Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2022-03-21

Molecular analysis of five controversial Balkanic species of Allolobophora (sensu lato) Eisen, 1873 (Lumbricidae, Clitellata) with emendation of the genus Cernosvitovia Omodeo, 1956

University of Kragujevac, Faculty of Science, Institute of Biology and Ecology, Radoja Domanovića 12, 34000 Kragujevac, Serbia;
University of Kragujevac, Faculty of Science, Institute of Biology and Ecology, Radoja Domanovića 12, 34000 Kragujevac, Serbia;
Grupo de Ecoloxía Animal (GEA), Universidade de Vigo, E-36310 Vigo, Spain
University of Kragujevac, Institute for Information Technologies Kragujevac, Department of Science, Jovana Cvijića bb, 34000 Kragujevac, Serbia
University of Kragujevac, Faculty of Science, Institute of Biology and Ecology, Radoja Domanovića 12, 34000 Kragujevac, Serbia;
Grupo de Ecoloxía Animal (GEA), Universidade de Vigo, E-36310 Vigo, Spain. CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
Annelida Cernosvitovia earthworm Balkan Peninsula molecular phylogenetics systematics

Abstract

Allolobophora (sensu lato) is one of the most controversial genera in the taxonomy of Lumbricidae. Due to its poor definition, this genus is plagued by extensive taxonomic confusion, and its generic composition and internal relationships have remained uncertain, especially in species of the Balkan Peninsula. In this study, we have combined the study of morphological data and molecular phylogenetics based on five genetic markers, regions of the nuclear 28S rRNA and mitochondrial 16S rRNA, 12S rRNA, NADH dehydrogenase (ND1) and cytochrome oxidase C subunit 1 (COI), to delimit the taxonomic status of five controversial Balkanic endemic species, Allolobophora (s.l.) dofleini, Allolobophora (s.l.) serbica, Allolobophora (s.l.) strumicae, Allolobophora (s.l.) paratuleskovi and Allolobophora (s.l.) treskavicensis, sampled in the Kopaonik Mountain. Phylogenetic analyses based on our sampling of these five species recovered a well-supported clade containing the species Allolobophora (s.l.) robusta, Allolobophora (s.l.) mehadiensis mehadiensis, Allolobophora (s.l.) sturanyi dacica, Cernosvitovia rebeli and Cernosvitovia dudichi. Based on these results and previous evidence, the aforementioned Balkanic species are transferred to a redefined Cernosvitovia. We further present a revised list of all species currently included in Cernosvitovia., which includes now 21 species and subspecies taxa, 13 of them newly combined here. Serbiona Mršić & Šapkarev, 1988 is considered a junior synonym of Cernosvitovia Omodeo, 1956.

 

References

  1. Akaike, H. (1973) Maximum likelihood identification of Gaussian autoregressive moving 415 average models. Biometrika, 60 (2), 255–265. https://doi.org/10.1093/biomet/60.2.255
    Bouché, M.B. (1972) Lombriciens de France – Écologie et Systématique. I.N.R.A. Publications 72 (2). Institut National de la Recherche Agronomique, Paris, 671 pp.
    Cech, G., Szederjesi, T. & Csuzdi, C. (2014) Phylogeny of the family Lumbricidae; morphological and molecular overview. Magyar Tudomány, 175 (4), 394–399. [in Hungarian]
    Černosvitov, L. (1937) Die Oligochaetenfauna Bulgariens. Mitteilungen aus den Königlich Naturwissenschaftlichen Instituten in Sofia, 10, 62–92.
    Cognetti di Martiis, L. (1905) Lombrichi liguri del Museo civico di Genova. Annali di Museo civico di storia naturale di Genova, 42 (2), 102–127.
    Csuzdi, C. & Zicsi, A. (2003) Earthworms of Hungary (Annelida: Oligochaeta, Lumbricidae). Natural History Museum, Budapest, 271 pp.
    Csuzdi, C. (2012) Earthworm species, a searchable database. Opuscula Zoologica Budapest, 43 (1) 97–99.
    Csuzdi, C., Pop, V.V. & Pop, A.A. (2011) The earthworm fauna of the Carpathian Basin with new records and description of three new species (Oligochaeta: Lumbricidae). A Journal of Comparative Zoology, 250 (1) 2–18. https://doi.org/10.1016/j.jcz.2010.10.001
    Cuvier, G. (1826) Analyse des travaux de l'Académie royale des sciences pendant l'année 1822. Mémoires de l'Académie Royale des Sciences de l'Institut de France, 5 (Histoire de l'Académie), 153–203.
    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new 413 heuristics and parallel computing. Nature methods, 9 (8), p. 772. https://doi.org/10.1038/nmeth.2109
    De Sosa, I., Díaz Cosín, D.J., Csuzdi, C., Paoletti, M.G. & Marchán, D.F. (2019) Placing Eophila tellinii (Oligochaeta, Lumbricidae) in a molecular phylogenetic context advances the century-old controversy around the problematic genus. European Journal of Soil Biology, 94, 103–114. https://doi.org/10.1016/j.ejsobi.2019.103114
    Domínguez, J., Aira, M., Breinholt, J.W., Stojanovic, M., James, S.W. & Pérez-Losada, M. (2015) Underground evolution: new roots for the old tree of lumbricid earthworms. Molecular phylogenetics and evolution, 83, 7–19. https://doi.org/10.1016/j.ympev.2014.10.024
    Domínguez, J., Aira, M., Porto, P.G., Díaz Cosín, D.J. & Pérez-Losada, M. (2018) Multigene phylogeny reveals two new isolated and relic earthworm genera (Oligochaeta: Lumbricidae). Zoological Journal of the Linnean Society, 182 (2), 258–274. https://doi.org/10.1093/zoolinnean/zlx031
    Eisen, G. (1873) Om Skandinaviens Lumbricider. Öfversigt af Kongliga Vetenskaps-Akademiens Förhandligar, 30 (8), 43–56.
    Google Maps (2022) Tectonic and geographic map of the Kopaonik Mountain in Serbia (Toljić et al. 2019; Google Maps 2022). Google Maps [online]. Available from: https://www.google.com/maps/d/edit? (accessed 25 Jan. 2022)
    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and 410 analysis program for Windows 95/98/NT. In: Nucleic acids symposium series (Vol. 41, No. 41,). Information Retrieval Ltd., c1979–c2000, London, pp. 95–98
    Jiménez Pinadero, S., Marchán, D.F., Novo, M., Trigo, D., Domínguez, J. & Díaz Cosín, D.J. (2021) Sorry atlanticus, you are not my type: molecular assessment splits Zophoscolex (Lumbricidae: Crassiclitellata) into French and Iberian genera. Zoological Journal of the Linnean Society, https://doi.org/10.1093/zoolinnean/zlab011
    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 406 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780. https://doi.org/10.1093/molbev/mst010
    Marchán, D.F., Jiménez, S., Decaëns, T. & Domínguez, J. (2022) Systematic revision of Gatesona (Crassiclitellata, Lumbricidae), an endemic earthworm genus from the Massif Central (France). Plos ONE. [in press]
    Marchán, D.F., Fernández, R., de Sosa, I., Sánchez, N., Díaz Cosín, D.J. & Novo, M. (2018) Integrative systematic revision of a Mediterranean earthworm family: Hormogastridae (Annelida, Oligochaeta). Invertebrate Systematics, 32 (3), 652–671. https://doi.org/10.1071/IS17048
    Marchán, D.F., Fernández, R., Novo, M. & Cosín, D.J. (2014) New light into the hormogastrid riddle: morphological and molecular description of Hormogaster joseantonioi sp. n. (Annelida, Clitellata, Hormogastridae). ZooKeys, 414, 1–17. https://doi.org/10.3897/zookeys.414.7665.
    Marchán, D.F., Novo, M., Fernández, R., De Sosa, I., Trigo, D. & Cosín, D.J.D. (2016) Evaluating evolutionary pressures and phylogenetic signal in earthworms: a case study-the number of typhlosole lamellae in Hormogastridae (Annelida, Oligochaeta). Zoological Journal of the Linnean Society, 178 (1), 4–14. https://doi.org/10.1111/zoj.12410
    Marchán, D.F., Csuzdi, C., Decaëns, T., Szederjesi, T., Pizl, V. & Domínguez, J. (2021) The disjunct distribution of relict earthworm genera clarifies the early historical biogeography of the Lumbricidae (Crassiclitellata, Annelida). Journal of Zoological Systematics and Evolutionary Research, 59 (8), 1703–1717. https://doi.org/10.1111/jzs.12514
    Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for 420 inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), 1–8. https://doi.org/10.1109/GCE.2010.5676129
    Mýsýrlýoðlu, M., Stojanović, M. & Tsekova, R. (2018) Species richness of the earthworm fauna (Clitellata: Acanthodrilidae, Lumbricidae) of the marmara region in Turkey: Zoogeographical overview. North-Western Journal of Zoology, 14 (2), 259–264.
    Mršić, N. & Šapkarev, J. (1988) Revision of the genus Allolobophora Eisen, 1874 (sensu Pop, 1941) (Lumbricidae, Oligochaeta). Acta Musei Macedonici Scinetarium Naturalium, 19, 1–38.
    Mršić, N. (1991) Monograph on earthworms (Lumbricidae) of the Balkans I–II. Slovenska Akademija Znanosti i Umetnosti, Ljubljana, pp. 1–757
    Novo, M., Almodóvar, A., Fernández, R., Giribet, G. & Díaz Cosín, D.J. (2011) Understanding the biogeography of a group of earthworms in the Mediterranean basin – The phylogenetic puzzle of Hormogastridae (Clitellata: Oligochaeta). Molecular Phylogenetics and Evolution, 61 (1), 125–135. https://doi.org/10.1016/j.ympev.2011.05.018
    Omodeo, P. (1952) Materiali zoologici raccolti dal Dr. Marcuzzi sule Alpi Dolomitiche Archivio Zoologico Italiano, 37, 29–59.
    Omodeo, P. (1956) Contributo alla revisione dei Lumbricidae. Archivio Zoologico Italiano, 41, 129–212.
    Omodeo, P. (1988) The genus Eophila (Lumbricidae, Oligochaeta). Bolletino di Zoologia, 55, 73–88. https://doi.org/10.1080/11250008809386603
    Örley, L. (1885) A palaearktikus övben élõ Terrikoláknak revíziója és elterjedése. Értekezések a Természettudományok Körébõl, Magyar Akad., 15 (18), 1–34.
    Paoletti, M.G. Blakemore, R.J., Csuzdi, C., Dorigo, L., Dreon, A.L., Gavinelli, F., Lazzarini, F., Manno, N., Moretto, E., Porco, D., Ruzzier, E., Toniello, V., Squartini, A., Concheri, G., Zanardo, M. & Alba-Tercedor, J. (2016) Barcoding Eophila crodabepis sp. nov. (Annelida, Oligochaeta, Lumbricidae), a Large Stripy Earthworm from Alpine Foothills of Northeastern Italy Similar to Eophila tellinii (Rosa, 1888). PLoS ONE, 11 (3). https://doi.org/10.1371/journal.pone.0151799
    Perel, T.S. (1976) A critical analysis of the Lumbricidae genera system (with key to the USSR fauna genera). Revue d'écologie et de Biologie du Sol,13, 635–643.
    Pérez-Losada, M., Breinholt, J.W., Aira, M. & Domínguez, J. (2015) An updated multilocus phylogeny of the Lumbricidae (Annelida: Clitellata: Oligochaeta) earthworms. Journal of Phylogenetics & Evolutionary Biology, 3 (1), 1–4. https://doi.org/10.4172/2329-9002.1000140
    Pérez-Losada, M., Breinholt, J.W., Porto, P.G., Aira, M. & Domínguez, J. (2011) An earthworm riddle: systematics and phylogeography of the Spanish lumbricid Postandrilus. PLoS ONE, 6 (11), e28153. https://doi.org/10.1371/journal.pone.0028153
    Pérez-Losada, M., Ricoy, M., Marshall, J.C. & Domínguez, J. (2009) Phylogenetic assessment of the earthworm Aporrectodea caliginosa species complex (Oligochaeta: Lumbricidae) based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 52 (2), 293–302. https://doi.org/10.1016/j.ympev.2009.04.003
    Pop, A.A., Cech, G., Csuzdi, C., Wink, M. & Pop, V.V. (2005) An attempt to reconstruct the molecular phylogeny of the genus Allolobophora Eisen, 1874 (sensu lato, Pop, 1941) using 16S rDNA and COI sequences (Oligochaeta, Lumbricidae) In: Pop, V.V. & Pop, A.A. (Eds.), Advances in Earthworm Taxonomy II Cluj. University Press, Cluj-Napoca. pp. 155–165.
    Pop, A.A., Csuzdi, C., Wink, M. & Pop, V.V. (2008) Molecular taxonomy and phylogeny of the genera Octolasion Örley, 1885, Octodrilus Omodeo, 1956 and Octodriloides Zicsi, 1986 (Oligochaeta, Lumbricidae) based on nucleotide sequences of mitochondrial 16S rDNA and COI genes. In: Pavlíček, T. & Cardet, P. (Eds.), Advances in earthworm taxonomy III. (Annelida, Oligochaeta). The Environment of Service of the Ministry of Agriculture, Natural Resources and Environment of Cyprus, Nicosia, pp.109–125.
    Pop, A.A., Pop, V.V. & Csuzdi, C. (2011) Significance of the Apuseni Mountains (the Carpathians) in the origin and distribution of Central European earthworm fauna, Zoology in the Middle East, 51 (S2), 89–110. https://doi.org/10.1080/09397140.2010.10638462
    Pop, V. (1941) Zur Phylogenie und Systematik der Lumbriciden. Zoologische Jahrbücher Abtheilung für Systematik, Ökologie und Geographie der Tiere, 74, 487–522.
    Qiu, J.P. & Bouché, M.B. (1998a) Révision des taxons supraspécifiques de Lumbricoidea. Documents Pedozoologiques & Integrologiques, 3, 179–216.
    Qiu, J.P. & Bouché, M.B. (1998b) La decouverte de Postandrilus gen. nov. (Oligochaeta: Lumbricidae) et remarques sur la reproduction des lombriciens. Documents Pedozoologiques & Integrologiques, 4, 65–72.
    Qiu, J.P. & Bouché, M.B. (1998c). Zophoscolex, un nouveau genre de Lumbricidae (Annelida: Oligochaeta) d’Iberie et de France. Documents Pedozoologiques & Integrologiques, 4, 20–36.
    Qiu, J.P. & Bouché, M.B. (1998d). L’interprétation des caractéristiques lombriciennes. Documents Pedozoologiques & Integrologiques, 3, 119–178.
    Rafinesque-Schmaltz, C.S. (1815) Analyse de la nature ou tableau de l’univers et des corps organisés. Palermo, 224 pp. https://doi.org/10.5962/bhl.title.106607
    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under 418 mixed models. Bioinformatics, 19 (12), 1572–1574.
    https://doi.org/10.1093/bioinformatics/btg180
    Rosa, D. (1893) Revisione dei lumbricidi. Memoire della Reale Academia delle Scienze di Torino (Serie 2), 43, 399–477.
    Rosa, D. (1897) Nuovi lombrichi dell’Europa orientale (Seconda serie). Bolletino dei Musei di Zoologia ed Anatomia Comparata della Reale Universita di Torino, 12 (269), 1–5. https://doi.org/10.5962/bhl.part.4563
    Rota, E. & de Jong, Y. (2015) Fauna Europaea: Annelida-Terrestrial Oligochaeta (Enchytraeidae and Megadrili), Aphanoneura and Polychaeta. Biodiversity Data Journal, 3, e5737. https://doi.org/10.3897/BDJ.3.e5737
    Šapkarev, J. (1973) The fauna of earthworms of Macedonia. 4. The earthworms (Oligochaeta:Lumbricidae) of the valley of Strumica. Godišen Zbornik PMF, 25, 41–49.
    Šapkarev J (1975) Eine neue Regenwurm-Art aus Serbien, Jugoslawien (Allolobophora paratuleskovi n.sp.). Godišen Zbornik PMF, 27–28, 55–58.
    Šapkarev, J. (1977) Contribution to the knowledge of earthworms (Oligochaeta: Lumbricidae) from Slovenia, Yugoslavia. Godišen Zbornik PMF, 30, 47–56.
    Šapkarev, J. (1978) Fauna na Makedonija. IV. Doždovni glisti - Lumbricidae (Oligochaeta - Annelida). Fanua Makedonije, 4, 1–116.
    Schwarz, G. (1978) Estimating the dimension of a model. Annals of Statistics, 6 (2), 461–464. https://doi.org/10.1214/aos/1176344136
    Stojanović, M., Sekulić, J. & Trakić, T. (2017) Distribution and threat status of endemic earthworm Allolobophora dofleini (Oligochaeta, Lumbricida) on the Balkan Peninsula. North-Western Journal of Zoology, 13 (1), 136–143.
    Stojanović, M., Sekulić, J. & Trakić, T. (2018) Checklist of earthworms (Oligochaeta: Lumbricidae) from Serbia. A review. Zootaxa, 4496 (1), 124–155. https://doi.org/10.11646/zootaxa.4496.1.9
    Stojanović-Petrović, M. Trakić, T. & Sekulić, J. (2020) Kišne gliste (Oligochaeta: Lumbricidae) Srbije. Univerzitet u Novom Sadu, 276 pp. [In Serbian]
    Szederjesi, T., Pop, V., Marton, O., Krízsik, V. & Csuzdi, C. (2016) The Allolobophora sturanyi species group revisited: Integrated taxonomy and new taxa (Clitellata: Megadrili). Opuscula Zoologica (Budapest), 47 (1), 87–92. https://doi.org/10.18348/opzool.2016.1.87
    Toljić, M., Stojadinović, U. & Krstekanic, N. (2019) Vardar Zone: New insights into the tectono-depositional subdivision. II Congres Geologist Bosnia and Hercegovina. Laktaši, Bosnia and Hercegovina, 90 pp.
    Trakić, T., Valchovski, H. & Stojanović, M. (2016) Endemic earthworms (Oligochaeta: Lumbricidae) of the Balkan Peninsula: a review. Zootaxa, 4189 (2), 251–274. https://doi.org/10.11646/zootaxa.4189.2.3
    Ude, H. (1922) Regenwürmer aus Mazedonien. Archiv für Naturgeschichte, 88, 155–162.
    Valchovski, H. & Szederjesi, T. (2016) New and additional records of earthworms (Oligochaeta: Lumbricidae) from Bulgaria: First finding of endemic species Cernosvitovia munteniana on the Balkan Peninsula. North-Western Journal of Zoology, 12 (2), 356–360.
    Zicsi, A. (1981) Probleme der Lumbriciden-Systematik sowie die Revision zweier Gattungen (Oligochaeta). Acta Zoologica Hungarica, 27, 431–442.

  2.