The lack of recombination drives the fixation of transposable elements on the fourth chromosome of Drosophila melanogaster

Abstract

In regions of suppressed recombination, where selection is expected to be less efficient in removing slightly deleterious mutations, transposable element (TE) insertions should be more likely to drift to higher frequencies, and even to reach fixation. In the absence of excision events, once a TE is fixed it cannot be eliminated from the population, and accumulation of elements thus should become an irreversible process. In the long term, this can drive the degeneration of large non-recombining fractions of the genomes. Chromosome 4 of Drosophila melanogaster has very low levels of recombination, if any, and this could be causing its degeneration. Here we report the results of a PCR-based analysis of the population frequencies of TE insertions in a sample from three African natural populations. We investigated 27 insertions from 12 TE families, located in regions of either suppressed or free recombination. Our results suggest that TE insertions tend to be fixed in the non-recombining regions, particularly on the fourth chromosome. We have also found that this involves all types of elements, and that fixed insertions are significantly shorter and more divergent from the canonical sequence than those segregating in the sample (28.1% vs 86.3% of the canonical length, and average nucleotide divergence (D(XY)) = 0.082 vs 0.008, respectively). Finally, DNA-based elements seem to show a greater tendency to reach fixation than retrotransposons. Implications of these findings for the population dynamics of TEs, and the evolutionary forces that shape the patterns of genetic variation in regions of reduced recombination, are discussed.