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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Phylogenetic evaluation of systematics and biogeography of the leech family Glossiphoniidae

Mark E. Siddall A B , Rebecca B. Budinoff A and Elizabeth Borda A
+ Author Affiliations
- Author Affiliations

A Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA.

B Corresponding author. Email: siddall@amnh.org

Invertebrate Systematics 19(2) 105-112 https://doi.org/10.1071/IS04034
Submitted: 24 November 2004  Accepted: 14 April 2005   Published: 28 June 2005

Abstract

The phylogenetic relationships of Glossiphoniidae, a leech family characterised by its high degree of parental care, were investigated with the combined use of morphological data and three molecular datasets. There was strong support for monophyly of most accepted genera in the group, many of which are consistent with eyespot morphology. The genera Desserobdella Barta & Sawyer, 1990 and Oligobdella Moore, 1918 are suppressed as junior synonyms of Placobdella Blanchard, 1893 and thus recognising each of Placobdella picta (Verrill, 1872) Moore, 1906, Placobdella phalera (Graf, 1899) Moore, 1906, and Placobdella biannulata (Moore, 1900), comb. nov. The species Glossiphonia elegans (Verrill, 1872) Castle, 1900 and Helobdella modesta (Verrill, 1872), comb. nov. are resurrected for the North American counterparts to European non-sanguivorous species. Glossphonia baicalensis (Stschegolew, 1922), comb. nov. is removed from the genus Torix Blanchard 1898 and Alboglossiphonia quadrata (Moore, 1949) Sawyer, 1986 is removed from the genus Hemiclepsis Vejdovsky, 1884. The biogeographic implications of the phylogenetic hypothesis are evaluated in the context of what is already known for vertebrate hosts and Tertiary continental arrangements.


Acknowledgments

Thanks to: Johan Coetze, Adrian Armstrong, Jérémy Bouyer, Rodolphe Rougerie, Gene Burreson, Elizabeth and Lorenzo Prendini, Ann and Dorian Harcourt-Baldwin, Lai Yetai, Paola Magnetti, Renato Bacchetta, Patricio and Ani Torres, Wojt Wodzicki, Kate Gregory-Wodzicki, Jeff Boundy and Jessica Light for their invaluable assistance in the acquisition of various species newly included in these studies. We thank Louise Crowley, Kenneth Macdonald and Megan Harrison for their comments on drafts of the manuscript. This work was supported by a Partnerships for Enhancing Expertise in Taxomony (PEET) Grant from the National Science Foundation (BIO-DEB 0119329) by award DEB 0108163 from the National Science Foundation as well as by the Louis and Dorothy Cullman Program in Molecular Systematic Studies, the Ambrose Monell Foundation and the Richard Lounsbery Foundation.


References


Apakupakul K., Siddall M. E., Burreson E. M. (1999) Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences. Molecular Phylogenetics and Evolution 12, 350–359.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Auden D. T. (1974) Studies on the development of Rhodnius prolixus and the effects of its symbiote Nocardia rhodnii. Journal of Medical Entomology 11, 68–71.
PubMed |
open url image1

Barta J. R., Sawyer R. T. (1990) Definition of a new genus of glossiphoniid leech and a redescription of the type species, Clepsine picta Verrill, 1872. Canadian Journal of Zoology 68, 1942–1950. open url image1

Blankenship D. T., Brankamp R. G., Manley G. D., Cardin A. D. (1990) Amino acid sequence of ghilanten: anticoagulant-antimetastatic principle of the South American leech, Haementeria ghilianii. Biochemical and Biophysical Research Communications 166, 1384–1389.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Böhning-Gaese K., González-Guzmán L. I., Brown J. (1998) Constraints on dispersal and the evolution of the avifauna of the Northern Hemisphere. Evolutionary Ecology 12, 767–783.
Crossref | GoogleScholarGoogle Scholar | open url image1

Borda E., Siddall M. E. (2004) Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): Phylogenetic Relationships and Evolution. Molecular Phylogenetics and Evolution 30, 213–225.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chopin V., Matias I., Stefano G. B., Salzet M. (1998a) Amino acid sequence determination and biological activity of therin, a naturally occuring specific trypsin inhibitor from the leech Theromyzon tessulatum. European Journal of Biochemistry 254, 565–570.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chopin V., Stefano G. B., Salzet M. (1998b) Amino-acid-sequence determination and biological activity of tessulin, a naturally occurring trypsin-chymotrypsin inhibitor isolated from the leech Theromyzon tessulatum. European Journal of Biochemistry 258, 662–668.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chopin V., Salzet M., Baert J., Vandenbulcke F., Sautiere P. E., Kerckaert J. P., Malecha J. (2000) Therostasin, a novel clotting factor Xa inhibitor from the rhynchobdellid leech, Theromyzon tessulatum. The Journal of Biological Chemistry 275, 32701–32707.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chudzinski-Tavassi A. M., Kelen E. M., de Paula Rosa A. P., Loyau S., Sampaio C. A., Bon C., Angles-Cano E. (1998) Fibrino(geno)lytic properties of purified hementerin, a metalloproteinase from the leech Haementeria depressa. Thrombosis and Haemostasis 80, 155–160.
PubMed |
open url image1

Connolly T. M., Jacobs J. W., Condra C. (1992) An inhibitor of collagen-stimulated platelet activation from the salivary glands of the Haementeria officinalis leech. I. Identification, isolation, and characterization. The Journal of Biological Chemistry 267, 6893–6898.
PubMed |
open url image1

Faria F., Kelen E. M., Sampaio C. A., Bon C., Duval N., Chudzinski-Tavassi A. M. (1999) A new factor Xa inhibitor (lefaxin) from the Haementeria depressa leech. Thrombosis and Haemostasis 82, 1469–1473.
PubMed |
open url image1

Feldman C. R., Parham J. F. (2002) Molecular phylogenetics of emydine turtles: Taxonomic revision and the evolution of shell kinesis. Molecular Phylogenetics and Evolution 22, 388–398.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fritz U. (1998). Introduction to zoogeography and subspecific differentiation in Emys orbicularis (Linnaeus, 1758). In ‘Proceedings of the EMYS Symposium Dresden 96. Mertensiella 10’. (Eds U. Fritz, U. Joger, R. Podloucky and J. Servan.) pp. 127. (Warlich: Rheinbach, Germany.)

Hill P., Campbell J. A., Petrie I. A. (1976) Rhodnius prolixus and its symbiontic actinomycete: a microbiological, physiological and behavioral study. Proceedings of the Royal Society of London. Series B. Biological Sciences 194, 501–525. open url image1

Holt G. D., Krivan H. C., Gasic G. J., Ginsburg V. (1989) Antistasin, an inhibitor of coagulation and metastasis, binds to sulfatide (Gal(3–SO4) beta 1–1Cer) and has a sequence homology with other proteins that bind sulfated glycoconjugates. The Journal of Biological Chemistry 264, 12138–12140.
PubMed |
open url image1

Hoegg S., Vences M., Brinkmann H., Meyer A. (2004) Phylogeny and comparative substitution rates of frogs inferred from sequences of three nuclear genes. Molecular Biology and Evolution 21, 1188–1200.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hovingh P., Linker A. (1999) Hyaluronidase activity in leeches (Hirudinea). Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 124, 319–326.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Huizinga E. G., Schouten A., Connolly T. M., Kroon J., Sixma J. J., Gros P. (2001) The structure of leech anti-platelet protein, an inhibitor of haemostasis. Acta Crystallographica. Section D, Biological Crystallography 57, 1071–1078.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hypsa V., Askoy S. (1997) Phylogenetic characterization of two transovarially transmitted endosymbionts of the bedbug Cimex lectularius (Heteroptera: Cimicidae). Insect Molecular Biology 6, 301–304.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jones S. R. M., Woo P. T. K. (1990) Redescription of the leech, Desserobdella phalera (Graf, 1899) n. comb. (Rhynchobdellida: Glossiphoniidae), with notes on its biology and occurrence on fishes. Canadian Journal of Zoology 68, 1951–1955. open url image1

Kikuchi Y., Fukatsu T. (2002) Endosymbiotic Bacteria in the Esophageal Organ of Glossiphoniid Leeches. Applied and Environmental Microbiology 68, 4637–4641.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lenk P., Fritz U., Joger U., Wink M. (1999) Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758) Molecular Ecology 8, 1911–1922.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Light J. E., Siddall M. E. (1999) Phylogeny of the leech family Glossiphoniidae based on mitochondrial gene sequences and morphological data. The Journal of Parasitology 85, 815–823.
PubMed |
open url image1

Lukin E. I. (1976). ‘Fauna SSSR. Pijavki. Tom 1, Izdatel’stvo.’ (Nauka: Leningrad, Russia.)

Mayr E. (1946) History of the North American bird fauna. The Wilson Bulletin 58, 1–68. open url image1

Mazur P., Henzel W. J., Seymour J. L., Lazarus R. A. (1991) Ornatins: potent glycoprotein IIb-IIIa antagonists and platelet aggregation inhibitors from the leech Placobdella ornata. European Journal of Biochemistry 202, 1073–1082.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Malinconico S. M., Katz J. B., Budzynski A. Z. (1984) Hementin: anticoagulant protease from the salivary gland of the leech Haementeria ghilianii. The Journal of Laboratory and Clinical Medicine 103, 44–58.
PubMed |
open url image1

Mann K. H. (1962). ‘Leeches (Hirudinea): Their Structure, Physiology, Ecology, and Embryology.’ (Pergamon Press: New York, USA.)

Moore J. P. (1906) Hirudinea and Oligochaeta collected in the Great Lakes region. Bulletin of the Bureau of Fisheries 25, 153–171. open url image1

Noda H., Munderloh U. G., Kurtti T. J. (1997) Endosymbionts of ticks and their relationships to Wolbachia spp. And tick-borne pathogens of humans and animals. Applied and Environmental Microbiology 63, 3926–3932.
PubMed |
open url image1

Oosthuizen J. H. (1991) An annotated checklist of the leeches (Annelida: Hirudinea) of the Kruger National Park with a key to the species. Koedoe 34, 25–38. open url image1

Oosthuizen J. H., and Siddall M. E. (2002). Hirudinea. In ‘Guides to the Freshwater Invertebrates of Southern Africa. Vol. 5 – Non-arthropods’. (Eds J. A. Day, B. A. Stewart, I. J. de Moor and A. E. Louw.) pp. 237–263. (Water Research Commission: Pretoria, South Africa.)

Reichenow E. (1921). Über intrazelluläre Symbionten bei Blutsaugern. Archiv fuer Schiffs-und Tropen-Hygiene 25.

Reichenow E. (1922). Intrazelluläre Symbionten bei blutaugenden Milben und Egeln. Archive für Protistenkunde 45.

Richardson R. L. (1949) The occurrence of the leech Batracobdella picta (Verrill) in the dorsal sub-cutaneous lymph spaces of Rana catesbiana. Canadian Field Naturalist 63, 85–86. open url image1

Ringuelet R. A. (1985). ‘Fauna de agua dulce de la República Argentina. Vol. XVII: Annulata, Hirudinea.’ (Fundacion para la Educacion La Ciencia y La Cultura: Buenos Aires, Argentina.)

Salzet M., Chopin V., Baert J., Matias I., Malecha J. (2000) Theromin, a novel leech thrombin inhibitor. The Journal of Biological Chemistry 275, 30774–30780.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sawyer R. T. (1986). ‘Leech Biology and Behavior.’ (Clarendon Press: Oxford, UK.)

Seale L., Finney S., Sawyer R. T., Wallis R. B. (1997) Tridegin, a novel peptidic inhibitor of factor XIIIa from the leech, Haementeria ghilianii, enhances fibrinolysis in vitro. Thrombosis and Haemostasis 77, 959–963.
PubMed |
open url image1

Siddall M. E. (2002) Phylogeny and revision of the leech family Erpobdellidae (Hirudinida: Oligochaeta). Invertebrate Systematics 16, 1–6.
Crossref | GoogleScholarGoogle Scholar | open url image1

Siddall M. E., Borda E. (2003) Phylogeny of the leech genus Helobdella (Glossiphoniidae) based on mitochondrial gene sequences and morphological data and a special consideration of the triserialis complex. Zoologica Scripta 32, 23–33.
Crossref | GoogleScholarGoogle Scholar | open url image1

Siddall M. E., Apakupakul K., Burreson E. M., Coates K. A., Erséus C., Gelder S. R., Källersjö M., Trapido-Rosenthal H. (2001) Validating Livanow: molecular data agree that leeches, branchiobdellidans and Acanthobdella peledina form a monophyletic group of oligochaetes. Molecular Phylogenetics and Evolution 21, 346–351.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Siddall M. E., Perkins S. L., Desser S. S. (2004) Leech mycetome endosymbionts are a new lineage of alphaproteobacteria related to the Rhizobiaceae. Molecular Phylogenetics and Evolution 30, 178–186.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Swofford D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.’ (Sinauer Associates: Sunderland, MA, USA.)

Tuszynski G. P., Gasic T. B., Gasic G. J. (1987) Isolation and characterization of antistasin. An inhibitor of metastasis and coagulation. The Journal of Biological Chemistry 262, 9718–9723.
PubMed |
open url image1

Trontelj P., Sket B. (2000) Molecular re-assessment of some phylogenetic, taxonomic and biogeographic relationships between the leech genera Dina and Trocheta (Hirudinea: Erpobdellidae). Hydrobiologia 438, 227–235.
Crossref | GoogleScholarGoogle Scholar | open url image1

Trontelj P., Sket B., Steinbruck G. (1996) Phylogenetic relationships in European erpobdellid leeches (Hirudinea: Erpobdellidae) inferred from restriction-site data of the 18S ribosomal gene and ITS2 region. Journal of Zoological Systematics and Evolutionary Research 34, 85–93. open url image1

Trontelj P., Sket B., Steinbruck 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. open url image1

Van Der Lande V. M., Tinsley R. C. (1976) Studies on the anatomy, life history, and behavior of Marsupiobdella africana (Hirudinea: Glossiphoniidae). Journal of the Zoological Society of London 180, 537–563. open url image1

Verrill A. E. (1872) Descriptions of North American fresh-water leeches. American Journal of Science 3, 126–139. open url image1