Abstract

Understanding the extent of local adaptation in natural populations and the mechanisms that allow individuals to adapt to their native environment is a major avenue in molecular ecology research. Evidence for the frequent occurrence of diverging ecotypes in species that inhabit multiple ecological habitats is accumulating, but experimental approaches to understanding the biological pathways as well as the underlying genetic mechanisms are still rare. Parasites are invoked as one of the major selective forces driving evolution and are themselves dependent on the ecological conditions in a given habitat. Immunological adaptation to local parasite communities is therefore expected to be a key component of local adaptation in natural populations. Here, we use next-generation sequencing technology to compare the transcriptome-wide response of experimentally infected three-spined sticklebacks from a lake and a river population, which are known to evolve under selection by distinct parasite communities. By comparing overall gene expression levels as well as the activation of functional pathways in response to parasite exposure, we identified potential differences between the two stickleback populations at several levels. Our results suggest locally adapted patterns of gene regulation in response to parasite exposure, which may reflect different local optima in the trade-off between the benefits and the disadvantages of mounting an immune response because of quantitative differences of the local parasite communities.

Highlights

  • The need for individuals to survive and reproduce successfully in a given environment is the ultimate driver of evolution

  • Combining the depth and unbiasedness of next-generation sequencing technology with the interpretational strength of a hypothesis-driven experimental approach, we were able to detect potential differences in the transcriptome-wide response to parasite exposure between families of two stickleback ecotypes, suggesting a significant extent of local immunological adaptation to the distinct parasite-mediated selection regimes in their respective habitats

  • River sticklebacks appeared overall more susceptible to our experimental parasite exposure, which was most apparent for Diplostomum pseudospathaceum

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Summary

Introduction

The need for individuals to survive and reproduce successfully in a given environment is the ultimate driver of evolution. Nolte et al 2009; Goetz et al 2010; Jeukens et al 2010) between distinct populations or ecotypes Such exploratory studies often pave the way for subsequent candidate gene approaches that allow for a more detailed investigation of the underlying selection pressures and mechanisms of local adaptation (Bernatchez et al 2010). The latter approaches have been tremendously facilitated by the onset of next-generation sequencing technologies and have improved our understanding of the genetic basis of local adaptation and population differentiation on a broader scale (Tautz et al 2010). With these new technologies becoming more and more affordable, they offer an exciting and unprecedented opportunity for evolutionary ecology research of model and nonmodel species (Ellegren 2008; Ekblom & Galindo 2011)

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