Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5284 No. 2: 11 May 2023
Type: Article
Published: 2023-05-11
DOI: 10.11646/zootaxa.5284.2.7
Page range: 351-363
Abstract views: 453
PDF downloaded: 191

Actinarctus doryphorus (Tanarctidae) DNA barcodes and phylogenetic reinvestigation of Arthrotardigrada with new A. doryphorus and Echiniscoididae sequences

Department of Biology; University of Copenhagen; Denmark
Department of Biology; University of Copenhagen; Denmark
Department of Biology; University of Copenhagen; Denmark
Tardigrada 18S rRNA 28S rRNA Bayesian inference COI Maximum Likelihood phylogenetics

Abstract

Little is still known about the diversity and evolution of marine arthrotardigrades, as they are generally difficult to sample, resulting in a limited amount of molecular data for barcoding and phylogenetic studies. With the current study, we provide the first investigation into COI haplotype diversity in a marine tanarctid and at the same time readdress arthrotardigrade phylogeny. Specifically, we provide COI mtDNA, 18S and 28S rDNA sequences from a population of Actinarctus doryphorus (Tanarctidae) sampled off the coast of Roscoff, France and further provide new 18S sequences from two marine echiniscoidids. A. doryphorus COI sequences confirmed the presence of a single species and further revealed five haplotypes shared among nine sequenced individuals. Our 18S and 28S rDNA datasets were individually and combined analysed with Bayesian inference and Maximum Likelihood. Actinarctus doryphorus was placed together with Tanarctus sequences within a maximally supported Tanarctidae, confirming previous interpretations that the clade is distinct from Halechiniscidae. Although several studies in recent decades have concluded that the marine arthrotardigrades are paraphyletic, recent studies have argued that the clade may not be paraphyletic. Our phylogenetic analyses consistently inferred Arthrotardigrada as paraphyletic, as the clade includes the monophyletic Echiniscoidea. Accordingly, we propose that it is time to suppress the order Arthrotardigrada as it clearly does not reflect tardigrade phylogeny.

 

References

  1. Bertolani, R., Guidetti, R., Marchioro, T., Altiero, T., Rebecchi, L. & Cesari, M. (2014) Phylogeny of Eutardigrada: new molecular data and their morphological support lead to the identification of new evolutionary lineages. Molecular Phylogenetics and Evolution, 76, 110–126. https://doi.org/10.1016/j.ympev.2014.03.006
  2. Blaxter, M.L., De Ley, P., Garey, J.R., Liu, L.X., Scheldeman, P., Vierstraete, A., Vanfleteren, J.R., Mackey, L.Y., Dorris, M., Frisse, L.M., Vida, J.T. & Thomas, W.K. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature, 392 (6671), 71–75. https://doi.org/10.1038/32160
  3. Cádiz, A., Nagata, N., Díaz, L.M., Suzuki-Ohno, Y., Echenique-Díaz, L.M., Akashi, H.D., Makino, T. & Kawata, M. (2018) Factors affecting interspecific differences in genetic divergence among populations of Anolis lizards in Cuba. Zoological Letters, 4 (1), 21. https://doi.org/10.1186/s40851-018-0107-x
  4. Capella-Gutiérrez, S., Silla-Martínez, J.M. & Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25 (15), 1972–1973. https://doi.org/10.1093/bioinformatics/btp348
  5. Chapman, P.A., Owen, H., Flint, M., Traub, R.J., Cribb, T.H. & Mills, P.C. (2016) Molecular characterization of coccidia associated with an epizootic in green sea turtles (Chelonia mydas) in South East Queensland, Australia. PLoS One, 11 (2), e0149962. https://doi.org/10.1371/journal.pone.0149962
  6. Chernomor, O., Von Haeseler, A. & Minh, B.Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology, 65 (6), 997–1008. https://doi.org/10.1093/sysbio/syw037
  7. Cuénot, L. (1892) Tardigrades. Commensaux et parasites des Echinodermes, I. Revue Biologique du Nord de la France, 5, 1–22.
  8. Degma, P. & Guidetti, R. (2009–2023) Actual checklist of Tardigrada species. 2009–2023, 42th Edition: 09-01-2023, 67 pp. Available from: https://iris.unimore.it/handle/11380/1178608 (accessed 14 February 2023) https://doi.org/10.25431/11380_1178608
  9. De la Torre-Bárcena, J.E., Kolokotronis, S-O., Lee, E.K., Stevenson, D.W., Brenner, E.D., Katari, M.S., Coruzzi, G.M. & DeSalle, R. (2009) The impact of outgroup choice and missing data on major seed plant phylogenetics using genome-wide EST data. PLoS One, 4 (6), e5764. https://doi.org/10.1371/journal.pone.0005764
  10. Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5 (1), 113. https://doi.org/10.1186/1471-2105-5-113
  11. Fleming, J.F. & Arakawa, K. (2021) Systematics of Tardigrada: a reanalysis of tardigrade taxonomy with specific reference to Guil et al. (2019). Zoologica Scripta, 50 (3), 376–382. https://doi.org/10.1111/zsc.12476
  12. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294–299.
  13. Fujimoto, S., Miyazaki, K. & Suzuki, A.C. (2013) A new marine tardigrade, Tanarctus diplocerus (Arthrotardigrada: Halechiniscidae) from Japan. Journal of the Marine Biological Association of the United Kingdom, 93 (4), 955–961. https://doi.org/10.1017/S0025315412000689
  14. Fujimoto, S. (2014) A new Stygarctus (Arthrotardigrada: Stygarctidae) from Japan, with entangled seminal receptacle ducts. Zootaxa, 3784 (2), 187–195. https://doi.org/10.11646/zootaxa.3784.2.8
  15. Fujimoto, S. (2015) Halechiniscidae (Heterotardigrada, Arthrotardigrada) of Oura Bay, Okinawajima, Ryukyu Islands, with descriptions of three new species. ZooKeys 483: 149–166. https://doi.org/10.3897/zookeys.483.8936
  16. Fujimoto, S, Jørgensen, A. & Hansen, J.G. (2017) A molecular approach to arthrotardigrade phylogeny (Heterotardigrada, Tardigrada). Zoologica Scripta, 46, 496–505. https://doi.org/10.1111/zsc.12221
  17. Fujimoto, S., Suzuki, A.C., Ito, M., Tamura, T. & Tsujimoto, M. (2020) Marine tardigrades from Lützow-Holm Bay, East Antarctica with the description of a new species. Polar Biology, 43, 679–693. https://doi.org/10.1007/s00300-020-02671-w
  18. Gąsiorek, P. & Michalczyk, Ł. (2020) Phylogeny of Itaquasconinae in the light of the evolution of the flexible pharyngeal tube in Tardigrada. Zoologica Scripta, 49 (4), 499–515. https://doi.org/10.1111/zsc.12424
  19. Gąsiorek, P. & Kristensen, R.M. (2022) New marine heterotardigrade lineages (Echiniscoididae) from the tropics. The European Zoological Journal, 89 (1), 719–754. https://doi.org/10.1080/24750263.2022.2079737
  20. Gross, V., Epple, L. & Mayer, G. (2021) Organization of the central nervous system and innervation of cephalic sensory structures in the water bear Echiniscus testudo (Tardigrada: Heterotardigrada) revisited. Journal of Morphology, 282 (9), 1298–1312. https://doi.org/10.1002/jmor.21386
  21. Giribet, G., Carranza, S., Baguna, J., Riutort. M. & Ribera, C. (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution, 13 (1), 76–84. https://doi.org/10.1093/oxfordjournals.molbev.a025573
  22. Giribet, G. & Edgecombe, G.D. (2017) Current understanding of Ecdysozoa and its internal phylogenetic relationships. Integrative and Comparative Biology, 57 (3), 455–466. https://doi.org/10.1093/icb/icx072
  23. Guil, N. & Giribet, G. (2009) Fine scale population structure in the Echiniscus blumi-canadensis series (Heterotardigrada, Tardigrada) in an Iberian mountain range—When morphology fails to explain genetic structure. Molecular Phylogenetics and Evolution, 51 (3), 606–13. https://doi.org/10.1016/j.ympev.2009.02.019
  24. Guil, N., Jørgensen, A., Giribet, G. & Kristensen, R.M. (2013) Congruence between molecular phylogeny and cuticular design in Echiniscoidea (Tardigrada, Heterotardigrada). Zoological Journal of the Linnean Society, 169 (4), 713–736. https://doi.org/10.1111/zoj.12090
  25. Guil, N., Jørgensen, A. & Kristensen, R. (2019) An upgraded comprehensive multilocus phylogeny of the Tardigrada tree of life. Zoologica Scripta, 48 (1), 120–137. https://doi.org/10.1111/zsc.12321
  26. Hansen, J., Kristensen, R.M. & Jørgensen, A. (2012) The armoured marine tardigrades (Arthrotardigrada, Tardigrada). Vol. 2. The Royal Danish Academy of Sciences and Letters, Copenhagen, 91 pp.
  27. Huelsenbeck, J.P. & Rannala, B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology, 53 (9), 904–913. https://doi.org/10.1080/10635150490522629
  28. Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (8), 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
  29. Jørgensen, A., Møbjerg, N. & Kristensen, R.M. (2007) A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area. Journal of Limnology, 66, 77–83. https://doi.org/10.4081/jlimnol.2007.s1.77
  30. Jørgensen, A., Faurby, S., Hansen, J.G., Møbjerg, N. & Kristensen, R.M. (2010) Molecular phylogeny of Arthrotardigrada (Tardigrada). Molecular Phylogenetics and Evolution, 54 (3), 1006–1015. https://doi.org/10.1016/j.ympev.2009.10.006
  31. Jørgensen, A., Faurby, S., Persson, D.K., Halberg, A.K., Kristensen, R. & Møbjerg, N. (2013) Genetic diversity in the parthenogenetic reproducing tardigrade Echiniscus testudo (Heterotardigrada: Echiniscoidea). Journal of Limnology, 72 (s1), e17. https://doi.org/10.4081/jlimnol.2013.s1.e17
  32. Jørgensen, A., Boesgaard, T.M., Møbjerg, N. & Kristensen, R.M. (2014) The tardigrade fauna of Australian marine caves: With descriptions of nine new species of Arthrotardigrada. Zootaxa, 3802 (4), 401–443. https://doi.org/10.11646/zootaxa.3802.4.1
  33. Jørgensen, A., Kristensen, R.M. & Møbjerg, N. (2018) Phylogeny and integrative taxonomy of Tardigrada. In: Schill, R.O. (Ed.), Water Bears: The Biology of Tardigrades. Vol. 2. Springer, Cham, pp. 95–114. https://doi.org/10.1007/978-3-319-95702-9_3
  34. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., Von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14 (6), 587–589. https://doi.org/10.1038/nmeth.4285
  35. Kristensen, R.M. (1981) Sense organs of two marine arthrotardigrades (Heterotardigrada, Tardigrada). Acta Zoologica, 62 (1), 27–41. https://doi.org/10.1111/j.1463-6395.1981.tb00614.x
  36. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874. https://doi.org/10.1093/molbev/msw054
  37. Madeira, F., Park, Y.M., Lee, J., Buso, N., Gur, T., Madhusoodanan, N., Basutkar, P., Tivey, A.R.N., Potter, S.C., Finn, R.D. & Lopez, R. (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Research, 47 (W1), W636–W641. https://doi.org/10.1093/nar/gkz268
  38. Møbjerg, N., Kristensen, R.M. & Jørgensen, A. (2016) Data from new taxa infer Isoechiniscoides gen. nov. and increase the phylogenetic and evolutionary understanding of echiniscoidid tardigrades (Echiniscoidea: Tardigrada). Zoological Journal of the Linnean Society, 178 (4), 804–818. https://doi.org/10.1111/zoj.12500
  39. Møbjerg, N., Jørgensen, A., Kristensen, R.M. & Neves, R.C. (2018) Morphology and functional anatomy. In: Schill, R.O. (Ed.), Water Bears: The Biology of Tardigrades. Vol. 2. Springer, Switzerland, pp. 57– 95. https://doi.org/10.1007/978-3-319-95702-9_2
  40. Møbjerg, N., Jørgensen, A. & Kristensen, R.M. (2020) Ongoing revision of Echiniscoididae (Heterotardigrada: Echiniscoidea), with the description of a new interstitial species and genus with unique anal structures. Zoological Journal of the Linnean Society, 188 (3), 663–680. https://doi.org/10.1093/zoolinnean/zlz122
  41. Morek, W., Surmacz, B., López-López, A. & Michalczyk, Ł. (2021) “Everything is not everywhere”: time-calibrated phylogeography of the genus Milnesium (Tardigrada). Molecular Ecology, 30 (14), 3590–3609. https://doi.org/10.1111/mec.15951
  42. Neves, R.C, Kristensen R.M. & Møbjerg, N. 2021.New records on the rich loriciferan fauna of Trezen ar Skoden (Roscoff, France): Description of two new species of Nanaloricus and the new genus Scutiloricus. PLoS ONE, 16 (5), e0250403. https://doi.org/10.1371/journal.pone.0250403
  43. Nguyen. L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32 (1), 268–274. https://doi.org/10.1093/molbev/msu300
  44. Persson, D.K., Halberg, K.A., Jørgensen, A., Møbjerg, N. & Kristensen, R.M. (2012) Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): Tardigrade brain structure supports the clade Panarthropoda. Journal of Morphology, 273 (11), 1227–1245. https://doi.org/10.1002/jmor.20054
  45. Persson, D.K., Halberg, K.A., Neves, R.C., Jørgensen, A., Kristensen, R.M. & Møbjerg, N. (2019) Comparative myoanatomy of Tardigrada: new insights from the heterotardigrades Actinarctus doryphorus (Tanarctidae) and Echiniscoides sigismundi (Echiniscoididae). BMC Evolutionary Biology, 19 (1), 206. https://doi.org/10.1186/s12862-019-1527-8
  46. Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67 (5), 901–904. https://doi.org/10.1093/sysbio/syy032
  47. Renaud-Mornant, J. (1971) Campagne d`essais du “Jean Charcot” (3 - 8 Décembre 1968) 8. Méiobenthos. II. Tardigrades. Bulletin du Muséum National d’Histoire Naturelle, Paris, Série 2, 42, 957–969.
  48. Renaud-Mornant, J. (1981) Raiarctus colurus n.g., n. sp., et R. aureolatus n. sp., tardigrades (Arthrotardigrada) marins nouveaux de sédiments calcaires. Bulletin du Muséum National d’Histoire Naturelle, 3 (2), 512–522.
  49. Renaud-Mornant, J. (1982) Species diversity in marine Tardigrada. In: Nelson, D.R. (Ed.), Proceedings of the Third International Symposium on Tardigrada, 1980. Tennessee State University Press, Nashville, Tennessee, pp. 149–178.
  50. Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
  51. Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E. & Sánchez-Gracia, A. (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34 (12), 3299–3302. https://doi.org/10.1093/molbev/msx248
  52. Ryu, S.H., Lee, J.M., Jang, K.H., Choi, E.H., Park, S.J., Chang, C.Y., Kim, W. & Hwang, U.W. (2007) Partial mitochondrial gene arrangements support a close relationship between Tardigrada and Arthropoda. Molecules & Cells, 24 (3), 351–357.
  53. Schulz, E. (1955) Studien an marinen Tardigraden. Kieler Meeresforschungen, 11 (1), 74–79.
  54. Schwendinger, P.J. & Giribet, G. (2005) The systematics of the south-east Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae). Invertebrate Systematics, 19 (4), 297–323. https://doi.org/10.1071/IS05023
  55. Stec, D., Krzywański, Ł., Arakawa, K. & Michalczyk, Ł. (2020) A new redescription of Richtersius coronifer, supported by transcriptome, provides resources for describing concealed species diversity within the monotypic genus Richtersius (Eutardigrada). Zoological Letters, 6, 1–25. https://doi.org/10.1186/s40851-020-0154-y
  56. Whiting, M.F. (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta, 31 (1), 93–104. https://doi.org/10.1046/j.0300-3256.2001.00095.x
  57. Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. & Wheeler, W.C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46 (1), 1–68. https://doi.org/10.1093/sysbio/46.1.1