Patterns of selection in the evolution of a transposable element

Abstract

Transposable elements are a major component of most eukaryotic genomes. Here, we present a new approach which allows us to study patterns of natural selection in the evolution of transposable elements over short time scales. The method uses the alignment of all elements with intact gag/pol genes of a transposable element family from a single genome. We predict that the ratio of nonsynonymous to synonymous variants in the alignment should decrease as a function of the frequency of the variants, because elements with nonsynonymous variants that reduce transposition will have fewer progeny. We apply our method to Sirevirus long-terminal repeat retrotransposons that are abundant in maize and other plant species and show that nonsynonymous to synonymous variants declines as variant frequency increases, indicating that negative selection is acting strongly on the Sirevirus genome. The asymptotic value of nonsynonymous to synonymous variants suggests that at least 85% of all nonsynonymous mutations in the transposable element reduce transposition. Crucially, these patterns in nonsynonymous to synonymous variants are only predicted to occur if the gene products from a particular transposable element insertion preferentially promote the transposition of the same insertion. Overall, by using large numbers of intact elements, this study sheds new light on the selective processes that act on transposable elements.

Keywords: adaptive evolution; maize; plants; purifying selection; transposable elements.

Fig. 1.

The value of vN/vS as a function of the frequency of the variants in the alignment for the 5 families of Sireviruses in maize. Ji and Opie are sampled to 130 sequences each, while Giepum, Hopie, and Jienv are the full datasets. P0.015625 refers to the frequency category 0 < x ≤ 2⁻⁶, P0.03125 to 2⁻⁶ < x ≤ 2⁻⁵…, and so on.

Fig. 2.

The distribution of relative ages across TE copies from each family. Histogram plots show the distribution of divergence (numbers of point mutations and indels per site) between the LTRs of each element. The green line represents the median within each family. Note that the x-axis is on a log10 scale.

Fig. 3.

a) The value of vN/vS as a function of the frequency of the variants in the alignment for the 5 genes in the Sirevirus element, with the families combined. b) The length variation of the 5 maize families for each gene.

Fig. 4.

The value of vN/vS as a function of the frequency of the variants in the alignment for Sirevirus families in various plant species.