The Evolution Of Eriophyoidea Based On Mitochondrial Genomes

Eriophyoid mites(Acari:Eriophyoidea)represent more than 4,400 species and are distributed worldwide.Eriophyoid mites have distinct morphological characters as having four legs,reduced setae and vermiform or fusiform body shape.They are totally phytophagous,with highly host-specificity.Nearly 80%eriophyoid species were reported from only one host plant.Besides treated as pest in forestry and agriculture,some species are potential bio-control agents of weeds.The study of eriophyoid mites has been carried out for more than a century,mainly focused on morphological descriptions of new species.According to their unique morphological features,the eriophyoid mites belong to the superorder Acari,treated as an independent superfamily.Although in the current classification systems,Eriophyoidea is assign to the Arachnida,Acari,Acariformes,Trombidiformes,but lack more convincing phylogenetic evidences.The mitochondrion of the metazoan is very important in cell oxidative phosphorylation,which contains 37 genes.Usually,the pattern of gene arrangement in mitochondrion is conserved,like which in most of the ticks,but which is not the case in mites.Highly rearranged mt genes were consistently found in all the sequenced mites.Typically,the secondary structure of mitochondrial(mt)tRNA is clover leaf structure.While,in the superorder Acariformes,the sequenced mitochondrial genomes of 27 species were all highly rearranged,and the secondary structure of tRNA has more or less truncation.The characteristics of the mitochondrial genome are generally considered to be suitable for high-level phylogenetic analyses;moreover gene rearrangements and atypical tRNA secondary structures are also considered suitable in the phylogenetic analyses.We annotated the mitochondrial genomes of 5 eriophyoid mites,including 2 families(Eriophyidae and Diptilomiopidae),those five species are Phyllocoptes taishanensis,Epitrimerus sabinae,Neocalepitrimerus rosa,Leipothrix sp.and Rhinotergum shaoguanense.Results show that all 5 species have gene rearranged comparing with the ancestral order of the arthropods,but the degree of rearrangement was the lowest in the Acariformes.All five species have truncated tRNA,and are the highest degree in the Acariformes.Based on the available mt genome data of Acariformes,we inferred the ancestral mt gene arrangement of Acariformes,which retained the ancestral pattern of mt gene arrangement of arthropods with slight modifications.Phylogenetic trees were constructed using mitochondrial genome sequences of 110 species(including 4 eriophyoid species)and the nuclear small subunit(18S)rRNA gene sequences of 231 species(including 25 eriophyoid species).Results support the previous opinion that Eriophyoidea was monophyletic,while monophyly of Trombidiformes was rejected.The topologies were slightly differences when using different analysis methods:one is eriophyoid mites grouped with the sarcoptiform mites,and the other is eriophyoid mites and sarcoptiform mites + non-eriophyoid are sister groups.However,our results indicate that the Eriophyoidea may not belong to the Trombidiformes.Eriophyoidea is extremely special in morphology,and very different from other Acari.Moreover,the divergence time of eriophyoid mites with other mites and ticks is not yet well discussed.The fossils of eriophyoid mites were dated in Triassic,overthrow the conclusion that Eriophyoidea is a recent derivative lineage.It is speculated that the Eriophyoidea may be occurred with the gymnosperms,with the proliferation of plants spread to the world.Our results show that eriophyoid mites diverged from other mites in the Devonian(about 384Mya).The origin of gall mites can be traced back to the Permian(about 262 Mya),mostly prior to the radiation of gymnosperms(Triassic-Jurassic)and angiosperms(early Cretaceous),also much earlier than previous studies.In conclusion,the placement of Eriophyoidea in the order Trombidiformes under the current classification system should be reviewed,based on the analyses of mitochondrial genomes and unclear 18S genes.Further,more data(morphological,ecological,and other nuclear genes)should be included to shed light on the phylogenetic position of eriophyoid mites in the Acariformes.Our results provide the foundation in the phylogenetic and evolutionary study of Acari.