{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T23:36:01Z","timestamp":1777505761543,"version":"3.51.4"},"reference-count":94,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,11,11]],"date-time":"2019-11-11T00:00:00Z","timestamp":1573430400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,11,11]],"date-time":"2019-11-11T00:00:00Z","timestamp":1573430400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Freshwater mussels (Unionida) are one of the most imperiled animal groups worldwide, revealing the fastest rates of extinction. Habitat degradation, river pollution and climate change are the primary causes of global decline. However, biological threats for freshwater mussels are still poorly known. Here, we describe a diverse ecological group of leeches (Hirudinea: Glossiphoniidae) inhabiting the mantle cavity of freshwater mussels. So far, examples of mussel-associated leech species are recorded from East Asia, Southeast Asia, India and Nepal, Africa, and North America. This group comprises a dozen glossiphoniid species with a hidden life style inside the mantle cavity of their hosts largely overlooked by researchers. We show that the association with freshwater mussels evolved independently in three leech clades, i.e. <jats:italic>Batracobdelloides<\/jats:italic>, <jats:italic>Hemiclepsis<\/jats:italic>, and <jats:italic>Placobdella<\/jats:italic>, at least since the Miocene. Seven mussel-associated leech species and two additional free-living taxa are described here as new to science.<\/jats:p>","DOI":"10.1038\/s41598-019-52688-3","type":"journal-article","created":{"date-parts":[[2019,11,11]],"date-time":"2019-11-11T11:03:02Z","timestamp":1573470182000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":45,"title":["Freshwater mussels house a diverse mussel-associated leech assemblage"],"prefix":"10.1038","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3878-4192","authenticated-orcid":false,"given":"Ivan N.","family":"Bolotov","sequence":"first","affiliation":[]},{"given":"Anna L.","family":"Klass","sequence":"additional","affiliation":[]},{"given":"Alexander V.","family":"Kondakov","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8612-7736","authenticated-orcid":false,"given":"Ilya V.","family":"Vikhrev","sequence":"additional","affiliation":[]},{"given":"Yulia V.","family":"Bespalaya","sequence":"additional","affiliation":[]},{"given":"Mikhail Yu","family":"Gofarov","sequence":"additional","affiliation":[]},{"given":"Boris Yu","family":"Filippov","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4042-7706","authenticated-orcid":false,"given":"Arthur E.","family":"Bogan","sequence":"additional","affiliation":[]},{"given":"Manuel","family":"Lopes-Lima","sequence":"additional","affiliation":[]},{"given":"Zau","family":"Lunn","sequence":"additional","affiliation":[]},{"given":"Nyein","family":"Chan","sequence":"additional","affiliation":[]},{"given":"Olga V.","family":"Aksenova","sequence":"additional","affiliation":[]},{"given":"Gennady A.","family":"Dvoryankin","sequence":"additional","affiliation":[]},{"given":"Yulia E.","family":"Chapurina","sequence":"additional","affiliation":[]},{"given":"Sang Ki","family":"Kim","sequence":"additional","affiliation":[]},{"given":"Yulia S.","family":"Kolosova","sequence":"additional","affiliation":[]},{"given":"Ekaterina S.","family":"Konopleva","sequence":"additional","affiliation":[]},{"given":"Jin Hee","family":"Lee","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4932-9558","authenticated-orcid":false,"given":"Alexander A.","family":"Makhrov","sequence":"additional","affiliation":[]},{"given":"Dmitry M.","family":"Palatov","sequence":"additional","affiliation":[]},{"given":"Elena M.","family":"Sayenko","sequence":"additional","affiliation":[]},{"given":"Vitaly M.","family":"Spitsyn","sequence":"additional","affiliation":[]},{"given":"Svetlana E.","family":"Sokolova","sequence":"additional","affiliation":[]},{"given":"Alena A.","family":"Tomilova","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0623-0275","authenticated-orcid":false,"given":"Than","family":"Win","sequence":"additional","affiliation":[]},{"given":"Natalia A.","family":"Zubrii","sequence":"additional","affiliation":[]},{"given":"Maxim V.","family":"Vinarski","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2019,11,11]]},"reference":[{"key":"52688_CR1","unstructured":"Fuller, S. L. H. Clams and mussels (Mollusca: Bivalvia). In Pollution ecology of freshwater invertebrates (eds Hart, C. W. & Fuller, S. L. H.) 215\u2013273 (Academic Press, 1974)."},{"key":"52688_CR2","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1080\/10641260902879000","volume":"17","author":"JM Grizzle","year":"2009","unstructured":"Grizzle, J. M. & Brunner, C. J. Infectious diseases of freshwater mussels and other freshwater bivalve mollusks. Reviews in Fisheries Science 17, 425\u2013467, https:\/\/doi.org\/10.1080\/10641260902879000 (2009).","journal-title":"Reviews in Fisheries Science"},{"key":"52688_CR3","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.biocon.2019.06.037","volume":"237","author":"JI Brian","year":"2019","unstructured":"Brian, J. I. & Aldridge, D. C. Endosymbionts: An overlooked threat in the conservation of freshwater mussels? Biological Conservation 237, 155\u2013165, https:\/\/doi.org\/10.1016\/j.biocon.2019.06.037 (2019).","journal-title":"Biological Conservation"},{"key":"52688_CR4","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1645\/GE-3565.1","volume":"92","author":"DD Edwards","year":"2006","unstructured":"Edwards, D. D. & Vidrine, M. F. Host specificity among Unionicola spp. (Acari: Unionicolidae) parasitizing freshwater mussels. Journal of Parasitology 92, 977\u2013984, https:\/\/doi.org\/10.1645\/GE-3565.1 (2006).","journal-title":"Journal of Parasitology"},{"key":"52688_CR5","unstructured":"Edwards, D. D. & Vidrine, M. F. Mites of freshwater mollusks (Eunice, Malcolm F. Vidrine, 2013)."},{"key":"52688_CR6","unstructured":"Muller-Liebenau, I. & Heard, W. H. Symbiocloeon: A new genus of Baetidae from Thailand (Insecta, Ephemeroptera). In Proceedings of the Second International Conference on Ephemeroptera (eds Pasternak, K. & Sowa, R.) 57\u201365 (Warszawa-Krakow, 1979)."},{"key":"52688_CR7","doi-asserted-by":"crossref","unstructured":"Gillies, M. T. & Elouard, J. M. The mayfly-mussel association, a new example from the river Niger basin in mayflies and stoneflies (ed. Campbell, I. C.) 289\u2013297 (Kluwer Academic Publishers, 1990).","DOI":"10.1007\/978-94-009-2397-3_35"},{"key":"52688_CR8","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1080\/00305316.2009.10417579","volume":"43","author":"KA Subramanian","year":"2009","unstructured":"Subramanian, K. A. & Sivaramakrishnan, K. G. A new species of Symbiocloeon (Ephemeroptera: Baetidae) associated with a freshwater mussel from India. Oriental Insects 43, 71\u201376, https:\/\/doi.org\/10.1080\/00305316.2009.10417579 (2009).","journal-title":"Oriental Insects"},{"key":"52688_CR9","doi-asserted-by":"crossref","first-page":"399","DOI":"10.21900\/j.inhs.v5.419","volume":"5","author":"HM Kelly","year":"1899","unstructured":"Kelly, H. M. A statistical study of the parasites of the Unionidae. Bulletin of the Illinois State Laboratory of Natural History 5, 399\u2013418 (1899).","journal-title":"Bulletin of the Illinois State Laboratory of Natural History"},{"key":"52688_CR10","first-page":"141","volume":"90","author":"MG Curry","year":"1976","unstructured":"Curry, M. G. & Vidrine, M. F. New fresh-water mussel host records for the leech Placobdella montifera, with distributional notes. Nautilus 90, 141\u2013144 (1976).","journal-title":"Nautilus"},{"key":"52688_CR11","unstructured":"Curry, M. G.\u00a0New freshwater unionid clam hosts for three glossiphoniid leeches. The Wasmann Journal of Biology 37, 89\u201392 (1979)."},{"key":"52688_CR12","first-page":"43","volume":"40","author":"MG Curry","year":"1977","unstructured":"Curry, M. G. & Vidrine, M. F. New freshwater clam host records for the leeches Placobdella montifera Moore and Helobdella stagnalis L. Proceedings of the Louisiana Academy of Sciences 40, 43\u201346 (1977).","journal-title":"Proceedings of theLouisiana Academy of Sciences"},{"key":"52688_CR13","first-page":"1","volume":"46","author":"RT Sawyer","year":"1972","unstructured":"Sawyer, R. T. North American freshwater leeches, exclusive of the Piscicolidae, with a key to all species. Illinois Biological Monographs 46, 1\u2013154 (1972).","journal-title":"Illinois Biological Monographs"},{"key":"52688_CR14","first-page":"63","volume":"9","author":"DJL Klemm","year":"1976","unstructured":"Klemm, D. J. L. (Annelida: Hirudinea) found in North American mollusks. Malacological Review 9, 63\u201376 (1976).","journal-title":"Malacological Review"},{"key":"52688_CR15","first-page":"165","volume":"7","author":"AS Oka","year":"1910","unstructured":"Oka, A. S. der Japanischen Hirudineen, mit Diagnosen der Neuen Species. Annotationes Zoologicae Japonenses 7, 165\u2013183 (1910).","journal-title":"Annotationes Zoologicae Japonenses"},{"key":"52688_CR16","first-page":"157","volume":"6","author":"A Oka","year":"1917","unstructured":"Oka, A. Zoological result of a tour in the Far East: Hirudinea. Memoirs of the Asiatic Society of Bengal 6, 157\u2013176 (1917).","journal-title":"Memoirs of the Asiatic Society of Bengal"},{"key":"52688_CR17","doi-asserted-by":"publisher","first-page":"64","DOI":"10.2183\/pjab1912.4.64","volume":"4","author":"A Oka","year":"1928","unstructured":"Oka, A. Description de l\u2019Hemiclepsis kasmiana. Ibid 4, 64\u201366, https:\/\/doi.org\/10.2183\/pjab1912.4.64 (1928).","journal-title":"Ibid"},{"key":"52688_CR18","unstructured":"Sawyer, R. T. Leech biology and behavior. Vol. 2. Feeding biology, ecology, and systematics (Oxford, Clarendon Press, 1986)."},{"key":"52688_CR19","unstructured":"Yang, T. Annelida Hirudinea (Fauna Sinica) (Beijing, Science Press, 1996)."},{"key":"52688_CR20","unstructured":"Lai, Y. T. & Chen J. H. Leech fauna of Taiwan (Taipei, National Taiwan University Press, 2010)."},{"key":"52688_CR21","doi-asserted-by":"publisher","first-page":"386","DOI":"10.11646\/zootaxa.4319.2.1","volume":"4319","author":"IN Bolotov","year":"2017","unstructured":"Bolotov, I. N. et al. Discovery and natural history of the mussel leech Batracobdella kasmiana (Oka, 1910) (Hirudinida: Glossiphoniidae) in Russia. Zootaxa 4319, 386\u2013390, https:\/\/doi.org\/10.11646\/zootaxa.4319.2.1 (2017).","journal-title":"Zootaxa"},{"key":"52688_CR22","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1093\/mollus\/eyy016","volume":"84","author":"RW Wu","year":"2018","unstructured":"Wu, R. W., Chen, T. H., Zanatta, D. T., Ouyang, S. & Wu, X. P. Reproductive traits of nine freshwater mussel species (Mollusca: Unionidae) from Poyang Lake, China. Journal of Molluscan Studies 84, 324\u2013332, https:\/\/doi.org\/10.1093\/mollus\/eyy016 (2018).","journal-title":"Journal of Molluscan Studies"},{"key":"52688_CR23","doi-asserted-by":"publisher","first-page":"689","DOI":"10.5962\/bhl.part.1482","volume":"22","author":"T Kaburaki","year":"1921","unstructured":"Kaburaki, T. Notes on some leeches in the collection of the Indian Museum. Records of the Indian Museum 22, 689\u2013719 (1921).","journal-title":"Records of the Indian Museum"},{"key":"52688_CR24","unstructured":"Harding, W. A. & Moore, P. The Fauna of British India, including Ceylon and Burma: Hirudinea (London, Taylor and Francis, 1927)."},{"key":"52688_CR25","unstructured":"Chandra, M. The Leeches of India \u2013 A Handbook (Calcutta, Zoological Survey of India, 1991)."},{"key":"52688_CR26","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1007\/BF00027023","volume":"184","author":"JH Oosthuizen","year":"1989","unstructured":"Oosthuizen, J. H. Redescription of the African fish leech Batracobdelloides tricarinata (Blanchard, 1897) (Hirudinea: Glossiphoniidae). Hydrobiologia 184, 153\u2013164, https:\/\/doi.org\/10.1007\/BF00027023 (1989).","journal-title":"Hydrobiologia"},{"key":"52688_CR27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.4172\/2155-9546.1000551","volume":"9","author":"GM Elkhodary","year":"2018","unstructured":"Elkhodary, G. M., Omran, N. E., Hassan, A. A., El-Saidy, S. A. & Mona, M. H. Nutritional value of the Egyptian freshwater bivalve Spathopsis rubens arcuata under the effect of depuration. Journal of Aquaculture Research and Development 9, 1\u20139, https:\/\/doi.org\/10.4172\/2155-9546.1000551 (2018).","journal-title":"Journal of Aquaculture Research and Development"},{"key":"52688_CR28","first-page":"69","volume":"21","author":"H Nesemann","year":"1995","unstructured":"Nesemann, H. & Cs\u00e4nyi, B. Description of Batracobdelloides moogi n. sp., a leech genus and species new to the European fauna with notes on the identity of Hirudo paludosa Carena, 1824 (Hirudinea: Glossiphoniidae). Lauterbornia 21, 69\u201378 (1995).","journal-title":"Lauterbornia"},{"key":"52688_CR29","first-page":"233","volume":"7","author":"A Soos","year":"1967","unstructured":"Soos, A. On the genus Hemiclepsis Vejdovsky, 1884, with a key and catalogue of the species (Hirudinoidea: Glossiphoniidae). Opuscula Zoologica (Budapest) 7, 233\u2013240 (1967a).","journal-title":"Opuscula Zoologica (Budapest)"},{"key":"52688_CR30","first-page":"243","volume":"59","author":"A Soos","year":"1967","unstructured":"Soos, A. On the genus Batracobdella Viguier, 1879, with a key and catalogue to the species (Hirudinoidea: Glossiphoniidae). Annales Historico-Naturales Musei Nationales Hungarici (Pars Zoologica) 59, 243\u2013257 (1967b).","journal-title":"Annales Historico-Naturales Musei Nationales Hungarici (Pars Zoologica)"},{"key":"52688_CR31","first-page":"5","volume":"11","author":"H Nesemann","year":"1997","unstructured":"Nesemann, H. Rediscovery of the leech genus Ancyrobdella (Hirudinea, Glossiphoniidae). Miscellanea Zoologica Hungarica 11, 5\u201310 (1997).","journal-title":"Miscellanea Zoologica Hungarica"},{"key":"52688_CR32","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.ympev.2016.07.020","volume":"103","author":"IN Bolotov","year":"2016","unstructured":"Bolotov, I. N. et al. Multi-locus fossil-calibrated phylogeny, biogeography and a subgeneric revision of the Margaritiferidae (Mollusca: Bivalvia: Unionoida). Molecular Phylogenetics and Evolution 103, 104\u2013121, https:\/\/doi.org\/10.1016\/j.ympev.2016.07.020 (2016).","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"52688_CR33","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1007\/s13127-016-0262-x","volume":"16","author":"E Froufe","year":"2016","unstructured":"Froufe, E. et al. Who lives where? Molecular and morphometric analyses clarify which Unio species (Unionida, Mollusca) inhabit the southwestern Palearctic. Organisms Diversity & Evolution 16, 597\u2013611, https:\/\/doi.org\/10.1007\/s13127-016-0262-x (2016).","journal-title":"Organisms Diversity & Evolution"},{"key":"52688_CR34","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.gene.2005.01.008","volume":"349","author":"JG Inoue","year":"2005","unstructured":"Inoue, J. G., Miya, M., Venkatesh, B. & Nishida, M. The mitochondrial genome of Indonesian coelacanth Latimeria menadoensis (Sarcopterygii: Coelacanthiformes) and divergence time estimation between the two coelacanths. Gene 349, 227\u2013235, https:\/\/doi.org\/10.1016\/j.gene.2005.01.008 (2005).","journal-title":"Gene"},{"key":"52688_CR35","doi-asserted-by":"publisher","first-page":"2475","DOI":"10.1046\/j.1365-294X.2002.01652.x","volume":"11","author":"TL Shearer","year":"2002","unstructured":"Shearer, T. L., Van Oppen, M. J. H., Romano, S. L. & W\u00f6rheide, G. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 2475\u20132487, https:\/\/doi.org\/10.1046\/j.1365-294X.2002.01652.x (2002).","journal-title":"Molecular Ecology"},{"key":"52688_CR36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2148-6-2","volume":"6","author":"ME Hellberg","year":"2006","unstructured":"Hellberg, M. E. No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology 6, 1\u20138, https:\/\/doi.org\/10.1186\/1471-2148-6-2 (2006).","journal-title":"BMC Evolutionary Biology"},{"key":"52688_CR37","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1111\/j.1439-0426.2008.01088.x","volume":"24","author":"J Krieger","year":"2008","unstructured":"Krieger, J., Hett, A. K., Fuerst, P. A., Artyukhin, E. & Ludwig, A. The molecular phylogeny of the order Acipenseriformes revisited. Journal of Applied Ichthyology 24, 36\u201345, https:\/\/doi.org\/10.1111\/j.1439-0426.2008.01088.x (2008).","journal-title":"Journal of Applied Ichthyology"},{"key":"52688_CR38","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-02312-z","volume":"7","author":"IN Bolotov","year":"2017","unstructured":"Bolotov, I. N. et al. Ancient river inference explains exceptional Oriental freshwater mussel radiations. Scientific Reports 7, 1\u201314, https:\/\/doi.org\/10.1038\/s41598-017-02312-z (2017).","journal-title":"Scientific Reports"},{"key":"52688_CR39","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-11957-9","volume":"7","author":"IN Bolotov","year":"2017","unstructured":"Bolotov, I. N. et al. New taxa of freshwater mussels (Unionidae) from a species-rich but overlooked evolutionary hotspot in Southeast Asia. Scientific Reports 7, 1\u201318, https:\/\/doi.org\/10.1038\/s41598-017-11957-9 (2017).","journal-title":"Scientific Reports"},{"key":"52688_CR40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-018-28385-y","volume":"8","author":"IN Bolotov","year":"2018","unstructured":"Bolotov, I. N. et al. A new genus and tribe of freshwater mussel (Unionidae) from Southeast Asia. Scientific Reports 8, 1\u201312, https:\/\/doi.org\/10.1038\/s41598-018-28385-y (2018).","journal-title":"Scientific Reports"},{"key":"52688_CR41","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1007\/s10750-017-3104-8","volume":"810","author":"A Zieritz","year":"2018","unstructured":"Zieritz, A. et al. Diversity, biogeography and conservation of freshwater mussels (Bivalvia: Unionida) in East and Southeast Asia. Hydrobiologia 810, 29\u201344, https:\/\/doi.org\/10.1007\/s10750-017-3104-8 (2018).","journal-title":"Hydrobiologia"},{"key":"52688_CR42","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.ympev.2018.09.019","volume":"130","author":"XC Huang","year":"2019","unstructured":"Huang, X. C. et al. Towards a global phylogeny of freshwater mussels (Bivalvia: Unionida): Species delimitation of Chinese taxa, mitochondrial phylogenomics, and diversification patterns. Molecular Phylogenetics and Evolution 130, 45\u201359, https:\/\/doi.org\/10.1016\/j.ympev.2018.09.019 (2019).","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"52688_CR43","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-018-29451-1","volume":"8","author":"OV Aksenova","year":"2018","unstructured":"Aksenova, O. V. et al. Species richness, molecular taxonomy and biogeography of the radicine pond snails (Gastropoda: Lymnaeidae) in the Old World. Scientific Reports 8, 1\u201317, https:\/\/doi.org\/10.1038\/s41598-018-29451-1 (2018).","journal-title":"Scientific Reports"},{"key":"52688_CR44","doi-asserted-by":"publisher","unstructured":"R\u00fcber, L., Tan, H. H. & Britz, R. Snakehead (Teleostei: Channidae) diversity and the Eastern Himalaya biodiversity hotspot. Journal of Zoological Systematics and Evolutionary Research, https:\/\/doi.org\/10.1111\/jzs.12324 (2019).","DOI":"10.1111\/jzs.12324"},{"key":"52688_CR45","unstructured":"Sawyer, R.T. Leech Behavior. In Neurobiology of the Leech (eds Muller, K. J., Nichols, J. G. & Stent, G. S.) 7\u201326 (Cold Spring Harbor, Cold Spring Harbor Laboratory Publications, 1981)."},{"key":"52688_CR46","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1078\/1431-7613-00034","volume":"120","author":"U Kutschera","year":"2001","unstructured":"Kutschera, U. & Wirtz, P. The evolution of parental care in freshwater leeches. Theory in Biosciences 120, 115\u2013137, https:\/\/doi.org\/10.1078\/1431-7613-00034 (2001).","journal-title":"Theory in Biosciences"},{"key":"52688_CR47","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1139\/z79-060","volume":"57","author":"PM McKee","year":"1979","unstructured":"McKee, P. M. & Mackie, G. L. Incidence of Marvinmeyeria lucida (Hirudinea: Glossiphoniidae) in the fingernail clam, Sphaerium occidentale. Canadian Journal of Zoology 57, 499\u2013503, https:\/\/doi.org\/10.1139\/z79-060 (1979).","journal-title":"Canadian Journal of Zoology"},{"key":"52688_CR48","doi-asserted-by":"crossref","unstructured":"Karatayev, A. Y., Burlakova, L. E., Molloy, D. P. & Volkova, L. K. Endosymbionts of Dreissena polymorpha (Pallas) in Belarus. International Review of Hydrobiology 85, 543\u2013559, doi:10.1002\/1522-2632(200011)85:5\/6<543::AID-IROH543>3.0.CO;2-3 (2000).","DOI":"10.1002\/1522-2632(200011)85:5\/6<543::AID-IROH543>3.0.CO;2-3"},{"key":"52688_CR49","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1515\/helm-2017-0044","volume":"54","author":"DJ L\u00f3pez-Peraza","year":"2017","unstructured":"L\u00f3pez-Peraza, D. J., Hern\u00e1ndez-Rodr\u00edguez, M., Bar\u00f3n-Sevilla, B., B\u00fcckle-Ram\u00edrez, L. F. & Grano-Maldonado, M. I. First record of Stibarobdella moorei (Annelida, Hirudinea, Piscicolidae) a marine leech parasitizing Octopus bimaculatus (Mollusca: Octopodidae) from the Mexican Pacific coast. Helminthologia 54, 322\u2013329, https:\/\/doi.org\/10.1515\/helm-2017-0044 (2017).","journal-title":"Helminthologia"},{"key":"52688_CR50","doi-asserted-by":"publisher","first-page":"23","DOI":"10.3897\/zookeys.794.28088","volume":"794","author":"AL Klass","year":"2018","unstructured":"Klass, A. L. et al. An example of a possible leech-bryozoan association in freshwater. ZooKeys 794, 23\u201330, https:\/\/doi.org\/10.3897\/zookeys.794.28088 (2018).","journal-title":"ZooKeys"},{"key":"52688_CR51","doi-asserted-by":"publisher","first-page":"51","DOI":"10.3354\/meps020051","volume":"20","author":"NA Sloan","year":"1984","unstructured":"Sloan, N. A., Bower, S. M. & Robinson, S. M. C. Cocoon deposition on three crab species and fish parasitism by the leech Notostomum cyclostoma from deep fjords in northern British Columbia. Marine Ecology Progress Series 20, 51\u201358 (1984).","journal-title":"Marine Ecology Progress Series"},{"key":"52688_CR52","first-page":"95","volume":"41","author":"TA Hall","year":"1999","unstructured":"Hall, T. A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95\/98\/NT. Nucleic Acids Symposium Series 41, 95\u201398 (1999).","journal-title":"Nucleic Acids Symposium Series"},{"issue":"3","key":"52688_CR53","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1111\/j.1471-8286.2007.01678.x","volume":"7","author":"SUJEEVAN RATNASINGHAM","year":"2007","unstructured":"Ratnasingham, S. & Hebert, P. D. BOLD: The Barcode of Life Data System, http:\/\/www.barcodinglife.org. Molecular Ecology Notes 7, 355\u2013364, https:\/\/doi.org\/10.1111\/j.1471-8286.2007.01678.x (2007).","journal-title":"Molecular Ecology Notes"},{"key":"52688_CR54","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","volume":"215","author":"SF Altschul","year":"1990","unstructured":"Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. Journal of Molecular Biology 215, 403\u2013410, https:\/\/doi.org\/10.1016\/S0022-2836(05)80360-2 (1990).","journal-title":"Journal of Molecular Biology"},{"key":"52688_CR55","doi-asserted-by":"publisher","first-page":"1870","DOI":"10.1093\/molbev\/msw054","volume":"33","author":"S Kumar","year":"2016","unstructured":"Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870\u20131874, https:\/\/doi.org\/10.1093\/molbev\/msw054 (2016).","journal-title":"Molecular Biology and Evolution"},{"key":"52688_CR56","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1080\/10635150701472164","volume":"56","author":"G Talavera","year":"2007","unstructured":"Talavera, G. & Castresana, J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564\u2013577, https:\/\/doi.org\/10.1080\/10635150701472164 (2007).","journal-title":"Systematic Biology"},{"key":"52688_CR57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S1055-7903(02)00326-3","volume":"26","author":"X Xia","year":"2003","unstructured":"Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1\u20137, https:\/\/doi.org\/10.1016\/S1055-7903(02)00326-3 (2003).","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"52688_CR58","doi-asserted-by":"crossref","unstructured":"Xia, X. & Lemey, P. Assessing substitution saturation with DAMBE. In The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny, Second Edition (eds Lemey, P., Salemi, M. & Vandamme, A.) 615\u2013630 (Cambridge University Press, 2009).","DOI":"10.1017\/CBO9780511819049.022"},{"key":"52688_CR59","unstructured":"Swofford, D.L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b10 (Sunderland, Sinauer Associates, 2002)."},{"key":"52688_CR60","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1016\/j.ympev.2011.07.016","volume":"61","author":"NV Whelan","year":"2011","unstructured":"Whelan, N. V., Geneva, A. J. & Graf, D. L. Molecular phylogenetic analysis of tropical freshwater mussels (Mollusca: Bivalvia: Unionoida) resolves the position of Coelatura and supports a monophyletic Unionidae. Molecular Phylogenetics and Evolution 61, 504\u2013514 (2011).","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"52688_CR61","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1111\/j.1471-8286.2007.01821.x","volume":"7","author":"P Villesen","year":"2007","unstructured":"Villesen, P. FaBox: an online toolbox for fasta sequences. Molecular Ecology Notes 7, 965\u2013968, https:\/\/doi.org\/10.1111\/j.1471-8286.2007.01821.x (2007).","journal-title":"Molecular Ecology Notes"},{"key":"52688_CR62","doi-asserted-by":"publisher","first-page":"W232","DOI":"10.1093\/nar\/gkw256","volume":"44","author":"J Trifinopoulos","year":"2016","unstructured":"Trifinopoulos, J., Nguyen, L. T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44, W232\u2013W235, https:\/\/doi.org\/10.1093\/nar\/gkw256 (2016).","journal-title":"Nucleic Acids Research"},{"key":"52688_CR63","doi-asserted-by":"publisher","first-page":"518","DOI":"10.1093\/molbev\/msx281","volume":"35","author":"DT Hoang","year":"2017","unstructured":"Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518\u2013522, https:\/\/doi.org\/10.1093\/molbev\/msx281 (2017).","journal-title":"Molecular Biology and Evolution"},{"key":"52688_CR64","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1038\/nmeth.4285","volume":"14","author":"S Kalyaanamoorthy","year":"2017","unstructured":"Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587\u2013589, https:\/\/doi.org\/10.1038\/nmeth.4285 (2017).","journal-title":"Nature Methods"},{"key":"52688_CR65","doi-asserted-by":"publisher","first-page":"486","DOI":"10.1093\/molbev\/msx302","volume":"35","author":"X Zhou","year":"2017","unstructured":"Zhou, X., Shen, X. X., Hittinger, C. T. & Rokas, A. Evaluating fast maximum likelihood-based phylogenetic programs using empirical phylogenomic data sets. Molecular Biology and Evolution 35, 486\u2013503, https:\/\/doi.org\/10.1093\/molbev\/msx302 (2017).","journal-title":"Molecular Biology and Evolution"},{"key":"52688_CR66","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1093\/sysbio\/sys029","volume":"61","author":"F Ronquist","year":"2012","unstructured":"Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539\u2013542, https:\/\/doi.org\/10.1093\/sysbio\/sys029 (2012).","journal-title":"Systematic Biology"},{"key":"52688_CR67","doi-asserted-by":"publisher","first-page":"901","DOI":"10.1093\/sysbio\/syy032","volume":"67","author":"A Rambaut","year":"2018","unstructured":"Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901\u2013904, https:\/\/doi.org\/10.1093\/sysbio\/syy032 (2018).","journal-title":"Systematic Biology"},{"key":"52688_CR68","doi-asserted-by":"crossref","unstructured":"Miller, M., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Gateway Computing Environments Workshop (GCE) 1\u20138 (IEEE, 2010).","DOI":"10.1109\/GCE.2010.5676129"},{"key":"52688_CR69","doi-asserted-by":"publisher","first-page":"1630","DOI":"10.1093\/bioinformatics\/btx025","volume":"33","author":"P Kapli","year":"2017","unstructured":"Kapli, P. et al. Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33, 1630\u20131638, https:\/\/doi.org\/10.1093\/bioinformatics\/btx025 (2017).","journal-title":"Bioinformatics"},{"key":"52688_CR70","doi-asserted-by":"publisher","first-page":"848","DOI":"10.2478\/s11756-011-0100-8","volume":"66","author":"A Bielecki","year":"2011","unstructured":"Bielecki, A. et al. Batracobdelloides moogi Nesemann et Cs\u00e1nyi, 1995 (Hirudinida: Glossiphoniidae): Morphometry and structure of the alimentary tract and reproductive system. Biologia 66, 848\u2013855, https:\/\/doi.org\/10.2478\/s11756-011-0100-8 (2011).","journal-title":"Biologia"},{"key":"52688_CR71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/ve\/vey016","volume":"4","author":"MA Suchard","year":"2018","unstructured":"Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution 4, 1\u20135, https:\/\/doi.org\/10.1093\/ve\/vey016 (2018).","journal-title":"Virus Evolution"},{"key":"52688_CR72","doi-asserted-by":"publisher","first-page":"20971","DOI":"10.1073\/pnas.1218879109","volume":"109","author":"B Bomfleur","year":"2012","unstructured":"Bomfleur, B., Kerp, H., Taylor, T. N., Moestrup, \u00d8. & Taylor, E. L. Triassic leech cocoon from Antarctica contains fossil bell animal. Proceedings of the National Academy of Sciences 109, 20971\u201320974, https:\/\/doi.org\/10.1073\/pnas.1218879109 (2012).","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"52688_CR73","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.ympev.2018.05.001","volume":"127","author":"M Tessler","year":"2018","unstructured":"Tessler, M. et al. Worms that suck: phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida. Molecular Phylogenetics and Evolution 127, 129\u2013134, https:\/\/doi.org\/10.1016\/j.ympev.2018.05.001 (2018).","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"52688_CR74","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.1111\/pala.12129","volume":"57","author":"L Parry","year":"2014","unstructured":"Parry, L., Tanner, A. & Vinther, J. The origin of annelids. Palaeontology 57, 1091\u20131103, https:\/\/doi.org\/10.1111\/pala.12129 (2014).","journal-title":"Palaeontology"},{"key":"52688_CR75","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.ympev.2015.03.008","volume":"87","author":"Y Yu","year":"2015","unstructured":"Yu, Y., Harris, A. J., Blair, C. & He, X. J. RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Molecular Phylogenetics and Evolution 87, 46\u201349, https:\/\/doi.org\/10.1016\/j.ympev.2015.03.008 (2015).","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"52688_CR76","first-page":"153","volume":"25","author":"JP Moore","year":"1906","unstructured":"Moore, J. P. Hirudinea and Oligochaeta collected in the Great Lakes region. Bulletin of the Bureau of Fisheries 25, 153\u2013172 (1906).","journal-title":"Bulletin of the Bureau of Fisheries"},{"key":"52688_CR77","unstructured":"Say, T. Class Vermes. Order Cryptobranchia. Hirudo in Narrative of an expedition to the source of St. Peter\u2019s River, Lake Winnepeek, Lake of the Woods, etc. etc. performed in the year 1823, vol. 2 (compiler Keating, W. H.) 266\u2013268 (Philadelphia, H.C. Carey & I. Lea, 1824)."},{"key":"52688_CR78","doi-asserted-by":"publisher","first-page":"44","DOI":"10.22621\/cfn.v123i1.673","volume":"123","author":"CM Davy","year":"2009","unstructured":"Davy, C. M., Shim, K. C. & Coombes, S. M. Leech (Annelida: Hirudinea) infestations on Canadian turtles, including the first Canadian record of Helobdella modesta from freshwater turtles. The Canadian Field-Naturalist 123, 44\u201347, https:\/\/doi.org\/10.22621\/cfn.v123i1.673 (2009).","journal-title":"The Canadian Field-Naturalist"},{"key":"52688_CR79","unstructured":"Nesemann, H. et al. Aquatic invertebrates of the Ganga river system: Volume 1: Mollusca, Annelida, Crustacea (in part) (Kathmandu, Hasko Nesemann & Chandi Press, 2007)."},{"key":"52688_CR80","doi-asserted-by":"publisher","first-page":"25","DOI":"10.4102\/koedoe.v34i2.421","volume":"34","author":"JH Oosthuizen","year":"1991","unstructured":"Oosthuizen, J. H. An annotated check list of the leeches (Annelida: Hirudinea) of the Kruger National Park with a key to the species. Koedoe 34, 25\u201338, https:\/\/doi.org\/10.4102\/koedoe.v34i2.421 (1991).","journal-title":"Koedoe"},{"key":"52688_CR81","first-page":"29","volume":"4","author":"C Grosser","year":"2005","unstructured":"Grosser, C. & Pe\u0161i\u0107, V. First record of Batracobdelloides moogi (Hirudinea: Glossiphoniidae) in the Balkans. Natura Montenegrina 4, 29\u201332 (2005).","journal-title":"Natura Montenegrina"},{"key":"52688_CR82","first-page":"19","volume":"15","author":"T Yamauchi","year":"2008","unstructured":"Yamauchi, T., Itoh, T., Yamaguchi, K. & Nagasawa, K. Some leeches (Annelida: Hirudinida: Piscicolidae, Glossiphoniidae) in the Hii River system, Shimane Prefecture, Japan. Laguna 15, 19\u201323 (2008).","journal-title":"Laguna"},{"key":"52688_CR83","unstructured":"Kearn, G. C. Leeches, lice and lampreys: a natural history of skin and gill parasites of fishes (Springer Science & Business Media, 2005)."},{"key":"52688_CR84","doi-asserted-by":"publisher","first-page":"37","DOI":"10.3897\/zookeys.545.6053","volume":"545","author":"IA Kaygorodova","year":"2015","unstructured":"Kaygorodova, I. A. Annotated checklist of the leech species diversity in the Maloe More Strait of Lake Baikal, Russia. ZooKeys 545, 37\u201352, https:\/\/doi.org\/10.3897\/zookeys.545.6053 (2015).","journal-title":"ZooKeys"},{"key":"52688_CR85","first-page":"1","volume":"109","author":"EI Lukin","year":"1976","unstructured":"Lukin, E. I. Leeches of fresh and brackish water bodies. Fauna of the USSR 109, 1\u2013484 (1976).","journal-title":"Fauna of the USSR"},{"key":"52688_CR86","doi-asserted-by":"publisher","first-page":"51","DOI":"10.2183\/pjab1912.8.51","volume":"8","author":"A Oka","year":"1932","unstructured":"Oka, A. Sur une nouvelle esp\u00e8ce de Placobdella, Pl. japonica n. sp. Proceedings of the Imperial Academy 8, 51\u201353 (1932).","journal-title":"Proceedings of the Imperial Academy"},{"key":"52688_CR87","first-page":"27","volume":"6","author":"T Yang","year":"1981","unstructured":"Yang, T. Two new species of parasitic leeches from freshwater fishes in China. Acta Zootaxonomica Sinica 6, 27\u201330 (1981).","journal-title":"Acta Zootaxonomica Sinica"},{"key":"52688_CR88","first-page":"289","volume":"3","author":"E-G Tan","year":"2001","unstructured":"Tan, E.-G. & Liu, X.-Q. One new species of the genus Hemiclepsis (Rhynchobdellida: Glossiphoniidae). Acta Zootaxonomica Sinica 3, 289\u2013291 (2001).","journal-title":"Acta Zootaxonomica Sinica"},{"key":"52688_CR89","first-page":"343","volume":"76","author":"JP Moore","year":"1924","unstructured":"Moore, J. P. Notes on some Asiatic leeches (Hirudinea) principally from China, Kashmir, and British India. Proceedings of the Academy of Natural Sciences of Philadelphia 76, 343\u2013388 (1924).","journal-title":"Proceedings of the Academy of Natural Sciences of Philadelphia"},{"key":"52688_CR90","first-page":"203","volume":"48","author":"HOP Shrivastav","year":"1971","unstructured":"Shrivastav, H. O. P. & Shah, H. L. Occurrence of the leech Hemiclepsis marginata asiatica in the bile duct of a pig (Sus scrofa domestica). Indian Veterinary Journal 48, 203\u2013204 (1971).","journal-title":"Indian Veterinary Journal"},{"key":"52688_CR91","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1017\/S0031182000025403","volume":"50","author":"SC Baugh","year":"1960","unstructured":"Baugh, S. C. Studies on Indian Rhynchobdellid leeches. Parasitology 50, 287\u2013301, https:\/\/doi.org\/10.1017\/S0031182000025403 (1960).","journal-title":"Parasitology"},{"key":"52688_CR92","doi-asserted-by":"crossref","first-page":"265","DOI":"10.26515\/rzsi\/v80\/i3-4\/1982\/161193","volume":"80","author":"M Chandra","year":"1983","unstructured":"Chandra, M. A check-list of leeches of India. Records of the Zoological Survey of India 80, 265\u2013290 (1983).","journal-title":"Records of the Zoological Survey of India"},{"key":"52688_CR93","first-page":"153","volume":"113","author":"CK Mandal","year":"2013","unstructured":"Mandal, C. K. Hemiclepsis chharwardamensis sp. nov. (Hirudinea: Glossiphonidae) a new species of leech from Jharkhand. India. Records of the Zoological Survey of India 113, 153\u2013155 (2013).","journal-title":"India. Records of the Zoological Survey of India"},{"key":"52688_CR94","first-page":"345","volume":"36","author":"JE Chelladurai","year":"1934","unstructured":"Chelladurai, J. E. On a new Indian leech Hemiclepsis viridis sp. nov. Records of the Indian Museum 36, 345\u2013352 (1934).","journal-title":"Records of the Indian Museum"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-52688-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-52688-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-52688-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T15:43:13Z","timestamp":1671291793000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-52688-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,11,11]]},"references-count":94,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["52688"],"URL":"https:\/\/doi.org\/10.1038\/s41598-019-52688-3","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,11,11]]},"assertion":[{"value":"6 October 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 October 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 November 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"16449"}}