Transposable elements in natural populations of Drosophila 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.

Figure 1.

The two modes of replicative transposition of TEs in eukaryotes. The left panel shows the mechanism of retrotransposition in which the TE genome is transcribed into RNA (dashed) and then reverse transcribed into DNA and integrated at a new location by proteins (grey fill), some of which are coded in the TE genome. On the right is a sketch of the mechanism typically used by the second class of TEs in which the double-stranded TE genome is excised from one of the two sister chromatids by the TE-encoded transposase protein (grey fill) that also catalyses the integration elsewhere in the genome of the host's germline. The double-strand break left by the excision is repaired off by the sister chromatid yielding a net increase in copy number. The grey-filled rectangular blocks are the replicated copies of the TEs. The rounded, grey-filled structures depict typical roles of TE proteins in reverse transcription, integration and excision.

Figure 2.

Cytological detection of TEs on Drosophila giant salivary gland chromosomes and their frequency spectrum in a sample from a natural population. (a) The photomicrograph shows portions of the X and 3R chromosomes in an inbred line from a natural population. The intensely dark bands are sites labelled by histochemically detectable in situ hybridization of biotinylated sequences of the roo TE family. (b) The graph is of the frequency spectra of three TE families among 20 independently sampled X chromosomes from a natural population of D. melanogaster (redrawn from Montgomery & Langley 1983). Black bar, 297; grey bar, 412; striped bar, copia.

Figure 3.

Three forms of interaction among deleterious mutations. In the additive model (unbroken line), the fitness decline due to deleterious mutations is the sum of the effects, e.g. (1 − ns). Under the synergistic epistasis model (stippled, concave curve), as the number of mutations increases, the deleterious interactions grow stronger, resulting in an ever faster decline in fitness, e.g. (1 − n²s). In the multiplicative model (dashed convex curve), the deleterious effects of mutations are weaker in individuals with greater numbers of other deleterious mutations, (1−s)ⁿ.

Figure 4.

Predicted frequency spectra of TE insertions. If the number of possible insertion sites in the genome, T, is much larger than TE copy number (n ≪ T) and α < 1, the frequency spectrum is dominated by β (see text and equations (2.4)–(2.6) for definitions). Note that at equilibrium . These three figures depict the impact of β as population size, N_e, goes from 10⁴ (β = 0.4) to 10⁵ (β = 4) and then to 10⁶ (β = 40). The probability a TE insertion will occur at intermediate or high frequencies increases dramatically. Other assumed parameters are u = 10⁻⁵, T = 4 × 10⁴ and . (a) α = 0.0005, β = 0.4; (b) α = 0.005, β = 4 and (c) α = 0.05, β = 40.

Figure 5.

Ectopic exchange leading to a duplicated and deleted chromosome. TEs at different locations along homologous chromosomes can exchange during meiosis to yield daughter chromosomes in the gametes that are complementarily duplicated (grey regions) and deleted. Single ‘ectopic’ exchanges between nonhomologous chromosomes or in an antiparallel direction produce even greater aneuploidy in the gametes.

Figure 6.

The ping-pong model: piRNA generation process is coupled with RNA interference mediated by Piwi proteins (PIWI, AUB and AGO3) (redrawn from fig. 2 of Aravin et al. 2007). PIWI and AUB preferentially bind to antisense piRNAs. Guided by piRNAs, PIWI and AUB cleave TE transcripts having complementary sequences to the piRNA sequences, which lead to the inactivation of TE transcript as well as the generation of new sense piRNAs. AGO3 mainly binds sense piRNAs to target antisense TE transcripts, generate new antisense piRNA and complete the other half of the amplification cycle. The source of the primary piRNAs that initiate the amplification cycle may be maternally inherited (Blumenstiel & Hartl 2005; Brennecke et al. 2008; Malone et al. 2009). Recent studies suggest a modified picture, namely that PIWI is responsible for piRNA generation through another pathway in the somatic tissue of Drosophila ovaries, while AUB and AGO3 are involved in the above ping-pong model in germline tissues (Li et al. 2009; Malone et al. 2009).