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Expression of Cytoplasmic Incompatibility and Host Fitness Effects in Field Populations of Sogatella Furcifera Infected with Cardinium

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Expression of Cytoplasmic Incompatibility and Host Fitness Effects in Field Populations of Sogatella Furcifera Infected with Cardinium MOLECULAR ENTOMOLOGY Expression of Cytoplasmic Incompatibility and Host Fitness Effects in Field Populations of Sogatella furcifera Infected With Cardinium 1 1 2 XIANG-FEI ZHANG, DONG-XIAO ZHAO, HAO-SEN LI, AND XIAO-YUE HONG Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China Downloaded from https://academic.oup.com/jee/article/105/6/2161/797780 by guest on 23 September 2021 J. Econ. Entomol. 105(6): 2161Ð2166 (2012); DOI: http://dx.doi.org/10.1603/EC12268 ABSTRACT ÔCandidatus CardiniumÕ is a maternally inherited intracellular bacterium that infects a wide range of arthropods and causes diverse reproductive alterations of its arthropod hosts, including cytoplasmic incompatibility (CI), parthenogenesis and feminization. CI is the most common effect and is expressed as a reduction in the number of offspring in crosses between infected males and uninfected females (or females infected with a different bacterial strain). The white-backed planthopper Sogatella furcifera (Horva´th) is a major rice pest in Asia and is a vector of the Southern rice black-streaked dwarf virus (SRBSDV). In this study, we found severe CI expression induced by Cardinium in Yunnan and Guangxi populations of S. furcifera by performing four crosses of Cardinium-infected (C) and uninfected (U) planthoppers: &U ϫ (U, &U ϫ (C, &C ϫ (U, &C ϫ (C. Investigations of the Þtness costs and beneÞts of Cardinium infection in these populations showed that it had no effect on the fecundity of females, but could shorten the developmental time of nymphs. KEY WORDS Cardinium, Sogatella furcifera, CI, sex ratio, Þtness Cardinium (Flexibacteriaceae, Class Sphingobacteria, mon effect associated with endosymbiont infection Phylum Bacteroidetes) is a bacterial endosymbiont (Stouthamer et al. 1999, OÕNeill et al. 1997), and has that was Þrst found in cell cultures established from been observed in crosses between infected males the tick Ixodes scapularis Say (Kurtti et al. 1996). and either uninfected females (unidirectional CI) Compared with Wolbachia bacteria, which have been or females infected by a different strain (bidirec- known to manipulate arthropod reproduction since tional CI). Cardinium-induced CI has been found in 1970s (Werren et al. 2008), Cardinium bacteria are the spider mite Eotetranychus suginamensis (Gotoh relatively new to biological study. Cardinium has been et al. 2007), the red poultry mite Dermanyssus gal- detected in Hymenoptera (Hunter et al. 2003, Matalon linae (De Luna et al. 2009), the parasitoid wasp et al. 2007, Weeks et al. 2003, ZchoriÐFein et al. 2001, Encarsia pergandiella (Hunter et al. 2003), and the ZchoriÐFein and Perlman 2004), Hemiptera (Weeks sexual spider mite Bryobia sarothamni (Ros and et al. 2003, ZchoriÐFein et al. 2004, Bigliardi et al. 2006, Breeuwer 2009). Perlman et al. 2006), Acari (Enigl and Schausberger The whitebacked planthopper Sogatella furcifera 2007, Gotoh et al. 2007, Groot and Breeuwer 2006, Hoy (Horva´th) (Hemiptera: Delphacidae) is a major rice et al. 2008, Weeks et al. 2001), and Areneae (Duron et pest in Asia. The nymphs and adults suck sap from rice al. 2008). Cardinium was found in Þve of Þve species plants, resulting in leaf yellowing, reduced tillering, (100%) of spider mites (Gotoh et al. 2007), and in 9 of stunting, unÞlled grains and hopperburn. S. furcifera 22 species (22%) of spider mites, in 4 of 25 species (16%) of biting midges Culicoides (Diptera: Cera- has caused intermittent famines in eastern Asia after topogonidae) and in 27 of 57 species (47.4%) of pl- the so-called Green Revolution of the 1960s (Noda et anthoppers (Nakamura et al. 2009, Zhang et al. 2012a). al. 2008). Particularly, S. furcifera is an important vec- Cardinium can induce a number of reproductive tor of the Southern rice black-streaked dwarf virus manipulations in arthropods similar to those in- (SRBSDV). We previously showed that the infection duced by Wolbachia to optimize its transmission. frequency of Cardinium was high in Chinese popula- Cardinium can induce parthenogenesis in scale in- tions of S. furcifera (Zhang et al. 2012b). Here, we sects (Provencher et al. 2005) and Encarsia hispida, investigated the reproductive manipulations and Þt- and feminization in Brevipalpus phoenicis (Weeks et ness costs and beneÞts by Cardinium in S. furcifera. We al. 2001, Groot et al. 2006). Cardinium can also induce determined the phylogenetic relationships of the Car- cytoplasmic incompatibility (CI). CI is the most com- dinium strains found in two S. furcifera populations and measured their effects on CI, the female ratio, 1 These authors contribute equally. fecundity, survival, and development times under lab- 2 Corresponding author, e-mail: [email protected]. oratory conditions. 0022-0493/12/2161Ð2166$04.00/0 ᭧ 2012 Entomological Society of America 2162 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 6 Materials and Methods Sample Collection. S. furcifera were collected from Guangxi Zhuang Autonomous Region (GX) and Yun- nan Province (YN) in south China in July 2010. Field- collected planthoppers were reared on rice seedlings in a climate-controlled room (25ЊC, 60% relative hu- midity [RH], and a photoperiod of 16:8 [L:D]). Preparation of a Singly Cardinium-Infected Strain. Single pairs of male and female adult planthoppers of a natural population were placed in plastic cups (120 mm in height and 80 mm in diameter) containing rice seedlings. The test pairs laid eggs in the rice seedlings Downloaded from https://academic.oup.com/jee/article/105/6/2161/797780 by guest on 23 September 2021 and were removed from the cups after 2 wk. The females were checked for Wolbachia and Cardinium infection by polymerase chain reaction (PCR) ampli- Þcation. The offspring from the singly Cardinium- infected (Wolbachia-free) mothers were separately reared in plastic cups. For each group, pairs of males and females were bred as in the Þrst generation. Off- spring from females that did not have the same infec- tion status as their mothers were discarded. This se- lection regime was maintained for Þve successive generations until 100% Cardinium-infected popula- Fig. 1. Phylogenetic tree based on 16S rDNA sequences tions were obtained. of Cardinium, constructed by using a neighbor-joining pro- cedure in CLUSTAL X. Each Cardinium is shown by its host PCR and Cloning. DNA was extracted from single name. Numbers on the nodes indicate bootstrap values (%). planthopper according to the method of OÕNeill et al. S. furcifera populations were collected from Guangxi Zhuang (1992). DNA was extracted by homogenizing a single Autonomous region (GX) and Yunnan Province (YN) in individual in a 40 ␮l mixture of STE buffer (100 mM south China, respectively. Asterisks designate symbiont se- NaCl, 10 mM Tris-HCl, 1 mM EDTA, and pH 8.0) in quences obtained in this study. a 1.5 ml Eppendorf tube and incubated with 2.5 ␮l proteinase K (10 mg/ml, 2.5 ␮l) at 37ЊC for 30 min, then heated at 95ЊC for 5 min. The samples were then removed from the tube. After another week, centrifuged brießy, then used at once for the PCR newly hatched nymphs by this time were counted, and reactions or stored at Ϫ20Њ. PCR detection of Wolba- the remaining deposited eggs in the seedlings were chia was performed using primers wsp-81 F and wsp- dissected to microscopically observe the develop- 691R (Braig et al. 1998). Thermal cycles were as fol- ment. Eye pigmentation (red in color) was examined lows: 95ЊC for 3 min; followed by 35 cycles of 95ЊC for as an indicator of egg development (Noda et al. 2001). 30 s, 55ЊC for 45 s, 72ЊC for 1 min, and 72ЊC for 5 min Emerging adult offspring (sons and daughters) were as a Þnal extension after the last cycle. PCR detection scored per cross to determine the sex ratio (the num- for Cardinium was performed using primers CLOf and ber of daughter offspring). Data were analyzed with CLOr (Weeks et al. 2003). Thermal cycles were as one-way analysis of variance (ANOVA) and means follows: 94ЊC for 2 min, 35 cycles at 94ЊC for 30 s, 57ЊC were compared using a Tukey-honestly signiÞcant dif- for 30 s, 72ЊC for 30 s, and 72ЊC for 5 min as a Þnal ference (HSD) test (SPSS 17.0). To normalize the extension after the last cycle. The sequences were data, an arcsine square-root transformation was used determined for at least three clones having opposite for egg hatchability and sex ratio. orientations. The PCR products were cloned into a Fitness Effects. The Þtness costs and/or beneÞts of pEASY-T3 Cloning Vector (TransGen, Beijing, the different infection statuses (Cardinium-infected China), sequenced in both directions using the uni- and uninfected) in S. furcifera were investigated by versal primer pairs M13, m13R. The sequence was analyzing the fecundity and the developmental dura- determined by the Dye Terminator Sequencing tion of females. The effects of different infection types method with a DNA Sequencer (model 377 and 3700, on female fecundity were tested by comparing the Applied Biosystems). number of eggs laid in 15 d by infected and uninfected Cross Experiments. The effects of crosses: &U ϫ females in crosses involving infected and uninfected (U, &U ϫ (C, &C ϫ (U, &C ϫ (C. Singly Car- males. dinium-infected planthopper on CI were determined Development time was measured by placing Ϸ150 (Fig. 1). For each cross, nymphal planthoppers were newly hatched nymphs into individual tubs containing individually reared in a test tube containing rice seed- rice seedlings. They were moved to fresh rice seed- lings and checked daily for emergence (to ensure they lings every 5 d until hatching. Hatching was checked were virgins). Upon emergence a female and a male daily. Data were analyzed with one-way ANOVA and were introduced into a test tube and allowed to lay means were compared using a Tukey-HSD test (SPSS eggs into the rice seedlings at 25Ð26ЊCfor2wkand 17.0).
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