An integrative taxonomic study of the genus Theromyzon (Hirudinea: Glossiphoniidae), with description of a new North American species
Maddy Foote![https://orcid.org/0000-0001-9837-6329](/media/client/orcid_16x16.png)
A Department of Natural History, Royal Ontario Museum, 100 Queens Park, Toronto, ON, M5S 2C6, Canada.
B Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
Invertebrate Systematics 36(7) 631-646 https://doi.org/10.1071/IS21062
Submitted: 16 September 2021 Accepted: 20 February 2022 Published: 27 July 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
Theromyzon Philippi, 1867 is a genus of sanguivorous, freshwater leeches in the family Glossiphoniidae. The genus is broadly distributed across the globe, possibly due to the frequent feeding in the nasopharyngeal cavities of migratory waterfowl that may allow for long distance dispersal. The genus has a history of taxonomic confusion resulting from mischaracterisations of key morphological features of type specimens that have produced several re-descriptions and synonyms. Here, we bring partial order to this confusion through robust morphological investigations of newly collected North American (and a single South American) specimens, representing most of the known species diversity from this continent. We also produce the first species-level phylogeny for Theromyzon and attempt to understand species boundaries regarding both morphology and genetics. Our results demonstrate that there are at least five species of Theromyzon present in North America (T. bifarium, T. tessulatum, T. rude, T. trizonare, and a clade that needs further investigation), and a hitherto undescribed taxon that does not conform to any previously published description, and represents a unique lineage in the phylogeny; we describe this new species under the name Theromyzon tigris sp. nov. This study sheds light on the discriminatory power of select morphological characters and the distribution of phenotypes within the genus. We also provide a comprehensive classification framework for the known species within the genus designed to facilitate identification and minimise future taxonomic confusion.
Keywords: Glossiphoniidae, Hirudinea, Hirudinida, leech, phylogenetics, species diversity, taxonomy, Theromyzon, Theromyzon tigris.
References
Anderson, K, Braoudakis, G, and Kvist, S (2020). Genetic variation, pseudocryptic diversity, and phylogeny of Erpobdella (Annelida: Hirudinida: Erpobdelliformes), with emphasis on Canadian species. Molecular Phylogenetics and Evolution 143, 106688.| Genetic variation, pseudocryptic diversity, and phylogeny of Erpobdella (Annelida: Hirudinida: Erpobdelliformes), with emphasis on Canadian species.Crossref | GoogleScholarGoogle Scholar |
Baird, W (1869). Descriptions of some new suctorial annelids in the collection of the British Museum. Proceedings of the Zoological Society of London 37, 310–318.
| Descriptions of some new suctorial annelids in the collection of the British Museum.Crossref | GoogleScholarGoogle Scholar |
Bielecki, A, Jelen, I, Cichocka, J, and Walerzak, A (2016). Theromyzon tessulatum (O.F. Muller, 1774) (Clitellata: Hirudinida: Glossiphoniidae) – morphometry and structure of the digestive and reproductive systems. Annals of Parasitology 62, 45.
Blanchard, R (1893). Révision des Hirudinées du Musée de Dresde. Abhandlungen und Berichte des Konigl. Zoologischen und Anthropologisch-Etnographischen Museums zu Dresden 4, 1–8.
Borda, E, and Siddall, ME (2004). Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Molecular Phylogenetics and Evolution 30, 213–225.
| Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution.Crossref | GoogleScholarGoogle Scholar |
Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, C-H, Xie, D, Suchard, MA, Rambaut, A, and Drummond, AJ (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
| BEAST 2: a software platform for Bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar |
Christoffersen, ML (2007). Clitellate evolution and leech diversity : Glossiphoniidae excl. Helobdella (Annelida : Hirudinea : Rhynchobdellida) from South America. Gaia. Scientia 1, 131–140.
Davies, RW, and Oosthuizen, JH (1993). A new species of duck leech from North America formerly confused with Theromyzon rude (Rhynchobdellida: Glossiphoniidae). Canadian Journal of Zoology 71, 770–775.
| A new species of duck leech from North America formerly confused with Theromyzon rude (Rhynchobdellida: Glossiphoniidae).Crossref | GoogleScholarGoogle Scholar |
de Carle, D, Oceguera-Figueroa, A, Tessler, M, Siddall, ME, and Kvist, S (2017). Phylogenetic analysis of Placobdella (Hirudinea: Rhynchobdellida: Glossiphoniidae) with consideration of COI variation. Molecular Phylogenetics and Evolution 114, 234–248.
| Phylogenetic analysis of Placobdella (Hirudinea: Rhynchobdellida: Glossiphoniidae) with consideration of COI variation.Crossref | GoogleScholarGoogle Scholar |
Elliott, JM, and Tullett, PA (1982). Leech parasitism of waterfowl in the British Isles. Wildfowl 33, 164–170.
Folmer, O, Black, M, Hoeh, W, Lutz, R, and Vrijenhoek, R (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
Goloboff, PA, and Catalano, SA (2016). TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32, 221–238.
| TNT version 1.5, including a full implementation of phylogenetic morphometrics.Crossref | GoogleScholarGoogle Scholar |
Huelsenbeck, JP, and Ronquist, F (2001). MrBAYES; Bayesian inference for phylogeny. Bioinformatics 17, 754–755.
| MrBAYES; Bayesian inference for phylogeny.Crossref | GoogleScholarGoogle Scholar |
Iwama, RE, Oceguera-Figueroa, A, de Carle, D, Manglicmot, C, Erséus, C, Miles, NM-S, Siddall, ME, and Kvist, S (2019). Broad geographic sampling and DNA barcoding do not support the presence of Helobdella stagnalis (Linnaeus, 1758) (Clitellata: Glossiphoniidae) in North America. Zootaxa 4671, 1–25.
| Broad geographic sampling and DNA barcoding do not support the presence of Helobdella stagnalis (Linnaeus, 1758) (Clitellata: Glossiphoniidae) in North America.Crossref | GoogleScholarGoogle Scholar |
Katoh, K, and Standley, DM (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar |
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P, and Drummond, A (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |
Klemm DJ (1985) Freshwater leeches (Annelida: Hirudinea). In ‘A guide to the freshwater Annelida (Polychaeta, naidid and tubificid Oligochaeta, and Hirudinea) of North America’. (Kendall/Hunt Publishing Co.: Dubuque, IA, USA)
Livanow, N (1902). Die Hirudineen-Gattung Hemiclepsis Vejd. Zoologische Jahrbucher 17, 339–362.
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA, USA. INSPEC Accession Number 11705685. (IEEE)
| Crossref |
Moore, PJ (1911). Hirudinea of Southern Patagonia. Reports of the Princeton University Expeditions to Patagonia 1896–1899, 669–687.
Nakano, T, Suzuki, H, Suzuki, N, Kimura, Y, Sato, T, Kamigaichi, H, Tomita, N, and Yamasaki, T (2020). Host-parasite relationships between seabirds and the haemadipsid leech Chtonobdella palmyrae (Annelida: Clitellata) inhabiting oceanic islands in the Pacific Ocean. Parasitology 147, 1765–1773.
| Host-parasite relationships between seabirds and the haemadipsid leech Chtonobdella palmyrae (Annelida: Clitellata) inhabiting oceanic islands in the Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Nguyen, LT, Schmidt, HA, Von Haeseler, A, and Minh, BQ (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.
| IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Crossref | GoogleScholarGoogle Scholar |
Oka, A (1930). Sur un nouveau genre d’Hirudinees provenant de l’Amérique du Sud. Proceeding of the Imperial Academy (Tokyo) 6, 239–242.
| Sur un nouveau genre d’Hirudinees provenant de l’Amérique du Sud.Crossref | GoogleScholarGoogle Scholar |
Oosthuizen, JH (1993). Redescription of the African duck leech Theromyzon cooperi (Harding, 1932) (Hirudinea:Glossiphoniidae). South African Journal of Zoology 28, 67–70.
| Redescription of the African duck leech Theromyzon cooperi (Harding, 1932) (Hirudinea:Glossiphoniidae).Crossref | GoogleScholarGoogle Scholar |
Oosthuizen, JH, and Davies, RW (1992). Redescription of the duck leech, Theromyzon rude (Baird, 1869) (Rhynchobdellida: Glossiphoniidae). Canadian Journal of Zoology 70, 2028–2033.
| Redescription of the duck leech, Theromyzon rude (Baird, 1869) (Rhynchobdellida: Glossiphoniidae).Crossref | GoogleScholarGoogle Scholar |
Oosthuizen, JH, and Davies, RW (1993). A new species of Theromyzon (Rhynchobdellida: Glossiphoniidae), with a review of the genus in North America. Canadian Journal of Zoology 71, 1311–1318.
| A new species of Theromyzon (Rhynchobdellida: Glossiphoniidae), with a review of the genus in North America.Crossref | GoogleScholarGoogle Scholar |
Oosthuizen, JH, and Fourie, FL (1985). Mortality amongst waterbirds caused by the African duck leech Theromyzon cooperi. South African Journal of Wildlife Research 15, 98–106.
Philippi, RA (1867). Kurze Notiz über zwei Chilenische Blutegel. Archiv für Naturgeschichte 33, 76–78.
Rambaut, A, Drummond, AJ, Xie, D, Baele, G, and Suchard, MA (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
| Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar |
Ringuelet R (1985) ‘Fauna de agua dulce de la República Argentina.’ (Fundacion para la Educacion, la Ciencia y la Cultura: Buenos Aires, Argentina)
Saglam, N, Kutschera, U, Saunders, R, Saidel, WM, Balombini, KLW, and Shain, DH (2018). Phylogenetic and morphological resolution of the Helobdella stagnalis species-complex (Annelida: Clitellata: Hirudinea). Zootaxa 4403, 61–86.
| Phylogenetic and morphological resolution of the Helobdella stagnalis species-complex (Annelida: Clitellata: Hirudinea).Crossref | GoogleScholarGoogle Scholar |
Sawyer, RT (1986). ‘Leech Biology and Behaviour.’ (Clarendon Press: Oxford, UK)
Schulmeister, S (2003). Simultaneous analysis of basal Hymenoptera (Insecta): introducing robust-choice sensitivity analysis. Biological Journal of the Linnean Society. Linnean Society of London 79, 245–275.
| Simultaneous analysis of basal Hymenoptera (Insecta): introducing robust-choice sensitivity analysis.Crossref | GoogleScholarGoogle Scholar |
Siddall, ME, and Burreson, EM (1998). Phylogeny of leeches (Hirudinea) based on mitochondrial cytochromecoxidase subunit I. Molecular Phylogenetics and Evolution 9, 156–162.
| Phylogeny of leeches (Hirudinea) based on mitochondrial cytochromecoxidase subunit I.Crossref | GoogleScholarGoogle Scholar |
Siddall, ME, Rood-Goldman, R, Barrio, A, and Barboutis, C (2013). The eyes have it: long-distance dispersal by an intraorbital leech parasite of birds. The Journal of Parasitology 99, 1137–1139.
| The eyes have it: long-distance dispersal by an intraorbital leech parasite of birds.Crossref | GoogleScholarGoogle Scholar |
Simon, C, Frati, F, Beckenbach, A, Crespi, B, Liu, H, and Flook, P (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.
| Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers.Crossref | GoogleScholarGoogle Scholar |
Sket, B, and Trontelj, P (2008). Global diversity of leeches (Hirudinea) in freshwater. Hydrobiologia 595, 129–137.
| Global diversity of leeches (Hirudinea) in freshwater.Crossref | GoogleScholarGoogle Scholar |
Stecher, G, Tamura, K, and Kumar, S (2020). Molecular Evolutionary Genetics Analysis (MEGA) for macOS. Molecular Biology and Evolution 37, 1237–1239.
| Molecular Evolutionary Genetics Analysis (MEGA) for macOS.Crossref | GoogleScholarGoogle Scholar |
Tessler, M, de Carle, D, Voiklis, ML, Gresham, OA, Neumann, JS, Cios, S, and Siddall, ME (2018). Worms that suck: phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida. Molecular Phylogenetics and Evolution 127, 129–134.
| Worms that suck: phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida.Crossref | GoogleScholarGoogle Scholar |
Trontelj, P, Sket, B, and Steinbrück, G (1999). Molecular phylogeny of leeches: Congruence of nuclear and mitochondrial rDNA data sets and the origin of bloodsucking. Journal of Zoological Systematics and Evolutionary Research 37, 141–147.
| Molecular phylogeny of leeches: Congruence of nuclear and mitochondrial rDNA data sets and the origin of bloodsucking.Crossref | GoogleScholarGoogle Scholar |
Whiting, MF (2002). Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–104.
| Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera.Crossref | GoogleScholarGoogle Scholar |