Abstract
Whole-genome resequencing of experimental populations evolving under a specific selection regime has become a popular approach to determine genotype–phenotype maps and understand adaptation to new environments. Despite its conceptual appeal and success in identifying some causative genes, it has become apparent that many studies suffer from an excess of candidate loci. Several explanations have been proposed for this phenomenon, but it is clear that information about the linkage structure during such experiments is needed. Until now only Pool-Seq (whole-genome sequencing of pools of individuals) data were available, which do not provide sufficient information about the correlation between linked sites. We address this problem in two complementary analyses of three replicate Drosophila melanogaster populations evolving to a new hot temperature environment for almost 70 generations. In the first analysis, we sequenced 58 haploid genomes from the founder population and evolved flies at generation 67. We show that during the experiment linkage disequilibrium (LD) increased almost uniformly over much greater distances than typically seen in Drosophila. In the second analysis, Pool-Seq time series data of the three replicates were combined with haplotype information from the founder population to follow blocks of initial haplotypes over time. We identified 17 selected haplotype-blocks that started at low frequencies in the base population and increased in frequency during the experiment. The size of these haplotype-blocks ranged from 0.082 to 4.01 Mb. Moreover, between 42% and 46% of the top candidate single nucleotide polymorphisms from the comparison of founder and evolved populations fell into the genomic region covered by the haplotype-blocks. We conclude that LD in such rising haplotype-blocks results in long range hitchhiking over multiple kilobase-sized regions. LD in such haplotype-blocks is therefore a major factor contributing to an excess of candidate loci. Although modifications of the experimental design may help to reduce the hitchhiking effect and allow for more precise mapping of causative variants, we also note that such haplotype-blocks might be well suited to study the dynamics of selected genomic regions during experimental evolution studies.
Highlights
Evolve and resequence studies (E&R; Turner et al 2011; Schlo€tterer et al 2014), the combination of experimental evolution and whole-genome sequencing of pooled individuals (Pool-Seq), hold great promise in identifying targets of selection on a genome-wide scale
We investigate to what extent changes in linkage disequilibrium (LD) are related to several factors, such as chromosome, distance, initial LD, recombination rate, and inversions
Implications from Haplotype Analysis for Design and Analysis of E&R Studies Here, we demonstrated that in experimental evolution studies haplotype-blocks ranging from several kilobases up to few megabases could strongly increase in frequency within a few generations
Summary
Evolve and resequence studies (E&R; Turner et al 2011; Schlo€tterer et al 2014), the combination of experimental evolution and whole-genome sequencing of pooled individuals (Pool-Seq), hold great promise in identifying targets of selection on a genome-wide scale. E&R studies have been applied to address two major aims: 1) Determination the genotype–phenotype map often carried out by explicit truncating selection on a trait of interest (e.g., Burke et al 2010; Turner et al 2011) or 2) understanding the processes of adaption through laboratory natural selection operating on fitness in a new environment with no explicit link to a specific trait (e.g., Orozco-terWengel et al 2012).
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