Dynamics and Impacts of Transposable Element Proliferation in the Drosophila nasuta Species Group Radiation

Abstract

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 TE 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 TEs 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 a 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. Thus, while horizontal transfer followed by invasion of a naïve genome has been highlighted to explain the long-term survival of TEs, our analysis suggests that evasion of host suppression of resident TEs is a major strategy to persist over evolutionary times. 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.

A quantitative, genome-wide analysis inDrosophilareveals transposable elements’ influence on gene expression is species-specific

“…However, we find an increase in H3K9me3 enrichment associated with high TE insertion numbers, but only in D. simulans and for TE insertions within introns and upstream genes (0 departure t test; within introns: mean difference = 0.003, pvalue = 0.0005; upstream: mean difference = 0.003, p-value = 0.0019). These results are congruent with recent studies, which observed a clear association between TE insertions and heterochromatin but no predominant negative impact on the expression of neighboring genes (Huang et al, 2022;Wei et al, 2022).…”

“…For instance, in their pool-seq analysis of D. melanogaster and D. simulans, Kofler et al found that half of the TE families showed evidence of variation of activity through time and were not the same depending on the species (Kofler et al, 2015b). It is congruent with the conclusions of Wei et al, working on the Drosophila nasuta complex of species, who emphasize that TE insertions can have multiple effects on gene expression, from no effect to silencing or over-expression (Wei et al, 2022). This also echoes the work of Malone et al and Sienski et al, who described different groups of TEs depending on their sensitivity to different piRNA pathways and thus different effects on neighboring genes Sienski et al, 2012).…”

“…Control of TEs generally consists in the targeting of particular chromatin marks to TE copies, which induce transcriptional and post-transcriptional gene silencing and may spread to neighboring sequences and impact gene expression. In this regard, few attempts were made to finely analyze and quantify TEs' influence at the whole genome scale (Cridland et al, 2015;Hollister and Gaut, 2009;Huang et al, 2016;Lee and Karpen, 2017;Uzunović et al, 2019;Wei et al, 2022). In addition, since the very beginning of TE studies, species-specific differences in TE contents, activities and control pathways have been reported in nature, and particularly between D. melanogaster and D. simulans (Akkouche et al, 2013(Akkouche et al, , 2012Fablet et al, 2014;Kofler et al, 2015b;Lee and Karpen, 2017;Mérel et al, 2020;Vieira et al, 2012Vieira et al, , 1999.…”

Transposable element and host silencing activity in gigantic genomes

“…Transposable element expression is higher in R. sibiricus testes than ovaries, a pattern also reported in Drosophila (Wei et al, 2022) and Oryzias latipes (the medaka fish) (Saint-Leandre et al, 2020;Dechaud et al, 2021), but opposite the pattern reported in Corvus corone (carrion crow) (Warmuth et al, 2022) and different from the non-sex-biased TE expression in the fire-bellied newt Cynops orientalis (Carducci et al, 2021). In Drosophila, testes expression levels of TE-mapping piRNAs and piRNA pathway genes, as well as the pingpong signature, are lower than ovary expression levels, suggesting that lower male piRNAmediated silencing contributes to higher male TE expression (Saint-Leandre et al, 2020;Chen et al, 2021).…”

“…Transposable elements and the silencing machinery of their hosts are engaged in an arms race in which a novel TE family initially proliferates, the host evolves silencing based on TE sequence identification, and the TE subsequently diverges to evade silencing ¾ or that particular TE remains permanently silenced, but a novel TE invades the host genome and begins the cycle anew (Luo et al, 2020;Zhang et al, 2020;Said et al, 2022;Wei et al, 2022). If balanced by deletion of TE sequences, this arms-race dynamic can be associated with fairly stable genome size over evolutionary timescales, despite turnover in TE content (Kapusta et al, 2017).…”