Transposable elements contribute to the evolution of host shift–related genes in cactophilic Drosophila species

Abstract

Host shifts in insects are considered a key process with the potential to contribute to reproductive isolation and speciation. Both genomic and transcriptomic variation are attributed to such a process, in which gene families with functions associated with host localization, acceptance, and usage are proposed to evolve. In this context, cactophilic Drosophila species serve as an excellent model to study host shift evolution, because they use a wide range of cacti as hosts, and many species display different preferences. Transposable elements are a source of genetic novelty between populations and species, driving rapid adaptive evolution. However, the extent of TEs’ contribution to host shift remains unexplored. Here, we perform genomic and transcriptomic analyses in six genomes of cactophilic species/subspecies to investigate how TEs interact with genes associated with host shift. Our results reveal enrichment of TEs at promoter regions of host shift-related genes, with ∼39% of the odorant receptors containing their transcription factor binding sites within TEs. We observe that ∼50% of these TEs are Helitrons, demonstrating an unprecedented putative cis-regulatory role of Helitrons in Drosophila. Differential expression analysis between species with different preferred hosts reveals divergence in gene expression in heads and larvae. Although TEs’ presence does not affect overall gene expression, we observe 6.27% of the expressed genes generating gene–TE chimeric transcripts, including those with function affecting host preference. Our combined genomic and transcriptomic approaches provide evidence of TE-driven divergence between species, highlighting the evolutionary role of TEs in the context of host shift, a key adaptive process that can cause reproductive isolation.