MicroRNAs and Phylogenomics Resolve the Relationships of Tardigrada and Suggest That Velvet Worms Are the Sister Group of Arthropoda

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2011 Sep 8

PMID 21896763

Citations 84

Authors

Lahcen I Campbell

Omar Rota-Stabelli

Gregory D Edgecombe

Trevor Marchioro

Stuart J Longhorn

Maximilian J Telford

Herve Philippe

Lorena Rebecchi

Kevin J Peterson

Davide Pisani

Affiliations

Soon will be listed here.

Abstract

Morphological data traditionally group Tardigrada (water bears), Onychophora (velvet worms), and Arthropoda (e.g., spiders, insects, and their allies) into a monophyletic group of invertebrates with walking appendages known as the Panarthropoda. However, molecular data generally do not support the inclusion of tardigrades within the Panarthropoda, but instead place them closer to Nematoda (roundworms). Here we present results from the analyses of two independent genomic datasets, expressed sequence tags (ESTs) and microRNAs (miRNAs), which congruently resolve the phylogenetic relationships of Tardigrada. Our EST analyses, based on 49,023 amino acid sites from 255 proteins, significantly support a monophyletic Panarthropoda including Tardigrada and suggest a sister group relationship between Arthropoda and Onychophora. Using careful experimental manipulations--comparisons of model fit, signal dissection, and taxonomic pruning--we show that support for a Tardigrada + Nematoda group derives from the phylogenetic artifact of long-branch attraction. Our small RNA libraries fully support our EST results; no miRNAs were found to link Tardigrada and Nematoda, whereas all panarthropods were found to share one unique miRNA (miR-276). In addition, Onychophora and Arthropoda were found to share a second miRNA (miR-305). Our study confirms the monophyly of the legged ecdysozoans, shows that past support for a Tardigrada + Nematoda group was due to long-branch attraction, and suggests that the velvet worms are the sister group to the arthropods.

Citing Articles

Preservation and early evolution of scalidophoran ventral nerve cord.

Wang D, Vannier J, Martin-Duran J, Herranz M, Yu C Sci Adv. 2025; 11(2):eadr0896.

PMID: 39792685 PMC: 11721716. DOI: 10.1126/sciadv.adr0896.

CAT-Posterior Mean Site Frequencies Improves Phylogenetic Modeling Under Maximum Likelihood and Resolves Tardigrada as the Sister of Arthropoda Plus Onychophora.

Giacomelli M, Vecchi M, Guidetti R, Rebecchi L, Donoghue P, Lozano-Fernandez J Genome Biol Evol. 2024; 17(1).

PMID: 39715362 PMC: 11756273. DOI: 10.1093/gbe/evae273.

Expression of distal limb patterning genes in Hypsibius exemplaris indicate regionalization and suggest distal identity of tardigrade legs.

Mapalo M, Game M, Smith F, Ortega-Hernandez J Evodevo. 2024; 15(1):15.

PMID: 39538290 PMC: 11562647. DOI: 10.1186/s13227-024-00235-1.

Storage cell proliferation during somatic growth establishes that tardigrades are not eutelic organisms.

Quiroga-Artigas G, Moriel-Carretero M Biol Open. 2024; 13(2).

PMID: 38411464 PMC: 10924213. DOI: 10.1242/bio.060299.

Phylogenomics of weevils revisited: data curation and modelling compositional heterogeneity.

Li Y, Engel M, Tihelka E, Cai C Biol Lett. 2023; 19(9):20230307.

PMID: 37727076 PMC: 10509570. DOI: 10.1098/rsbl.2023.0307.

References

Dunn C, Hejnol A, Matus D, Pang K, Browne W, Smith S . Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 2008; 452(7188):745-9. DOI: 10.1038/nature06614. View

Pisani D, Benton M, Wilkinson M . Congruence of morphological and molecular phylogenies. Acta Biotheor. 2007; 55(3):269-81. DOI: 10.1007/s10441-007-9015-8. View

Giribet G, Ribera C . The position of arthropods in the animal kingdom: a search for a reliable outgroup for internal arthropod phylogeny. Mol Phylogenet Evol. 1998; 9(3):481-8. DOI: 10.1006/mpev.1998.0494. View

Mallatt J, Giribet G . Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phylogenet Evol. 2006; 40(3):772-94. DOI: 10.1016/j.ympev.2006.04.021. View

Bartel D . MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136(2):215-33. PMC: 3794896. DOI: 10.1016/j.cell.2009.01.002. View

Andrew D . A new view of insect-crustacean relationships II. Inferences from expressed sequence tags and comparisons with neural cladistics. Arthropod Struct Dev. 2011; 40(3):289-302. DOI: 10.1016/j.asd.2011.02.001. View

Lartillot N, Philippe H . Improvement of molecular phylogenetic inference and the phylogeny of Bilateria. Philos Trans R Soc Lond B Biol Sci. 2008; 363(1496):1463-72. PMC: 2615818. DOI: 10.1098/rstb.2007.2236. View

Lartillot N, Lepage T, Blanquart S . PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009; 25(17):2286-8. DOI: 10.1093/bioinformatics/btp368. View

Sperling E, Peterson K, Pisani D . Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol Biol Evol. 2009; 26(10):2261-74. DOI: 10.1093/molbev/msp148. View

10.

Heimberg A, Cowper-Sal-lari R, Semon M, Donoghue P, Peterson K . microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci U S A. 2010; 107(45):19379-83. PMC: 2984222. DOI: 10.1073/pnas.1010350107. View

11.

Zwickl D, Hillis D . Increased taxon sampling greatly reduces phylogenetic error. Syst Biol. 2002; 51(4):588-98. DOI: 10.1080/10635150290102339. View

12.

Rota-Stabelli O, Kayal E, Gleeson D, Daub J, Boore J, Telford M . Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biol Evol. 2010; 2:425-40. PMC: 2998192. DOI: 10.1093/gbe/evq030. View

13.

Schierwater B, Eitel M, Jakob W, Osigus H, Hadrys H, Dellaporta S . Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoon" hypothesis. PLoS Biol. 2009; 7(1):e20. PMC: 2631068. DOI: 10.1371/journal.pbio.1000020. View

14.

Mallatt J, Garey J, Shultz J . Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol Phylogenet Evol. 2004; 31(1):178-91. DOI: 10.1016/j.ympev.2003.07.013. View

15.

Aguinaldo A, Turbeville J, Linford L, Rivera M, Garey J, Raff R . Evidence for a clade of nematodes, arthropods and other moulting animals. Nature. 1997; 387(6632):489-93. DOI: 10.1038/387489a0. View

16.

Philippe H, Brinkmann H, Lavrov D, Littlewood D, Manuel M, Worheide G . Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 2011; 9(3):e1000602. PMC: 3057953. DOI: 10.1371/journal.pbio.1000602. View

17.

Sperling E, Robinson J, Pisani D, Peterson K . Where's the glass? Biomarkers, molecular clocks, and microRNAs suggest a 200-Myr missing Precambrian fossil record of siliceous sponge spicules. Geobiology. 2009; 8(1):24-36. DOI: 10.1111/j.1472-4669.2009.00225.x. View

18.

Regier J, Shultz J, Zwick A, Hussey A, Ball B, Wetzer R . Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature. 2010; 463(7284):1079-83. DOI: 10.1038/nature08742. View

19.

Zrzavy J, Mihulka S, Kepka P, Bezdek A, Tietz D . Phylogeny of the Metazoa Based on Morphological and 18S Ribosomal DNA Evidence. Cladistics. 2021; 14(3):249-285. DOI: 10.1111/j.1096-0031.1998.tb00338.x. View

20.

Edgecombe G . Arthropod phylogeny: an overview from the perspectives of morphology, molecular data and the fossil record. Arthropod Struct Dev. 2009; 39(2-3):74-87. DOI: 10.1016/j.asd.2009.10.002. View