Population Genomics of Transposable Elements in Drosophila Maite

Studies of the population dynamics of transposable elements (TEs) in Drosophila melanogaster indicate that consistent forces are affecting TEs independently of their modes of transposition and regulation. New sequencing technologies enable biologists to sample genomes at an unprecedented scale in order to quantify genome-wide polymorphism for annotated and novel TE insertions. In this review, we first present new insights gleaned from high-throughput data for population genomics studies of D. melanogaster. We then consider the latest population genomics models for TE evolution and present examples of functional evidence revealed by genome-wide studies of TE population dynamics in D. melanogaster. Although most of the TE insertions are deleterious or neutral, some TE insertions increase the fitness of the individual that carries them and play a role in the genome adaptation. 561 Review in Advance first posted online on October 1, 2014. (Changes may still occur before final publication online and in print.) Changes may still occur before final publication online and in print A nn u. R ev . G en et . 2 01 4. 48 . D ow nl oa de d fr om w w w . a nn ua lr ev ie w s. or g by S ta nf or d U ni ve rs ity M ai n C am pu s L an e M ed ic al L ib ra ry o n 10 /1 1/ 14 . F or p er so na l u se o nl y. GE48CH24-Petrov ARI 23 September 2014 14:37 Nonautonomous TE elements: elements that do not encode the machinery to transpose but can still be mobile using the machinery of the autonomous TE copies Autonomous TE elements: elements that encode the machinery to transpose Ectopic recombination: exchange of DNA sequences, between two similar sequences located at nonhomologous regions of the genome leading to a chromosomal rearrangement Polytene chromosomes: giant chromosomes that display a characteristic band-interband morphology; present in several tissue, they are commonly found in the salivary glands of flies; formed as the result of several rounds of DNA replication without cell division TRANSPOSABLE ELEMENTS ARE AN ABUNDANT, DIVERSE, AND ACTIVE COMPONENT OF GENOMES Transposable elements (TEs) are mobile DNA sequences that encode an ability to copy themselves to other sites in the genome and increase their copy number in the process. Certain TEs, known as nonautonomous, rely on the enzymatic machinery of autonomous copies to move around the genome. Owing to mobility and self-replication ability, TEs can be abundant, diverse, and active components of genomes. TEs are present in virtually all eukaryotic organisms studied to date and in 80% of the sequenced prokaryotes (112). In all of these organisms, TEs represent a sizable portion of the genome that can vary from ∼1% (e.g., in the filamentous fungus Fusarium graminearum) to ∼85% in Zea mays and Zea luxurians (32, 111). TEs are diverse components of genomes. They are classified into two different classes on the basis of whether their transposition mechanism is DNA-based or RNA-based; into different orders on the basis of structural relationships; and into families on the basis of sequence similarities (62, 116). Within each TE family, order, and class, the age and the number of copies can also drastically vary. TEs are also active components of genomes that generate mutations both when they transpose from one genomic location to another and when they induce structural rearrangements, most commonly via ectopic recombination between TE copies. TE-induced mutations vary greatly in size, ranging from small-scale nucleotide changes, e.g., when a few nucleotides are left behind after a TE excises, to large chromosomal rearrangements. TE-induced mutations are also diverse in terms of their molecular effect: TEs can inactivate or duplicate genes, add or remove regulatory regions, induce new patterns of alternative splicing, and cause epigenetic changes, affecting the expression and/or structure of nearby genes (2). TE abundance, diversity, and activity are highly variable from one species to another. For example, mammalian genomes tend to harbor a small number of high copy-number families comprising few currently active TEs and thus primarily old TEs, whereas organisms such as plants and insects tend to harbor a much larger number of smaller copy-number families composed of very young TEs (114). TE content also varies among individuals from the same species: Whereas the total copy number might be similar between different individuals, the location of particular TE insertions can vary substantially. Understanding the dynamics of TEs in populations, i.e., which factors explain the number of TEs that belong to a particular TE family, order, or class, the diversity of TEs present in a given genome, and the frequency distribution of individual TE insertions is crucial if we want to understand the complex organization, function, and evolution of genomes. DROSOPHILA MELANOGASTER AS A MODEL ORGANISM TO STUDY TRANSPOSABLE ELEMENT DYNAMICS Drosophila melanogaster has been used as a model organism for the study of TE population dynamics for more than 25 years. The possibility of physically mapping, by in situ hybridization into polytene chromosomes, the location of individual TE copies in the genome provided the first insights into TE dynamics in populations (24, 90). The small genome size of D. melanogaster and its relatively small TE content (approximately 20% of the genome), made it an obvious choice for obtaining the first genome sequence of a complex animal (1). D. melanogaster is still to date one of the best sequenced, assembled and annotated eukaryotic genomes (87). Additionally, the wealth of functional information available for D. melanogaster and the multiple genetic manipulation techniques that are available make this organism ideal for the study of the evolutionary forces