High Rate of Recent Transposable Element–Induced Adaptation in Drosophila melanogaster

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.

Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila

“…The frequency spectrum of TE insertions is a useful metric to understand the evolutionary forces underlying the insertions Montgomery and Langley 1983; Capy et al Petrov et al 2003;Neafsey et al 2004;Gonzalez et al 2008Gonzalez et al , 2009). The relatively greater advantage of piRT over targetRT insertions is also manifested by the difference in the frequency spectra of new insertions.…”

“…We excluded 344 TEs because their boundary sites cannot be unambiguously mapped on the reference genome, and thus the strategy we used cannot accurately determine the frequencies of the insertions in the nine strains (Methods). TE insertions are generally rare in the populations of D. melanogaster; however, some of them can be fixed or even conserved across divergent Drosophila species (Petrov et al 2003;Caspi and Pachter 2006;Begun et al 2007;Gonzalez et al 2008). To exclude the possibility that the frequency spectrum is biased by genealogy, in this analysis we further exclude 835 TE insertions that putatively have conserved boundary sequences in Drosophila simulans (Methods).…”

“…TEs can mediate evolution of genome structures through their tendency to nucleate chromosomal rearrangements (Hoogland and Biemont 1996;Petrov et al 2003;Biemont and Vieira 2006), their contribution to the creation of new genes (Britten 2006;Kaessmann et al 2009), and their de novo generation of new regulatory motifs for neighboring genes (Lowe et al 2007). TE insertions can be adaptive through their influence on gene expression levels (Daborn et al 2002;Brookfield 2004;Schlenke and Begun 2004;Aminetzach et al 2005;Gonzalez et al 2008), and recently it was demonstrated that such adaptive TE insertion events have occurred often in the genome of Drosophila melanogaster (Gonzalez et al 2008).…”

“…It was also found that the piRNAs are evolutionarily dynamic in rodents (Assis and Kondrashov 2009) as well as in Drosophila ). In Drosophila, transposition/retrotransposition and excision of TEs occur frequently, and TE insertions are highly polymorphic among individuals (Montgomery and Langley 1983;Charlesworth and Langley 1989;Nuzhdin 1999;Petrov et al 2003;Gonzalez et al 2008). Since the majority of piRNAs were generated from TE loci, one would expect that piRNAs would similarly experience rapid population dynamics.…”

Transposable elements in natural populations ofDrosophila melanogaster

“…The most recent builds on the clear picture from the reference sequence and simply asks which if any of the TEs identified in the sequenced laboratory strain can be found in genomes sampled from natural populations. González et al (2008) used polymerase chain reaction to survey the presence versus absence in six pools of eight to 12 independent strains each. Three hundred and forty-four of the 902 euchromatic TE insertions in the reference genome were not observed in the pools, while 76 per cent of the 902 were observed to be present in low frequency in at least one or more of six surveyed populations.…”