Divergent selection on locally adapted major histocompatibility complex immune genes experimentally proven in the field

Christophe Eizaguirre,Martin Kalbe,Manfred Milinski,Tobias L Lenz,Gabriele Sorci

doi:10.1111/j.1461-0248.2012.01791.x

Abstract

Although crucial for the understanding of adaptive evolution, genetically resolved examples of local adaptation are rare. To maximize survival and reproduction in their local environment, hosts should resist their local parasites and pathogens. The major histocompatibility complex (MHC) with its key function in parasite resistance represents an ideal candidate to investigate parasite-mediated local adaptation. Using replicated field mesocosms, stocked with second-generation lab-bred three-spined stickleback hybrids of a lake and a river population, we show local adaptation of MHC genotypes to population-specific parasites, independently of the genetic background. Increased allele divergence of lake MHC genotypes allows lake fish to fight the broad range of lake parasites, whereas more specific river genotypes confer selective advantages against the less diverse river parasites. Hybrids with local MHC genotype gained more body weight and thus higher fitness than those with foreign MHC in either habitat, suggesting the evolutionary significance of locally adapted MHC genotypes.

Highlights

The origin and extent of local adaptation among individuals in natural populations are a key aspect of adaptive evolution (Coyne & Orr 2004; Hoekstra et al 2006)
We found that fish with river major histocompatibility complex (MHC) genotypes harbour MHC genotypes with lower MHC divergence than fish carrying LL or pure lake MHC genotypes (All pairwise wilcoxon tests between lake and river P < 0.001, Fig. 4)
Identifying a genetic basis for local adaptation is of prime interest in evolutionary biology (Hoekstra et al 2006; Barrett et al 2008)

Summary

Introduction

The origin and extent of local adaptation among individuals in natural populations are a key aspect of adaptive evolution (Coyne & Orr 2004; Hoekstra et al 2006). Gandon et al 1996; Nosil et al 2005; Bridle & Vines 2007; Greischar & Koskella 2007), the extent and the genetic basis for local adaptation in natural populations are still poorly understood (Hereford 2009). This is due to the difficulty of identifying the exact selection pressure, the underlying mechanisms and the genes involved. Contrasting environments are likely to support distinct parasite communities, which would in turn require contrasting local immunogenetic adaptation of the hosts (Gandon et al 1996; Hedrick 2002; Eizaguirre et al 2009)

Methods

Results

Conclusion