes, ascogregarines develop 134 103 tatorina), and together, they have been recently included in a new in the Malpighian tubules and oocysts are defecated, while in the 135 104 family Ascogregarinidae (Desportes, 2013). The genus Ascogregari- sand flies, the gregarines are located in the body cavity, their 136 105 na comprises species parasitizing mostly Diptera, particularly mos- oocysts are injected into the accessory glands of females and 137 106 quitoes, bat flies (Nycteribiidae) and hump-backed flies (Phoridae) attached to the chorion of oviposited eggs. These life history differ- 138 107 but also fleas (Siphonaptera). The genus Psychodiella is found only ences were strongly supported by phylogenetical study of SSU 139 108 in sand flies. The terminology and history of the final designation of rDNA showing disparate position of mosquito and sand fly grega- 140 109 these parasites is complex. Originally, both these groups were rines; therefore, Votypka et al. (2009) reclassified