Unveiling cryptic diversity: two new species of Dugesia from northern China, including one sibling species (Platyhelminthes, Tricladida, Dugesiidae)
Authors/Creators
- 1. College of Life Science, Henan Normal University, Xinxiang, China
- 2. Naturalis Biodiversity Center, Leiden, Netherlands
Description
Two new species of Dugesia from the Taihang and Funiu Mountains, including one sibling species, are described by applying an integrative approach, including morphological, karyological, histological, and molecular information. Dugesia cylindrica Chen & Dong, sp. nov. is characterized by the following features, among others: sac-shaped copulatory bursa located immediately posterior to the pharyngeal pocket; stubby, cylindrical penis papilla with a blunt tip; large and pointed diaphragm; a long connecting duct between the seminal vesicle and diaphragm; slightly ventrally displaced ejaculatory duct with a terminal opening; chromosome complement diploid, with 16 metacentric chromosomes. Dugesia elongata Chen & Dong, sp. nov. is characterized by the following features, among others: barrel-shaped penis papilla; elongated, dumb-bell shaped seminal vesicle; long connecting duct between the seminal vesicle and low-conical diaphragm; ventrally displaced ejaculatory duct opening at the tip of the penis papilla, albeit at its ventral portion; asymmetrical openings of the oviducts; mixoploid karyotype, with diploid metacentric chromosome complements of 2n = 16 and triploid metacentric complements of 3n = 24. In the molecular phylogenetic tree, the two new species belong to two different subclades of the group comprising Eastern Palearctic/Oriental/Australasian species, with the two clades forming sister taxa. The distinct specific status of these two new species is also supported by their genetic distances. The distribution records of the two new species underscore the rich diversity of freshwater planarians in this region, and the discovery of the sibling species highlights the efficacy of integrative taxonomy in delimiting cryptic species.
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References
- Abascal F, Zardoya R, Telford MJ (2010) TranslatorX: Multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Research 38 (suppl. 2): W7–13. https://doi.org/10.1093/nar/gkq291
- Ball IR (1970) Freshwater triclads (Turbellaria, Tricladida) from the Oriental region. Zoological Journal of the Linnean Society 49(4): 271–294. https://doi.org/10.1111/j.1096-3642.1970.tb00742.x
- Chen G-W, Wang L, Wu F, Sun X-J, Dong Z-M, Sluys R, Yu F, Yu-wen Y-Q, Liu D-Z (2022) Two new species of Dugesia (Platyhelminthes, Tricladida, Dugesiidae) from the subtropical monsoon region in Southern China, with a discussion on reproductive modalities. BMC Zoology 7(1): 25. https://doi.org/10.1186/s40850-022-00127-8
- Chen G-W, Wang Y-L, Wang H-K, Fu R-M, Zhang J-F, Liu D-Z (2008) Chromosome and karyotype analysis of Polycelis wutaishanica (Turbellaria, Tricladida) from Shanxi province, China. Acta Zootaxonomica Sinica 33(3): 449–452. https://doi.org/10.1186/1471-2164-13-290
- Dahm AG (1958) Taxonomy and ecology of five species groups in the family Planariidae (Turbellaria Tricladida Paludicola). Malmö: Nya Litografen, 241 pp.
- Dessimoz C, Gil M (2010) Phylogenetic assessment of alignments reveals neglected tree signal in gaps. Genome biology 11(4): R37. https://doi.org/10.1186/gb-2010-11-4-r37
- Dols-Serrate D, Leria L, Aguilar JP, Stocchino GA, Riutort M (2020) Dugesia hepta and Dugesia benazzii (Platyhelminthes: Tricladida): two sympatric species with occasional sex? Organisms Diversity and Evolution 20: 369–386. https://doi.org/10.1007/s13127-020-00438-z
- Dols-Serrate D, Stocchino GA, Sluys R, Riutort M (2024a) Fantastic beasts and how to delimit them: an integrative approach using multispecies coalescent methods reveals two new, endemic Dugesia species (Platyhelminthes: Tricladida) from Corsica and Sardinia. Zoological Journal of the Linnean Society 201(3): zlad135. https://doi.org/10.1093/zoolinnean/zlad135
- Dols-Serrate D, Stocchino GA, Nuin-Villabona P, Sluys R, Riutort M (2024b) New insights into the evolution and biogeography of freshwater planarians on islands in the Tyrrhenian Sea, Western Mediterranean Basin, with the integrative description of a new endemic species from Corsica (Platyhelminthes: Tricladida: Dugesia). Zoological Journal of the Linnean Society 201(4): zlae080. https://doi.org/10.1093/zoolinnean/zlae080
- Dong Z-M, Chen G-W, Zhang H-C, Liu D-Z (2017) A new species of Polycelis (Platyhelminthes, Tricladida, Planariidae) from China. Acta Zoologica Academiae Scientiarum Hungaricae 63(3): 263–276. https://doi.org/10.17109/AZH.63.3.263.2017
- Dong Y-P, Shi X-H, Sun S-S, Sun J-P, Hui B, He D-F, Chong F-B, Yang Z (2022) Co-evolution of the Cenozoic tectonics, geomorphology, environment and ecosystem in the Qinling Mountains and adjacent areas, Central China. Geosystems and Geoenvironment 1(2): 100032. https://doi.org/10.1016/j.geogeo.2022.100032
- Hall FR (1999) Precision farming: Technologies and information as risk-reduction tools. Nucleic Acids Symposium Series, vol. 734, no. 41, pp. 95–98. https://doi.org/10.1021/bk-1999-0734.ch008
- Harrath AH, Sluys R, Aldahmash W, Al-Razaki A, Alwasel S (2013) Reproductive strategies, karyology, parasites, and taxonomic status of Dugesia populations from Yemen (Platyhelminthes: Tricladida: Dugesiidae). Zoological Science 30(6): 502-508. https://doi.org/10.2108/zsj.30.502
- Harrath AH, Mansour L, Sluys R, Aldahmash W, Riutort M, Alwasel S (2025) The first Dugesia species (Platyhelminthes, Tricladida, Dugesiidae) documented for Saudi Arabia: an integrative description. Zootaxa 5583(1): 113–127. https://doi.org/10.11646/zootaxa.5583.1.6
- Katoh K, Standley D-M (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4): 772–780. https://doi.org/10.1093/molbev/mst010
- Kawakatsu M (1968) On the origin and phylogeny of Turbellarians Suborder Paludicola. Japanese Society of Systematic Zoology, Circular no. 38–41: 11–22. [in Japanese]
- Lanfear R, Calcott B, Ho S-Y, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29(6): 1695–1701. https://doi.org/10.1093/molbev/mss020
- Lanfear R, Frandsen P-B, Wright A-M, Senfeld T, Calcott B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34(3): 772–773. https://doi.org/10.1093/molbev/msw260
- Lázaro E-M, Sluys R, Pala M, Stocchino G-A, Baguñà J, Riutort M (2009) Molecular barcoding and phylogeography of sexual and asexual freshwater planarians of the genus Dugesia in the Western Mediterranean (Platyhelminthes, Tricladida, Dugesiidae). Molecular Phylogenetics and Evolution 52: 835–845. https://doi.org/10.1016/j.ympev.2009.04.022
- Leria L, Vila-Farré M, Álvarez-Presas M, Sánchez-Gracia A, Rozas J, Sluys R, Riutort M (2020) Cryptic species delineation in freshwater planarians of the genus Dugesia (Platyhelminthes, Tricladida): Extreme intraindividual genetic diversity, morphological stasis, and karyological variability. Molecular Phylogenetics and Evolution 143: 106496. https://doi.org/10.1016/j.ympev.2019.05.010
- Levan A, Fredga K, Sandberg A-A (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52: 201–220. https://doi.org/10.1111/j.1601-5223.1964.tb01953.x
- Li J-K, Peng J-F, Wei X-X, Peng M, Li X, Liu Y-M, Li J-X (2024) Stability assessment of tree ring growth of Pinus armandii Franch in response to climate change based on slope directions at the Lubanling in the Funiu Mountains, China. Journal of Forestry Research 35(03): 88–99. https://doi.org/10.1007/s11676-024-01698-7
- Li X-N, Huo J-X, Yang L, Peng J-F (2020) Development and climatic response of the tree-ring width chronology of Pinus armandii at Muzhaling Mountain. Journal of Nanjing Forestry University 44(3): 157–162. https://doi.org/10.3969/j.issn.1000-2006.201901030
- Liu D-Z (1996) Notes on four new species of the genus Polycelis from China (Tricladida: Paludicola: Planariidae). Acta Zootaxonomica Sinica 21(4): 389–398. [in Chinese] https://doi.org/10.3724/issn1000-3207-1995-2-152-c
- Mo R-R, Yan Y-H, Wang G-Q, Li W-H, Murányi D (2019) Holomorphology of Kamimuria peppapiggia sp. n. (Plecoptera: Perlidae) from the foothills of Taihang Mountains, Henan Province of China. Zootaxa 4668(4): 575–587. https://doi.org/10.11646/zootaxa.4668.4.9
- Oki I, Tamura S, Yamayoshi T, Kawakatsu M (1981) Karyological and taxonomic studies of Dugesia japonica Ichikawa & Kawakatsu in the Far East. Hydrobiologia 84: 53–68. https://doi.org/10.1007/bf00026163
- Puillandre N, Brouillet S, Achaz G (2021) ASAP: Assemble Species by Automatic Partitioning. Molecular Ecology Resources 21(2): 609–620. https://doi.org/10.1111/1755-0998.13281
- Puillandre N, Lambert A, Brouillet S, Achaz G (2011) ABGD, Automatic Barcode Gap Discovery for Primary Species Delimitation. Molecular Ecology 21(8): 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
- Rambaut A, Drummond A-J, Xie D, Baele G, Suchard M-A (2018) Posterior summarization in Bayesian Phylogenetics Using Tracer 1.7. Systematic Biology 67(5): 901–904. https://doi.org/10.1093/sysbio/syy032
- Ronquist F, Teslenko M, van der Mark P, Ayres D-L, Darling A, Höhna 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. https://doi.org/10.1093/sysbio/sys029
- Sluys R, Kawakatsu M, Winsor L (1998) The genus Dugesia in Australia, with its phylogenetic analysis and historical biogeography (Platyhelminthes, Tricladida, Dugesiidae). Zoologica Scripta 27(4): 273–289. https://doi.org/10.1111/j.1463-6409.1998.tb00461.x
- Sluys R, Riutort M (2018) Planarian diversity and phylogeny. In: Rink JC (ed.), Planarian Regeneration: Methods and Protocols. Methods in Molecular Biology, vol. 1774, Humana Press, Springer Science+Business Media. New Yrok, 1–56. https://doi.org/10.1007/978-1-4939-7802-1
- Sluys R, Sola E, Gritzalis K, Vila-Farre M, Mateos E, Riutort M (2013) Integrative delineation of species of Mediterranean freshwater planarians (Platyhelminthes: Tricladida: Dugesiidae). Zoological Journal of the Linnean Society 169(3): 523–547. https://doi.org/10.1111/zoj.12077
- Solà E, Leria L, Stocchino G-A, Bagherzadeh R, Balke M, Daniels S-R, Harrath AH, Khang T-F, Krailas D, Kumar B, Li M-H, Maghsoudlou A, Matsumoto M, Naser N, Oben B, Segev O, Thielicke M, Tong X-L, Zivanovic G, Manconi R, Baguñà J, Riutort M (2022) Three dispersal routes out of Africa: a puzzling biogeographical history in freshwater planarians. Journal of Biogeography 49(7): 1219–1233. https://doi.org/10.1111/jbi.14371
- Solà E, Sluys R, Gritzalis K, Riutort M (2013) Fluvial basin history in the northeastern Mediterranean region underlies dispersal and speciation patterns in the genus Dugesia (Platyhelminthes, Tricladida, Dugesiidae). Molecular Phylogenetics and Evolution 66: 877–888. https://doi.org/10.1016/j.ympev.2012.11.010
- Sun X-X, Wang L, Li N, Sluys R, Liu D-Z, Dong Z-M, Chen G-W (2024) Two species of Polycelis (Platyhelminthes, Tricladida, Planariidae) newly recorded for the Qinling Mountains and the Loess Plateau in China, with a comparative discussion on their karyotypes. Zootaxa 5536(4): 581–599. https://doi.org/10.11646/zootaxa.5536.4.5
- Song X-Y, Li W-X, Sluys R, Huang S-X, Wang A-T (2020) A new species of Dugesia (Platyhelminthes, Tricladida, Dugesiidae) from China, with an account on the histochemical structure of its major nervous system. Zoosystematics and Evolution 96(2): 431–447. https://doi.org/10.3897/zse.96.52484
- Stocchino GA, Sluys R, Riutort M, Solà E, Manconi R (2017) Freshwater planarian diversity (Platyhelminthes: Tricladida: Dugesiidae) in Madagascar: new species, cryptic species, with a redefinition of character states. Zoological Journal of the Linnean Society 181: 727–756. https://doi.org/10.1093/zoolinnean/zlx017
- Stocchino GA, Manconi R, Corso G, Pala M (2004) Karyology and karyometric analysis of an Afrotropical freshwater planarian (Platyhelminthes, Tricladida). Italian Journal of Zoology 71: 89–93. https://doi.org/10.1080/11250000409356557
- Stocchino GA, Sluys R, Solà E, Riutort M, Manconi R (2024) The long-eared freshwater planarians of Madagascar form a separate phylogenetic clade within the genus Dugesia (Platyhelminthes: Tricladida), with the description of two new species. Zoological Journal of the Linnean Society 202: zlae143. https://doi.org/10.1093/zoolinnean/zlae143
- Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56(4): 564–577. https://doi.org/10.1080/10635150701472164
- 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. https://doi.org/10.1093/molbev/mst197
- Tan G, Muffato M, Ledergerber C, Herrero J, Goldman N, Gil M, Dessimoz C (2015) Current methods for automated filtering of multiple sequence alignments frequently worsen single-gene phylogenetic inference. Systematic Biology 64(5): 778–791. https://doi.org/10.1093/sysbio/syv033
- Vowinckel C, Marsden JR (1971) Reproduction of Dugesia tigrina under short-day and long-day conditions at different temperatures. II. Asexually derived individuals. Journal of Embryology and Experimental Morphology 49(5): 659–663. https://doi.org/10.1242/dev.26.3.587
- Wang B, Jiang J-P, Xie F, Chen X-H, Dubois A, Liang G, Wagner S (2009) Molecular phylogeny and genetic identification of populations of two species of Feirana frogs (Amphibia: Anura, Ranidae, Dicroglossinae, Paini) endemic to China. Zoological Science 26(7): 500–509. https://doi.org/10.2108/zsj.26.500
- Wang L, Chen J-Z, Dong Z-M, Chen G-W, Sluys R, Liu D-Z (2021a) Two new species of Dugesia (Platyhelminthes, Tricladida, Dugesiidae) from the tropical monsoon forest in Southern China. ZooKeys 1059: 89–116. https://doi.org/10.3897/zookeys.1059.65633
- Wang L, Dong Z-M, Chen G-W, Sluys R, Liu D-Z (2021b) Integrative descriptions of two new species of Dugesia from Hainan Island, China (Platyhelminthes, Tricladida, Dugesiidae). ZooKeys 1028: 1–28. https://doi.org/10.3897/zookeys.1028.60838
- Wang L, Wang Y-X, Dong Z-M, Chen G-W, Sluys R, Liu D-Z (2022) Integrative taxonomy unveils a new species of Dugesia (Platyhelminthes, Tricladida, Dugesiidae) from the southern portion of the Taihang Mountains in northern China, with the description of its complete mitogenome and an exploratory analysis of mitochondrial gene order as a taxonomic character. Integrative Zoology 17(6): 1193–1214. https://doi.org/10.1111/1749-4877.12605
- Wang L, Zhu S-Q, Ma F-H, Li X-J, Zhao Y-H, Sun X-X, Li N, Sluys R, Liu D-Z, Dong Z-M, Chen G-W (2024) Two new species of freshwater planarian (Platyhelminthes, Tricladida, Dugesiidae, Dugesia) from Southern China exhibit unusual karyotypes, with a discussion on reproduction in aneuploid species. Journal of Zoological Systematics and Evolutionary Research 2024: 8299436. https://doi.org/10.1155/2024/8299436
- Wang L, Chang Y-F, Sun X-X, Sluys R, Liu D-Z, Dong Z-M, Chen G-W (2025) Two new species of Dugesia from Hainan Island and Leizhou Peninsula (Platyhelminthes, Tricladida, Dugesiidae). ZooKeys 1233: 289–313. https://doi.org/10.3897/zookeys.1233.142976
- Winsor L, Sluys R (2018) Basic histological techniques for planarians. In: Rink JC (Ed.) Planarian Regeneration: Methods and Protocols. Methods in Molecular Biology, Vol. 1774. Humana Press, Springer Science+Business Media, New York, 285–351. https://doi.org/10.1007/978-1-4939-7802-1_9
- Wu F, Wang L, Sluys R, Sun XX, Liu DZ, Dong ZM, Chen GW (2025) An integrative analysis and account of two new species of Dugesia (Platyhelminthes, Tricladida, Dugesiidae) from the Hengduan Mountains, southwest China, with reflections on the historical biogeography of Eastern Palearctic/Oriental lineages. Zoosystematics and Evolution 101(4): 1513–1529. https://doi.org/10.3897/zse.101.156742
- Wu L, Wang F, Yang J-H, Wang Y-Z, Zhang W-B, Yang L-K, Shi W-B (2020) Meso-Cenozoic uplift of the Taihang Mountains, North China: Evidence from zircon and apatite thermochronology. Geological Magazine 157(7): 1097–1111. https://doi.org/10.1017/S0016756819001377
- Zeng Z-Y, Wang J, Sluys R, Guo Z-P, Sun T, Huang X-Z, Li S-F, Wang A-T (2024) Integrative description of a new species of Dugesia (Platyhelminthes, Tricladida, Dugesiidae) from Shennongjia, Central China. Zootaxa 5406(4): 535–550. https://doi.org/10.11646/zootaxa.5406.4.3
- Zhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li W-X, Wang G-T (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20: 348–355. https://doi.org/10.1111/1755-0998.13096
- Zhang J-J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics (29)22: 2869–2876. https://doi.org/10.1093/bioinformatics/btt499
- Zhao B, Yin Z-F, Man X, Wang Q-C (2012) AFLP analysis of genetic variation in wild populations of five rhododendron species in Qinling mountain in China. Biochemical Systematics and Ecology 45: 198–205. https://doi.org/10.1016/j.bse.2012.07.033
- Zhong H-W, Zhao X, Yin S-M, Zhao X, Zhao T (2010) Late Cenozoic geomorphology, geochronology and physiography of Yuntaishan in Southern Taihang Mountain, North China. Bulletin of the Geological Society of China 84: 230–239. https://doi.org/10.1111/j.1755-6724.2010.00185.x