Comparative Genomics Reveals Insights into the Divergent Evolution of Astigmatic Mites and Household Pest Adaptations

Abstract Highly diversified astigmatic mites comprise many medically important human household pests such as house dust mites causing roughly 1–2% of the allergic diseases globally; however, their evolutionary origin, diverse lifestyles including reversible parasitism and quick adaptation to rather new human household environments have not been illustrated at genomic level, which hamper the allergy prevention and our exploration of these household pests. Using six high-quality assembled and annotated genomes, this comparative genomics study not only refuted the monophyly of mites and ticks, but also thoroughly explored the divergence of Acariformes and the divergent evolution of astigmatic mites. In the monophyletic Acariformes, Prostigmata known as notorious plant pests first evolved, then rapidly evolving Astigmata diverged from soil oribatid mites. Within astigmatic mites, a wide range of gene families rapidly expanded via tandem gene duplications, including ionotropic glutamate receptors, triacylglycerol lipases, serine proteases and UDP glucuronosyltransferases (UGTs), which enriched their capacities of adapting to rapidly changing household environments. The gene diversification after tandem duplications provided plenty of genetic resources for their adaptations of sensing environmental signals, digestion, and detoxification. Whilst many gene decay events only occurred in the skin-burrowing parasitic mite Sarcoptes scabiei. Throughout the evolution of Acariformes, massive horizontal gene transfer events occurred in gene families such as UGTs and several important fungal cell wall lytic enzymes, which enable the detoxification and associated digestive functions and provide perfect drug targets for pest control. Our comparative study sheds light on the rapid divergent evolution of astigmatic mites from the divergence of Acariformes to their diversification and provides novel insights into the genetic adaptations and even control of human household pests.