Spatiotemporal Tracking of Three Novel Transposable Element Invasions in Drosophila melanogaster over the Last 30 Years

Abstract

Transposable elements (TEs) are repetitive sequences capable of mobilizing within genomes, exerting a significant influence on evolution throughout the tree of life. Using a novel approach that does not require prior knowledge of the sequence of repeats, we identified three novel TE invasions in Drosophila melanogaster: McLE spread between 1990-2000, Souslik between 2009-2012, and Transib1 between 2013-2016. We recapitulate previous findings, revealing that a total of 11 TEs invaded D. melanogaster over the past two centuries. These 11 invasions increased the fly genome by ∼1 Mbp. Using data from over 1,400 arthropod genomes, we provide evidence that these TE invasions were triggered by horizontal transfers, with Drosophila simulans and species of the Drosophila willistoni group acting as putative donors. Through the analysis of ∼600 short-read datasets spanning diverse geographic regions, we reveal the rapidity of TE invasions: Transib1 swiftly multiplied from three isolated epicenters in 2014 to all investigated populations in just 2 years. Our findings suggest that anthropogenic activities, which facilitate the range and population expansions of D. melanogaster, could have accelerated the rate of horizontal transposon transfer as well as the spread of the TEs into the worldwide population. Given the significant impact of TEs on evolution and the potential involvement of humans in their dispersal, our research has crucial implications for both evolution and ecology.

Keywords: Drosophila; genome evolution; horizontal gene transfer; transposable elements; transposon invasions.

Fig. 1.

Overview of the HTs of TEs in D. melanogaster during the last two centuries from long-read assemblies. a) Illustration of our approach to find TE invasions. A novel TE invasion can be detected by gaps in the coverage, when reads of an old strain (e.g. Canton-S, sampled 1935) are aligned to the assembly of a recent strain (e.g. Tom008; sampled 2016; top panel). The gap in the example is due to Souslik. By contrast, no coverage gap is found if reads from the same strain are aligned (bottom panel). IGV was used for the visualization (Robinson et al. 2011). b) Overview of sequences with similarity to the 11 TEs in the long-read assemblies of Canton-S and Tom008. Horizontal bars represent the matching regions between the TE insertions and the consensus sequence. Colors represent divergence from the consensus sequence. Based on a divergence threshold of 1.5%, we refer to the fragments as canonical (≤1.5%) and degraded (>1.5%). Note that canonical insertions are present in the young but absent in the old strain. The first three TEs spread before 1935, which explains the presence of canonical insertions in both strains.

Fig. 2.

Complete invasion history of D. melanogaster during the last two centuries. We tracked the copy numbers of TEs (y-axis) and the frequency of SNPs diagnostic for canonical insertions (color) in D. melanogaster strains and pooled populations sampled over the last two centuries. A recent invasion is indicated by a sharp increase in two key metrics, i.e. the copy numbers of the TE and the frequency of canonical SNPs (which captures the ratio of canonical to degraded insertions for a given TE family).

Fig. 3.

Geographic spread of canonical Transib1 insertions in D. melanogaster samples (strains or pooled populations) collected from Europe and North America between 2013 and 2016. Colors indicate the frequency of SNPs diagnostic for the presence of the canonical Transib1 insertions.

Fig. 4.

The Souslik and Transib1 invasions were triggered by HT from D. simulans, whereas McLE was transferred from a species of the willistoni group. a) Similarity of the 11 TEs that recently invaded D. melanogaster with insertions in 266 high-quality assemblies of 242 Drosophila species. The barplots show, for each species, the similarity between the given TE and the best match in an assembly. The species were arranged by relatedness. Colors indicate species or species groups with full-length insertions (>80% of length). b) Bayesian tree of McLE, Souslik, and Transib1 insertions in species having at least one full-length insertion.