Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes

Abstract

Background: Horizontal transfer (HT) could play an important role in the long-term persistence of transposable elements (TEs) because it provides them with the possibility to avoid the checking effects of host-silencing mechanisms and natural selection, which would eventually drive their elimination from the genome. However, despite the increasing evidence for HT of TEs, its rate of occurrence among the TE pools of model eukaryotic organisms is still unknown.

Results: We have extracted and compared the nucleotide sequences of all potentially functional autonomous TEs present in the genomes of Drosophila melanogaster, D. simulans and D. yakuba - 1,436 insertions classified into 141 distinct families - and show that a large fraction of the families found in two or more species display levels of genetic divergence and within-species diversity that are significantly lower than expected by assuming copy-number equilibrium and vertical transmission, and consistent with a recent origin by HT. Long terminal repeat (LTR) retrotransposons form nearly 90% of the HT cases detected. HT footprints are also frequent among DNA transposons (40% of families compared) but rare among non-LTR retroelements (6%). Our results suggest a genomic rate of 0.04 HT events per family per million years between the three species studied, as well as significant variation between major classes of elements.

Conclusions: The genome-wide patterns of sequence diversity of the active autonomous TEs in the genomes of D. melanogaster, D. simulans and D. yakuba suggest that one-third of the TE families originated by recent HT between these species. This result emphasizes the important role of horizontal transmission in the natural history of Drosophila TEs.

Figure 1

Natural history of TEs and their hosts. On the left, if TEs are vertically transmitted (VT), their evolutionary history (red) follows that of their hosts (grey). At copy number equilibrium (3), TE abundance is constant along the generations, and speciation events of the hosts cause diversification of TE lineages. The possibility of stochastic loss (5) means that any TE family can be randomly lost over the generations in a given host. In the long term, this would cause the vertical extinction of all TEs from the genomes. On the right, HT of TEs (blue arrow) allows the possibility of recurrent invasions and long term persistence of TEs. TE arrival into a new host by horizontal transfer (HT) (1) is followed by a period of copy number increase (2) until transposition-selection equilibrium is reached (3). Upon speciation and the concomitant diversification of hosts and TEs (4), the stochastic loss of a family in a given lineage (5) can be reversed by HT. However, this should leave a genetic footprint. Neutral genetic differentiation is a direct function of time since divergence. If TEs and host nuclear genes are subject to similar evolutionary forces, the synonymous divergence of vertically transmitted extant orthologous TE families (K_STEs) is expected to be similar to that of the nuclear genes of the hosts (K_SNGs) as the same time has elapsed since their split (t₀-t₂; continuous line). But TEs that jumped between these species have had time to accumulate differences only since the HT event (t₀-t₁; dotted line), so that reduced levels of divergence relative to host genes are expected.

Figure 2

Euler-Venn diagram of the numbers of TE families found in the genomes of D. melanogaster, D. simulans and D. yakuba. Numbers of TE families found in each species are indicated. TEs found in more than one species are represented in the corresponding overlapping sections of the circles.

Figure 3

Distribution of the synonymous divergence (K_S) values for TEs and nuclear genes. (a) D. melanogaster versus D. simulans. (b) D. melanogaster versus D. yakuba. (c) D. simulans versus D. yakuba. Vertical dotted lines indicate the bootstrap estimate of the lower 2.5% quantile of the distributions of K_S for nuclear genes.

Figure 4

Estimates of the average pairwise synonymous divergence (K_S) between orthologous TE families. (a) D. melanogaster versus D. simulans. (b) D. melanogaster versus D. yakuba. (c) D. simulans versus D. yakuba. Error bars indicate bootstrap 95% confidence limits of the average. Horizontal lines indicate mean synonymous divergence between nuclear loci of the two species compared (dashed) and the bootstrap estimates of the 2.5% and 97.5% quantiles (solid). TEs are grouped into LTR, non-LTR RTs, and DNA transposons.

Figure 5

Mean Tajima's D values for the major TE groups across species (mel, D. melanogaster; sim, D. simulans; yak, D. yakuba). Error bars indicate 95% confidence intervals. Transp, transposon.