Disentangling earthworm taxonomic stumbling blocks using molecular markers
Main Article Content
Abstract
Taxonomic classification of earthworms based on anatomical features has created several challenges for systematics and population genetics. This study examines the application of molecular markers, in particular mitochondrial cytochrome oxidase (COI), to facilitate discrimination of closely related earthworm species. Molecular markers have also provided insights into population genetics by aiding assessment of genetic diversity, lineage sorting, and genealogical distributions of populations for several species. Phylogeography—a study that evaluates the geographical distribution of these genealogical lineages and the role of historical processes in shaping their distribution—has also provided insights into ecology and biodiversity. Such studies are also essential to understand the distribution patterns of invasive earthworm species that have been introduced in non-native ecosystems globally. The negative consequences of these invasions on native species include competition for food resources and altered ecosystems. We anticipate that molecular markers such as COI and DNA barcoding offer potential solutions to disentangling taxonomic impediments in earthworms and advancing their systematics and population genetics.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors own the copyright to the articles published in JoTT. This is indicated explicitly in each publication. The authors grant permission to the publisher Wildlife Information Liaison Development (WILD) Society to publish the article in the Journal of Threatened Taxa. The authors recognize WILD as the original publisher, and to sell hard copies of the Journal and article to any buyer. JoTT is registered under the Creative Commons Attribution 4.0 International License (CC BY), which allows authors to retain copyright ownership. Under this license the authors allow anyone to download, cite, use the data, modify, reprint, copy and distribute provided the authors and source of publication are credited through appropriate citations (e.g., Son et al. (2016). Bats (Mammalia: Chiroptera) of the southeastern Truong Son Mountains, Quang Ngai Province, Vietnam. Journal of Threatened Taxa 8(7): 8953–8969. https://doi.org/10.11609/jott.2785.8.7.8953-8969). Users of the data do not require specific permission from the authors or the publisher.
References
Aspe, N.M., H. Kajihara & S.W. James (2016). A molecular phylogenetic study of pheretimoid species (Megascolecidae) in Mindanao and associated islands, Philippines. European Journal of Soil Biology 73: 119–125. https://doi.org/10.1016/j.ejsobi.2016.02.006
Atopkin, D.M. & G.N. Ganin (2015). Genetic differentiation of black and grey colored forms of the earthworm Drawida ghilarovi Gates, 1969 (Moniligastridae, Oligochaeta) on Russian Far East. European Journal of Soil Biology 67: 12–16. https://doi.org/10.1016/j.ejsobi.2014.12.003
Avise, J.C. (2000). Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, 447 pp.
Avise, J.C., J. Arnold, R.M. Ball, E. Bermingham, T. Lamb, J.E. Neigel, C.A. Reeb & N.C. Saunders (1987). Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology, Evolution and Systematics 18(1): 489–522. https://doi.org/10.1146/annurev.es.18.110187.002421
Bastos, A.D., D. Nair, P.J. Taylor, H. Brettschneider, F. Kirsten, E. Mostert, E. Von Maltitz, J.M. Lamb, P. Van Hooft, S.R. Belmain & G. Contrafatto (2011). Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in South Africa. BMC Genetics 12(1): 1–18. https://doi.org/10.1186/1471-2156-12-26
Beddard, F.E. (1895). A monograph of the order of Oligochaeta. Clarendon press, Oxford, 753 pp. https://doi.org/10.5962/bhl.title.56335
Bely, A.E. & G.A. Wray (2004). Molecular phylogeny of naidid worms (Annelida, Clitellata) based on cytochrome oxidase I. Molecular Phylogenetic Evolution 30(1): 50–63. https://doi.org/10.1016/S1055-7903(03)00180-5
Benham, W.B. (1890). An attempt to classify earthworms. Quarterly Journal of Microscopical Society (NS) 33: 201, 315.
Bickford, D., D.J. Lohman, N.S. Sodhi, P.K. Ng, R. Meier, K. Winker, K.K. Ingram & I. Das (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22(3): 148–155. https://doi.org/10.1016/j.tree.2006.11.004
Blakemore, R.J. (2013). Earthworms newly from Mongolia (Oligochaeta, Lumbricidae, Eisenia). ZooKeys 285: 1–21. https://doi.org/10.3897/zookeys.285.4502
Bohlen, P.J., P.M. Groffman, T.J. Fahey, M.C. Fisk, E. Suárez, D.M. Pelletier & R.T. Fahey (2004a). Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7(1): 1–12. https://doi.org/10.1007/s10021-003-0126-z
Bohlen, P.J., D.M Pelletier, P.M. Groffman, T.J. Fahey & M.C. Fisk (2004b). Influences of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7(1): 13–27. https://doi.org/10.1007/s10021-003-0127-y
Bozorgi, F., M. Seiedy, M. Malek, M. Aira, M. Pérez-Losada & J. Domínguez (2019). Multigene phylogeny reveals a new Iranian earthworm genus (Lumbricidae: Philomontanus) with three new species. PLoS One. 14(1): e0208904. https://doi.org/10.1371/journal.pone.0208904
Buckley, T.R., S. James, J. Allwood, S. Bartlam, R. Howitt & D. Prada (2011). Phylogenetic analysis of New Zealand earthworms (Oligochaeta. Megascolecidae) reveals ancient clades and cryptic taxonomic diversity. Molecular Phylogenetics Evolution 58(1): 85–96. https://doi.org/10.1016/j.ympev.2010.09.024
Cameron, E.K., E.M. Bayne & D.W. Coltman (2008). Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms. Molecular Ecology 17(5): 1189–1197. https://doi.org/10.1111/j.1365-294X.2007.03603.x
Casellato, S. (1987). On polyploidy in Oligochaetes with particular reference to Lumbricids, pp. 75–87. In: Pagliai A.M.B. & P. Omodeo (eds.). On Earthworms. Mucchi, Modena.
Cech, G., C. Csuzdi & K. Marialigeti (2005). Remarks on the molecular phylogeny of the genus Dendrobaena (sensu Pop 1941) based on the investigation of 18S rDNA sequences, pp. 85–98. In: Pop, A.A. & V.V. Pop (eds.). On Advances in Earthworm Taxonomy II (Annelida: Oligochaeta). Cluj University Press, Romania.
Chang, C.H. & J.H. Chen (2005). Taxonomic status and intraspecific phylogeography of two sibling species of Metaphire (Oligochaeta: Megascolecidae) in Taiwan. Pedobiologia 49(6): 591–600. https://doi.org/10.1016/j.pedobi.2005.07.002
Chang, C.H. & S. James (2011). A critique of earthworm molecular phylogenetics. Pedobiologia 54: S3–S9. https://doi.org/10.1016/j.pedobi.2011.07.015
Chang, C.H., S.M. Lin & J.H. Chen (2008). Molecular systematics and phylogeography of the gigantic earthworms of the Metaphire formosae species group (Clitellata:Megascolecidae). Molecular Phylogenetics Evolution 49(3): 958–968. https://doi.org/10.1016/j.ympev.2008.08.025
Chang, C.H., Y.H. Lin, I.H. Chen, S.C. Chuang & J.H. Chen (2007). Taxonomic re-evaluation of the Taiwanese montane earthworm Amynthas wulinensis Tsai, Shen & Tsai, 2001 (Oligochaeta: Megascolecidae): polytypic species or species complex? Organisms Diversity & Evolution 7(3): 231–240. https://doi.org/10.1016/j.ode.2006.06.001
Chang, C.H., R. Rougerie & J.H. Chen (2009). Identifying earthworms through DNA barcodes: Pitfalls and promise. Pedobiologia 52(3): 171–180. https://doi.org/10.1016/j.pedobi.2008.08.002
Cosín, D.J.D., M. Novo, R. Fernández, D.F. Marchán & M. Gutiérrez (2014). A new earthworm species within a controversial genus: Eiseniona gerardoi sp. n. (Annelida: Lumbricidae) description based on morphological and molecular data. ZooKeys 399: 71–87. https://doi.org/10.3897/zookeys.399.7273
Csuzdi, C., C.H. Chang, T. Pavlícek, T. Szederjesi, D. Esopi & K. Szlávecz (2017). Molecular phylogeny and systematics of native North American lumbricid earthworms (Clitellata: Megadrili). PLoS One 12(8): e0181504. https://doi.org/10.1371/journal.pone.0181504
de Faria Siqueira, F., S.H. de Cicco Sandes, M.A. Drumond, S.H. Campos, R.P. Martins, C.G. da Fonseca & M.R.S. Carvalho (2013). Genetic diversity and population genetic structure in giant earthworm Rhinodrilus alatus (Annelida: Clitellata: Glossoscolecidae). Pedobiologia 56(1): 15–21. https://doi.org/10.1016/j.pedobi.2012.08.006
Decaëns, T., D. Porco, S.W. James, G.G. Brown, V. Chassany, F. Dubs, L. Dupont, E. Lapied, R. Rougerie, J.P. Rossi & V. Roy (2016). DNA barcoding reveals diversity patterns of earthworm communities in remote tropical forests of French Guiana. Soil Biology & Biochemistry 92: 171–183. https://doi.org/10.1016/j.soilbio.2015.10.009
Decaëns, T., D. Porco, R. Rougerie, G.G. Brown & S.W. James (2013). Potential of DNA barcoding for earthworm research in taxonomy and ecology. Applied Soil Ecology 65: 35–42. https://doi.org/10.1016/j.apsoil.2013.01.001
Des Roches, S., D.M. Post, N.E. Turley, J.K. Bailey, A.P. Hendry, M.T. Kinnison, J.A. Schweitzer & E.P. Palkovacs (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution 2(1): 57–64. https://doi.org/10.1038/s41559-017-0402-5
Dobzhansky, T. (1973). Nothing in Biology makes Sense Except in the light of Evolution. The American Biology Teacher 35: 125–129. https://doi.org/10.2307/4444260
Domínguez, J., M. Aira, J.W. Breinholt, M. Stojanovic, S.W. James & M. Pérez-Losada (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., M. Aira, P.G. Porto, D.J. Díaz Cosín & M. Pérez-Losada (2017). 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
Dong, Y., J. Jiang, Z. Yuan, Q. Zhao & J. Qiu (2020). Population genetic structure reveals two lineages of Amynthas triastriatus (Oligochaeta: Megascolecidae) in China, with notes on a new subspecies of Amynthas triastriatus. International Journal of Environmental Research and Public Health 17(5): 1538. https://doi.org/10.3390/ijerph17051538
Donnelly, R.K., G.L. Harper, A.J. Morgan, G.A. Pinto-Juma & M.W. Bruford (2014). Mitochondrial DNA and morphological variation in the sentinel earthworm species Lumbricus rubellus. European Journal of Soil Biology 64: 23–29. https://doi.org/10.1016/j.ejsobi.2014.07.002
Edwards, C.A. (2004). Earthworm Ecology. CRC Press, Boca Raton, 456pp. https://doi.org/10.1201/9781420039719
Enckell, P.H., M. Niklasson, B. Stille & P. Douwes (1986). Insulation and isolation: factors influencing the genetic variation in Lumbricus rubellus Hoffm. (Lumbricidae) in the Faroe Islands. Hereditas 104(2): 263–271. https://doi.org/10.1111/j.1601-5223.1986.tb00540.x
Erséus, C. (2005). Phylogeny of oligochaetous Clitellata. Hydrobiologia 535(1): 357–372.
Escudero, G.J., J. Lagerlöf, C.M. Debat & P.C. Alberto (2019). Identification of earthworm species in Uruguay based on morphological and molecular methods. Agrociencia 23(1): 37–46. https://doi.org/10.31285/AGRO.23.1.12
Fernández, R., A. Almodóvar, M. Novo, M. Gutiérrez & D.J.D. Cosín (2011). A vagrant clone in a peregrine species: phylogeography, high clonal diversity and geographical distribution in the earthworm Aporrectodea trapezoides (Dugès, 1828). Soil Biology and Biochemistry 43(10): 2085–2093. https://doi.org/10.1016/j.soilbio.2011.06.007
Fernández, R., A. Almodóvar, M. Novo, B. Simancas & D.J.D. Cosín (2012). Adding complexity to the complex: new insights into the phylogeny, diversification and origin of parthenogenesis in the Aporrectodea caliginosa species complex (Oligochaeta, Lumbricidae). Molecular Phylogenetics and Evolution 64(2): 368–379. https://doi.org/10.1016/j.ympev.2012.04.011
Fernández, R., M. Novo, D.F. Marchán & D.J.D. Cosín (2016). Diversification patterns in cosmopolitan earthworms: similar mode but different tempo. Molecular Phylogenetics and Evolution 94: 701–708. https://doi.org/10.1016/j.ympev.2015.07.017
Folino-Rorem, N.C., J.A. Darling & C.A. D’Ausilio (2009). Genetic analysis reveals multiple cryptic invasive species of the hydrozoan genus Cordylophora. Biological Invasions 11(8): 1869–1882. https://doi.org/10.1007/s10530-008-9365-4
Frelich, L.E., C.M. Hale, P.B. Reich, A.R. Holdsworth, S. Scheu, L. Heneghan & P.J. Bohlen (2006). Earthworm invasion into previously earthworm-free temperate and boreal forests. Biological invasions 8: 1235–1245. https://doi.org/10.1007/978-1-4020-5429-7_5
Ganin, G.N. & D.M. Atopkin (2018). Molecular differentiation of epigeic and anceic forms of Drawida ghilarovi Gates, 1969 (Moniligastridae, Clitellata) in the Russian Far East: Sequence data of two mitochondrial genes. European Journal of Soil Biology 86: 1–7. https://doi.org/10.1016/j.ejsobi.2018.02.004
Giska, I., P. Sechi & W. Babik (2015). Deeply divergent sympatric mitochondrial lineages of the earthworm Lumbricus rubellus are not reproductively isolated. BMC Evolutionary Biology 15(1): 1–13. https://doi.org/10.1186/s12862-015-0488-9
Gregory, T.R. (2005). DNA barcoding does not compete with taxonomy. Nature 434(7037): 1067–1067. https://doi.org/10.1038/4341067b
Hebert, P.D., A. Cywinska, S.L. Ball & J.R. Dewaard (2003). Biological identifications through DNA barcodes. Proceeding of Royal Society of London 270(1512): 313–321. https://doi.org/10.1098/rspb.2002.2218
Hebert, P.D., M.Y. Stoeckle, T.S. Zemlak & C.M. Francis (2004). Identification of birds through DNA barcodes. PLoS Biology 2(10): 312. https://doi.org/10.1371/journal.pbio.0020312
Heethoff, M., K. Etzold & S. Scheu (2004). Mitochondrial COI sequences indicate that the parthenogenetic earthworm Octolasion tyrtaeum (Savigny 1826) constitutes of two lineages differing in body size and genotype. Pedobiologia 48(1): 9–13. https://doi.org/10.1016/j.pedobi.2003.04.001
Hendrix, P.F. & P.J. Bohlen (2002). Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52(9): 801–811. https://doi.org/10.1641/0006-3568(2002)052[0801:EEIINA]2.0.CO;2
Hogg, I.D., M.L. Stevens, K.E. Schnabel & M. Chapman (2006). Deeply divergent lineages of the widespread New Zealand amphipod Paracalliope fluviatilis revealed using allozyme and mitochondrial DNA analyses. Freshwater Biology 51(2): 236–248. https://doi.org/10.1111/j.1365-2427.2005.01491.x
Hong, Y. & C. Csuzdi (2016). New data to the earthworm fauna of the Korean peninsula with redescription of Eisenia koreana (Zicsi) and remarks on the Eisenia nordenskioldi species group (Oligochaeta, Lumbricidae). Zoological Studies 55: 1–15. http://doi.org/10.6620/ZS.2016.55-12
Huang, J., Q. Xu, Z.J. Sun, G.L. Tang & Z.Y. Su (2007). Identifying earthworms through DNA barcodes. Pedobiologia 51(4): 301–309. https://doi.org/10.1016/j.pedobi.2007.05.003
Huhta, V. (1979). Effects of liming and deciduous litter on earthworm (Lumbricidae) populations of a apruce forest, with an inoculation experiment on Allobophora caliginosa. Pedobiologia 19: 340-345.
Hulme, P.E., D.B. Roy, T. Cunha & T.B. Larsson (2009). A pan-European inventory of alien species: rationale, implementation and implications for managing biological invasions, pp. 1-14. In: Dais, I.E. (ed.). Handbook of Alien Species in Europe. Springer, Netherlands. https://doi.org/10.1007/978-1-4020-8280-1_1
James, S.W., D. Porco, T. Decaëns, B. Richard, R. Rougerie & C. Erséus (2010). DNA barcoding reveals cryptic diversity in Lumbricus terrestris L., 1758 (Clitellata): resurrection of L. herculeus (Savigny, 1826). PLoS One 5(12): e15629. https://doi.org/10.1371/journal.pone.0015629
Jamieson, B.G. (1988). On the phylogeny and higher classification of the Oligochaeta. Cladistics 4(4): 367–401. https://doi.org/10.1111/j.1096-0031.1988.tb00520.x
Jamieson, B.G., S. Tillier, A. Tillier, J.L. Justine, E. Ling, S. James, K. McDonald & A.F. Hugall (2002). Phylogeny of the Megascolecidae and Crassiclitellata (Annelida, Oligochaeta): combined versus partitioned analysis using nuclear (28S) and mitochondrial (12S, 16S) rDNA. Zoosystema 24(4): 707–734. http://doi.org/10.5281/zenodo.4524860
Jeratthitikul, E., U. Bantaowong & S. Panha (2017). DNA barcoding of the Thai species of terrestrial earthworms in the genera Amynthas and Metaphire (Haplotaxida: Megascolecidae). European Journal of Soil Biology 81: 39–47. https://doi.org/10.1016/j.ejsobi.2017.06.004
Jirapatrasilp, P., P. Prasankok, C. Sutcharit, R. Chanabun & S. Panha (2016). Two new Cambodian semi-aquatic earthworms in the genus Glyphidrilus Horst, 1889 (Oligochaeta, Almidae), based on morphological and molecular data. Zootaxa 4189(3): 543–558. https://doi.org/10.11646/zootaxa.4189.3.5
Kautenburger, R. (2006). Genetic structure among earthworms (Lumbricus terrestris L.) from different sampling sites in western Germany based on random amplified polymorphic DNA. Pedobiologia 50(3): 257–266. https://doi.org/10.1016/j.pedobi.2006.02.005
King, R.A., A.L. Tibble & W.O. Symondson (2008). Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricid earthworms. Molecular Ecology 17(21): 4684–4698. https://doi.org/10.1111/j.1365-294X.2008.03931.x
Klarica, J., A. Kloss-Brandstätter, M. Traugott & A. Juen (2012). Comparing four mitochondrial genes in earthworms-Implications for identification, phylogenetics, and discovery of cryptic species. Soil Biology and Biochemistry 45: 23–30. https://doi.org/10.1016/j.soilbio.2011.09.018
Kumari, N. & S.K. Thakur (2014). Randomly amplified polymorphic DNA-a brief review. American Journal of Animal and Veterinary Sciences 9(1): 6–13. http://doi.org/10.3844/ajavsp.2014.6.13
Lalthanzara, H., R. Lalfelpuii, C. Zothansanga, M. Vabeiryureilai, N.S. Kumar & G. Gurusubramanium (2018). Oligochaete taxonomy–The rise of earthworm DNA barcode in India. Science Vision 18(1): 1–10. https://doi.org/10.33493/scivis.18.01.01
Lalthanzara, H., C. Zothansanga, M. Lalchhanhima, N.S. Kumar, J. Ngukir, A. Kimsing & M. Vabeiryureilai (2020). Diversity and New Records of Earthworms in Arunachal Pradesh, Northeast India. Journal of Environmental Biology 41(4): 874–883. http://doi.org/10.22438/jeb/4(SI)/MS_1921
Lavelle, P., L. Brussaard & P. Hendrix (Eds.) (1999). Earthworm Management in Tropical Agroecosystems. CABI Publishing, New York, 300 pp.
Liu, Y., S.V. Fend, S. Martinsson, X. Luo, A. Ohtaka & C. Erséus (2017). Multi-locus phylogenetic analysis of the genus Limnodrilus (Annelida: Clitellata: Naididae). Molecular Phylogenetics and Evolution 112: 244–257. https://doi.org/10.1016/j.ympev.2017.04.019
Lone, A.R., N. Tiwari, S.S. Thakur, O. Pearlson, T. Pavlíček & S. Yadav (2020). Exploration of four new Kanchuria sp. of earthworms (Oligochaeta: Megascolecidae) from the North Eastern Region of India using DNA bar-coding approach. Journal of Asia-Pacific Biodiversity 13(2): 268–281. https://doi.org/10.1016/j.japb.2020.02.004
Maekawa, K., M. Kon, K. Araya & T. Matsumoto (2001). Phylogeny and biogeography of wood-feeding cockroaches, genus Salganea Stål (Blaberidae: Panesthiinae), in southeast Asia based on mitochondrial DNA sequences. Journal of Molecular Evolution 53(6): 651–659. https://doi.org/10.1007/s002390010252
Marchán, D.F., R. Fernández, M. Novo & D.J.D. Cosín (2014). New light into the hormogastrid riddle: morphological and molecular description of Hormogaster joseantonioi sp. n. (Annelida, Clitellata, Hormogastridae). ZooKeys 414: 1–17. http://doi.org/10.3897/zookeys.414.7665
Marchán, D.F., R. Fernández, I. de Sosa, D.J.D. Cosin & M. Novo (2017). Pinpointing cryptic borders: fine-scale phylogeography and genetic landscape analysis of the Hormogaster elisae complex (Oligochaeta, Hormogastridae). Molecular Phylogenetics and Evolution 112: 185–193. https://doi.org/10.1016/j.ympev.2017.05.005
Martin, P., I. Kaygorodova, D.Y. Sherbakov & E. Verheyen (2000). Rapidly evolving lineages impede the resolution of phylogenetic relationships among Clitellata (Annelida). Molecular Phylogenetics and Evolution 15(3): 355–368. https://doi.org/10.1006/mpev.1999.0764
Martinsson, S. & C. Erséus (2014). Cryptic diversity in the well-studied terrestrial worm Cognettia sphagnetorum (Clitellata: Enchytraeidae). Pedobiologia 57(1): 27–35. https://doi.org/10.1016/j.pedobi.2013.09.006
Martinsson, S. & E. Erséus (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
McHugh, D. (2001). Molecular phylogenetic analyses indicate a rapid radiation of polychaete annelids. American Zoologist 41: 1520–1521
Michaelsen, W. (1900). Das Tierreich 10: Vermes, Oligochaeta. Friedländer and Sohn, Berlin, 575 pp.
Minamiya, Y., J. Yokoyama & T. Fukuda (2009). A phylogeographic study of the Japanese earthworm, Metaphire sieboldi (Horst, 1883) (Oligochaeta: Megascolecidae): Inferences from mitochondrial DNA sequences. European Journal of Soil Biology 45(5–6): 423–430. https://doi.org/10.1016/j.ejsobi.2009.06.004
Novo, M., A. Almodóvar & D.J. Díaz‐Cosín (2009). High genetic divergence of hormogastrid earthworms (Annelida, Oligochaeta) in the central Iberian Peninsula: evolutionary and demographic implications. Zoologica Scripta 38(5): 537–552. https://doi.org/10.1111/j.1463-6409.2009.00389.x
Novo, M., A. Almodóvar, R. Fernández, D. Trigo & D.J.D. Cosín (2010). Cryptic speciation of hormogastrid earthworms revealed by mitochondrial and nuclear data. Molecular Phylogenetics and Evolution 56(1): 507–512. https://doi.org/10.1016/j.ympev.2010.04.010
Novo, M., A. Almodóvar, R. Fernández, G. Giribet & D.J.D. Cosín (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
Novo, M., R. Fernández, D.F. Marchan, D. Trigo, D.J.D. Cosin & G. Giribet (2015a). Unearthing the historical biogeography of Mediterranean earthworms (Annelida: hormogastridae). Journal of Biogeography 42(4): 751–762. https://doi.org/10.1111/jbi.12447
Novo, M., L. Cunha, A. Maceda-Veiga, J.A. Talavera, M.E. Hodson, D. Spurgeon, M.W. Bruford, A.J. Morgan & P. Kille (2015b). Multiple introductions and environmental factors affecting the establishment of invasive species on a volcanic island. Soil Biology and Biochemistry 85: 89–100. https://doi.org/10.1016/j.soilbio.2015.02.031
O’Grady, P.M. & R. DeSalle (2018). Phylogeny of the genus Drosophila. Genetics 209(1): 1–25. https://doi.org/10.1534/genetics.117.300583
Otomo, P.V., B.J.V. Vuuren & S.A. Reinecke (2009). Usefulness of DNA barcoding in ecotoxicological investigations: resolving taxonomic uncertainties using Eisenia as an example. Bulletin of Environmental Contamination and Toxicology 82(3): 261–264. https://doi.org/10.1007/s00128-008-9585-4
Pejchar, L. & H.A. Mooney (2009). Invasive species, ecosystem services and human well-being. Trends in Ecology and Evolution 24(9): 497–504. https://doi.org/10.1016/j.tree.2009.03.016
Pérez-Losada, M., J. Eiroa, S. Mato & J. Domínguez (2005). Phylogenetic species delimitation of the earthworms Eisenia fetida (Savigny, 1826) and Eisenia Andrei Bouche´, 1972 (Oligochaeta, Lumbricidae) based on mitochondrial and nuclear DNA sequence. Pedobiologia 49(4): 317–324. https://doi.org/10.1016/j.pedobi.2005.02.004
Pérez-Losada, M., M. Ricoy, J.C. Marshall & J. Domínguez (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., M. Wink & V.V. Pop (2003). Use of 18S, 16S rDNA and cytochrome c oxidase sequences in earthworm taxonomy (Oligochaeta, Lumbricidae): The 7th international symposium on earthworm ecology Cardiff· Wales. Pedobiologia 47(5–6): 428–433. https://doi.org/10.1078/0031-4056-00208
Pop, A.A. & M. Wink (2004). Molecular taxonomy and phylogeny of earthworms (Oligochaeta, Lumbricidae): 16S rDNA and COI gene corroborate numerical taxonomy in the genus Octodrilus, Omode, 1956, pp. 347–360. In: Moreno A.G. & S. Borges (eds.). Advances in Taxonomy of Closing Worms. Advances in Earthworm Taxonomy. Editorial Complutense, Madrid.
Pop, A.A., G. Cech, M. Wink, C. Csuzdi & V.V. Pop (2007). Application of 16S, 18S rDNA and COI sequences in the molecular systematics of the earthworm family Lumbricidae (Annelida, Oligochaeta). European Journal of Soil Biology 43: S43–S52. https://doi.org/10.1016/j.ejsobi.2007.08.007
Pop, A.A., C. Csuzdi, M. Wink & V.V. Pop (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, pp. 109–128. In: Pavlicek, T. & P. Cardet (eds.). Advances in Earthworm Taxonomy III (Annelida: Oligochaeta). Nicosia, Cyprus.
Porco, D., T. Decaëns, L. Deharveng, S.W. James, D. Skarżyński, C. Erséus, K.R. Butt, B. Richard & P.D. Hebert (2013). Biological invasions in soil: DNA barcoding as a monitoring tool in a multiple taxa survey targeting European earthworms and springtails in North America. Biological Invasions 15(4): 899–910. https://doi.org/10.1007/s10530-012-0338-2
Proudlove, G. & P.J. Wood (2003). The blind leading the blind: cryptic subterranean species and DNA taxonomy. Trends in Ecology and Evolution 6(18): 272–273. http://doi.org/10.1016/S0169-5347(03)00095-8
Qiu, J. (2015). A global synthesis of the effects of biological invasions on greenhouse gas emissions. Global Ecology and Biogeography 24(11): 1351–1362. https://doi.org/10.1111/geb.12360
Richard, B., T. Decaëns, R. Rougerie, S.W. James, D. Porco & P.D.N. Hebert (2010). Re-integrating earthworm juveniles into soil biodiversity studies: species identification through DNA barcoding. Molecular Ecology Resources 10(4): 606–614. https://doi.org/10.1111/j.1755-0998.2009.02822.x
Römbke, J., M. Aira, T. Backeljau, K. Breugelmans, J. Domínguez, E. Funke, N. Graf, M. Hajibabaei, M. Pérez-Losada, P.G. Porto & R.M. Schmelz (2016). DNA barcoding of earthworms (Eisenia fetida/andrei complex) from 28 ecotoxicological test laboratories. Applied Soil Ecology 104: 3–11. https://doi.org/10.1016/j.apsoil.2015.02.010
Rougerie, R., T. Decaëns, L. Deharveng, D. Porco, S.W. James, C.H. Chang, B. Richard, M. Potapov, Y. Suhardjono & P.D.N. Hebert (2009). DNA barcodes for soil animal taxonomy. Pesquisa Agropecuária Brasileira 44(8): 789–802. https://doi.org/10.1590/S0100-204X2009000800002
Sakai, A.K., F.W. Allendorf, J.S. Holt, D.M. Lodge, J. Molofsky, K.A. With, S. Baughman, R.J. Cabin, J.E. Cohen, N.C. Ellstrand & D.E. McCauley (2001). The population biology of invasive species. Annual Review of Ecology and Systematics 32(1): 305–332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037
Schult, N., K. Pittenger, S. Davalos & D. McHugh (2016). Phylogeographic analysis of invasive Asian earthworms (Amynthas) in the northeast United States. Invertebrate Biology 135(4): 314–327.
Seesamut, T., C. Sutcharit, P. Jirapatrasilp, R. Chanabun & S. Panha (2018). Morphological and molecular evidence reveal a new species of the earthworm genus Pontodrilus Perrier, 1874 (Clitellata, Megascolecidae) from Thailand and Peninsular Malaysia. Zootaxa 4496(1): 218–237. https://doi.org/10.11646/zootaxa.4496.1.18
Shekhovtsov, S.V., E.V. Golovanova & S.E. Peltek (2013). Cryptic diversity within the Nordenskiold’s earthworm, Eisenia nordenskioldi subsp. nordenskioldi (Lumbricidae, Annelida). European Journal of Soil Biology 58: 13–18. https://doi.org/10.1016/j.ejsobi.2013.05.004
Shekhovtsov, S.V., E.V. Golovanova & S.E. Peltek (2014). Invasive lumbricid earthworms of Kamchatka (Oligochaeta). Zoological Studies 53(1): 1–15. https://doi.org/10.1186/s40555-014-0052-0
Shekhovtsov, S.V., D.I. Berman, N.E. Bazarova, N.A. Bulakhova, D. Porco & S.E. Peltek (2016a). Cryptic genetic lineages in Eisenia nordenskioldi pallida (Oligochaeta, Lumbricidae). European Journal of Soil Biology 75: 151–156. https://doi.org/10.1016/j.ejsobi.2016.06.004
Shekhovtsov, S.V., E.V. Golovanova & S.E. Peltek (2016b). Mitochondrial DNA variation in Eisenia n. nordenskioldi (Lumbricidae) in Europe and Southern Urals. Mitochondrial DNA 27(6): 4643–4645. https://doi.org/10.3109/19401736.2015.1101594
Shekhovtsov, S.V., Golovanova, E.V & S.E. Peltek (2016c). Different dispersal histories of lineages of the earthworm Aporrectodea caliginosa (Lumbricidae, Annelida) in the Palearctic. Biological Invasions 18(3): 751–761. http://doi.org/10.1007/s10530-015-1045-6
Shekhovtsov, S.V., D.I. Berman, N.A. Bulakhova, O.L. Makarova & S.E. Peltek (2018a). Phylogeography of earthworms from high latitudes of Eurasia. Acta Zoologica Academiae Scientiarum Hungaricae 64(4): 369–382. http://doi.org/10.17109/AZH.64.4.369.2018
Shekhovtsov, S.V., D.I. Berman, N.A. Bulakhova, N.N. Vinokurov & S.E. Peltek
(2018b). Phylogeography of Eisenia nordenskioldi nordenskioldi (Lumbricidae, Oligochaeta) from the north of Asia. Polar Biology 41(2): 237–247. https://doi.org/10.1007/s00300-017-2184-2
Siddall, M.E., K. Apakupakul, E.M. Burreson, K.A. Coates, C. Erséus, S.R. Gelder, M. Källersjö & H. Trapido-Rosenthal (2001). Validating Livanow: molecular data agree that leeches, Branchiobdellidans and Acanthobdella peledina form a monophyletic group of Oligochaetes. Molecular Biology and Evolution 21(3): 346–351. https://doi.org/10.1006/mpev.2001.1021
Stange, M., R.D. Barrett & A.P. Hendry (2020). The importance of genomic variation for biodiversity, ecosystems and people. Nature Reviews Genetics 1–17. https://doi.org/10.1038/s41576-020-00288-7
Su, Z.H., Y. Imura & S. Osawa (2001). Evolutionary discontinuity of the carabine ground beetles. Journal of Molecular Evolution 53(4-5): 517–529. https://doi.org/10.1007/s002390010242
Szederjesi, T., V.V. Pop, T. PavlÍČek, O. MÁrton, V. KrÍzsik & C. Csuzdi (2018). Integrated taxonomy reveals multiple species in the Dendrobaena byblica (Rosa, 1893) complex (Oligochaeta: Lumbricidae). Zoological Journal of the Linnaean Society 182(3): 500–516. https://doi.org/10.1093/zoolinnean/zlx049
Terhivuo, J. & A. Saura (1993). Genic and morphological variation of the parthenogenetic earthworm Aporrectodea rosea in southern Finland (Oligochaeta, Lumbricidae). Annales zoologici fennici 30(12): 215–224. http://www.jstor.org/stable/23735649
Terhivuo, J. & A. Saura (1997). Island biogeography of North European parthenogenetic Lumbricidae: I. Clone pool affinities and morphometric differentiation of Åland populations. Ecography 20(2): 185–196. https://doi.org/10.1111/j.1600-0587.1997.tb00361.x
Thakur, S.S., A.R. Lone, N. Tiwari & S. Yadav (2020). Exploring new records of Eutyphoeus sp.(haplotaxida: Octochaetidae) from garo hills, Meghalaya, North Eastern state of India with use of DNA barcodes. Mitochondrial DNA Part A 31(7): 265–272. https://doi.org/10.1080/24701394.2020.1781834
Tiwari, N., A.R. Lone, S.S. Thakur & S. Yadav (2020). Interrogation of earthworm (Clitellata: Haplotaxida) taxonomy and the DNA sequence database. Journal of Asia-Pacific Biodiversity 14(1): 40–52. https://doi.org/10.1016/j.japb.2020.09.015
Torres-Leguizamon, M., J. Mathieu, T. Decaens & L. Dupont (2014). Genetic structure of earthworm populations at a regional scale: inferences from mitochondrial and microsatellite molecular markers in Aporrectodea icterica (Savigny 1826). PLoS One 9(7): e101597. https://doi.org/10.1371/journal.pone.0101597
Tsutsui, N.D., A.V. Suarez, D.A. Holway & T.J. Case (2000). Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences 97(11): 5948–5953. https://doi.org/10.1073/pnas.100110397
Vabeiryureilai, M., C. Zothansanga, M. Lalchhanhima, N.S. Kumar & H. Lalthanzara (2020). Study on the Amynthas (Kinberg, 1867) earthworm (Megascolecidae: Oligochaeta) diversity through DNA barcoding from Northeast India. Journal of Environmental Biology 41(4): 867–873. http://doi.org/10.22438/jeb/4(SI)/MS_1919
Vilà, M., J.L. Espinar, M. Hejda, P.E. Hulme, V. Jarošík, J.L. Maron, J. Pergl, U. Schaffner, Y. Sun & P. Pyšek (2011). Ecological impacts of invasive alien plants: a meta‐analysis of their effects on species, communities and ecosystems. Ecology Letters 14(7): 702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x
Vivien, R., S. Wyler, M. Lafont & J. Pawlowski (2015). Molecular barcoding of aquatic oligochaetes: Implications for biomonitoring. PLoS One 10(4): e0125485. https://doi.org/10.1371/journal.pone.0125485
Voua Otomo, P., M.S. Maboeta & C. Bezuidenhout (2013). Inadequate taxonomy and highly divergent COI haplotypes in laboratory and field populations of earthworms used in ecotoxicology: a case study. African Zoology 48(2): 290–297. https://hdl.handle.net/10520/EJC145793
Wishart, M.J. & J.M. Hughes (2003). Genetic population structure of the net-winged midge, Elporia barnardi (Diptera: Blephariceridae) in streams of the southwestern Cape, South Africa. Implications for dispersal. Freshwater Biology 48(1): 28–38. https://doi.org/10.1046/j.1365-2427.2003.00958.x
Yassin, A., P. Capy, L. Madi‐Ravazzi, D. Ogereau & J.R. David (2008). DNA barcode discovers two cryptic species and two geographical radiations in the invasive Drosophilid zaprionus indianus. Molecular Ecology Resources 8(3): 491–501. https://doi.org/10.1111/j.1471-8286.2007.02020.x
Zhang, L., P. Sechi, M. Yuan, J. Jiang, Y. Dong & J. Qiu (2016). Fifteen new earthworm mitogenomes shed new light on phylogeny within the Pheretima complex. Scientific Reports 6(1): 1–11. https://doi.org/10.1038/srep20096
Zhao, Q., D. Cluzeau, J.B. Jiang, E.J. Petit, C. Briard, J. Sun, A. Prinzing & J.P. Qiu (2015). Molecular Phylogeny of Pheretimoid Earthworms (Haplotaxina: Megascolecidae) Based on Mitochondrial DNA in Hainan Island, China. Molecular Biology 4(4): 1–16. http://doi.org/10.4172/2168-9547.1000138