Hitchhiking Mapping Reveals a Candidate Genomic Region for Natural Selection in Three-Spined Stickleback Chromosome VIII

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ABSTRACT

Identification of genes and genomic regions under directional natural selection has become one of the major goals in evolutionary genetics, but relatively little work to this end has been done by applying hitchhiking mapping to wild populations. Hitchhiking mapping starts from a genome scan using a randomly spaced set of molecular markers followed by a fine-scale analysis in the flanking regions of the candidate regions under selection. We used the hitchhiking mapping approach to narrow down a selective sweep in the genomic region flanking a candidate locus (Stn90) in chromosome VIII in the three-spined stickleback (Gasterosteus aculeatus). Twenty-four microsatellite markers were screened in an ~800-kb region around the candidate locus in three marine and four freshwater populations. The patterns of genetic diversity and differentiation in the candidate region were compared to those of a putatively neutral set of markers. The Bayesian FST-test indicated an elevated genetic differentiation, deviating significantly from neutral expectations, at a continuous region of ~20 kb upstream from the candidate locus. Furthermore, a method developed for an array of microsatellite markers rejected neutrality in a region of ~90 kb flanking the candidate locus supporting the selective sweep hypothesis. Likewise, the genomewide pattern of genetic diversity differed from the candidate region in a bottleneck analysis suggesting that selection, rather than demography, explains the reduced genetic diversity at the candidate interval. The neutrality tests suggest that the selective sweep had occurred mainly in the Lake Pulmanki population, but the results from bottleneck analyses indicate that selection might have operated in other populations as well. These results suggest that the narrow interval around locus Stn90 has likely been under directional selection, but the region contains several predicted genes, each of which can be the actual targets of selection. Understanding of the functional significance of this genomic region in an ecological context will require a more detailed sequence analysis.

UNDERSTANDING the genetic basis of evolutionary change is of fundamental interest in evolutionary biology (Orr 2005a,b; Ungerer et al. 2007; Stinchcombe and Hoekstra 2007). However, the molecular basis of the specific mutations underlying evolutionary shifts in mean trait values has seldom been uncovered in any detail (but see Colosimo et al. 2005; Storz et al. 2007). In recent years, QTL-mapping studies have shed light on the genetic architecture of some ecologically important morphological traits (e.g., Colosimo et al. 2004, 2005; Shapiro et al. 2004). From the methodological point of view, a standard QTLmapping approach requires that the association between the phenotype and genotype can be established (Mackay 2001). However, many traits underlying adaptive divergence are not always easily detectable at the phenotypic level and not well-suited to QTL mapping (Schlötterer 2003). In such cases, one possible approach to tackle the genetic basis of adaptation is to use neutral genetic markers to identify targets of natural selection (Schlötterer 2002, 2003). Based on principles of population genetics, natural selection is expected to create a skew in allele frequencies of the genes under selection and also on the flanking neutral sites-commonly known as genetic hitchhiking (Maynard Smith and Haigh 1974; Schlötterer 2003). Theory further predicts that natural selection leaves predictable "footprints" in the degree of genetic differentiation and diversity of linked neutral markers, which are distinguishable from neutral processes (Nielsen 2005). Genomic regions under directional selection are expected to show decreased within population diversity and increased among population differentiation, whereas the effects of balancing selection are expected to be roughly opposite (e.g., Nielsen 2005; Charlesworth 2006).

The identification of targets of natural selection can be compromised by several factors. …