Abstract
Experimental evolution in combination with whole-genome sequencing (evolve and resequence [E&R]) is a promising approach to define the genotype–phenotype map and to understand adaptation in evolving populations. Many previous studies have identified a large number of putative selected sites (i.e., candidate loci), but it remains unclear to what extent these loci are genuine targets of selection or experimental noise. To address this question, we exposed the same founder population to two different selection regimes—a hot environment and a cold environment—and quantified the genomic response in each. We detected large numbers of putative selected loci in both environments, albeit with little overlap between the two sets of candidates, indicating that most resulted from habitat-specific selection. By quantifying changes across multiple independent biological replicates, we demonstrate that most of the candidate SNPs were false positives that were linked to selected sites over distances much larger than the typical linkage disequilibrium range of Drosophila melanogaster. We show that many of these mid- to long-range associations were attributable to large segregating inversions and confirm by computer simulations that such patterns could be readily replicated when strong selection acts on rare haplotypes. In light of our findings, we outline recommendations to improve the performance of future Drosophila E&R studies which include using species with negligible inversion loads, such as D. mauritiana and D. simulans, instead of D. melanogaster.
Highlights
Turner et al 2011)—provides a flexible and powerful approach to elucidate population genomic responses to Understanding the process of adaptation at the genomic level adaptation.remains one of the fundamental questions for 21st centuryMany recent E&R studies have utilized Drosophila melanobiology (Stapley et al 2010)
Despite using a conservative significance threshold and being robust to false positives caused by drift in low recombining regions, the detection of such a large number of candidate SNPs suggests that our estimates for both treatments were probably inflated by a large number of false positives
To reconcile the anomaly of thousands of putative selected SNPs being detected despite an apparent lack of linkage disequilibrium (LD) in our study, we propose that associations beyond 200 bp—which is widely regarded the limit of LD in D. melanogaster (Mackay et al 2012)—may be prevalent within our experimental populations
Summary
Turner et al 2011)—provides a flexible and powerful approach to elucidate population genomic responses to Understanding the process of adaptation at the genomic level adaptation.remains one of the fundamental questions for 21st centuryMany recent E&R studies have utilized Drosophila melanobiology (Stapley et al 2010). In addition to being a model organthe prospect of identifying the majority of causal loci under- ism for genetic research, D. melanogaster has the advanlying adaptation is foreseeable. To realize this objective, a tage of having a well-annotated reference genome and a large series of recent studies have leveraged the power of NGS in collection of mutant and RNAi lines. A common feature of published in experimental populations under environmental and demo- D. melanogaster E&R studies is that a very large number of graphic parameters of the experimenters’ choice (Kawecki SNPs (at least hundreds) are identified as targets of selection et al 2012).
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