Abstract

Although transposable elements (TEs) are known to be potent sources of mutation, their contribution to the generation of recent adaptive changes has never been systematically assessed. In this work, we conduct a genome-wide screen for adaptive TE insertions in Drosophila melanogaster that have taken place during or after the spread of this species out of Africa. We determine population frequencies of 902 of the 1,572 TEs in Release 3 of the D. melanogaster genome and identify a set of 13 putatively adaptive TEs. These 13 TEs increased in population frequency sharply after the spread out of Africa. We argue that many of these TEs are in fact adaptive by demonstrating that the regions flanking five of these TEs display signatures of partial selective sweeps. Furthermore, we show that eight out of the 13 putatively adaptive elements show population frequency heterogeneity consistent with these elements playing a role in adaptation to temperate climates. We conclude that TEs have contributed considerably to recent adaptive evolution (one TE-induced adaptation every 200–1,250 y). The majority of these adaptive insertions are likely to be involved in regulatory changes. Our results also suggest that TE-induced adaptations arise more often from standing variants than from new mutations. Such a high rate of TE-induced adaptation is inconsistent with the number of fixed TEs in the D. melanogaster genome, and we discuss possible explanations for this discrepancy.

Highlights

  • The recent years have seen a burst in studies searching for signatures of genetic adaptation in a variety of organisms, including natural populations and domesticated plants and animals [1,2,3,4,5,6,7,8,9,10,11,12]

  • For most of the polymerase chain reaction (PCR), we obtained a single band of the expected size, indicating that the primers were amplifying the region of the genome where the transposable element (TE) was identified

  • Diverse genes located next to the putatively adaptive TEs provide a rich collection for a follow-up investigation of adaptive processes in D. melanogaster

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Summary

Introduction

The recent years have seen a burst in studies searching for signatures of genetic adaptation in a variety of organisms, including natural populations and domesticated plants and animals [1,2,3,4,5,6,7,8,9,10,11,12]. These studies suggest that adaptation is a pervasive force in evolution. TEs (1) play an important role in the structural evolution of genomes through the generation of various types of rearrangements [14,16], (2) donate regulatory sequences that control the expression of nearby genes [17,18,19,20], (3) become incorporated into coding sequences at the transcript level [21,22,23,24], and (4) have their genes recruited by the host genomes for key functions [25]

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