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Two new bioluminescent Henlea from Siberia and lack of molecular support for Hepatogaster (Annelida, Clitellata, Enchytraeidae)

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Abstract

Two bioluminescent enchytraeids, Henlea petushkovi sp. n. and Henlea rodionovae sp. n., are described from the Krasnoyarsk and Irkutsk regions in Eastern Siberia. These large potworms exhibit the typical light-production pattern reported repeatedly in the genus and recently elucidated by Russian researchers in its main biophysical and biochemical aspects. Morphology and DNA indicate that the two species are very closely related, but clearly divergent in the strength of the body wall (thick and opaque in H. petushkovi), structure of the prostomium (in H. rodionovae unprecedentedly wrinkled and mobile), brain shape (almost equilateral in H. petushkovi), size of coelomocytes (60–85 μm in H. petushkovi) and structure of intestinal diverticula (tulip-shaped in H. petushkovi, apple-shaped in H. rodionovae). Limited hybridization seems to occur between them, supported by a single case of conflict between COI and morphology, and a few intermediate morphotypes were noted in greenhouse populations. The new species are phylogenetically distant from all known congeners so far DNA-barcoded, even those that, like them, respond to the diagnosis of the putative subgenus Hepatogaster Čejka, 1910 (multitubular gut diverticula in VIII, indented brain, dorsal blood vessel from IX, prominent spermathecal glands, and nephridia from 5/6). In fact, our phylogenetic analyses dismiss Hepatogaster as an artificial (polyphyletic) taxon. Issues related to the definition of H. nasuta (Eisen, 1878), H. ochracea (Eisen, 1878) and H. irkutensis Burov, 1929, three species originally described from Siberia, indicate that Henlea taxonomy is still in a state of flux, as regards not only species interrelationships but also species definitions.

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References

  • Bretscher, K. (1899). Beitrag zur Kenntnis die Oligochaeten-Fauna der Schweiz. Revue Suisse de Zoologie, 3, 369–426.

    Article  Google Scholar 

  • Burov, V. S. (1929). Eine neue Henlea-Art aus der Umgegend von Irkutsk: Henlea irkutensis sp.n. Bulletin de l’Institut Scientifique de Biologie et de Géographie à l’Université d’Irkoutsk, 4, 99–132 (In Russian).

    Google Scholar 

  • Čejka, B. (1910). Die Oligochaeten der Russischen in den Jahren 1900–1903 unternommenen Nordpolarexpedition. I. Über eine neue Gattung der Enchytraeiden (Hepatogaster). Mémoires de l’Académie Impériale des Sciences de St-Pétersbourg, 29(2), 1–29.

    Google Scholar 

  • Čejka, B. (1912). Die Oligochaeten der Russischen in den Jahren 1900–1903 unternommenen Nordpolarexpedition. II. Über neue Bryodrilus- und Henlea-Arten. Mémoires de l'Académie Impériale des Sciences de St-Pétersbourg, 29(6), 1–19.

    Google Scholar 

  • Čejka, B. (1914). Die Oligochaeten der Russischen in den Jahren 1900–1903 unternommenen Nordpolarexpedition. I. Über neue Mesenchytraeus-Arten. Mémoires de l’Académie Impériale des Sciences de St-Pétersbourg, 29(9), 1–24.

    Google Scholar 

  • Cekanovskaja, O. V. (1962). Vodnje maloscetnikovje cervi fauni SSSR [the aquatic Oligochaeta of USSR]. Opredeliteli po faune SSSR, izdavaemye Zoologicheskim Institutom Akademii Nauk SSSR, 78, 1–411.

  • Černosvitov, L. (1929). Communication préliminaire sur les Oligochètes récoltés par M. P. Remy pendant la croisière arctique effectuée par le “Pourquois-Pas?” en 1926 sous la direction du Dr. J. B. Charcot. Bulletin du Muséum d’Histoire Naturelle, 2(1), 144–149.

    Google Scholar 

  • Černosvitov, L. (1931). Sur quelques oligochètes de la région arctique et des Iles Faeroer. Annales des Sciences Naturelles, Zoologie, 14, 65–110.

    Google Scholar 

  • Černosvitov, L. (1937). System der Enchytraeiden. Bulletin de l’Association Russe pour les recherches scientifiques à Prague (section des sciences naturelles et matématiques), 5, 263–295.

    Google Scholar 

  • Christensen, B. (1961). Studies on cyto-taxonomy and reproduction in the Enchytraeidae with notes on parthenogenesis and polyploidy in the animal kingdom. Hereditas, 47, 387–450.

    Article  Google Scholar 

  • Christensen, B., & Dózsa-Farkas, K. (1999). The enchytraeid fauna of the Siberian tundra (Oligochaeta, Enchytraeidae). Biologiske Skrifter, 52, 1–37.

    Google Scholar 

  • Christensen, B., & Dózsa-Farkas, K. (2006). Invasion of terrestrial enchytraeids into two postglacial tundras: North-eastern Greenland and the Arctic Archipelago of Canada (Enchytraeidae, Oligochaeta). Polar Biology, 29, 454–466.

    Article  Google Scholar 

  • Clement, M., Snell, Q., Walke, P., Posada, D., & Crandall, K. (2002). TCS: estimating gene genealogies. Proceedings of the 16th International Parallel and Distributed Processing Symposium, vol. 2, p. 184. https://doi.org/10.1109/IPDPS.2002.1016585.

  • de Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56, 879–886.

    Article  PubMed  Google Scholar 

  • Dózsa-Farkas, K., & Christensen, B. (2002). A new enchytraeid species Bryodrilus tunicatus (Enchytraeidae, Oligochaeta) from Alaska. With preliminary notes on the enchytraeid fauna of the Alaskan tundra and taiga. Natura Jutlandica, Occasional Papers, 2, 68–74.

    Google Scholar 

  • Dózsa-Farkas, K., Felföldi, T., & Hong, Y. (2015). New enchytraeid species (Enchytraeidae, Oligochaeta) from Korea. Zootaxa, 4006, 171–197.

    Article  PubMed  Google Scholar 

  • Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • d'Udekem, J. (1854). Description d’une nouvelle espèce d’Enchytraeus. Bulletins de l’Académie Royale des Sciences de Belgique, 21, 853–865.

    Google Scholar 

  • Dupont, L., Porco, D., Symondson, W. O., & Roy, V. (2016). Hybridization relics complicate barcode-based identification of species in earthworms. Molecular Ecology Resources, 16, 883–894. https://doi.org/10.1111/1755-0998.12517.

    Article  PubMed  CAS  Google Scholar 

  • Eisen, G. (1878). Redogörelse för Oligochaeter, samlade under de Svenska expeditionerna till Arktiska trakter. Öfversigt af Kongliga Vetenskaps-Akademiens Förhandlingar, 3, 63–79.

    Google Scholar 

  • Eisen, G. (1879). On the Oligochaeta collected during the Swedish expeditions to the Arctic regions in the years 1870, 1875 and 1876. Kongliga Svenska Vetenskaps-akademiens Handlingar, 15(7), 1–49.

    Google Scholar 

  • Erséus, C., Rota, E., Matamoros, L., & De Wit, P. (2010). Molecular phylogeny of Enchytraeidae (Annelida, Clitellata). Molecular Phylogenetics and Evolution, 57, 849–858.

    Article  PubMed  CAS  Google Scholar 

  • Friend, H. (1919). Luminous worms. Nature (London), 103, 446.

    Article  Google Scholar 

  • Harker, A. (1887). On a luminous oligochaete. Report of the British Association for the Advancement of Science, 56, 767.

    Google Scholar 

  • Klinth, M. J., Martinsson, S., & Erséus, C. (2017a). Phylogeny and species delimitation of North European Lumbricillus (Clitellata, Enchytraeidae). Zoologica Scripta, 46(1), 96–110. https://doi.org/10.1111/zsc.12187.

    Article  Google Scholar 

  • Klinth, M. J., Rota, E., & Erséus, C. (2017b). Taxonomy of North European Lumbricillus (Clitellata, Enchytraeidae). Zookeys, 703, 15–96.

    Article  Google Scholar 

  • Leigh, 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.12410.

    Article  Google Scholar 

  • Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.

    Article  PubMed  CAS  Google Scholar 

  • Linsbauer, K. (1917). Selbstleuchtende Regenwürmer. Die Umschau, 21, 67–69.

    Google Scholar 

  • Martinsson, S., & Erséus, C. (2017). Cryptic speciation and limited hybridization within Lumbricus earthworms (Clitellata: Lumbricidae). Molecular Phylogenetics and Evolution, 106, 18–27. https://doi.org/10.1016/j.ympev.2016.09.011.

    Article  PubMed  Google Scholar 

  • Martinsson, S., & Erséus, C. (2018). Cryptic diversity in supposedly species-poor genera of Enchytraeidae (Annelida:Clitellata). Zoological Journal of the Linnean Society, 183, 749–762. https://doi.org/10.1093/zoolinnean/zlx084.

  • Martinsson, S., Dózsa-Farkas, K., Rota, E., & Erséus, C. (2017). Placing the forgotten: on the positions of Euenchytraeus and Chamaedrilus in an updated enchytraeid phylogeny (Clitellata: Enchytraeidae). Invertebrate Systematics, 31(1), 85–90. https://doi.org/10.1071/IS16042.

    Article  Google Scholar 

  • Michaelsen, W. (1886). Über Chylusgefässsysteme bei Enchytraeiden. Archiv für Mikroskopische Anatomie, 28, 292–304.

    Article  Google Scholar 

  • Michaelsen, W. (1889). Synopsis der Enchytraeiden. Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg, 11, 1–61.

    Google Scholar 

  • Michaelsen, W. (1900). Oligochaeta. Berlin: R. Friedländer und Sohn.

    Google Scholar 

  • Molisch, H. (1912). Leuchtende Pflanzen: eine physiologische Studie. Jena: G. Fischer.

    Google Scholar 

  • Nielsen, C. O., & Christensen, B. (1959). The Enchytraeidae. Critical revision and taxonomy of European species (Studies on Enchytraeidae VII). Natura Jutlandica, 8–9, 1–160.

    Google Scholar 

  • Nurminen, M. (1970). Records of Enchytraeidae (Oligochaeta) from the west coast of Greenland. Annales Zoologici Fennici, 7, 199–209.

    Google Scholar 

  • Nurminen, M. (1973a). Enchytraeidae (Oligochaeta) from the vicinity of Lake Baikal, Siberia. Annales Zoologici Fennici, 10, 478–482.

    Google Scholar 

  • Nurminen, M. (1973b). Enchytraeidae (Oligochaeta) from the Arctic archipelago of Canada. Annales Zoologici Fennici, 10, 403–411.

    Google Scholar 

  • Nurminen, M. (1980). Notes on the Enchytraeidae (Oligochaeta) of the USSR. Annales Zoologici Fennici, 17, 175–179.

    Google Scholar 

  • O’Connor, F. B. (1963). Marionina cambrensis sp. nov.: a new enchytraeid worm (Oligochaeta) from North Wales. Annals and Magazine of Natural History, 6(13), 761–766.

    Article  Google Scholar 

  • Owsiannikow, P. (1864). Über das Leuchten der Larven von Lampyris noctiluca. Bulletin de l’Académie impériale des sciences de St.-Pétersbourg, 7, 55–61 (In Russian).

    Google Scholar 

  • Petushkov, V. N., & Rodionova, N. S. (2005). New types of luminescent systems of soil enchytraeids (Annelida: Clitellata: Oligochaeta: Enchytraeidae). Doklady Biochemistry and Biophysics, 401, 115–118.

    Article  PubMed  CAS  Google Scholar 

  • Petushkov, V. N., Rodionova, N. S., Purtov, K. V., & Bondar, V. S. (2002). The luminescence system of soil enchytraeids, Henlea sp., (Annelida: Clitellata: Oligochaeta: Enchytraeidae). Doklady Biological Science, 385, 310–312.

    Article  CAS  Google Scholar 

  • Petushkov, V. N., Rodionova, N. S., & Bondar, V. S. (2003). Study of the luminescence system of the soil Enchytraeid Fridericia heliota (Annelida: Clitellata: Oligochaeta: Enchytraeidae). Doklady Biochemistry and Biophysics, 391, 204–207.

    Article  PubMed  CAS  Google Scholar 

  • Piper, S. R., MacLean, S. F., & Christensen, B. (1982). Enchytraeidae (Oligochaeta) from taiga and tundra habitats of northeastern U.S.S.R. Canadian Journal of Zoology, 60, 2594–2609.

    Article  Google Scholar 

  • Plytycz, B., Bigaj, J., Osikowski, A., Hofman, S., Falniowski, A., Panz, T., Grzmil, P., & Vandenbulcke, F. (2018). The existence of fertile hybrids of closely related model earthworm species, Eisenia andrei and E. fetida. PLoS ONE, 13, e0191711.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pratje, A. (1923). Das Leuchten der Organismen; eine Übersicht über die neuere Literatur. Ergebnisse der Physiologie, 21, 166–273.

    Article  Google Scholar 

  • Pütter, A. (1905). Leuchtende Organismen. Zeitschrift für Allgemeine Physiologie, 5, 17–53.

    Google Scholar 

  • Rambaut, A. (2014). FigTree v1.4.2. Available from http://tree.bio.ed.ac.uk/software/figtree/

  • Rambaut, A., Suchard, M. A., Xie, W., & Drummond, A. J. (2014). Tracer v1.6.1. Available via http://tree.bio.ed.ac.uk/software/tracer (last accessed on 28 February 2018).

  • Rodionova, N. S., Bondar, V. S., & Petushkov, V. N. (2002). Ca2+− activator of the luminescence system of the earthworms Henlea sp., (Annelida: Clitellata: Oligochaeta: Enchytraeidae). Doklady Biochemistry and Biophysics, 386, 260–263.

    Article  PubMed  Google Scholar 

  • Rodionova, N. S., Bondar, V. S., & Petushkov, V. N. (2003). ATP is a cosubstrate of the luciferase of the earthworm Fridericia heliota (Annelida: Clitellata: Oligochaeta: Enchytraeidae). Doklady Biochemistry and Biophysics, 392, 253–255.

    Article  PubMed  CAS  Google Scholar 

  • Rodionova, N. S., Rota, E., Tsarkova, A. S., & Petushkov, V. N. (2017). Progress in the study of bioluminescent earthworms. Photochemistry and Photobiology, 93, 416–428.

    Article  PubMed  CAS  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rota, E. (1994). Enchytraeidae (Oligochaeta) of western Anatolia: taxonomy and faunistics. Bollettino di Zoologia, 61, 241–260.

    Article  Google Scholar 

  • Rota, E. (1995). Italian Enchytraeidae (Oligochaeta), I. Bollettino di Zoologia, 62, 183–231.

    Article  Google Scholar 

  • Rota, E. (2009). Lights on the ground: a historical survey of light production in the Oligochaeta. In V. B. Meyer-Rochow (Ed.), Bioluminescence in focus—a collection of illuminating essays (pp. 105–138). Kerala: Research-Signpost.

    Google Scholar 

  • Rota, 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/S0952836903003777.

    Article  Google Scholar 

  • Schmelz, R. M., & Collado, R. (2012). An updated checklist of currently accepted species of Enchytraeidae (Oligochaeta, Annelida). Newsletter on Enchytraeidae, 12, 67–87.

    Google Scholar 

  • Stephens, M., & Donnelly, P. (2003). A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetic, 73, 1162–1169.

    Article  CAS  Google Scholar 

  • Stephens, M., Smith, N. J., & Donnelly, P. (2001). A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetic, 68, 978–989.

    Article  CAS  Google Scholar 

  • Stephenson, J. (1922). The Oligochaeta of the Oxford University Spitsbergen expedition. Proceedings of the Zoological Society of London, 74, 1109–1138.

    Google Scholar 

  • Stephenson, J. (1930). The Oligochaeta. Oxford: Clarendon Press.

    Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tynen, M. J., Coates, K. A., Smith, C. A. S., & Tomlin, A. D. (1991). Henlea yukonensis (Oligochaeta: Enchytraeidae), a new species from the Yukon Territory, with comments on Henlea Michaelsen, 1889 and Punahenlea Nurminen, 1980. Canadian Journal of Zoology, 69, 1375–1388.

    Article  Google Scholar 

  • Vejdovský, F. (1879). Beiträge zur vergleichenden Morphologie der Anneliden. I. Monographie der Enchytraeiden. Prag: Friedrich Tempsky.

    Book  Google Scholar 

  • Walter, A. (1909). Das Leuchten einer terrestrischen Oligochaeten. Travaux de la Société Imperiale des Naturalistes de St.-Pétersbourg, 40, 103–109 136–137 (In Russian, with German summary).

    Google Scholar 

  • Welch, P. S. (1914a). Studies on the Enchytraeidae of North America. Bulletin of the Illinois State Laboratory of Natural History, 10, 123–211.

    Google Scholar 

  • Welch, P. S. (1914b). A new Henlea (Enchytraeidae) from Northern Michigan. Transactions of the American Microscopical Society, 33, 155–164.

    Article  Google Scholar 

  • Welch, P. S. (1919). Oligochaeta, II. The Enchytraeidae. Report of the Canadian Arctic Expedition 1913–1918, 9(A), 9–19.

    Google Scholar 

  • Welch, P. S. (1920). The genera of the Enchytraeidae (Oligochaeta). Transactions of the American Microscopical Society, 39, 25–50.

    Article  Google Scholar 

  • Zalesskaja, N. T., Petushkov, V. N., & Rodionova, N. S. (1990). Luminous soil-dwelling enchytraeids (Oligochaeta, Enchytraeidae). Doklady Akademii Nauk SSSR (Biol.), 310, 496–498 (In Russian).

    Google Scholar 

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Acknowledgements

We are grateful to Valentin N. Petushkov and Natalja S. Rodionova (Institute of Biophysics, Siberian Branch of the Russian Academy of Sciences, Krasnoyarsk) for entrusting us with the study of this interesting material, to Daria Melnikova (Moscow State University) for forwarding the DNA sequences of the Gladkoye specimens, and to Anna Ansebo, Per Hjelmstedt and Mårten Klinth (University of Gothenburg) for skillful molecular lab assistance.

Funding

This study received financial support from the Swedish Research Council to CE, and by the Adlerbert Research Foundation/Royal Society of Arts and Sciences in Gothenburg to both CE and SM.

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  1. Department of Physics, Earth and Environmental Sciences, University of Siena, Via P.A. Mattioli 4, 53100, Siena, Italy

    Emilia Rota

  2. Systematics and Biodiversity, Department of Biological and Environmental Sciences, University of Gothenburg, Box 463, SE-40530, Göteborg, Sweden

    Svante Martinsson & Christer Erséus

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  1. Emilia Rota
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Rota, E., Martinsson, S. & Erséus, C. Two new bioluminescent Henlea from Siberia and lack of molecular support for Hepatogaster (Annelida, Clitellata, Enchytraeidae). Org Divers Evol 18, 291–312 (2018). https://doi.org/10.1007/s13127-018-0374-6

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