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 ∼1-2% of all allergic diseases globally; however, their evolutionary origin and diverse lifestyles including reversible parasitism have not been illustrated at the genomic level, which hampers allergy prevention and our exploration of these household pests. Using six high-quality assembled and annotated genomes, this study not only refuted the monophyly of mites and ticks, but also thoroughly explored the divergence of Acariformes and the diversification of astigmatic mites. In monophyletic Acariformes, Prostigmata known as notorious plant pests first evolved, and 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. Gene diversification after tandem duplications provides many genetic resources for adaptation to sensing environmental signals, digestion, and detoxification in rapidly changing household environments. 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 UDP glucuronosyltransferases and several important fungal cell wall lytic enzymes, which enable detoxification and digestive functions and provide perfect drug targets for pest control. This comparative study sheds light on the divergent evolution and quick adaptation to human household environments of astigmatic mites and provides insights into the genetic adaptations and even control of human household pests.

Keywords: astigmatic mites; comparative genomics; horizontal gene transfer; household pest adaptations; tandem gene duplication.

Fig. 1.

Morphology of six astigmatic mites and phylogenetic tree of Acari (mites and ticks). (A) Taxonomy and diverse morphology of six astigmatic mites (manually painted). High-quality genomes of the six astigmatic mites with diverse morphologies were presented and summarized in table 1. Taxonomy assignment used the NCBI taxonomy version. S. scabiei is the var. canis. All the six mites are classified as human household pests in this study. (B) Phylogenetic tree of mites and ticks (subclass: Acari). Two major groups Acariformes and Parasitiformes in the subclass Acari were interrupted by the pseudoscorpion Cordylochernes scorpioides. The phylogenetic tree was constructed based on the alignment of 13,133 conserved amino-acid residues in 47 overlapped single and complete BUSCO protein sequences of 28 genomes by RAxML in a ML algorithm and 100 bootstrap replicates. The MSRs of the five lineages of mites and ticks are marked. *** P < 0.001.

Fig. 2.

Phylogenomic analysis revealed a wide range of genetic changes. (A) Analysis of gene gain or loss in the evolution of mites. The numbers in brackets on nodes indicate the number of orthogroups under expansion (+ and green) or contraction (- and red) and rapidly evolving orthogroups (* and blue). The ultrametric time tree was adapted from supplementary figure S4, Supplementary Material online, and the proteome of D. melanogaster (UniProt ID: UP000000803) was used as an outgroup. (B) Venn diagram of orthogroups of the six astigmatic mites. Proteomes were assigned into orthogroups using OrthoFinder2, and the overlapped orthogroups of the six astigmatic mites were then presented using a Venn diagram.

Fig. 3.

Frequent tandem gene duplications of iGluRs. (A) Phylogenetic analysis of all iGluRs in the six astigmatic mites. All tandemly arrayed genes are connected using curved solid lines, whereas all proximally arrayed genes (separated by not more than 10 genes) are connected using dotted lines. Two large Clusters X and Y were highlighted, in which Cluster Y was further classified into Subclusters 1 and 2 (including the subcluster 2-1). Two small Clusters, a and b, were identified as IR25a and IR93a, respectively. (B) Phylogenetic analysis and similarity matrix of two adjacent iGluRs, IR25a and IR93a, of the six astigmatic mites. IR25a and IR93a of D. melanogaster were used as references. Tandem arrayed IR25a and IR93a were linked by solid curves in all six mites. The similarity matrix (BLOSUM62) was generated using the online tool SIAS with default parameters. (C) Gene synteny alignment of iGluRs in subcluster 2-1. Tandem gene duplications are highlighted; for example, such as five tandemly arrayed iGluRs in D. farinae are marked as iGluR (x5). The black turn arrow indicates reverse complement, and the red dotted lines indicate the genes of S. scabiei located on the opposite strand.

Fig. 4.

Remarkable tandem gene duplications in digestion and detoxification gene families. (A) Phylogenetic analysis and tandem gene duplications of triacylglycerol lipases in the six mites. Tandemly and proximally arrayed genes of glutamate receptors in six mites were connected using curved solid lines and dotted lines, respectively. A specific cluster with tandem gene duplications was marked as PTL1. (B) Phylogenetic analysis and tandem gene duplications of serine proteases. All serine proteases of the six astigmatic mites were identified and analyzed in a phylogenetic tree. Three species-specific clusters (T1, T2, and CT1) of serine proteases are highlighted. (C) Alignment of catalytic triads of serine proteases in three species-specific clusters. Three species-specific clusters of serine proteases in (figure 4B) were collected and aligned for their catalytic triads (H, histidine; D, aspartic acid; S, serine). Active, mutated, and missing sites are marked with colored triangles. (D) Phylogenetic analysis and tandem gene duplications of UGTs. UGTs of the six astigmatic mites were analyzed in a phylogenetic tree and divided into three large clusters, UGT1–3.

Fig. 5.

Phylogenetic analysis of HGT genes, UGTs and chitinases. (A) Phylogenetic analysis of UGTs from the six astigmatic mites. The closest UGTs from other taxonomic groups in the UniRef50 database, including those from bacteria, fungi, plants, other arthropods (excluding Acariformes) and other metazoa (excluding arthropods), were collected for the analysis with the UGTs of Acariformes. The rotifer sequences were collected from the NR database. (B) Phylogenetic analysis of chitinases in Cluster 1 (supplementary fig. S11A, Supplementary Material online) from the six astigmatic mites. The closest chitinases in the UniRef50 database from other taxonomic groups were collected for comparison of the chitinases of astigmatic and oribatid mites. All protein sequence accessions are listed in (supplementary tables S34 and S35, Supplementary Material online).

Fig. 6.

Graphical illustration of the evolutionary history of astigmatic mites. In the monophyletic Acariformes, Prostigmata (known as notorious plant pests) first branched out, and then Astigmata evolved from Oribatida (known as soil mites). HGT-gained genes are shown in blue font, with UGT and fungal cell wall lytic enzymes bolded. In the phylogenetic tree of astigmatic mites, colored tables show the variation events of 12 gene families in three categories (corresponding to the table in the upper left corner). Red box, gene loss; green box, gene gain; star symbol *, tandem gene duplication; blank box, no change identified.