Redescription of Semisulcospira reticulata (Mollusca, Semisulcospiridae) with description of a new species from Lake Biwa, Japan
Authors/Creators
- 1. Kyoto University, Kyoto, Japan
- 2. National Institute of Genetics, Shizuoka, Japan
- 3. Kochi University, Nankoku, Japan
- 4. Setsunan University, Hirakata, Japan
Description
Semisulcospira Boettger, 1886 is a freshwater snail genus divergent in Lake Biwa, Japan. Although recent taxonomic studies of the genus have arranged taxonomic accounts of many species in the lake, our knowledge of morphological traits has still been insufficient in S. reticulata Kajiyama & Habe, 1961, which belongs to the S. niponica-group in the genus. Among the various habitats of the lacustrine species, in addition, the species richness of this group in coastal sandy mud areas of the lake has not been completely clarified. In this study, we revisited the taxonomic account of S. reticulata and described a new S. niponica-group species, S. nishimurai sp. nov., from Lake Biwa by evaluating the genetic and morphological relationships within the group. The reconstructed maximum likelihood and singular value decomposition quartets trees, and ADMIXTURE analyses using genome-wide SNP data strongly supported the genetic distinctiveness of most S. niponica-group species. The Random Forest classification showed that S. reticulata possesses a unique, large protoconch without distinct keels, and that S. nishimurai sp. nov. is characterized by a small, less elongated teleoconch and tiny protoconch. The large protoconch of S. reticulata and the narrow radulae of S. reticulata and S. nishimurai sp. nov. suggest their specialization in life history and feeding habits, respectively. The discovery of the new species from sandy mud substrates highlights niche differentiation among Semisulcospira species, and provides new insights into the diversification of the genus in ancient lakes.
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References
- Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19: 1655–1664. https://doi.org/10.1101/gr.094052.109
- Andy L, Matthew W (2002) Classification and regression by randomForest. R News 2: 18–22.
- Annandale N (1916) Zoological Results of a Tour in the Far East. The Mollusca of Lake Biwa, Japan. Records of the Indian Museum 6: 41–74. https://doi.org/10.5962/bhl.title.46524
- Boettger O (1886) Zur Kenntniss der Melanien Chinas und Japans. Jahrbücher der Deutschen Malakozoologischen Gesellschaft 13: 1–16.
- Breiman L (2001) Random Forests. Machine Learning 45: 5–32. https://doi.org/10.1023/A:1010933404324
- Burch JB (1968) Cytotaxonomy of some Japanese Semisulcospira (Streptoneura: Pleuroceridae). Journal de Conchyliologie 107: 3–51.
- Burch JB, Davis GM (1967) A taxonomic study of some species of the freshwater snail genus Semisulcospira in Japan. Annual reports for 1967: 36–38.
- Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34: i884–i890. https://doi.org/10.1093/bioinformatics/bty560
- Chifman J, Kubatko L (2014) Quartet inference from SNP data under the coalescent model. Bioinformatics 30: 3317–3324. https://doi.org/10.1093/bioinformatics/btu530
- Davis GM (1969) A taxonomic study of some species of Semisulcospira in Japan (Mesogastropoda: Pleuroceridae). Malacologia 7: 211–294.
- Du L-N, Guo-Hua Y, Jun-xing Y (2019a) Systematic relationships of Chinese freshwater semisulcospirids (Gastropoda, Cerithioidea) revealed by mitochondrial sequences. Zoological Research 40: 1–11. https://doi.org/10.24272/j.issn.2095-8137.2019.033
- Du L-N, Köhler F, Yu G-H, Chen X-Y, Yang J-X (2019b) Comparative morpho-anatomy and mitochondrial phylogeny of Semisulcospiridae in Yunnan, south-western China, with description of four new species (Gastropoda: Cerithioidea). Invertebrate Systematics 33: 825–848. https://doi.org/10.1071/IS18084
- Habe T (1965) Semisulcospira decipiens. In: Okada Y (Ed.) New Illuscrated Encyclopedia of the Fauna of Japan. Hukuryu-kan Publishing Co. Ltd., Chiyoda, 57 pp.
- Habe T (1978) Fresh water molluscs in Korea and Japan as the intermediate hosts of trematodes. Yonsei Reports on Tropical Medicine 9: 91–96.
- Habe T (1986) Mollusca. In: Ueno M (Ed.) The late Tamiji Kawamura Freshwater Biology of Japan. 4th edn. Hukuryu-kan Publishing Co. Ltd., Chiyoda, 309–341.
- Jeschke JM, Kokko H (2009) The roles of body size and phylogeny in fast and slow life histories. Evolutionary Ecology 23: 867–878. https://doi.org/10.1007/s10682-008-9276-y
- Kawase M, Murase F, Hayase Y, Ichihara T, Morikawa A, Ieyama H (2012) Freshwater mollusks in Gifu city, Gifu prefecture, Japan. Limnology in Tokai Region of Japan 54: 33–42.
- Kihira H, Matsuda M (1990) Freshwater Molluscs of Lake Biwa and Yodo River. Tatara Shobo Publishers, Yonago, 131 pp.
- Kihira H, Matsuda M, Uchiyama R (2009) Guide of Japanese Freshwater Molluscs (1). Freshwater Molluscs in Lake Biwa and Yodo River, Revised Edition. Pieces Publishers, Yokohama, 159 pp.
- Kobelt W (1879) Fauna molluscorum extramarinorum Japoniae. Nach den von Professor Rein Gemachten Sammlungen. Christian Winter, Frankfurt, 171 pp. https://doi.org/10.5962/bhl.title.12881
- Köhler F (2016) Rampant taxonomic incongruence in a mitochondrial phylogeny of Semisulcospira freshwater snails from Japan (Cerithioidea: Semisulcospiridae). Journal of Molluscan Studies 82: 268–281. https://doi.org/10.1093/mollus/eyv057
- Köhler F (2017) Against the odds of unusual mtDNA inheritance, introgressive hybridisation and phenotypic plasticity: systematic revision of Korean freshwater gastropods (Semisulcospiridae, Cerithioidea). Invertebrate Systematics 31: 249–268. https://doi.org/10.1071/IS16077
- Kuroda T (1929) On Japanese melanians. Venus 1: 179–193. https://doi.org/10.1515/crll.1929.161.179
- Matsuda M (2000) Semisulcospira (Biwamelania) reticulata. In: Japan (Ed.) Data Book on Rare Wild Aquatic Organism in Japan. Japan Fisheries Resource Conservation Association, Chuo, 8–9.
- Matsuda Y, Miura O (2022) Sexual dimorphism in the East Asian freshwater snail Semisulcospira libertina. Journal of Molluscan Studies 88: eyac028. https://doi.org/10.1093/mollus/eyac028
- Matsuoka K (1985) Pliocene freshwater gastropods from the Iga formation of the Kobiwako group, Mie Prefecture, central Japan. Transactions and proceedings of the Paleontological Society of Japan 139: 180–195.
- Minato H (1991) Biwamelania decipiens. In: Okutani T (Ed.) Illustrations of Animals and Plants. Mollusca. Third Edition. Sekaibunkasha Com., Chiyoda, 391 pp.
- Miura O, Urabe M, Nishimura T, Nakai K, Chiba S (2019) Recent lake expansion triggered the adaptive radiation of freshwater snails in the ancient Lake Biwa. Evolution Letters 3: 43–54. https://doi.org/10.1002/evl3.92
- Miura O, Urabe M, Mori H, Chiba S (2020) Ancient drainage networks mediated a large-scale genetic introgression in the East Asian freshwater snails. Ecology and Evolution 10: 8186–8196. https://doi.org/10.1002/ece3.6523
- Miura O, Toyoda A, Sakurai T (2023) Chromosome-scale genome assembly of the freshwater snail Semisulcospira habei from the Lake Biwa drainage system. Genome Biology and Evolution 15: evad208. https://doi.org/10.1093/gbe/evad208
- Morita K, Saito T, Uechi T, Sawada N, Miura O (2024) Out of the ancient lake: Multiple riverine colonizations and diversification of the freshwater snails in the genus Semisulcospira around Lake Biwa. Molecular Phylogenetics and Evolution 191: 107987./https://doi.org/10.1016/j.ympev.2023.107987
- Morrison JPE (1952) World relations of the melanians. American Malacological Union News Bulletin and Annual report 1951: 6–9.
- 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: 268–274. https://doi.org/10.1093/molbev/msu300
- Nishimura T (2024) Semisulcospira (Biwamelania) sp. https://tansuigyo.net/a_biwae/21.html
- Nishino M (2021) Semisulcospira (Biwamelania) reticulata. In: Scientific Committee for Research into the Wildlife in Shiga Prefecture (Ed.) Red Data Book of Shiga Prefecture 2020. Sunrise Publishing Co. , Ltd., Hikone, 618 pp.
- Nishino M, Watanabe NC (2000) Evolution and endmism in Lake Biwa, with special reference to its gastropod mollusc fauna. Advances in Ecological Research 31: 151–180. https://doi.org/10.1016/s0065-2504(00)31011-x
- Nishino M, Tanida K (2018) Illustration of Lake Biwa Benthic Fauna. Second Edition. Incorporated Administrative Agency Japan Water Agency Lake Biwa Development Integrated Operation & Maintenance Office, Otsu, 335 pp.
- Nomoto Y (2001) Studies on the explosive radiation in freshwater snails of the genus Biwamelania. PhD Thesis, The University of Tokyo, Bunkyo, Japan.
- Onuki K, Fuke Y (2022) Rediscovery of a native freshwater shrimp, Neocaridina denticulata, and expansion of an invasive species in and around Lake Biwa, Japan: genetic and morphological approach. Conservation Genetics 23: 967–980. https://doi.org/10.1007/s10592-022-01467-1
- Ota H (2011) Nagamasa Azai and the Battle of Anegawa, its prosperity and downfall. Sunrise Publishing Co. , Ltd., Hikone, 240 pp.
- R Core Team (2019) R for Windows, Version 3.6.1. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
- Reynolds J (2003) Life histories and extinction risk. In: Blackburn TM, Gaston KJ (Eds) Macroecology. Blackwell Publishing, Oxford, 195–217.
- Rintelen T von, Wilson AB, Meyer A, Glaubrecht M (2004) Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia. Proceedings of the Royal Society of London. Series B: Biological Sciences 271: 2541–2549. https://doi.org/10.1098/rspb.2004.2842
- Rochette NC, Rivera-Colón AG, Catchen JM (2019) Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology 28: 4737–4754. https://doi.org/10.1111/mec.15253
- Sahlin K (2022) Strobealign: flexible seed size enables ultra-fast and accurate read alignment. Genome Biology 23: 260. https://doi.org/10.1186/s13059-022-02831-7
- Sawada N, Fuke Y (2022) Systematic revision of the Japanese freshwater snail Semisulcospira decipiens (Mollusca: Semisulcospiridae): implications for diversification in the ancient Lake Biwa. Invertebrate Systematics 36: 1139–1177. https://doi.org/10.1071/IS22042
- Sawada N, Fuke Y (2023) Diversification in ancient Lake Biwa: integrative taxonomy reveals overlooked species diversity of the Japanese freshwater snail genus Semisulcospira (Mollusca: Semisulcospiridae). Contributions to Zoology 92: 1–37. https://doi.org/10.1163/18759866-bja10035
- Sawada N, Nakano T (2021) Revisiting a 135-year-old taxonomic account of the freshwater snail Semisulcospira multigranosa: designating its lectotype and describing a new species of the genus (Mollusca: Gastropoda: Semisulcospiridae). Zoological Studies 60: 7.
- Sawada N, Nakano T (2022) Insights into sex-related size and shape dimorphism in Semisulcospira niponica (Caenogastropoda: Cerithioidea: Semisulcospiridae). Journal of Molluscan Studies 88(2): eyac013. https://doi.org/10.1093/mollus/eyac013
- Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675. https://doi.org/10.1038/nmeth.2089
- Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland. https://paup.phylosolutions.com/
- Strong EE, Köhler F (2009) Morphological and molecular analysis of "Melania" jacqueti Dautzenberg & Fischer, 1906: From anonymous orphan to critical basal offshoot of the Semisulcospiridae (Gastropoda: Cerithioidea). Zoologica Scripta 38: 483–502. https://doi.org/10.1111/j.1463-6409.2008.00385.x
- Suyama Y, Matsuki Y (2015) MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Scientific Reports 5: 16963. https://doi.org/10.1038/srep16963
- Suyama Y, Hirota SK, Matsuo A, Tsunamoto Y, Mitsuyuki C, Shimura A, Okano K (2022) Complementary combination of multiplex high-throughput DNA sequencing for molecular phylogeny. Ecological Research 37: 171–181. https://doi.org/10.1111/1440-1703.12270
- Takami A (1994) The number and size of newborns in Semisulcospira nakasekoae and S. habei (Prosobranchia: Pleuroceridae). Venus 53: 201–209. https://doi.org/10.18941/venusjjm.53.3_201
- Takigawa Y, Kato S, Nakano T, Nakai K, Tomikawa K, Ishiwata S, Fujita T, Hosoya K, Kawase S, Senou H, Yoshino T, Nishino M (2020) The Vega collection at the end of the nineteenth-century survey of Lake Biwa. In: Kawanabe H, Nishino M, Maehata M (Eds) Lake Biwa: Interactions between Nature and People. Second Edition. Springer International Publishing, Cham, 248–257. https://doi.org/10.1007/978-3-030-16969-5_2
- Watanabe NC (1970a) Studies on three species of Semisulcospira in Lake Biwa: i) comparative studies of shell form and habitat. Venus 29: 13–30. https://doi.org/10.18941/venusjjm.29.1_13
- Watanabe NC (1970b) Studies on three species of Semisulcospira in Lake Biwa II) comparative studies of radulae. Venus 29: 93–98. https://doi.org/10.18941/venusjjm.29.3_93
- Watanabe NC (1980) Some factors affecting the distribution and abundance of the two melanian snails, Semisulcospira decipiens and S. reticulata, in Lake Biwa. Japanese Journal of Limnology 41: 212–224. https://doi.org/10.3739/rikusui.41.212
- Watanabe NC, Nishino M (1995) A study on taxonomy and distribution of the freshwater snail, genus Semisulcospira in Lake Biwa, with descriptions of eight new species. Lake Biwa Study Monographs 6: 1–36.
- Wenz W (1939) Gastropoda: Teil 1: Allgemeiner Teil und Prosobranchia. In: Schindewolf OH (Ed.) Handbuch der Paläozoologie. Bornträger, Berlin, 481–720.