Comparative morpho-anatomy and mitochondrial phylogeny of Semisulcospiridae in Yunnan, south-western China, with description of four new species (Gastropoda : Cerithioidea)
Li-Na Du A E , Frank Köhler B E , Guo-Hua Yu C E F , Xiao-Yong Chen A D F and Jun-Xing Yang A F
+ Author Affiliations
- Author Affiliations
A Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China.
B Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia.
C Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Guangxi Normal University), Ministry of Education, Guilin, Guangxi 541004, China.
D Southeast Asia Biodiversity Research Institute, Chinese Academy of Science, Yezin, Nay Pyi Taw 05282, Myanmar.
E These authors contributed equally to this work.
F Corresponding authors. Email: yugh2018@126.com; chenxy@mail.kiz.ac.cn; yangjx@mail.kiz.ac.cn
Invertebrate Systematics 33(6) 825-848 https://doi.org/10.1071/IS18084
Submitted: 26 November 2018 Accepted: 2 June 2019 Published: 10 December 2019
Abstract
The taxonomic history of Chinese semisulcospirids is confusing. Originally placed in Melania by late 19th century authors, species have subsequently been dispersed into four different genera, i.e. Semisulcospira Böttger, 1886, Senckenbergia Yen, 1939, Hua Chen, 1943, and Namrutua Abbott, 1948; however, these placements were not conducted within a phylogenetic context. Based on examination of newly collected samples from the Chinese provinces Yunnan, Guizhou, Jiangxi, Anhui and Chongqing, we revised the systematics of the Chinese Semisulcospiridae based on comparative anatomy and mitochondrial phylogenetics. We have examined shell, radular, and reproductive features and employed Bayesian and Maximum Likelihood analyses of partial sequences of mitochondrial genes cytochrome c oxidase I and 16S rRNA to resolve the phylogenetic relationships. The results revealed that Semisulcospiridae is represented by three genera in China, which differ in their reproductive strategy, including Semisulcospira, which is viviparous and contains three species (S. ningpoensis, S. gredleri, and S. pleuroceroides); Hua, which is oviparous and contains 11 species; and Koreoleptoxis, which is oviparous and contains one species. Namrutua and Senckenbergia are identified here as junior subjective synonyms of Semisulcospira. All taxa recognised herein formed well differentiated clades in three mitochondrial phylogeny, and could be reliably distinguished by differences in shell shape and sculpture. Four new species of Hua are described from Yunnan Province. This is the first comprehensive study to review the taxonomy of semisulcospirids in China. These species are sensitive to water quality, and economic development and infrastructure expansion have negatively impacted many populations. We fear that some species may have disappeared before being investigated or described scientifically. Therefore, this research will hopefully inspire further studies and surveys to foster our understanding of freshwater gastropod diversity in China.
http://zoobank.org/urn:lsid:zoobank.org:pub:EF2147FD-9EEE-4922-90DC-76651EF9E6AE
Additional keywords: Hua, Namrutua, Semisulcospira, Senckenbergia, taxonomy.
References
Abbott, R. T. (1948). Handbook of medically important molluscs of the Orient and the western Pacific. Bulletin of the Museum of Comparative Zoology 100, 245–328.Bavay, A., and Dautzenberg, P. (1910). Contributions à la faune fluviatile de l’extrème-Orient (Chine et Indo-Chine). Journal de Conchyliologie 58, 1–21.
Benson, W. H. (1842). Mollusca, in Theodor Cantor’s General Features of Chusan, with remarks on the flora and fauna of that island. The Annals and Magazine of Natural History, Zoology (Jena, Germany) 9, 481–493.
| Mollusca, in Theodor Cantor’s General Features of Chusan, with remarks on the flora and fauna of that island.Crossref | GoogleScholarGoogle Scholar |
Böttger, O. (1886). Zur Kenntniss der Melanien Chinas. Jahrbucher der Deutschen Malakologischen Gesellschaft 13, 1–16.
Böttger, O. (1887). Die ostasiatischen Vertreter der Gattung Rissoina. Ahrbucher der Deuschen Malakologischen Gesellschaft 14, 125–135.
Bouchet, P., and Rocroi, J. P. (2005). Classification and nomenclator of gastropod families, with classification by Fryda, J., Hausdorf, B., Ponder, W., Valdés A., and Warén, A. Malacologia 47, 245–279.
Brandt, R. A. M. (1974). The non-marine aquatic Mollusca of Thailand. Archiv fur Molluskenkunde 105, 184–189.
Brot, A. (1874–1879). Die Melaniacean (Melanidae) in Abbildungen der Natur mit Beschreibungen. In ‘Systematisches Conchylien-Cabinet von Martini und Chemnitz, Ersten Bandes, vierundzwanzigste Abtheilung’. (1) 24 (229): 1–32, pls. 1–6 (1874); (1) 24 (235): 33–80, pls. 7–12 (1875); (1) 24 (244): 81–128, pls. 13–18 (1875); (1) 24 (249): 129–192, pls. 19–24 (1876); (1) 24 (259): 193–272, pls. 25–30 (1877); (1) 24 (264): 273–352, pls. 31–36 (1877); (1) 24 (271): 353–400, pls. 37–42 (1878); (1) 24 (280): 401–456, pls. 43–48 (1879); (1) 24 (283): 457–488, pl. 49 (1879). (Bauer and Raspe: Nürnberg.)
Burch, J. B. (1968). Cytotaxonomy of some Japanese Semisulcospira (Streptoneura: Pleuroceridae). Journal de Conchyliologie 107, 3–51.
Burch, J. B., and Jung, Y (1988). A new freshwater prosobranch snail (Mesogastropoda: Pleuroceridae) for Korea. Walkerana 2, 187–194.
Burch, J. B., Chung, P. R., and Jung, Y. (1988). A guide to the freshwater snails of Korea. Walkerana 2, 195–232.
Chen, S. F. (1937). Four new species of freshwater molluscs from China. Journal of the Washington Academy of Sciences 27, 444–448.
Chen, S. F. (1943). Two new genera, two new species and two new names of Chinese Melaniidae. Nautilis 57, 19–21.
Chen, X. Y. (2013). Checklist of fishes of Yunnan. Zoological Research 34, 281–343.
| 23913883PubMed |
Cheng, Y. Z., Hou, J., He, X. H., Hong, Z. K., Li, L. S., Lin, G. H., and Chen, S. H. (2011). Prevalence of Paragonimus and Angiostrongylus cantonensis infections in snails in southeastern China. Journal of Animal and Veterinary Advances 10, 2599–2602.
| Prevalence of Paragonimus and Angiostrongylus cantonensis infections in snails in southeastern China.Crossref | GoogleScholarGoogle Scholar |
Davis, G. M. (1969). A taxonomic study of some species of Semisulcospira in Japan (Mesogastropoda: Pleuroceridae). Malacologia 7, 211–294.
Davis, G. M. (1972). Geographic variation in Semisulcospira libertina (Mesogastropoda: Pleuroceridae). Proceedings of the Royal Society of London 40, 7–32.
| Geographic variation in Semisulcospira libertina (Mesogastropoda: Pleuroceridae).Crossref | GoogleScholarGoogle Scholar |
Du, L. N., Yang, J. X., and Chen, X. Y. (2011a). A new species of Trochotaia (Caenogastropoda: Viviparidae) from Yunnan, China. Molluscan Research 31, 85–89.
Du, L. N., Li, Y., Chen, X. Y., and Yang, J. X. (2011b). Effect of eutrophication on molluscan community composition in the Lake Dianchi (China, Yunnan). Limnologica 41, 213–219.
| Effect of eutrophication on molluscan community composition in the Lake Dianchi (China, Yunnan).Crossref | GoogleScholarGoogle Scholar |
Du, L. N., Chen, X. Y., and Yang, J. X. (2017). Morphological redescription and neotype designation of Sulcospira paludiformis (Yen, 1939) from Hainan, China. Molluscan Research 37, 66–71.
| Morphological redescription and neotype designation of Sulcospira paludiformis (Yen, 1939) from Hainan, China.Crossref | GoogleScholarGoogle Scholar |
Fulton, H. C. (1904). On some new species of Melania and Jullienia from Yunnan and Java. Journal of Malacology 11, 51–52.
Fulton, H. C. (1914). Descriptions of new species of Melania from Yunnan, Java, and the Tsushima Islands. The Journal of Molluscan Studies 11, 163–164.
| Descriptions of new species of Melania from Yunnan, Java, and the Tsushima Islands.Crossref | GoogleScholarGoogle Scholar |
Glaubrecht, M. (1999). Systematics and the evolution of viviparity in tropical freshwater gastropods (Cerithioidea: Thiaridae sensu lato) – an overview. Courier Forschungsinstitut Senckenberg 125, 91–96.
Gredler, P. V. (1887). Zur Conchylien-Fauna von China. Annalen des Naturhistorischen Museums in Wien 2, 283–290.
Heude, P. M. (1882–1890). Mémoires concernant l’histoire naturelle de l’empire chinois par des pères de la Compagnie de Jésus. Notes sur les Mollusques terrestres de la vallée du Fleuve Bleu. Mission Catholique, Chang-Hai, 188 pp.
Heude, P. M. (1888). Diagnoses molluscorum novarum in Sinis. Journal de Conchyliologie 36, 305–309.
Holznagel, W. E. (1998). A non-destructive method for cleaning gastropod radulae from frozen, alcohol-fixed, or dried material. American Malacological Bulletin 14, 181–183.
Jung, Y., Park, G. M., Park, J., Kim, J. J., Min, D. Y., and Chung, P. R. (1999). Allozyme variability in three species of genus Semisulcospira (Prosobranchia: Pleuroceridae). The Korean Journal of Malacology 15, 13–20.
Karube, Z. I., Sakai, Y., Takeyama, T., Okuda, N., Kohzu, A., Yoshimizu, C, Nagata, T, and Tayasu, I (2010). Carbon and nitrogen stable isotope ratios of macroinvertebrates in the littoral zone of Lake Biwa as indicators of anthropogenic activities in the watershed. Ecological Research 25, 847–855.
| Carbon and nitrogen stable isotope ratios of macroinvertebrates in the littoral zone of Lake Biwa as indicators of anthropogenic activities in the watershed.Crossref | GoogleScholarGoogle Scholar |
Katoh, K., Misawa, K., Kuma, K. I., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.
| MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.Crossref | GoogleScholarGoogle Scholar | 12136088PubMed |
Kim, J. J. (1995). Isozyme variations of the genus Semisulcospira (Pleuroceridae: Gastropoda) in Korea. The Korean Journal of Malacology 11, 171–179.
Kim, S. S., Kim, D. C., Chung, P. R., and Chung, Y. J. (1987). A cytological study on two species of the genus Semisulcospira (Gastropoda: Pleuroceridae) in Korea. The Korean Journal of Malacology 420, 73–90.
Kim, W. J., Kim, D. H., Lee, J. S., Bang, I. C., Lee, W. O., and Jung, H. (2010). Systematic relationships of Korean freshwater snails of Semisulcospira, Koreanomelania, and Koreoleptoxis (Cerithioidea: Pleuroceridae) revealed by mitochondrial cytochrome oxidase I sequences. The Korean Journal of Malacology 26, 275–283.
Kimura, M., and Oniwa, K. (1984). Protein polymorphism in the freshwater snail Semisulcospira libertina. Animal Blood Groups and Biochemical Genetics 15, 71–76.
| Protein polymorphism in the freshwater snail Semisulcospira libertina.Crossref | GoogleScholarGoogle Scholar | 6742518PubMed |
Ko, J. H., Lee, J. S., and Kwon, O. K. (2001). Study on radulae of seven species of the family Pleuroceridae in Korea. The Korean Journal of Malacology 17, 105–115.
Kobayashi, T. (1986). Karyotypes of four species of the genus Semisulcospira in Japan. Venus (Fukuyama-Shi, Japan) 45, 127–137.
Köhler, F. (2016). Rampant taxonomic incongruence in a mitochondrial phylogeny of Semisulcospira freshwater snails from Japan (Gastropoda, Cerithioidea, Semisulcospiridae). The Journal of Molluscan Studies 82, 268–281.
| Rampant taxonomic incongruence in a mitochondrial phylogeny of Semisulcospira freshwater snails from Japan (Gastropoda, Cerithioidea, Semisulcospiridae).Crossref | GoogleScholarGoogle Scholar |
Köhler, F. (2017). Against the odds of unusual mtDNA inheritance, introgressive hybridization and phenotypic plasticity: systematic revision of Korean freshwater gastropods (Semisulcospiridae, Cerithioidea). Invertebrate Systematics 31, 249–268.
| Against the odds of unusual mtDNA inheritance, introgressive hybridization and phenotypic plasticity: systematic revision of Korean freshwater gastropods (Semisulcospiridae, Cerithioidea).Crossref | GoogleScholarGoogle Scholar |
Köhler, F., and Glaubrecht, M. (2006). A systematic revision of the southeast Asian freshwater gastropod Brotia (Cerithioidea: Pachychilidae). Malacologia 48, 159–251.
Köhler, F., Holford, M., Tu, D. V., and Hai, H. T. (2009). Exploring a largely unknown fauna: on the diversity of pachychilid freshwater gastropods in Vietnam (Caenogastropoda: Cerithioidea). Molluscan Research 29, 121–146.
Komiya, Y., Suzuki, N., and Ito, Y. (1961). Infection experiment of Paragonimus westermani in its first intermediate host, Semisulcospira libertina. Japanese Journal of Medical Science & Biology 14, 39–43.
| Infection experiment of Paragonimus westermani in its first intermediate host, Semisulcospira libertina.Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
Kurozumi, T., Ozaki, K., and Ohki, J. I. (2004). Species composition and ecological distributions of freshwater molluscs in dam lakes of Boso Hills, central Japan. Journal of the Natural History Museum and Institute Chiba Special Issue 7, 33–43.
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2016). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Lea, I. (1856). Description of fifteen new species of exotic Melaniana. Proceedings of the Academy of Natural Sciences of Philandelphia, 144.
Lee, T., Hong, H. C., Kim, J. J., and Foighil, D. (2007). Phylogenetic and taxonomic incongruence involving nuclear and mitochondrial markers in Korean populations of the freshwater snail genus Semisulcospira (Cerithioidea: Pleuroceridae). Molecular Phylogenetics and Evolution 43, 386–397.
| Phylogenetic and taxonomic incongruence involving nuclear and mitochondrial markers in Korean populations of the freshwater snail genus Semisulcospira (Cerithioidea: Pleuroceridae).Crossref | GoogleScholarGoogle Scholar | 17400481PubMed |
Li, W. H., Gojobori, T., and Nei, M. (1981). Pseudogenes as a paradigm of neutral evolution. Nature 292, 237–239.
| Pseudogenes as a paradigm of neutral evolution.Crossref | GoogleScholarGoogle Scholar | 7254315PubMed |
Liu, Y. Y., Zhang, W. Z., and Wang, E. Y. (1979). Freshwater molluscs. In ‘Economic Fauna of China’. (Eds Y. Y. Liu, W. Z. Zhang, Y. X. Wang and E. Y. Wang) pp. 41–45. (Science Press: Beijing.)
Liu, Y. Y., Zhang, W. Z., and Wang, Y. X. (1993). ‘Medical Malacology.’ (China Ocean Press: Beijing.)
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA’. pp. 1–8.
Miura, O., Köhler, F., Lee, T., Li, J., and O’Foighil, D. (2013). Rare, divergent Korean Semisulcospira spp. Mitochondrial haplotypes have Japanese sister lineages. The Journal of Molluscan Studies 79, 86–89.
| Rare, divergent Korean Semisulcospira spp. Mitochondrial haplotypes have Japanese sister lineages.Crossref | GoogleScholarGoogle Scholar |
Morrison, J. P. E. (1952). World relations of the melanians. American Malacological Union News Bulletin and Annual Report 1951, 6–9.
Morrison, J. P. E. (1954). The relationships of old and new world melanians. Proceedings of the United States National Museum 103, 357–394.
| The relationships of old and new world melanians.Crossref | GoogleScholarGoogle Scholar |
Oniwa, K., and Kimura, M. (1986). Genetic variability and relationships in six snail species of the genus Semisulcospira. Japanese Journal of Genetics 61, 503–514.
| Genetic variability and relationships in six snail species of the genus Semisulcospira.Crossref | GoogleScholarGoogle Scholar |
Palumbi, S. R., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. (1991). ‘The Simple Fool’s Guide to PCR.’ (University of Hawaii: Honolulu.)
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 18397919PubMed |
Reeve, L. A. (1859–1861). Monograph of the genus Melania. In ‘Conchologia Iconica’. Vol. 12, pl. 1–59 and unpaginated text. (L. Reeve and Co.: London.)
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., and Darling, A. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Stamatakis, A. (2014). RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
| RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |
Strong, E. E., and Köhler, F. (2009). Morphological and molecular analysis of ‘Melania’ jacqueti Dautzenberg and Fischer, 1906: from anonymous orphan to critical basal offshoot of the Semisulcospiridae (Gastropoda: Cerithioidea). Zoologica Scripta 38, 483–502.
| Morphological and molecular analysis of ‘Melania’ jacqueti Dautzenberg and Fischer, 1906: from anonymous orphan to critical basal offshoot of the Semisulcospiridae (Gastropoda: Cerithioidea).Crossref | GoogleScholarGoogle Scholar |
Strong, E. E., Gargominy, O., Ponder, W. F., and Bouchet, P. (2008). Global diversity of gastropods (Gastropoda: Mollusca) in freshwater. Hydrobiologia 595, 149–166.
| Global diversity of gastropods (Gastropoda: Mollusca) in freshwater.Crossref | GoogleScholarGoogle Scholar |
Tchang, S., and Tsi, C. Y. (1949). Liste des mollusques d’eau douce recueillis pendant les années 1938–1946 au Yunnan et description d’ éspèces nouvelles. Contributions from the Institute of Zoology, National Academy of Peiping 5, 205–220.
Urabe, M. (1993). Two types of freshwater snail Semisulcospira reiniana (Brot) (Mesogastropoda: Pleuroceridae) identified by electrophoresis. Japanese Journal of Limnology 54, 109–116.
| Two types of freshwater snail Semisulcospira reiniana (Brot) (Mesogastropoda: Pleuroceridae) identified by electrophoresis.Crossref | GoogleScholarGoogle Scholar |
Urabe, M. (1998). Contribution of genetic and environmental factors to shell shape variation in the lotic snail Semisulcospira reiniana (Prosobranchia: Pleuroceridae). The Journal of Molluscan Studies 64, 329–343.
| Contribution of genetic and environmental factors to shell shape variation in the lotic snail Semisulcospira reiniana (Prosobranchia: Pleuroceridae).Crossref | GoogleScholarGoogle Scholar |
Urabe, M. (2000). Phenotypic modulation by the substratum of shell sculpture in Semisulcospira reiniana (Prosobranchia: Pleuroceridae). The Journal of Molluscan Studies 66, 53–60.
| Phenotypic modulation by the substratum of shell sculpture in Semisulcospira reiniana (Prosobranchia: Pleuroceridae).Crossref | GoogleScholarGoogle Scholar |
Urabe, M. (2003). Trematode fauna of prosobranch snails of the genus Semisulcospira in Lake Biwa and the connected drainage system. Parasitology International 52, 21–34.
| Trematode fauna of prosobranch snails of the genus Semisulcospira in Lake Biwa and the connected drainage system.Crossref | GoogleScholarGoogle Scholar | 12543144PubMed |
Wenz, W. (1938–1944). Gastropoda. Allgemeiner Teil und Prosobranchia. In ‘Handbuch der Paläozoologie’. (Ed. O. H. Schindewolf.) (Borntraeger: Berlin.)
Wilson, A. B., Glaubrecht, M., and Meyer, A. (2004). Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proceedings of the Royal Society of London. Series B, Biological Sciences 271, 529–536.
| Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika.Crossref | GoogleScholarGoogle Scholar |
Xu, X. F. (2007). Classification and morphology on Pleuroceridae (Gastropoda: Mesogastropoda) of some area in middle reaches of Changjiang River. Ph.D. Thesis, Nancang University, China.
Yen, T. C. (1939). Die chinesischen Land- and Süßwasser-Gastropoden des Natur-Museums Senckenberg. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 444, 51–59.
Yen, T. C. (1942). A review of Chinese gastropods in the British Museum. Proceedings of the Malacological Society of London 24, 170–289.
| A review of Chinese gastropods in the British Museum.Crossref | GoogleScholarGoogle Scholar |
Yen, T. C. (1948). Notes on land and freshwater mollusks of Chekiang Province, China. Proceedings of the California Academy of Sciences 4, 79–81.
Zhang, N. G., Hao, T. X., Wu, C. Y., Chen, Y. X., Zhang, W., Li, J. K., and Zhang, Y. (1997). A research of freshwater Gastropoda from Yunnan. Studia Marina Sinica 39, 15–25.
