Comprehensive phylogeny of acariform mites (Acariformes) provides insights on the origin of the four-legged mites (Eriophyoidea)

Authors: KLIMOV, PAVEL - UNIVERSITY OF MICHIGAN; OCONNOR, BARRY - UNIVERSITY OF MICHIGAN; CHETVERIKOV, P. - ACADEMY OF SCIENCE OF RUSSIA; BOLTON, S. - THE OHIO STATE UNIVERSITY; AMIR, R. PEPATO - UNIVERSIDADE FEDERAL DE MINAS GERAIS; ABDOLAZIM, L. MORTAZAVI - UNIVERSITY OF MICHIGAN; ANDREY, V. TOLSTIKOV - RUSSIAN STATE DEPARTMENT; Bauchan, Gary; Ochoa, Ronald - Ron

Submitted to: Molecular Phylogenetics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/22/2017
Publication Date: 5/25/2018
Citation: Klimov, P., Oconnor, B.M., Chetverikov, P.E., Bolton, S.J., Amir, R., Abdolazim, L., Andrey, V., Bauchan, G.R., Ochoa, R. 2018. Comprehensive phylogeny of acariform mites (Acariformes) provides insights on the origin of the four-legged mites (Eriophyoidea). Molecular Phylogenetics and Evolution. 119:105-117.

Interpretive Summary: Eriophyoid, or four-legged mites, represent a large and ancient radiation of exclusively phytophagous organisms. Hypothesizing phylogenetic relatedness of Eriophyoidea among mites is a major challenge due to the absence of unambiguous morphological synapomorphies resulting in ten disparate 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, vermiform family Nematalycidae (Endeostigmata). This arrangement was supported by the rDNA and CO1 partitions. In contrast, the nuclear protein partition (3 genes) suggests that Eriophyoidea is sister to a lineage including Tydeidae, Ereynetidae, and Eupodidae (Eupodina: Trombidiformes). On both topologies eriophyoids appear as a long branch, probably due to the loss of basal diversity in early evolution rather than elevated substitution rates. 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 phylogenetically important traits, was likely derived from the plesiomorphic acariform chelicerae rather than from the modified chelicerae of some trombidiform linages with a reduced fixed digit; and (ii) two potential synapomorphies of Eriophyoidea+ Raphignathina (Trombidiformes) related to the reduction of genital papillae and terminal position of PS segment can be dismissed as result from convergent evolution. Our analyses substantially reduce the space of available hypotheses on eriophyoid relationships and provide insights on the early evolution of acariform mites.

Technical Abstract: Eriophyoid, or four-legged mites, represent a large and ancient radiation of exclusively phytophagous organisms. Hypothesizing phylogenetic relatedness of Eriophyoidea among mites is a major challenge due to the absence of unambiguous morphological synapomorphies resulting in ten disparate 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, vermiform family Nematalycidae (Endeostigmata). This arrangement was supported by the rDNA and CO1 partitions. In contrast, the nuclear protein partition (3 genes) suggests that Eriophyoidea is sister to a lineage including Tydeidae, Ereynetidae, and Eupodidae (Eupodina: Trombidiformes). On both topologies eriophyoids appear as a long branch, probably due to the loss of basal diversity in early evolution rather than elevated substitution rates. 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 phylogenetically important traits, was likely derived from the plesiomorphic acariform chelicerae rather than from the modified chelicerae of some trombidiform linages with a reduced fixed digit; and (ii) two potential synapomorphies of Eriophyoidea+ Raphignathina (Trombidiformes) related to the reduction of genital papillae and terminal position of PS segment can be dismissed as result from convergent evolution. Our analyses substantially reduce the space of available hypotheses on eriophyoid relationships and provide insights on the early evolution of acariform mites.