The adaptive role of transposable elements in the Drosophila genome

Abstract

Transposable elements (TEs) are short DNA sequences with the capacity to move between different sites in the genome. This ability provides them with the capacity to mutate the genome in many different ways, from subtle regulatory mutations to gross genomic rearrangements. The potential adaptive significance of TEs was recognized by those involved in their initial discovery although it was hotly debated afterwards. For more than two decades, TEs were considered to be intragenomic parasites leading to almost exclusively detrimental effects to the host genome. The sequencing of the Drosophila melanogaster genome provided an unprecedented opportunity to study TEs and led to the identification of the first TE-induced adaptations in this species. These studies were followed by a systematic genome-wide search for adaptive insertions that allowed for the first time to infer that TEs contribute substantially to adaptive evolution. This study also revealed that there are at least twice as many TE-induced adaptations that remain to be identified. To gain better understanding of the adaptive role of TEs in the genome we clearly need to (i) identify as many adaptive TEs as possible in a range of Drosophila species as well as (ii) carry out in-depth investigations of the effects of adaptive TEs on as many phenotypes as possible.Keywords transposable elements; adaptation; Drosophila; in situ; bottlenecks; selfish DNA What is a transposable element?Transposable Elements (TEs) are short DNA sequences, typically 1-10kb, capable of inserting copies of themselves into new genomic locations. TEs are an ancient, abundant and diverse component of eukaryotic genomes. They are present in virtually all eukaryotic species investigated so far where they represent from 3% to 80% of the total DNA (Hua- Van et al., 2005;Biemont and Vieira, 2006;Piegu et al., 2006). Most TEs can be assigned to one of two main classes defined according to their mode of transposition (Figure 1). Class I or retrotransposons use a "copy and paste" mechanism that involves an RNA intermediate. Retrotransposons are further subdivided into those that have long terminal repeats (LTRs) and those that do not (long and short interspersed nuclear elements (LINEs and SINEs)). Class II or DNA transposons utilize a "cut and paste" mechanism that involves a DNA intermediate. Inside these two classes, TEs are further classified into superfamilies according to featuresCorresponding author: Josefa González, Department of Biology, 371 Serra St., Stanford University, Stanford CA 94305-3020, e-mail: jgonzalp@stanford.edu, phone: 650-7362240. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and a...

Selfish genetic elements, genetic conflict, and evolutionary innovation

“…There is ample evidence of mutational costs of TE insertion events (21,32,33). There has been relatively little evidence that young insertions lead to adaptive mutations, although some possible cases have emerged recently (85). Examples include inserts associated with pesticide resistance in D. melanogaster and D. simulans as well as a genome-wide study implicating TE insertions with temperature adaptation in two separate latitudinal clines in D. melanogaster.…”

Transposons, Genome Size, and Evolutionary Insights in Animals

“…In this class the landscape is very variable: a clear correlation between genome size and methylation levels was not found, and species with a large genome and higher levels of genomic parasites, such as Culex , display a low level of methylation [Regev et al, 1998]. In Crassostrea it has been observed that only certain classes of repetitive elements represent methylation targets [Gonzalez and Petrov, 2009] and, unlike in vertebrates, methylation would not be the prevalent mechanism in silencing of genes located within the transposons, but it would act mainly at an intergenic level [Riviere, 2014].…”

Gene duplication in the major insecticide target site,Rdl, inDrosophila melanogaster

“…TEs and genome rearrangements have previously been implicated in adaptation to environmental pressures such as insecticide resistance (24,37,38). TEs contribute substantially to adaptive evolution and have the capacity to generate deletions, duplications, and regulatory changes with wide-ranging phenotypic effects that cannot be achieved by point mutations (39). Roo elements are the most common TE in the D. melanogaster genome (40), and are frequent initiators of chromosomal rearrangements such as duplications and deletions (41).…”