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. 2024 Mar 22;22(1):70.
doi: 10.1186/s12915-024-01870-9.

Phylogenomics resolves the higher-level phylogeny of herbivorous eriophyoid mites (Acariformes: Eriophyoidea)

Qi Zhang  1 , Yi-Wen Lu  1 , Xin-Yu Liu  1 , Ye Li  1 , Wei-Nan Gao  1 , Jing-Tao Sun  1 , Xiao-Yue Hong  1 , Renfu Shao  2 , Xiao-Feng Xue  3
Affiliations

Phylogenomics resolves the higher-level phylogeny of herbivorous eriophyoid mites (Acariformes: Eriophyoidea)

Qi Zhang et al. BMC Biol. .

Abstract

Background: Eriophyoid mites (Eriophyoidea) are among the largest groups in the Acariformes; they are strictly phytophagous. The higher-level phylogeny of eriophyoid mites, however, remains unresolved due to the limited number of available morphological characters-some of them are homoplastic. Nevertheless, the eriophyoid mites sequenced to date showed highly variable mitochondrial (mt) gene orders, which could potentially be useful for resolving the higher-level phylogenetic relationships.

Results: Here, we sequenced and compared the complete mt genomes of 153 eriophyoid mite species, which showed 54 patterns of rearranged mt gene orders relative to that of the hypothetical ancestor of arthropods. The shared derived mt gene clusters support the monophyly of eriophyoid mites (Eriophyoidea) as a whole and the monophylies of six clades within Eriophyoidea. These monophyletic groups and their relationships were largely supported in the phylogenetic trees inferred from mt genome sequences as well. Our molecular dating results showed that Eriophyoidea originated in the Triassic and diversified in the Cretaceous, coinciding with the diversification of angiosperms.

Conclusions: This study reveals multiple molecular synapomorphies (i.e. shared derived mt gene clusters) at different levels (i.e. family, subfamily or tribe level) from the complete mt genomes of 153 eriophyoid mite species. We demonstrated the use of derived mt gene clusters in unveiling the higher-level phylogeny of eriophyoid mites, and underlines the origin of these mites and their co-diversification with angiosperms.

Keywords: Divergence time; Eriophyoid mites; Gene order; Higher-level phylogeny; Mitochondrial genomes; Synteny.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Eriophyoid phylogram inferred by shared derived gene clusters from 153 complete mitochondrial genomes. Genes underlined have opposite transcription orientation to those not underlined. nad1–6 and nad4L for NADH dehydrogenase subunits 1–6 and 4L; rrnL and rrnS for large and small rRNA subunits; tRNA genes are indicated by the single-letter IUPAC-IUB abbreviations for their corresponding amino acids. Translocated or inverted genes are colour-coded (blue: inversion and translocation; green: translocation; orange: inversion)
Fig. 2
Fig. 2
Phylogenetic trees inferred from mitochondrial genome sequences using maximum likelihood and Bayesian methods. The tree topology is largely stable across all analyses; branch lengths presented here follow the Bayesian analysis using nucleotide sequence dataset partitioned by genes. Node numbers indicate Bayesian posterior probabilities (BPP). Maximum likelihood bootstrap proportion (BSP) and BPP values of major clades are shown with colour-coded squares. Green squares indicate clades support with BSP > 70% and BPP > 0.95; blue recovered with moderate or low support; white not recovered. The number of the corresponding mitochondrial genome arrangement pattern is marked after the name of each species (Patterns 1–54) in the Eriophyoidea. Red stars denote genome patterns that were assigned into clade ATA in Fig. 1
Fig. 3
Fig. 3
Dated phylogenetic tree of the Eriophyoidea inferred from mitochondrial nucleotide sequence dataset with MCMCTree in PAML. Blue bars at nodes represent 95% highest posterior density (HPD) interval. Numbers above branches represent Bayesian posterior probabilities. Node numbers correspond to the node ages are shown in Table 1. Calibration points are depicted by asterisks
Fig. 4
Fig. 4
The correlations between the rate of nucleotide substitutions (Ka) and breakpoints (Bp) in 111 arachnid species. Arachnid lineages were marked by different colours
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