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Evolutionary Dynamics of a Spatially Structured Host-Parasite Association: Drosophila Innubila and Male-Killing Wolbachia

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Evolutionary Dynamics of a Spatially Structured Host-Parasite Association: Drosophila Innubila and Male-Killing Wolbachia Evolution, 59(7), 2005, pp. 1518±1528 EVOLUTIONARY DYNAMICS OF A SPATIALLY STRUCTURED HOST-PARASITE ASSOCIATION: DROSOPHILA INNUBILA AND MALE-KILLING WOLBACHIA KELLY A. DYER1,2,3 AND JOHN JAENIKE1,4 1Department of Biology, University of Rochester, Rochester, New York 14627 2E-mail: [email protected] 4E-mail: [email protected] Abstract. The mode and tempo of host-parasite evolution depend on population structure and history and the strength of selection that the species exert on each other. Here we genetically and epidemiologically characterize populations of the mycophagous ¯y Drosophila innubila and its male-killing Wolbachia endosymbiont, with the aim of integrating the local through global nature of this association. Drosophila innubila inhabit the forested ``sky island'' regions of the of the southwestern United States and northern Mexico, where its distribution is highly fragmented. We examine geographically isolated sky island populations of D. innubila, surveying the frequency and expression of Wolbachia infection as well as the distribution of genetic variation within and among populations of the host and parasite. In all populations, Wolbachia infection is associated with virtually complete male-killing, thus providing no evidence for the evolution of population-speci®c interaction phenotypes or local resistance. Although Wolbachia infection occurs in each of the main populations, there is variation among populations in the prevalence of infection and the resulting population-level sex ratio of D. innubila. Among these populations, the nuclear genes of D. innubila show moderate, though signi®cant, differentiation. In contrast, the host mitochondrial DNA (mtDNA), which shares transmission with Wolbachia, exhibits substantially greater geographic differentiation, even after accounting for differences in trans- mission between nuclear and mitochondrial genes. We suggest that this pattern is caused by local WolbachiaÐbut not D. innubilaЯuctuations in prevalence that increase the severity of drift experienced only by the mtDNA. Overall, our data suggest that the association between D. innubila and male-killing Wolbachia is ecologically dynamic within local populations, but evolutionarily coherent across the species as a whole. Key words. Endosymbiont, founder effect, gene ¯ow, molecular polymorphism, population structure, sex ratio dis- tortion. Received November 1, 2004. Accepted April 4, 2005. Recent theoretical and empirical studies have begun to viewed in Hurst et al. 2003). In theory, factors that sterilize explore how population structure affects the ecological and or kill males can spread through a population if infected evolutionary dynamics of host-parasite interactions (e.g., females produce more daughters (or seeds, in the case of Thrall and Antonovics 1995; Lively and Jokela 1996; Burdon CMS) than uninfected individuals. In the case of CMS this and Thrall 2000). To date, however, virtually all studies re- can result from reallocation of resources from pollen to seed lating population structure to variation in host-parasite in- production (Charlesworth and Charlesworth 1978); for male- teractions have focused on horizontally transmitted parasites killing endosymbionts, this results when the death of males (e.g., Thompson and Cunningham 2002; Fischer and Foitzik bene®ts their surviving sisters via increased resource avail- 2004; Forde et al. 2004). Meanwhile, parasites that are ver- ability or decreased inbreeding. tically transmitted from mother to offspring are being dis- Demographically, sex-ratio distorters can affect the pop- covered at an accelerating pace (reviewed in Bandi et al. ulation-level sex ratio of the host, which in turn can in¯uence 2001), and may provide rich opportunities to explore the host population dynamics and potentially cause host extinc- connection between population structure and the nature of tion due to a paucity of males (Hatcher et al. 1999). Since host-parasite interactions. Compared to horizontally trans- both CMS and male-killing endosymbionts have been shown mitted parasites, maternally transmitted symbionts exhibit an to vary among populations in presence and frequency (e.g., additional layer of population structureÐat the level of the Taylor et al. 2001; Dyeson and Hurst 2004), their demo- host individualÐand may be evolutionarily more variable in graphic effects may also vary among populations (e.g., Olson their effects on host ®tness, ranging from mutualistic to vir- et al. 2005). ulently parasitic (reviewed in Moran and Baumann 2000; Sex-ratio distorters cause the death or sterility of a sub- Bandi et al. 2001). stantial fraction of the host population every generation, im- Some maternally transmitted factors promote their own posing strong selection on the host to evolve resistance. For spread by skewing the offspring sex ratio of their host. These instance, nuclear restorer loci have evolved repeatedly in sex-ratio distorters include mitochondrial variants that cause plants harboring CMS factors, contributing to the variation cytoplasmic male sterility (CMS) in normally hermaphroditic among populations in the frequency of CMS (e.g., Manicacci plants (reviewed in Budar and Pelletier 2001) and a taxo- et al. 1997; Taylor 1999). In contrast to the comparatively nomically diverse array of endosymbiotic microorganisms well-studied systems in plants, the evolution of resistance to that cause embryonic male-killing in various arthropods (re- the male-killing endosymbionts of arthropods has received very little empirical study. 3 Present address: Institute of Evolutionary Biology, School of In this paper, we use epidemiological and population ge- Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, netic data to explore the broad-scale ecological and evolu- United Kingdom. tionary interactions between the mushroom-feeding ¯y Dro- 1518 q 2005 The Society for the Study of Evolution. All rights reserved. SPATIAL DYNAMICS OF MALE-KILLING 1519 sophila innubila and a male-killing endosymbiont. About one-third of D. innubila females from the Chiricahua Moun- tains in southeastern Arizona are infected with a strain of Wolbachia that kills virtually all of their male offspring, re- sulting in a female bias in the population-level sex ratio (Dyer and Jaenike 2004). Two lines of evidence using patterns of polymorphism of the mitochondrial DNA (mtDNA; which is maternally co-transmitted with Wolbachia) indicate that the association between D. innubila and male-killing Wolbachia is evolutionarily old. First, all of the major mtDNA haplo- types are found in both infected and uninfected individuals, as would be expected if all individuals in the present pop- ulation were descended from one originally infected female. Second, the level of mtDNA nucleotide diversity corresponds very closely with equilibrium expectations based on observed levels of infection prevalence (Dyer and Jaenike 2004). The achievement of this equilibrium depends on the long-term input of mutations subsequent to the initial ®xation of the infected haplotype lineage. The Chiricahua population of D. innubila exhibits no ev- idence of resistance to the male-killing effects of these Wol- FIG. 1. Sky island populations surveyed in this study. The black bachia, even though the infection has been resident in the diamonds indicate collection localities. See Table 1 for full names population for a substantial period of time and DNA poly- of abbreviations. morphism data indicate that D. innubila has a very large effective population size (Dyer and Jaenike 2004; J. Jaenike, unpubl. data). In addition, there is no evidence for parthe- sum, we ask whether the evolution of the D. innubila±Wol- nogenetic reproduction in this system (Dyer et al. 2005). bachia association results from the integration of divergent Because the distribution of D. innubila is highly fragmented local processes, or whether dynamics in different local pop- within its range in Arizona and New Mexico, it is possible ulations proceed largely in parallel and are thus independent that the Chiricahua population has an atypical association of the spatial structure of these populations. with these Wolbachia. Drosophila innubila is restricted to mesic habitats, and in southern Arizona it is found in oak- MATERIALS AND METHODS juniper riparian woodlands at 1500 m elevation up through Sampling and Screening for Wolbachia coniferous forests at 3000 m (Patterson and Wagner 1943; Heed et al. 1962). These mesic mountain habitats form an Drosophila innubila were collected in woodland habitats archipelago of ``sky islands,'' each of which is surrounded from geographically isolated sky-island populations in south- by much more xeric lowland desert and grassland habitats ern Arizona and New Mexico (Fig. 1; Table 1). We chose (Brown 1994). Several other organisms with sky island dis- our collecting sites based on the known range (Heed et al. tributions in Arizona exhibit marked differentiation among 1962; Patterson and Wagner 1943) and on knowledge of local populations (Maddison and McMahon 2000; Masta 2000; habitats. Each population was surveyed one to three times Boyd 2002; K. R. Zamudio and H. W. Greene, unpubl. ms.), during August±September of 2001±2004, during which ¯ies indicating a signi®cant degree of evolutionary independence were collected by sweep-netting over baits of decaying mush- among the different populations. Because D. innubila is also rooms. All collection and population genetic data from the restricted to sky islands, this species and
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