Transposable elements in natural populations ofDrosophila melanogaster

Abstract

Transposable elements (TEs) are families of small DNA sequences found in the genomes of virtually all organisms. The sequences typically encode essential components for the replicative transposition sequences of that TE family. Thus, TEs are simply genomic parasites that inflict detrimental mutations on the fitness of their hosts. Several models have been proposed for the containment of TE copy number in outbreeding host populations such as Drosophila. Surveys of the TEs in genomes from natural populations of Drosophila have played a central role in the investigation of TE dynamics. The early surveys indicated that a typical TE insertion is rare in a population, which has been interpreted as evidence that each TE is selected against. The proposed mechanisms of this natural selection are reviewed here. Subsequent and more targeted surveys identify heterogeneity among types of TEs and also highlight the large role of homologous and possibly ectopic crossing over in the dynamics of the Drosophila TEs. The recent discovery of germline-specific RNA interference via the piwi-interacting RNA pathway opens yet another interesting mechanism that may be critical in containing the copy number of TEs in natural populations of Drosophila. The expected flood of Drosophila population genomics is expected to rapidly advance understanding of the dynamics of TEs.

Long-Term and Short-Term Evolutionary Impacts of Transposable Elements onDrosophila

“…Even though incidences of potentially adaptive individual TE insertions with high population frequencies have been reported (Daborn et al 2002;Aminetzach et al 2005;González et al 2008;Schmidt et al 2010), the mutagenic effects of TE insertions are typically deleterious because they disrupt gene structure and function (Finnegan 1992) and can lead to deleterious chromosomal rearrangement (Montgomery et al 1987(Montgomery et al , 1991Langley et al 1988). Supporting this, TEs in natural populations of Drosophila are generally found in intergenic regions (Aquadro et al 1986;Kaminker et al 2002;Bergman et al 2006) and present at low population frequencies (reviewed in Charlesworth and Langley 1989;Le Rouzic and Deceliere 2005;Lee and Langley 2010). Drosophila melanogaster strains with a larger copy number of several TE families surveyed also have lower fitness (Mackay 1989;Pasyukova et al 2004).…”

“…We assumed that there is complete linkage equilibrium among the invading TEs, and the TEs and the host resistance locus. The low frequency of virtually all TE insertions in natural populations of D. melanogaster (Aquadro et al 1986;Montgomery et al 1987;Charlesworth and Langley 1989;Lee and Langley 2010) coupled with the small scale of linkage disequilibrium between SNPs with more intermediate frequency in D. melanogaster (Miyashita and Langley 1988;Long et al 1998;Langley et al 2000Langley et al , 2012 ensures that the magnitude of linkage disequilibrium among elements is small and our assumption is reasonable. The assumption of no linkage disequilibrium and low TE frequencies motivates the further modeling of distribution of TE copy number as Poisson.…”

The population genetics of mutations: good, bad and indifferent

“…As reviewed in this themed issue by Lee & Langley (2010), there are various types of these elements that can move around in the genome and can copy, insert or excise themselves, sometimes in response to conditions such as stress. Mechanisms exist to control the frequency of transposition events to limit the damage from resulting deleterious mutations.…”

“…The extent to which deleterious, (near)-neutral or advantageous mutations shape DNA diversity (Stephan 2010), codon bias (Sharp et al 2010) and repetitive element distribution (Lee & Langley 2010) is fundamental to our understanding of genomic structure, and to develop this beyond models of individual loci often requires understanding how much mutations interact epistatically (Crow 2010;Lee & Langley 2010;Mackay 2010).…”

A naturalists guide to mobile genetic elements

“…As a consequence, population genetic models of TE evolution have usually considered how transposition and excision rate, selection, and drift may interact to determine whether the stable copy number of TEs in a population will be relatively high or low (Ågren and Wright 2015). Several recent reviews discuss the success and refinements of these models in light of the rapid influx of whole genome data from model and non-model organisms alike (Lee and Langley 2010;González and Petrov 2012;Barrón et al 2014). However, an almost equally striking observation, but one that has received less attention, is that the type of TEs that has become most abundant also differ dramatically between species.…”