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Dynamics of Double and Single Wolbachia Infections in Drosophila Simulans from New Caledonia

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Dynamics of Double and Single Wolbachia Infections in Drosophila Simulans from New Caledonia Heredity (2002) 88, 182–189 2002 Nature Publishing Group All rights reserved 0018-067X/02 $25.00 www.nature.com/hdy Dynamics of double and single Wolbachia infections in Drosophila simulans from New Caledonia AC James1, MD Dean1,2,3, ME McMahon2 and JWO Ballard1,2 1Department of Biology, University of Iowa, Iowa City, Iowa 52242, USA; 2The Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605, USA; 3The University of Illinois-Chicago, 845 W. Taylor Street, Chicago, IL 60607, USA The bacterial symbiont Wolbachia can cause cytoplasmic either the DNA of these bacterial isolates have diverged from incompatibility in Drosophila simulans flies: if an infected those previously collected, or the genetic background of the male mates with an uninfected female, or a female with a host has lead to a reduction in the phenotype of incompati- different strain of Wolbachia, there can be a dramatic bility. Mitochondrial sequence polymorphism at two sites reduction in the number of viable eggs produced. Here we within the host genome was assayed to investigate popu- explore the dynamics associated with double and single lation structure related to infection types. There was no cor- Wolbachia infections in New Caledonia. Doubly infected relation between sequence polymorphism and infection type females were compatible with all males in the population, suggesting that double infections are the stable type, with explaining the high proportion of doubly infected flies. In this singly infected and uninfected flies arising from stochastic study, males that carry only wHa or wNo infections showed segregation of bacterial strains. Finally, we discuss the reduced incompatibility when mated to uninfected females, nomenclature of Wolbachia strain designation. compared with previous reports. These data suggest that Heredity (2002) 88, 182–189. DOI: 10.1038/sj/hdy/6800025 Keywords: Drosophila simulans; Wolbachia; New Caledonia; cytoplasmic incompatibility; strain concept Introduction (mtDNA) appears to be non-randomly associated with the bacterial strains (Montchamp-Moreau et al, 1991; Wolbachia pipientis is a common symbiont of Drosophila Rousset and Solignac, 1995; James and Ballard, 2000). The simulans. Wolbachia may cause a number of reproductive wHa and wNo strains have only been detected in individ- abnormalities, including cytoplasmic incompatibility uals with the siI haplotype, wRi and wAu in flies with (Yen and Barr, 1971; Hoffmann et al, 1986). In D. simulans, siII haplotypes, and wMa in siIII individuals. The goal of incompatibility may occur when an infected male mates this study is to focus on the dynamics of flies that carry with an uninfected female, or a female with a different the siI haplotype and their wHa and/or wNo strains of strain of Wolbachia. In such a cross, there may be a dra- Wolbachia. matic reduction in the number of viable eggs produced. It has been demonstrated both theoretically (Caspari The reciprocal cross usually yields normal numbers of and Watson, 1959) and empirically (Turelli and progeny, unless the parents harbor different strains of Hoffmann, 1991) that Wolbachia infections that cause Wolbachia. The aim of this study is to explore the dynam- incompatibility spread once they reach a threshold fre- ics of a host population from New Caledonia with unin- quency. As a Wolbachia infection sweeps through a popu- fected, singly infected, and doubly infected individuals. lation, other cytoplasmic factors hitchhike with bacterial D. simulans is an excellent model system for investigat- transmission. For example, Nigro and Prout (1990) ing the host and symbiont population genetics. D. simul- started two sets of D. simulans population cages carrying ans is a cosmopolitan species that may harbor five strains two mitochondrial types (C and P), with one of the types of Wolbachia (wHa, wNo, wRi, wAu, and wMa). A sixth at a frequency of 20% in one set and 80% in the other. strain, wKi, has been described from Tanzania, but is The C type occurred in a host infected with Wolbachia homosequential with wMa at both the 16S rDNA and wsp whereas the P type was associated with an uninfected loci and is likely the same. In this study, we refer to wMa host. In all cages, there was a rapid increase in the instead of wKi because wMa has nomenclatural pre- frequency of the C type as the infection became pre- cedence. In D. simulans, mitochondrial variation is struc- dominant under unidirectional incompatibility. In the tured into three monophyletic haplotypic groups desig- mosquito Aedes albopictus, changes in mtDNA frequencies nated siI, siII, and siIII (Baba-Aı¨ssa et al, 1988; Solignac have also been associated with a spreading Wolbachia and Monnerot, 1986). Furthermore, mitochondrial DNA infection in the laboratory (Kambhampati et al, 1992). Wolbachia also causes shifts in mtDNA variation in natural populations. Incompatibility in Drosophila was Correspondence: AC James, Department of Biology, University of Iowa, first discovered in crosses between a predominantly Iowa City, IA 52242, USA. E-mail: avis-jamesȰuiowa.edu infected population of D. simulans near Riverside, Califor- Received 22 June 2001; accepted 31 October 2001 nia, with various uninfected populations in northern and Wolbachia infections in Drosophila simulans AC James et al 183 central California (Hoffmann et al, 1986). Initially, the CA, USA). The control lines used in the molecular classi- infection was limited to sites south of the Tehachapi fication of Wolbachia strains and mitochondrial haplo- transverse range that separates the Los Angeles basin types have been described in detail elsewhere (Ballard, from the Central Valley. However, infected flies became 2000a, b; James and Ballard, 2000). NC48 is infected with increasingly common in the Central Valley after 1988 and both wHa and wNo. TT01 carries the wHa infection, and a rapid spread north was observed from 1989 until 1994 RU07 carries the wMa infection (which differs from wNo (Turelli and Hoffmann, 1991; Turelli et al, 1992; Hoffmann by 1 bp in the 16S rDNA but is homosequential to wNo and Turelli, 1997). As the infection swept through popu- at the Wolbachia major surface protein [wsp] locus). lations, the mtDNA variant initially associated with the To assay for presence or absence of Wolbachia infection, infected D. simulans increased in frequency. Extending Wolbachia 16S rDNA was PCR amplified following a earlier work on incompatibility (Caspari and Watson, modified protocol of O’Neill et al (1992). The thermal pro- 1959), Turelli and colleagues (Turelli et al, 1992; file was shortened to 30 cycles, and the denaturation and Hoffmann and Turelli, 1997) developed a model with annealing steps were run for 15 s each instead of 1 min. intrapopulation dynamics for the joint frequency of Any uninfected result was checked by running the same incompatibility types and mtDNA genotypes. extraction and an independent extract of three flies from The existence of double infections in New Caledonia the isofemale line with primers that amplify a region of are somewhat of a mystery as the wNo infection type is the wsp locus (Zhou et al, 1998). not reported to elicit high incompatibility. To the north To survey the population for specific Wolbachia strains, and east of New Caledonia, wNo is not found. Popu- a multiplex PCR reaction that amplifies a region of the lations in Hawaii and Tahiti have very high frequencies wsp locus was designed. The forward primer 81F of Zhou of single infections with wHa individuals (O’Neill et al, et al (1998) and newly designed reverse primers 463R (5′- 1992; Rousset et al, 1992; Turelli and Hoffmann, 1995). To TACCATTTTGACTACTCACAGCG-3′) and 635R (5′- the southwest, Australian populations are infected with GATCTCTTTAGTAGCTGATAC-3′) were used. The 81F wAu (Hoffmann et al, 1996). The only other known primer anneals to both wHa and wNo sequence. With our locality where double infections have been reported is in protocol, 487R amplifies a 427 bp product from wHa and the Seychelles (Merc¸ot et al, 1995b; Merc¸ot and Poinsot, 658R amplifies a 570 bp product from wNo (Figure 1). 1998). The 10 ␮l PCR reactions consisted of 10 ng template Here we investigate empirically why these two strains DNA, 1 ␮l 81F, 1 ␮l 658R, 0.35 ␮l 487R (all primers at ␮ ␮ ␮ ␮ × coexist in a seemingly stable frequency in New Cale- 10 ng/ l), 1 l of 8 mM dNTP, 4.625 l ddH2O, 1 l10 donia. Are they acting synergistically, independently, or PCR buffer with 25 mM MgCl2+, and 0.25 units Taq poly- is wNo parasitizing wHa? To address these questions, we assayed infection types in a population known to harbor double infections, identified their incompatibility pheno- types, and sequenced two polymorphic regions in the mitochondrial genome of their host. One notable finding is that wHa does not always induce strong incompati- bility, as previously observed. Furthermore, infection status did not correlate with any detectable mitochon- drial substructure within the siI haplotype. These data suggest that the population has reached an equilibrium where singly infected or uninfected flies arise through stochastic segregation from doubly infected mothers. We discuss these results and link them back to an inclusive strain concept for Wolbachia. Materials and methods Drosophila lines and molecular classification of Wolbachia Fifty-five isofemale lines of D. simulans were established from flies collected in Noume´a, New Caledonia, on 29 and 31 December 1999. DNA was isolated from these lines within 1.5 months of them being established in the laboratory. To determine the Wolbachia infection status of these lines we employed a strain specific PCR assay that Figure 1 Detection of Wolbachia infections in D. simulans.(a) Sche- matic diagram of PCR amplification of surface binding protein gene generated an amplicon of specific size for each Wolbachia from Wolbachia (wsp). Primers 81F and 635R amplify a 570 bp frag- strain. We sequenced select lines to confirm the lines ment specific for wNo; primers 81F and 463R produce a 427 bp frag- were infected with the expected Wolbachia strains.
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