Abstract
The small synanthropic and peregrine earthworm Microscolex phosphoreus (Dugès, 1837) is reported for the first time from Siberia. Morphological and DNA barcode (COI) analyses of this and widely separate samples worldwide demonstrate that, as currently identified, M. phosphoreus is a heterogeneous taxon, with divergent lineages occurring often in the same locality and hardly providing geographically structured genetic signals. The combined morphological and genetic evidence suggests that at least four of the found clades should be reclassified as separate species, both morphologically and genetically distinct from each other. However, as the specimen number was limited and only the COI gene was studied for the genetic work, we hesitate in formally describing new species. There would also be the problem of assigning the available names to specific lineages. Our findings encourage careful external and anatomical examination and using reliable characters such as the interchaetal distances and spermathecal morphology for correct identification and for deeper evaluation of cryptic diversity in this interesting bioluminescent worm.
References
Anisimova, M. & Gascuel, O. (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Systematic Biology, 55, 539–552.
https://doi.org/10.1080/10635150600755453Beddard, F.E. (1892) On the earthworms collected in Algeria and Tunisia by Dr. Anderson. Proceedings of the Zoological Society of London, 1892, 28–37.
Beddard, F.E. (1893) Some new or little known Oligochaeta. Proceedings of the Royal Physical Society of Edinburgh, 12, 30–40.
Beddard, F.E. (1895) A Monograph of the Order of Oligochaeta, Clarendon Press, Oxford, 769 pp.
https://doi.org/10.5962/bhl.title.56335Blakemore, R.J. (1994) Earthworms of south-east Queensland and their agronomic potential in brigalow soils. Unpublished PhD Dissertation, University of Queensland, Brisbane, 605 pp.
Bouché, M.B. (1972) Lombriciens de France. Ecologie et systématique. Annales de Zoologie-Ecologie Animale, Numero Hors-Série, 1–671.
Clement, M., Snell, Q., Walke, P., Posada, D. & Crandall, K. (2002) TCS: estimating gene genealogies. Proceedings of the 16th International Parallel & Distributed Processing Symposium, 2, 184.
https://doi.org/10.1109/IPDPS.2002.1016585Csuzdi, Cs. (1986) Über ein Vorkommen von Microscolex phosphoreus (Dugès, 1837) (Oligochaeta: Acanthodrilidae) in Ungarn. Opuscula Zoologica Budapest, 22, 63–66.
Damoff, G.A. (2008) Earthworm populations in upland mixed pine-hardwood and bottomland hardwood communities of Caddo Lake National Wildlife Refuge. PhD Dissertation, Stephen F. Austin State University, Nacogdoches, Texas, 198 pp.
Díaz Cosín, D.J. & Moreno, A.G. (1979) Primera cita en la Peninsula Iberica de Microscolex phosphoreus (Dugès, 1837) (Oligochaeta, Megascolecidae). Boletín de la Real Sociedad Española de Historia Natural, Sección biológica, 77, 143–150.
Dugès, A. (1837) Nouvelles observations sur la zoologie et l’anatomie des Annélides abranches sétigères. Annales des Sciences Naturelles, Series 2, Zoologie, 8, 15–35.
Dyne, G.R. & Jamieson, B.G.M. (2004) Native Earthworms of Australia II (Megascolecidae, Acanthodrilinae). ABRS, Australian Government Department of Environment and Heritage, Canberra, Australian Capital Territory, 200 pp., CD-ROM.
Fletcher, J.J. (1887) Notes on Australian earthworms, Part III. Proceedings of the Linnean Society of New South Wales, 12, 375–402.
https://doi.org/10.5962/bhl.part.29187Folmer, 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, 294–299.
Gates, G.E. (1972) Burmese earthworms. An introduction to the systematics and biology of megadrile oligochaetes with special reference to Southeast Asia. Transactions of the American Philosophical Society, 62, 1–326.
https://doi.org/10.2307/1006214Gates, G.E. (1977) More on the earthworms genus Diplocardia. Megadrilogica, 3 (1), 1–48.
Giard, A. (1887) Sur un nouveau genre de Lombriciens phosphorescent et sur l’espèce type de ce genre, Photodrilus phosphoreus Dugès. Comptes rendus de l'Académie des Sciences, 105 (19), 872–874.
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.
https://doi.org/10.1093/sysbio/syq010Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.
https://doi.org/10.1093/nar/gkf436Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33, 1870–1874.
https://doi.org/10.1093/molbev/msw054Lee, K.E. (1959) The earthworm fauna of New Zealand. Bulletin New Zealand Department of Scientific and Industrial Research, Wellington, 130, 1–486.
Lefort, V., Longueville, J.E. & Gascuel, O. (2017) SMS: Smart Model Selection in PhyML. Molecular Biology and Evolution, 34, 2422–2424.
https://doi.org/10.1093/molbev/msx149Leigh, J.W. & Bryant, D. (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116.
https://doi.org/10.1111/2041-210X.12410Michaelsen, W. (1899) Beitrage zur Kenntniss der Oligochäten. Zoologische Jahrbücher, Jena, Abteilung für Systematik, 12, 105–144.
https://doi.org/10.5962/bhl.part.2028Michaelsen, W. (1900) Oligochaeta. Das Tierreich, 10, 1–575.
Michaelsen, W. (1907) Die Fauna Südwest-Australiens. Oligochaeta. In: Ergebnisse der Hamburger südwest-australischen Forschungsreise 1905. 1 (2). Gustav Fischer, Jena, pp. 117–232.
Minamiya, Y., Kawano, K., Kin, I. & Oba, Y. (2017) Terrestrial Megadriles of Shimane Prefecture, Western Honshu, Japan. Bulletin of the Hoshizaki Green Foundation, 20, 181–195. [in Japanese]
Oba, Y. (2012) Record of the luminous earthworm, Microscolex phosphoreus (Dugès, 1837), from 14 points in Nagoya University Higashiyama Campus. Bulletin of Nagoya University Museum, 28, 77–83. [in Japanese]
Oba, Y., Branham, M.A. & Fukatsu, T. (2011a) The terrestrial bioluminescent animals of Japan. Zoological Science, 28 (11), 771–789.
https://doi.org/10.2108/zsj.28.771Oba, Y., Komiyama, R., Naito, M., Kin, I. & Shibata, K. (2016) The northernmost distribution records of the luminous earthworm Microscolex phosphoreus in Japan. Bulletin of Firefly Museum of Toyota Town, 8, 1–4. [in Japanese]
Oba, Y., Matsuda, M., Fujimori, N., Ikeya, H. & Kawano, K. (2015) DNA barcoding of the luminous earthworm Pontodrilus litoralis in Japan. Bulletin of Firefly Museum of Toyota Town, 7, 1–10. [in Japanese]
Oba, Y., Shibata, K. & Yoshida, H. (2011b) The luminous earthworm, Microscolex phosphoreus (Dugès, 1837), found in Nagoya University campus, and its DNA barcoding. Bulletin of Nagoya University Museum, 27, 13–16. [in Japanese]
Omodeo, P. (1952) Oligocheti della Turchia. Annuario dell'Istituto e Museo di Zoologia dell'Università di Napoli, 4 (2), 1–10.
Perel, T.S. (1979) Range and regularities in the distribution of earthworms of the USSR fauna. Nauka, Moscow, 272 pp. [in Russian]
Pickford, G.E. (1937) A monograph of the Acanthodrilinae earthworms of South Africa. W. Heffer & Sons Ltd., Cambridge, 612 pp.
Ratnasingham, S. & Hebert, P.D.N. (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE, 8 (7), e66213.
https://doi.org/10.1371/journal.pone.0066213Rodionova, N.S., Rota, E., Tsarkova, A.S. & Petushkov, V.N. (2017) Progress in the study of bioluminescent earthworms. Photochemistry and Photobiology, 93, 416–428.
https://doi.org/10.1111/php.12709Rosa, D. (1887) Microscolex modestus n. gen., n. sp. Bollettino dei Musei di Zoologia ed Anatomia comparata della Regia Università di Torino, 2 (19), 1–2.
Rosa, D. (1888) Sui generi Pontodrilus, Microscolex e Photodrilus. Bollettino dei Musei di Zoologia ed Anatomia comparata della Regia Università di Torino, 3 (39), 1–4.
Rosa, D. (1890) I terricoli argentini raccolti dal Dott.Carlo Spegazzini. Annali del Museo civico di Storia naturale di Genova, Series 2, 29, 509–520.
Rota, E. (2009) Lights on the ground: A historical survey of light production in the Oligochaeta. In: Meyer-Rochow, V.B. (Ed.), Bioluminescence in Focus– A Collection of Illuminating Essays, Research Signpost, Kerala, pp. 105–138.
Rota, E. (2013) Fauna Europaea: Terrestrial Oligochaeta, Aphanoneura and Polychaeta. Fauna Europaea. Version 2.6.2. Available from: https://fauna-eu.org/ (accessed 11 June 2018)
Rota, E. & de Jong, Y. (2015) Fauna Europaea: Annelida - Terrestrial Oligochaeta (Enchytraeidae and Megadrili), Aphanoneura and Polychaeta. Biodiversity Data Journal, 3 (e5737), 1–48.
https://doi.org/10.3897/BDJ.3.e5737Rota, E., Zalesskaja, N.T., Rodionova, N.S. & Petushkov, V.N. (2003) Redescription of Fridericia heliota (Annelida, Clitellata: Enchytraeidae), a luminous worm from the Siberian taiga, with a review of bioluminescence in the Oligochaeta. Journal of Zoology, London, 260, 291–299.
https://doi.org/10.1017/S0952836903003777Stephenson, J. (1914) On a collection of Oligochaeta mainly from northern India. Records of the Indian Museum, 10, 321–365.
https://doi.org/10.5962/bhl.part.5632Stephenson, J. (1930) The Oligochaeta. Clarendon Press, Oxford, 978 pp.
Talavera, J.A. & Pérez, D.I. (2009) Occurrence of the genus Microscolex (Oligochaeta, Acanthodrilidae) at Western Canary Islands. Bonner zoologische Beiträge, 56 (1/2), 37–41.
Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.
Voua Otomo, P., Maboeta, M.S. & Bezuidenhout, C. (2013) Inadequate taxonomy and highly divergent COI haplotypes in laboratory and field populations of earthworms used in ecotoxicology, A case study. African Zoology, 48, 290–297.
https://doi.org/10.3377/004.048.0224Vsevolodova-Perel, T.S. (1997) The earthworms of the fauna of Russia: Cadaster and Key. Nauka, Moscow, 102 pp. [in Russian]
Wampler, J.E. (1982) The bioluminescence system of Microscolex phosphoreus and its similarities to those of other bioluminescent earthworms (Oligochaeta). Comparative Biochemistry and Physiology, 71A, 599–604.
https://doi.org/10.1016/0300-9629(82)90209-2Wampler, J.E. & Jamieson, B.G.M. (1980) Earthworm bioluminescence: comparative physiology and biochemistry. Comparative Biochemistry and Physiology, 66B, 43–50.
https://doi.org/10.1016/0305-0491(80)90081-4Yamaguchi, H. (1935) Occurrence of the luminous oligochaete Microscolex phosphoreus (Dug.) in Japan. Annotationes zoologicae japonenses, 15 (2), 200–202.