Divergent Macroparasite Infections in Parapatric Swiss Lake-Stream Pairs of Threespine Stickleback (Gasterosteus aculeatus).

Anssi Karvonen,David A Marques,Ole Seehausen,Kay Lucek

doi:10.1371/journal.pone.0130579

Abstract

Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most host-parasite interactions, but understanding of the evolutionary implications of such variation is limited. One possible outcome of infection heterogeneities is parasite-mediated divergent selection between host populations, ecotypes or species which may facilitate the process of ecological speciation. However, very few studies have described infections in population-pairs along the speciation continuum from low to moderate or high degree of genetic differentiation that would address the possibility of parasite-mediated divergent selection in the early stages of the speciation process. Here we provide an example of divergent parasitism in freshwater fish ecotypes by examining macroparasite infections in threespine stickleback (Gasterosteus aculeatus) of four Swiss lake systems each harbouring parapatric lake-stream ecotype pairs. We demonstrate significant differences in infections within and between the pairs that are driven particularly by the parasite taxa transmitted to fish from benthic invertebrates. The magnitude of the differences tended to correlate positively with the extent of neutral genetic differentiation between the parapatric lake and stream populations of stickleback, whereas no such correlation was found among allopatric populations from similar or contrasting habitats. This suggests that genetic differentiation is unrelated to the magnitude of parasite infection contrasts when gene flow is constrained by geographical barriers while in the absence of physical barriers, genetic differentiation and the magnitude of differences in infections tend to be positively correlated.

Highlights

Parasitism is an important selective factor in natural host populations, but the diversity and intensity of infections is often spatially heterogeneous
Examinations of parasitism in continuums of host genetic differentiation, i.e. speciation continuums [22, 23], are lacking such systems allow questions related to the role of parasites in the very early stages of a speciation process [24, 25]
By examining parasite infections in replicated pairs of geologically very young parapatric lake and stream threespine stickleback ecotypes in Switzerland, we explored the relationship between the magnitude of recent or current gene flow and distance in parasite infections in comparison to allopatric population pairs between different drainage systems

Summary

Introduction

Parasitism is an important selective factor in natural host populations, but the diversity and intensity of infections is often spatially heterogeneous. Studies describing differentiated parasite infections among ecologically specialized individuals, well-defined ecotypes, morphs or closely related species of freshwater fishes have begun to accumulate [1, 11,12,13,14,15,16,17,18,19,20] This shows that some of the key conditions for parasite-mediated divergent selection are often met in natural populations. There have been very few comparative studies of parasitism at different stages in a speciation continuum [22, 23], i.e. in host populations harbouring morphs or ecotypes from no to low, moderate and high degree of genetic differentiation and reproductive isolation [24, 25] Such approaches are important to learn more about the possible role of parasites in speciation processes. Knowledge about the when and where of infection divergence in the speciation process is important for understanding the cause and effect relationship between parasite-driven divergent selection and the build-up of reproductive isolation

Methods

Results

Conclusion