Mite Genome Miniaturization: Assembly of the biological control agent Floracarus perrepae reveals dynamic genome evolution in eriophyoid mites

Abstract

The eriophyoid mites (Acari: Eriophyoidea) represent an extreme case of genome streamlining, with genomes averaging just 32Mb, among the smallest of all animals. This clade of mites is highly diverse with more than 4000 species. Their morphologies are specialized for feeding on their host plants, including a simplified worm-like body plan with just two pairs of legs and modified mouth parts that can induce the formation of galls or plant deformities during feeding. Their generally strong host affinities make eriophyoid mites appealing for use as biological control agents, although their short generation times and small genomes could facilitate rapid evolution and impact their efficacy in management programs. Here, we sequenced the genome of the biological control mite Floracarus perrepae, producing a highly contiguous genome totalling just 23.1 Mb, among the smallest of all animals. We also assembled another non-eriophyid mite genome from accidental DNA bycatch (69.4Mb). We placed this new genomic resource in a phylogenetic context to reveal that mites have highly dynamic genome evolution, with a significant trend in genome downsizing in the eriophyoids. Our results suggest that this streamlining is associated with non-genic elements such as the suppression or excision of retrotransposons and purging of introns. As new sequencing techniques become available, novel genomic resources for tiny organisms such as F. perrepae will be more readily accessible, facilitating both fundamental genome evolutionary biology and applied sciences such as biological control programs which use eriophyoid mites for the management of invasive species. SIGNIFICANCE Eriophyid mites (Acari: Eriophyoidea) are a diverse group of miniscule mites averaging less than 0.2mm in length. The 4000 species in this clade are globally distributed and are commonly employed in biological control management of invasive species. Recent genome sequencing projects have revealed that these mites have some of the smallest genomes among animals. Here, we report on the genome assembly of the biological control eriophyoid mite Floracarus perrepae, which has one of the smallest genomes of any arthropod. Using this new resource, we investigate why these mites have such small genomes, focusing primarily on the loss of non-genic content such as repetitive elements and gene structure evolution. These small genomes, coupled with short generation times typical of eriophyoids, have important implications for rapid evolutionary changes, which are particularly relevant for biological control management programs.