Eriophyoid, or four-legged mites, represent a large and ancient radiation of exclusively phytophagous organisms known from the Triassic (230 Mya). Hypothesizing phylogenetic relatedness of Eriophyoidea among mites is a major challenge due to the absence of unambiguous morphological synapomorphies, resulting in ten published hypotheses placing eriophyoids in various places in the acariform tree of life. Here we test the evolutionary relationships of eriophyoids using six genes and a representative taxonomic sampling of acariform mites. The total evidence analysis places eriophyoids as the sister group of the deep soil-dwelling, vermiform family Nematalycidae (Endeostigmata). This arrangement was supported by the rDNA and CO1 partitions. In contrast, the nuclear protein partition (genes EF1-α, SRP54, HSP70) suggests that Eriophyoidea is sister to a lineage including Tydeidae, Ereynetidae, and Eupodidae (Eupodina: Trombidiformes). On both of these alternative topologies, eriophyoids appear as a long branch, probably involving the loss of basal diversity in early evolution. We analyze this result by using phylogenetically explicit hypothesis testing, investigating the phylogenetic signal from individual genes and rDNA stem and loop regions, and removing long branches and rogue taxa. Regardless of the two alternative placements, (i) the cheliceral morphology of eriophyoids, one of the traits deemed phylogenetically important, was likely derived directly from the plesiomorphic acariform chelicerae rather than from the modified chelicerae of some trombidiform lineages with a reduced fixed digit; and (ii) two potential synapomorphies of Eriophyoidea+Raphignathina (Trombidiformes) related to the reduction of genital papillae and to the terminal position of PS segment can be dismissed as result of convergent evolution. Our analyses substantially narrow the remaining available hypotheses on eriophyoid relationships and provide insights on the early evolution of acariform mites.
BackgroundAtypical tRNAs are functional minimal tRNAs, lacking either the D- or T-arm. They are significantly shorter than typical cloverleaf tRNAs. Widespread occurrence of atypical tRNAs was first demonstrated for secernentean nematodes and later in various arachnids. Evidence started to accumulate that tRNAs of certain acariform mites are even shorter than the minimal tRNAs of nematodes, raising the possibility that tRNAs lacking both D- and T-arms might exist in these organisms. The presence of cloverleaf tRNAs in acariform mites, particularly in the house dust mite genus Dermatophagoides, is still disputed.ResultsMitochondrial tRNAs of Dermatophagoides farinae are minimal, atypical tRNAs lacking either the T- or D-arm. The size (49-62, 54.4 ± 2.86 nt) is significantly (p = 0.019) smaller than in Caenorhabditis elegans (53-63, 56.3 ± 2.30 nt), a model minimal tRNA taxon. The shortest tRNA (49 nt) in Dermatophagoides is approaching the length of the shortest known tRNAs (45-49 nt) described in other acariform mites. The D-arm is absent in these tRNAs, and the inferred T-stem is small (2-3 bp) and thermodynamically unstable, suggesting that it may not exist in reality. The discriminator nucleotide is probably not encoded and is added postranscriptionally in many Dermatophagoides tRNAs.ConclusionsMitochondrial tRNAs of acariform mites are largely atypical, non-cloverleaf tRNAs. Among them, the shortest known tRNAs with no D-arm and a short and unstable T-arm can be inferred. While our study confirmed seven tRNAs in Dermatophagoides by limited EST data, further experimental evidence is needed to demonstrate extremely small and unusual tRNAs in acariform mites.
Long-term specialization may limit the ability of a species to respond to new environmental conditions and lead to a higher likelihood of extinction. For permanent parasites and other symbionts, the most intriguing question is whether these organisms can return to a free-living lifestyle and, thus, escape an evolutionary "dead end." This question is directly related to Dollo's law, which stipulates that a complex trait (such as being free living vs. parasitic) cannot re-evolve again in the same form. Here, we present conclusive evidence that house dust mites, a group of medically important free-living organisms, evolved from permanent parasites of warm-blooded vertebrates. A robust, multigene topology (315 taxa, 8942 nt), ancestral character state reconstruction, and a test for irreversible evolution (Dollo's law) demonstrate that house dust mites have abandoned a parasitic lifestyle, secondarily becoming free living, and then speciated in several habitats. Hence, as exemplified by this model system, highly specialized permanent parasites may drastically de-specialize to the extent of becoming free living and, thus escape from dead-end evolution. Our phylogenetic and historical ecological framework explains the limited cross-reactivity between allergens from the house dust mites and "storage" mites and the ability of the dust mites to inhibit host immune responses. It also provides insights into how ancestral features related to parasitism (frequent ancestral shifts to unrelated hosts, tolerance to lower humidity, and pre-existing enzymes targeting skin and keratinous materials) played a major role in reversal to the free-living state. We propose that parasitic ancestors of pyroglyphids shifted to nests of vertebrates. Later the nest-inhabiting pyroglyphids expanded into human dwellings to become a major source of allergens.
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