Genomes and transposable elements in the Drosophila nasuta species group

Transposable element (TE) mobilization is a constant threat to genome
integrity. Eukaryotic organisms have evolved robust defensive mechanisms
to suppress their activity, yet TEs can escape suppression and
proliferate, creating strong selective pressure for host defense to adapt.
This genomic conflict fuels a never-ending arms race that drives the rapid
evolution of TEs and recurrent positive selection of genes involved in
host defense; the latter has been shown to contribute to postzygotic
hybrid incompatibility. However, how TE proliferation impacts genome and
regulatory divergence remains poorly understood. Here, we report the
highly complete and contiguous (N50=33.8Mb - 38.0Mb) genome assemblies of
seven closely-related Drosophila species that belong to
the nasuta species group - a poorly studied group of
flies that radiated in the last 2 million years. We constructed a high
quality de novo TE library and gathered germline RNA-seq data, which
allowed us to comprehensively annotate and compare insertion patterns
between the species, and infer the evolutionary forces controlling their
spread. We find a strong negative association between TE insertion
frequency and expression of genes nearby; this likely reflects
survivor-bias from reduced fitness impact of TE inserting near lowly
expressed, non-essential genes, with limited TE-induced epigenetic
silencing. Phylogenetic analyses of insertions of 147 TE families reveal
that 53% of them show recent amplification in at least one species. The
most highly amplified TE is an non-autonomous DNA element DINE which has
gone through multiple bouts of expansions with thousands of full length
copies littered throughout each genome. Across all TEs, we find that TEs
expansions are significantly associated with high expression in the
expanded species consistent with suppression escape. Altogether, our
results shed light on the heterogenous and context-dependent nature in
which TEs affect gene regulation and the dynamics of rampant TE
proliferation amidst a recently radiated species group.