Abstract

BackgroundExperimental evolution studies, coupled with whole genome resequencing and advances in bioinformatics, have become a powerful tool for exploring how populations respond to selection at the genome-wide level, complementary to genome-wide association studies (GWASs) and linkage mapping experiments as strategies to connect genotype and phenotype. In this experiment, we analyzed genomes of Drosophila melanogaster from lines evolving under long-term directional selection for increased desiccation resistance in comparison with control (no-selection) lines.ResultsWe demonstrate that adaptive responses to desiccation stress have exerted extensive footprints on the genomes, manifested through a high degree of fixation of alleles in surrounding neighborhoods of eroded heterozygosity. These patterns were highly convergent across replicates, consistent with signatures of ‘soft’ selective sweeps, where multiple alleles present as standing genetic variation become beneficial and sweep through the replicate populations at the same time. Albeit much less frequent, we also observed line-unique sweep regions with zero or near-zero heterozygosity, consistent with classic, or ‘hard’, sweeps, where novel rather than pre-existing adaptive mutations may have been driven to fixation. Genes responsible for cuticle and protein deubiquitination seemed to be central to these selective sweeps. High divergence within coding sequences between selected and control lines was also reflected by significant results of the McDonald-Kreitman and Ka/Ks tests, showing that as many as 347 genes may have been under positive selection.ConclusionsDesiccation stress, a common challenge to many organisms inhabiting dry environments, proves to be a very potent selecting factor having a big impact on genome diversity.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2556-y) contains supplementary material, which is available to authorized users.

Highlights

  • Experimental evolution studies, coupled with whole genome resequencing and advances in bioinformatics, have become a powerful tool for exploring how populations respond to selection at the genome-wide level, complementary to genome-wide association studies (GWASs) and linkage mapping experiments as strategies to connect genotype and phenotype

  • We found a total of 1,217,242 polymorphic sites, 213,819 of which were fixed in all control lines and 603,702 were fixed in all desiccation lines

  • We notice that genomic signatures of adaptive responses to directional selection for increased desiccation resistance are highly convergent among selected lines, a pattern consistent with soft selective sweeps operating on standing genetic variation, similar to that found by others [26, 28, 54, 55]

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Summary

Introduction

Experimental evolution studies, coupled with whole genome resequencing and advances in bioinformatics, have become a powerful tool for exploring how populations respond to selection at the genome-wide level, complementary to genome-wide association studies (GWASs) and linkage mapping experiments as strategies to connect genotype and phenotype. In this experiment, we analyzed genomes of Drosophila melanogaster from lines evolving under long-term directional selection for increased desiccation resistance in comparison with control (no-selection) lines. Soft sweep footprints are less pronounced and more difficult to discern from surrounding neutral polymorphism, since lineages coalesce into two or more alleles, and adaptive loci may remain moderately diverse in the population [16, 17]

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