Population structure of a microparasite infecting Daphnia: spatio-temporal dynamics

Abstract

Background: Detailed knowledge of spatial and temporal variation in the genetic population structure of hosts and parasites is required for understanding of host - parasite coevolution. As hot-spots of contemporary coevolution in natural systems are difficult to detect and long-term studies are restricted to few systems, additional population genetic data from various host - parasite systems may provide important insights into the topic. This is particularly true for parasites, as these players have been under-investigated so far due to the lower availability of suitable molecular markers. Here, we traced genetic variation (based on sequence variants in the internal transcribed spacer region, ITS) among seven geographically isolated populations of the ichthyosporean Caullerya mesnili, a common microparasite of the cladoceran Daphnia (here, the D. longispina hybrid complex). At three sites, we also studied parasite genetic variation over time (three to four sampling points) and tested for associations between parasite genotypes and host species.

Results: Parasite (and host) populations were significantly structured across space, indicating limited dispersal. Moreover, the frequency of parasite genotypes varied significantly over time, suggesting rapid evolutionary change in Caullerya. However, the distribution of parasite genotypes was similar across different host species, which might in turn have important consequences for parasite epidemiology.

Conclusions: The approach proposed here can be applied to track spatial and temporal changes in the population structure of other microparasite species for which sequence variation in the ITS or other highly variable genome regions has been documented but other types of polymorphic markers are lacking. Screening of parasite sequence variants allows for reliable detection of cross-species infections and, using advanced sequencing techniques in the near future, for detailed studies of parasite evolution in natural host - parasite systems.

Figure 1

Location of sampling sites in the Czech Republic and schematic outlines of their morphology. A small arrow indicates the position of the dam and outflow of each reservoir. Map modified after Seda et al. [57].

Figure 2

Spatio-temporal population structure of Caullerya mesnili parasites. Principal component loadings on the PCA-axes are based on the frequency of parasite TCS-types; the first two axes account for 84% of the variation in the data. Parasite DNA was obtained from Daphnia hosts originating from seven lakes; some of the populations were sampled over a period of two to five years, resulting in 16 samples altogether (genotyped after pooling of 20 infected host, per sample; see Table 1). If the same lake was sampled 3–4 times, the samples are connected by a line. Three additional subsamples, for which 10 infected individuals (per population) were genotyped individually (Table 1), are shown in grey.

Figure 3

Distribution of representative ITS-sequence variants (TCS-types) in Caullerya mesnili . Parasite DNA was isolated from Daphnia hosts belonging to three different species (10 infected Daphnia per lake were genotyped individually; Table 1), and sampled across three different lakes. Species identity of Daphnia hosts was derived from the allelic variation at 15 microsatellite loci (see Additional file 1: Figure S1). Distribution of TCS-types varied among lakes but not among host species: n: number of host individuals per lake and species; **P <0.01, ***P <0.001 (Fisher’s exact tests).