TY - JOUR

T1 - Comprehensive phylogeny of acariform mites (Acariformes) provides insights on the origin of the four-legged mites (Eriophyoidea), a long branch

AU - Klimov, Pavel B.

AU - OConnor, Barry M.

AU - Chetverikov, Philipp E.

AU - Bolton, Samuel J.

AU - Pepato, Amir R.

AU - Mortazavi, Abdolazim L.

AU - Tolstikov, Andrey V.

AU - Bauchan, Gary R.

AU - Ochoa, Ronald

N1 - Funding Information: We thank José Miguel Ortega (Federal University of Minas Gerais, Brazil) for allowing us to use the UFMG computer cluster Sagarana and for related technical advise, Evert E. Lindquist (Agriculture & Agri-Food Canada) for comments, Hans Klompen (Ohio State University) for several specimens of Parasitiformes and comments, Roy Norton (State University of New York, Syracuse, New York, USA), Sergey Ermilov (Tyumen’ State University, Russia), Alexandr Khaustov (Tyumen’ State University, Russia), Dong Liu (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences), and the late Katarzyna Jesionowska (University of Szczecin, Poland) for specimen identification. We would like to thank Heather Proctor (University of Alberta, Canada) for her thorough and thoughtful review of the manuscript. ARP and PBK were supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior ( CAPES ) Ciência sem Fronteiras (Brazil; PVE 88881.064989/2014-01 ). PBK was supported by the Russian Science Foundation (project No. 16-14-10109 to Dr. A.A. Khaustov), the Ministry of Education and Science of the Russian Federation (No 6.1933.2014/K project code 1933), the Russian Foundation for Basic Research (No 15-04-0s5185-a ). PEC was supported by the Russian Science Foundation ( RSCF Grant # 14-14-00621 ). Specimens sequenced in this study originated from 19 countries. We thank 31 individuals who helped us to organize fieldtrips or sent us specimens. The molecular work of this study was conducted in the Genomic Diversity Laboratory of the University of Michigan Museum of Zoology. Computationally intensive analyses were conducted on Sagarana HPC cluster, CPAD-ICB- UFMG , Federal University of Minas Gerais, Brazil. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA ; USDA is an equal opportunity provider and employer. Publisher Copyright: © 2017 Elsevier Inc. Copyright: Copyright 2017 Elsevier B.V., All rights reserved.

PY - 2018/2

Y1 - 2018/2

N2 - 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.

AB - 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.

KW - Acariformes

KW - Gall mites

KW - Long branch

KW - Massive basal extinction

KW - Phylogenetic position

UR - http://www.scopus.com/inward/record.url?scp=85034105146&partnerID=8YFLogxK

UR - http://www.mendeley.com/research/comprehensive-phylogeny-acariform-mites-acariformes-provides-insights-origin-fourlegged-mites-erioph

U2 - 10.1016/j.ympev.2017.10.017

DO - 10.1016/j.ympev.2017.10.017

M3 - Article

C2 - 29074461

AN - SCOPUS:85034105146

VL - 119

SP - 105

EP - 117

JO - Molecular Phylogenetics and Evolution

JF - Molecular Phylogenetics and Evolution

SN - 1055-7903

ER -