Mission possible: An attempt toward a phylogenetic understanding of the genus Dendrobaena (Crassiclitellata, Lumbricidae)
Authors/Creators
- 1. Department of Zoology, Eszterházy Károly Catholic University, Eger, Hungary
- 2. Unaffiliated, Chafé, Portugal
- 3. Department of Agroecology and Plant Production, University of Agriculture in Krakow, Krakow, Poland
- 4. Unaffiliated, Piliscsaba, Hungary
Description
With approximately 115 described species, Dendrobaena is the most species-rich genus within the family Lumbricidae and is probably also the most heterogeneous, both morphologically and geographically. Early attempts at morphological revision led to the separation of some morphologically homogeneous groups as separate genera, such as Fitzingeria and Satchellius. Although molecular phylogenetic approaches are now widely applied, relatively few studies have focused on Dendrobaena, and those have generally been limited to the revision of individual species groups. To address this gap, we employed an integrative approach combining molecular and morphological data. Our dataset includes 40 Dendrobaena taxa from diverse regions of Europe and Asia, several Eisenia species representing their entire geographic range, and representatives of related genera (Dendrodriloides, Healyella, and Spermophorodrilus). Our results indicate the potential polyphyly of both Dendrobaena and Eisenia, with E. ebneri and related species forming a clade with Caucasian Dendrodriloides species instead of Eisenia s. str. This clade also includes Dendrobaena veneta and closely related taxa. Within Dendrobaena, five distinct clades were recovered. According to our results, the lineage comprising former Fitzingeria species and allied taxa, and also the D. byblica species group together with Philomontanus baloutchi, do not belong to the Dendrobaena s. str. clade.
Files
ZK_article_201330.pdf
Files
(4.5 MB)
| Name | Size | Download all |
|---|---|---|
|
md5:6094b0c6cbe4fbe375a5aaa7262a7887
|
4.4 MB | Preview Download |
|
md5:76d39ecf752c08c1a69c5be9b5ec7272
|
105.3 kB | Preview Download |
Linked records
Additional details
References
- Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrow BN, Csáki F (Eds) Proceedings of the 2nd International Symposium on Information. Akadémiai Kiadó, Budapest, 267–281.
- Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) Genbank. Nucleid Acids Research 40(D1): D48–D53. https://doi.org/10.1093/nar/gkr1202
- Casale A, Taglianti AV (1999) Caraboid beetles (excl. Cicindelidae) of Anatolia, and their biogeographical significance (Coleoptera, Caraboidea). Biogeographia 20: 277–406. https://doi.org/10.21426/B620110002
- Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17(4): 540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
- Cech G, Csuzdi Cs, Márialigeti K (2006) Remarks on the molecular phylogeny of the genus Dendrobaena (sensu Pop 1941) based on the investigation of 18S rDNA sequences. In: Pop VV, Pop AA (Eds) Advances in Earthworm Taxonomy II (Annelida: Oligochaeta). Cluj University Press, Cluj-Napoca, 85–98.
- Chen CA, Chen C-P, Fan TY, Yu JK, Hsieh H-L (2002) Nucleotide sequences of ribosomal internal transcribed spacers and their utility in distinguishing closely related Perinereis polychaetes (Annelida; Polychaeta; Nereididae). Marine Biotechnology 4: 17–29. https://doi.org/10.1007/s10126-001-0069-3
- Csuzdi Cs (1984) A Dendrobaena nem revíziója összehasonlító morfológiai és anatómiai vizsgálatok alapján [Revision of the genus Dendrobaena based on comparative morphological and anatomical studies]. MSc thesis, Eötvös Loránd University, Budapest.
- Csuzdi Cs (2012) Earthworm species, a searchable database. Opuscula Zoologica Budapest 43: 97–99. https://doi.org/10.5281/zenodo.1045525
- Csuzdi Cs, Zicsi A (2003) Earthworms of Hungary (Annelida: Oligochaeta; Lumbricidae). In: Csuzdi Cs, Mahunka S (Eds) Pedozoologica Hungarica 1. Hungarian Natural History Museum, Budapest, 271 pp.
- Csuzdi Cs, Pop AA, Pop VV, Wink M, Zicsi A (2005) Revision of the Dendrobaena alpina (Rosa, 1884) species group (Oligochaeta, Lumbricidae). In: Pop VV, Pop AA (Eds) Advances in Earthworm Taxonomy II. (Annelida: Oligochaeta). University Press Cluj, Cluj Napoca, 119–128.
- Csuzdi Cs, Valchovski H, Krízsik V, Pavlíček T, Szederjesi T (2023) On the molecular taxonomy of the Dendrobaena alpina species complex, with description of a new species (Crassiclitellata, Lumbricidae). Zootaxa 5255(1): 062–067. https://doi.org/10.11646/zootaxa.5255.1.10
- Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36 (suppl_2): W465–469. https://doi.org/10.1093/nar/gkn180
- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome oxidase c subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
- Kalyaanamoorthy S, Minh B, Wong T, von Haesler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285
- Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
- Krijgsman W, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400: 652–655. https://doi.org/10.1038/23231
- Kvavadze E (1993) A new genus of earthworms Omodeoia gen. nov. (Oligochaeta, Lumbricidae). Bulletin of the Georgian Academy of Sciences 148: 129–134.
- Kvavadze E (2000a) Novye Dannye o Sistematike Dozhdevykh Chervei (Oligochaeta, Lumbricidae). [New Data on Earthworms (Lumbricidae) Systematic]. Proceedings of the Institute of Zoology 20: 77–84.
- Kvavadze E (2000b) New genus of earthworms Dendrodriloides gen. nov. (Oligochaeta, Lumbricidae). Bulletin of the Georgian Academy of Sciences 161(2): 344–346.
- Lemmon AR, Emme SA, Lemmon EM (2012) Anchored hybrid enrichment for massively high-throughput phylogenomics. Systematic Biology 6(5): 727–744. https://doi.org/10.1093/sysbio/sys049
- Licht A, Métais G, Coster P, İbilioğlu D, Ocakoğlu F, Westerweel J, Mueller M, Campbell C, Mattingly S, Wood MC, Beard KC (2022) Balkanatolia: the insular mammalian biogeographic province that partly paved the way to the Grande Coupure. Earth-Science Reviews 226: 103929. https://doi.org/10.1016/j.earscirev.2022.103929
- Marchán DF, Csuzdi Cs, Decaëns T, Szederjesi T, Pižl V, Domínguez J (2021a) 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
- Marchán DF, Decaëns T, Domínguez J, Novo M (2021b) Perspectives in earthworm molecular phylogeny: recent advances in Lumbricoidea and standing questions. Diversity 14(1): 30. https://doi.org/10.3390/d14010030
- Mršić N (1991) Monograph on Earthworms (Lumbricidae) of the Balkans I–II. Slovenska Akademija Znanosti in Umetnosti, Ljubljana, 757 pp.
- Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1): 268–74. https://doi.org/10.1093/molbev/msu300
- Omodeo P, Rota E (1989) Earthworms of Turkey. Bolletino di Zoologia 56: 167–198. https://doi.org/10.1080/11250008909355639
- Palumbi S, Martin R, Romano S, McMillan WO, Stica L, Grabowski G (1991) The Simple Fool's Guide to PCR, Version 2. University of Hawaii, Honolulu, 47 pp.
- Perrot-Minnot MJ (2004) Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). International Journal of Parasitology 34: 45–54. https://doi.org/10.1016/j.ijpara.2003.10.005
- Pinadero SJ, Marchán DF, Navarro AM, Tilikj N, Novo N, Domínguez J, Díaz Cosín DJ, Trigo D (2023) Comparative phylogeography and integrative systematic revision of Iberian endemic earthworms (Crassiclitellata, Lumbricidae). Zoologica Scripta 52(4): 345–357. https://doi.org/10.1111/zsc.12586
- Pop V (1941) Zur phylogenie und systematik der Lumbriciden. Zoologische Jahrbücher Abteilung für Systematik, Ökologie und Geographie der Tiere 74: 487–522.
- Popović FJ, Sekulić JM, Trakić TB (2025) Morphological variability, distribution and taxonomic relationships of Dendrobaena illyrica (Cognetti, 1906) (Lumbricidae). Zootaxa 5589(1): 242–247. https://doi.org/10.11646/zootaxa.5589.1.19
- Poulakakis N, Kapli P, Lymberakis P, Trichas A, Vardinoyiannis K, Sfenthourakis S, Mylonas M (2015) A review of phylogeographic analyses of animal taxa from the Aegean and surrounding regions. Journal of Zoological Systematics and Evolutionary Research 53(1): 18–32. https://doi.org/10.1111/jzs.12071
- Rögl F (1999) Mediterranean and Paratetys. Facts and hypotheses of an Oligocene to Miocene paleogeography. Geologia Carpathica 50: 339–349.
- Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
- Schwarz GE (1978) Estimating the dimension of a model. Annals of Statistics 6: 461–464. https://doi.org/10.1214/aos/1176344136
- Shekhovtsov SV, Rapoport IB, Leonov PA, Poluboyarova TV, Yurlova GV, Shipova AA, Vasiliev GV, Golovanova EV, Roohi Aminjan A, Latif R (2024) Phylogeny of Lumbricidae based on mitochondrial genomes with emphasis on the genus Dendrobaena. Organism Diversity & Evolution 24: 477–487. https://doi.org/10.1007/s13127-024-00656-9
- Szederjesi T (2017) The first combined checklist of earthworms of the Northeastern Mediterranean region (Clitellata: Megadrili). Opuscula Zoologica Budapest 48(2): 77–116. https://doi.org/10.18348/opzool.2017.2.77
- Szederjesi T, Csuzdi Cs (2015) A new earthworm species and new records from Albania with remarks on the molecular phylogenetic relationships of the Eisenia species of the Balkan Peninsula (Oligochaeta: Lumbricidae). North-Western Journal of Zoology 11(1): 110–116.
- Szederjesi T, Csuzdi Cs (2016) Review of the species allocated to the genus Satchellius (Oligochaeta: Lumbricidae) with description of a new species. Biologia 71(2): 169–175. https://doi.org/10.1515/biolog-2016-0023
- Szederjesi T, Pop VV, Pavlíček T, Márton O, Krízsik V, Csuzdi Cs (2018) Integrated taxonomy reveals multiple species in the Dendrobaena byblica (Rosa, 1893) complex (Oligochaeta: Lumbricidae). Zoological Journal of the Linnean Society 182(3): 500–516. https://doi.org/10.1093/zoolinnean/zlx049
- Szederjesi T, Pavlíček T, Márton O, Krízsik V, Csuzdi Cs (2019) Integrative taxonomic revision of Dendrobaena veneta (Rosa, 1886) sensu lato with description of a new species and resurrection of Dendrobaena succinta (Rosa, 1905) (Megadrili: Lumbricidae). Journal of Natural History 53(5–6): 301–314. https://doi.org/10.1080/00222933.2019.1593537
- Szederjesi T, Pop AA, Horváth E, Krízsik V, Csuzdi Cs (2025) Remarks on the Dendrobaena alpina (Rosa, 1884) species complex in the Carpathian Basin (Oligochaeta, Lumbricidae). Zootaxa 5589(1): 201–209. https://doi.org/10.11646/zootaxa.5589.1.16
- Tamura K, Stetcher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38(7): 3022–3027. https://doi.org/10.1093/molbev/msab120
- Zhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li WX, Wang GT (2020) PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20(1): 348–355. https://doi.org/10.1111/1755-0998.13096
- Zicsi A (1978) Revision der Art Dendrobaena platyura (Fitzinger, 1833) (Oligochaeta: Lumbricidae). Acta Zoologica Academiae Scientiarum Hungaricae 24: 439–449.
- Zicsi A (1981) Probleme der Lumbriciden-Systematik sowie die Revision zweier Gattungen (Oligochaeta). Acta Zoologica Academiae Scientiarum Hungaricae 27: 431–442.
- Zicsi A, Csuzdi Cs (1986) Regenwürmer aus Bulgarien (Oligochaeta: Lumbricidae). Opuscula Zoologica, Budapest 22: 113–121.
- Zicsi A, Csuzdi Cs (1999) Weitere Angaben zur Regenwurmfauna Frankreichs mit Beschreibung fünf neuer Arten (Oligochaeta: Lumbricidae). Revue Suisse de Zoologie 106: 983–1003. https://doi.org/10.5962/bhl.part.80111
- Zicsi A, Michalis K (1981) Übersicht der Regenwurm-fauna Griechenlands (Oligochaeta: Lumbricidae). Acta Zoologica Academiae Scientiarum Hungaricae 27: 239–264.