Published April 22, 2026
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A new species of the genus Metaphire (Oligochaeta, Megascolecidae) from northern China with data from the mitochondrial genome
Authors/Creators
- 1. College of Life Science, Shenyang Normal University, Shenyang, China|College of Life Science, Langfang Normal University, Langfang, China
- 2. College of Life Science, Langfang Normal University, Langfang, China
- 3. College of Environment and Life Sciences, Mindanao State University at Naawan, Naawan, Philippines
- 4. Langfang Ecological Environment Monitoring Center of Hebei Province, Langfang, China
- 5. College of Life Science, Shenyang Normal University, Shenyang, China
Description
This study describes a new species, Metaphire wenanensis Liu & Zhao, sp. nov. integrating morphological characters and molecular data. The new species is assigned to the M. houlleti group, and is characterized by three pairs of spermathecal pores at 6/7–8/9, and absence of genital markings both anterior and posterior to the clitellum. The spermathecae are connected to the body wall through a disc-shaped atrium, which is interposed between them and the body wall. The molecular phylogenetic position of M. wenanensis Liu & Zhao, sp. nov. within the M. houlleti group was analyzed using mitochondrial genome data. This marks the initial documentation of a new species within the family Megascolecidae in northern China since the last decades.
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References
- Bantaowong U, Chanabun R, James SW, Panha S (2016) Seven new species of the earthworm genus Metaphire Sims & Easton, 1972 from Thailand (Clitellata: Megascolecidae). Zootaxa 4117: 63–84. https://doi.org/10.11646/zootaxa.4117.1.3
- Bely AE, Wray GA (2004) Molecular phylogeny of naidid worms (Annelida: Clitellata) based on cytochrome oxidase I. Molecular Phylogenetics and Evolution 30: 50–63. https://doi.org/10.1016/s1055-7903(03)00180-5
- Bi Y, Fan Y, Cheng X, Li N, Wang S, Zhang H, Zhang Y, Zhao H (2025) Earthworm Diversity of Tianjin, China. Chinese Journal of Soil Science 56: 1–8. https://doi.org/10.19336/j.cnki.trtb.2025012201
- Chang C-H, Chen J-H (2005) Taxonomic status and intraspecific phylogeography of two sibling species of Metaphire (Oligochaeta: Megascolecidae) in Taiwan. Pedobiologia 49: 591–600. https://doi.org/10.1016/j.pedobi.2005.07.002
- Chang C-H, James S (2011) A critique of earthworm molecular phylogenetics. Pedobiologia 54: S3–S9. https://doi.org/10.1016/j.pedobi.2011.07.015
- Chang C-H, Lin S-M, Chen J-H (2008) Molecular systematics and phylogeography of the gigantic earthworms of the Metaphire formosae species group (Clitellata, Megascolecidae). Molecular Phylogenetics and Evolution 49: 958–968. https://doi.org/10.1016/j.ympev.2008.08.025
- Chang C-H, Lin Y-H, Chen IH, Chuang S-C, Chen J-H (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: 231–240. https://doi.org/10.1016/j.ode.2006.06.001
- Chang C-H, Rougerie R, Chen J-H (2009) Identifying earthworms through DNA barcodes: Pitfalls and promise. Pedobiologia 52: 171–180. https://doi.org/10.1016/j.pedobi.2008.08.002
- Chen Y, Xu Z, Yang T, Feng X (1975) On some new earthworms from China. Acta Zoologica Sinica 21: 89–99.
- Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
- Dong Y, Jiang J, Zhang J, Shen Z, Sun J (2024) Three New Earthworm Species of the Genus Metaphire (Oligochaeta: Megascolecidae) From Eastern and Southern China. Chinese Journal of Zoology 59: 397–407. https://doi.org/10.13859/j.cjz.202423079
- Drummond A, Suchard M, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29(8): 1969–1973. https://doi.org/10.1093/molbev/mss075
- Ezard TH, Fujisawa T, Barraclough TG (2017) split: Species Limits and Phylogenetic Analysis (Version 1.0-19) [R Package].
- Feng X (1984) A new subspecies of terrestrial Oligochaeta from Lanzhou, Kansu Province. Zoological Research 5: 47–50.
- Feng X, Ma Z (1987) Notes on a new species of the genus Metaphire from Gansu Province, China (Oligochaeta: Megascolecidae). Acta Zootaxonomica Sinica 12: 248–250.
- Folmer 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
- Fujisawa T, Barraclough TG (2013) Delimiting Species Using Single-Locus Data and the Generalized Mixed Yule Coalescent Approach: A Revised Method and Evaluation on Simulated Data Sets. Systematic Biology 62(5): 707–724. https://doi.org/10.1093/sysbio/syt033
- Goulpeau A, Penel B, Maggia M-E, Marchán DF, Steinke D, Hedde M, Decaëns T (2022) OTU Delimitation with Earthworm DNA Barcodes: A Comparison of Methods. Diversity 14: 866. https://doi.org/10.3390/d14100866
- Han ACN (2025) Integrative Taxonomy and Distribution of Pheretimoid Earthworms in Northeastern China. Master thesis. Northeast Normal University. [In English]
- Han ACN, Zhang Y, Miao P, Wu S, Xiao N, Qin M, Zhao H, Wu D, Aspe NM (2024) Distribution and systematics of the cosmopolitan Amynthas carnosus complex (Crassiclitellata, Megascolecidae) from eastern Asia. Zoosystematics and Evolution 100: 1061–1073. https://doi.org/10.3897/zse.100.119292
- Han CAN, Zhao N, Aspe NM, Nob CJR, Zhang Y, Wu D, Zhao H (2026) A new species of the Amynthas corticis group with support from mitogenomic data and a new record of Metaphire agrestis (Goto & Hatai, 1899) (Oligochaeta, Megascolecidae) in northeastern China. ZooKeys 1266: 231–261. https//doi.org/10.3897/zookeys.1266.161903
- Huang J, Xu Q, Sun Z, Wang C, Zheng D (2006) Research on earthworm resources of China: I. Checklist and distribution. Journal of China Agricultural University: 9–20.
- Hudson RR (1991) Gene genealogies and the coalescent process. In: Futuyma D, Antonovics J (Eds) Oxford Surveys in Evolutionary Biology. Oxford University Press, New York, 1–44.
- Jeratthitikul E, Bantaowong U, Panha S (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
- Jiang J (2016) Taxonomy and molecular phylogeny of the family Megascolecidae earthworms from China. Doctoral dissertation, Shanghai Jiao Tong University. [In Chinese with English abstract]
- Jiang J, Qiu J (2018) Origin and evolution of earthworms belonging to the family Megascolecidae in China. Biodiversity Science 26: 1074–1082. https://doi.org/10.17520/biods.2018105
- Jiang J, Qiu J (2024) The Resource and Conservation of Earthworms in China. Science China 76: 47–52.
- Jin Q, Li J, Jiang J, Qiu J (2024) Four new earthworm species of the genera Amynthas and Metaphire (Oligochaeta, Megascolecidae) from Hunan and Anhui provinces, China. ZooKeys 1210: 247–271. https://doi.org/10.3897/zookeys.1210.125963
- Kim D, Lee K, Jee S, Seo S, Park S, Choo J (2005) Complete sequence analysis of the mitochondrial genome in the earthworm, Perionyx excavatus. Integrative Biosciences 9: A705.
- Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120. https://doi.org/10.1007/bf01731581
- Koo J, Hong Y (2023) The complete mitochondrial genome of the Korean endemic earthworm Amynthas deogyusanensis (Clitellata: Megascolecidae). Mitochondrial DNA Part B 8: 107–109. https://doi.org/10.1080/23802359.2022.2161839
- Liu M, Li J, Zhang Y, Aspe NM, Wu D, Zhao H, Zheng G (2025a) A new species of the Drawida ghilarovi species complex (Oligochaeta, Moniligastridae) in Changbai Mountain, Northeast China. Zoosystematics and Evolution 101: 627–641. https://doi.org/10.3897/zse.101.146587
- Liu M, Miao P, Liu Z, Aspe NM, Zhang Y, Zhao H (2025b) Two new species of the Drawida japonica species complex (Oligochaeta, Moniligastridae) from East Asia delimited by integrative taxonomic methods. ZooKeys 1264: 377–402. https://doi.org/10.3897/zookeys.1264.170881
- Meng G, Li Y, Yang C, Liu S (2019) MitoZ: a toolkit for animal mitochondrial genome assembly, annotation and visualization. Nucleic Acids Research 47: e63. https://doi.org/10.1093/nar/gkz173
- Michaelsen W (1928) Miscellanea oligochaetologiea. Arkiv för Zoologi 20: 1–15.
- Michaelsen W (1934) Oligochaeten von Franz Ösisch-Indochina. Archives de Zoologie Expérimentale et Générale 76: 493–546.
- Misirlioğlu M, Reynolds JW, Stojanović M, Trakić T, Sekulić J, James SW, Csuzdi C, Decaëns T, Lapied E, Phillips HRP, Cameron EK, Brown GG (2023) Earthworms (Clitellata, Megadrili) of the world: an updated checklist of valid species and families, with notes on their distribution. Zootaxa 5255(1): 417–438. https://doi.org/10.11646/zootaxa.5255.1.33
- Nguyen TT, Lam DH, Nguyen AD (2021) Notes on the earthworm species, Metaphire anomala (Michaelsen, 1907) (Clitellata, Megascolecidae) in Southern Vietnam, with descriptions of two new species. European Journal of Taxonomy 746: 94–111. https://doi.org/10.5852/ejt.2021.746.1321
- Nguyen TT, Ly VV, Lam DH, Nguyen TV, Nguyen AD (2022) A New Earthworm Species of the Genus Metaphire Sims & Easton, 1972 (Oligochaeta: Megascolecidae) from Southern Vietnam. Tropical Natural History 22(1): 72–84. https://doi.org/10.58837/tnh.22.1.256982
- Pérez-Losada M, Bloch R, Breinholt JW, Pfenninger M, Domínguez J (2012) Taxonomic assessment of Lumbricidae (Oligochaeta) earthworm genera using DNA barcodes. European Journal of Soil Biology 48: 41–47. https://doi.org/10.1016/j.ejsobi.2011.10.003
- Pérez-Losada M, Eiroa J, Mato S, Domínguez J (2005) Phylogenetic species delimitation of the earthworms Eisenia fetida (Savigny, 1826) and Eisenia andrei Bouché, 1972 (Oligochaeta, Lumbricidae) based on mitochondrial and nuclear DNA sequences. Pedobiologia 49: 317–324. https://doi.org/10.1016/j.pedobi.2005.02.004
- Phan QT, Lam DH, Tran MT, Pham QV, Nguyen AD (2026) Two new earthworm species of the genus Metaphire Sims & Easton, 1972 (Annelida: Oligochaeta: Megascolecidae) from Highlands of Vietnam. Zootaxa 5748(1): 101–112. https://doi.org/10.11646/zootaxa.5748.1.5
- Pop AA, Wink M, Pop VV (2003) Use of 18S, 16S rDNA and cytochrome c oxidase sequences in earthworm taxonomy (Oligochaeta, Lumbricidae). Pedobiologia 47: 428–433. https://doi.org/10.1078/0031-4056-00208
- Porco D, Decaëns T, Deharveng L, James SW, Skarżyński D, Erséus C, Butt KR, Richard B, Hebert PDN (2012) 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: 899–910. https://doi.org/10.1007/s10530-012-0338-2
- Puillandre N, Brouillet S, Achaz G (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21: 609–620. https://doi.org/10.1111/1755-0998.13281
- Qiu J, Bouché MB (1998) Révision des taxons supraspécifiques de Lumbricoidea. Documents Pédozoologiques et Intégrologiques 3: 179–216. https://doi.org/10.13140/RG.2.2.24269.49127
- Qiu J, Zhong Y (1993) Notes on a new species and a new subspecies of the genus Metaphire from Guizhou Province, China (Haplotaxida: Megascolecidae). Guizhou Science 11: 38–44.
- Rambaut A (2022) Figtree 1.4.4. http://tree.bio.ed.ac.uk/software/figtree/ [accessed on 1 July 2022]
- Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Systematic Biology 67: 901–904. https://doi.org/10.1093/sysbio/syy032
- Ratmanee C, Anuwat A, Teerapong S, Ueangfa B, Somsak P (2023) Four new terrestrial earthworm species from the northeast Thailand (Oligochaeta, Megascolecidae). ZooKeys 1176: 195–219. https://doi.org/10.3897/zookeys.1176.106517
- Ren J, Liu Y, Zhang S, Zheng C, Tan Y, Peng C, Gao J, Hou F (2025) Three New Earthworm Species of the Genera Amynthas and Metaphire (Oligochaeta: Megascolecidae) From Leshan, China. Zoological Society 42: 206–218 https://doi.org/10.2108/zs240010
- Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna 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
- Rougerie R, Decaëns T, Deharveng L, Porco D, James SW, Chang C-H, Richard B, Potapov M, Suhardjono Y, Hebert PDN (2009) DNA barcodes for soil animal taxonomy. Pesquisa Agropecuária Brasileira 44: 789–802. https://doi.org/10.1590/s0100-204x2009000800002
- Sato C, Nendai N, Nagata N, Okuzaki Y, Ikeda H, Minamiya Y, Sota T (2023) Origin and diversification of pheretimoid megascolecid earthworms in the Japanese Archipelago as revealed by mitogenomic phylogenetics. Molecular Phylogenetics and Evolution 182: 107735. https://doi.org/10.1016/j.ympev.2023.107735
- Shen H, Tsai SC, Tsai CF (2005) Occurrence of the Earthworms Pontodrilus litoralis (Grube, 1855), Metaphire houlleti (Perrier, 1872), and Eiseniella tetraedra (Savigny, 1826) from Taiwan. Taiwania 50: 11–21. https://doi.org/10.6165/tai.2005.50(1).11
- Shukla R, Soni J, Kumar A, Pandey R (2024) Uncovering the diversity of pathogenic invaders: insights into protozoa, fungi, and worm infections. Frontiers in Microbiology 15: 1374438. https://doi.org/10.3389/fmicb.2024.1374438
- Sims RW, Easton EG (1972) A numerical revision of the earthworm genus Pheretima auct. (Megascolecidae, Oligochaeta) with the recognition of new genera and an appendix on the earthworms collected by the Royal Society North Borneo Expedition. Biological Journal of the Linnaean Society 4: 169–268. https://doi.org/10.1111/j.1095-8312.1972.tb00694.x
- Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
- Sun J (2013) Taxonomy and Molecular Phylogeny of Amynthas earthworms from China. Doctoral dissertation, Shanghai Jiao Tong University. [In Chinese with English abstract]
- Sun J, Jiang J, Scott B, Qiu J, Feng H (2018) Four new Amynthas and Metaphire earthworm species from nine provinces in southern China. Zootaxa 4496: 287–301. https://doi.org/10.11646/zootaxa.4496.1.24
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739. https://doi.org/10.1093/molbev/msr121
- Tan T, Zhong Y (1986) A new species of the genus Metaphire from Hunan (Oligochaeta: Megascolecidae). Acta Zootaxonomica Sinica 11: 144–147.
- Tan T, Zhong Y (1987) Two new species of the genus Metaphire from Hunan Province (Oligochaeta: Megascolecidae). Acta Zootaxonomica Sinica 12: 128–132.
- Thai TB, Do VN, Huyhn TKH (1992) New species of earthworm of genus Pheretima Kinberg, 1867 (Megascolecidae-Oligochaeta) belonging the bank of streams Xuan Nha Moc Chau (Son La Province) and Dac No, Dac Ken (Dac Lac Province). Tap chi Sinh hoc 14(4): 1–3.
- Thai TB, Le VT (1993) Two new earthworms of the genus Pheretima Kinberg, 1897 (Megascolecidae-Oligochaeta) from Catba National Park (Cat Ba Island, Hai Phong). Tap chi Sinh hoc 15(4): 33–35.
- Tiwari N, Shilpi K, James SW, Gupta N, Yadav S (2025) Three Novel Species of Earthworms of Genus Metaphire Sims and Easton, 1972 from Manipur, India. Zootaxa 5589: 166–189. https://doi.org/10.11646/zootaxa.5589.1.14
- Wu C (2008) Landform environment and its formation in North China. Science Press, Beijing, 64–66.
- Xu Q, Xiao N (2011) Terrestrial earthworms (Opisthopora: Oligochaeta) of China. China Agriculture Press, Beijing, 66–269.
- Yu X, Yang H, Liu J, Qi Y, Sun L, Tian X (2022) A strategy for a high enrichment of insect mitochondrial DNA for mitogenomic analysis. Gene 808: 145986. https://doi.org/10.1016/j.gene.2021.145986
- Zhang L, Jiang J, Dong Y, Qiu J (2015) Complete mitochondrial genome of four pheretimoid earthworms (Clitellata: Oligochaeta) and their phylogenetic reconstruction. Gene 574: 308–316. https://doi.org/10.1016/j.gene.2015.08.020
- Zhang L, Jiang J, Dong Y, Qiu J (2016a) Complete mitochondrial genome of a Pheretimoid earthworm Metaphire vulgaris (Oligochaeta: Megascolecidae). Mitochondrial DNA Part A 27: 297–298. https://doi.org/10.3109/19401736.2014.892085
- Zhang L, Jiang J, Dong Y, Qiu J (2016b) Complete mitochondrial genome of an Amynthas earthworm, Amynthas aspergillus (Oligochaeta: Megascolecidae). Mitochondrial DNA Part A 27: 1876–1877. https://doi.org/10.3109/19401736.2014.971267
- Zhang L, Sechi P, Yuan M, Jiang J, Dong Y, Qiu J (2016c) Fifteen new earthworm mitogenomes shed new light on phylogeny within the Pheretima complex. Scientific Reports 6: 20096. https://doi.org/10.1038/srep20096
- Zhang Y, Bi Y, Li G, Shen L (2017) Relationship between earthworm diversity and soil environment in Hebei area. Journal of China Agricultural University 22: 60–68. https://doi.org/10.11841/j.issn.1007-4333.2017.03.08
- Zhao H, Fan S, Aspe NM, Feng L, Zhang Y (2022) Characterization of 15 Earthworm Mitogenomes from Northeast China and Its Phylogenetic Implication (Oligochaeta: Lumbricidae, Moniligastridae). Diversity 14: 714. https://doi.org/10.3390/d14090714
- Zhao H, Han ACN, Liu M, Zhang Y, Aspe NM, Miao P, Wu D (2025) A new pheretimoid earthworm of the genus Metaphire Sims & Easton, 1972 (Oligochaeta, Megascolecidae) from northeastern China with data from the mitochondrial genome. Zoosystematics and Evolution 101: 81–89. https://doi.org/10.3897/zse.101.136027
- Zhao Q (2015) Taxonomy, phylogeny and paleogeography of pheretimoid earthworm species in Hainan island (China). Doctoral dissertation, Shanghai Jiao Tong University. [In Chinese with English abstract]
- Zhong Y, Xu X, Wang D (1984) On a new species of the earthworm genus Pheretima and its reproductive organ polymorphism. Acta Zootaxonomica Sinica 9: 356–360.