Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution
Introduction
Arhynchobdellida are characterized by their possession of muscular jaws for feeding and the lack of a proboscis. Arhynchobdellid leeches are remarkably diverse in morphology and in life-history strategies, and are found globally in freshwater and terrestrial habitats. Some widely recognized species include the sanguivorous ‘medicinal’ leeches found in freshwater lakes and ponds, and terrestrial leeches found in tropical jungles where “they are among the most dominant and self-assertive elements” (Moore, 1927: p. 224). Arhynchobdellid leeches are well known for their bloodletting capacity and have been frequently encountered in historical and contemporary medical applications, with some of the earliest accounts dating as far back as 200 AD (Kunja Lal Sharma’s Sus’ruta Samhitá). The 19th century saw increased exploitation of the European medicinal leech, Hirudo medicinalis. Overharvesting for therapeutic phlebotomy throughout Europe (Sawyer, 1986; Shipley, 1927), rendered wild populations either threatened or endangered in over 15 European countries (Elliott and Tullett, 1984, Elliott and Tullett, 1992; Council of Europe, 1998; IUCN, 1993; Wells et al., 1983). This traditional use led to medical and biochemical uses for post-operative haematoma treatment (Lent, 1986; Walsmann and Markwardt, 1985), as well as to the discovery of anti-thrombin and anti-platelet activities in their salivary secretions (Baskova et al., 1987; Hong et al., 1999; Munro et al., 1992a, Munro et al., 1992b; Vindigni et al., 1994; Yang et al., 1997).
In addition to the sanguivorous aquatic and terrestrial jungle leeches, other arhynchobdellid groups occupy various niches as non-sanguivorous predators of oligochaetes or of aquatic invertebrate larvae. Arhynchobdellida also entails temperate terrestrial leeches and even ‘eyeless’ cave-dwelling species. Exhibiting a marked scope of morphology and life history strategies, as well as a diversity of feeding and reproductive behaviors, arhynchobdellid species have been used as model organisms in several fields of biology. These include neurobiology and development (Aisemberg et al., 2001; Burrell et al., 2003; Munro et al., 1992b), phenology (Demirsoy et al., 2001), ecology (Dall, 1987; Schalk et al., 2002), environmental science (Shapkarev and Vagner, 1989), and conservation (Council of Europe, 1998; Kasparek et al., 2000; Sawyer, 1979, Sawyer, 1981).
The evolutionary relationships of leeches and their relationship to other annelids, have included work based on morphology (Brinkhurst and Gelder, 1989; Holt, 1989; Siddall and Burreson, 1995), life history (Siddall and Burreson, 1996), nuclear and mitochondrial gene sequences (Siddall and Burreson, 1998; Siddall et al., 2001), combined morphology and molecular data at the familial level (Apakupakul et al., 1999; Light and Siddall, 1999; Siddall, 2002), and at the generic level (Siddall and Borda, 2003). Recent phylogenetic assessments have suggested and accepted that many traditional groupings of leeches are artificial and not monophyletic (Apakupakul et al., 1999; Sawyer, 1986; Siddall and Burreson, 1995, Siddall and Burreson, 1998; Trontelj et al., 1999).
In a continued effort towards resolving the ingroup relationships of the Hirudinida, the evolutionary relationships and divergence patterns of the seven families of Arhynchobdellida, as recognized by Sawyer (1986), are investigated here.
Section snippets
Taxa
Thirty-nine species included for phylogenetic analyses were chosen to represent the seven arhynchobdellid families (Table 1): Americobdellidae, Cylicobdellidae, Erpobdellidae, Haemopidae, Haemadipsidae, Hirudinidae, and Salifidae. Collectively these cover an extensive global distribution (Table 2). Species not included in previous phylogenetic studies are Aliolimnatis africana, Americobdella valdiviana, Cylicobdella coccinea, Erpobdella costata, Haemadipsa picta, Haemadipsa sumatrana, Haemopis
Results
Parsimony analysis of 24 morphological characters resulted in 181 most-parsimonious trees with a tree length (L) of 46 steps, an RI of 0.958 and CI of 0.717. The strict consensus of all morphological trees did not fully resolve higher taxonomic groups (Fig. 1). There was some resolution with respect to the Hirudiniformes, Americobdellidae, Cylicobdellidae, and Haemadipsidae. Members of the Hirudinidae and Haemopidae each were polyphyletic.
Analysis of all molecular data combined (3620 characters
Discussion
The resulting cladogram from the combined, total-evidence approach, analyzing two nuclear genes, two mitochondrial genes and morphology, yielded a hypothesis which conflicts with most traditional classifications of Arhynchobdellida (e.g. Sawyer, 1986). With respect to higher taxonomic subdivisions, monophyly of an erpobdelliform and hirudiniform clade was well supported. Current classification (Table 1) divides arhynchobdellid leeches into seven families (Sawyer, 1986). This phylogenetic
Conclusion
Inasmuch as this study points to several difficulties associated with hirudiniform systematics, like the need for separation of the so-called Haemadipsidae and Hirudinidae into two and three groups, respectively, revision on the basis of the currently included taxa might be premature. There are, for example, dozens of terrestrial leech species known, with doubtless many more yet to be collected, discovered and described (Table 1). The phylogenetic hypothesis outlined here should provide a
Acknowledgements
We thank Rebecca Budinoff, Louise Crowley, Megan Harrison, Kirsten Jensen, Kenneth Macdonald, Susan Perkins, Vincent Rousset, and Stephanie Westergren for critical comments on early drafts of the manuscripts. We also thank Chris Boyko, Daniel Brooks, Lisa Curran, Adrian Garda, Ke Won Kang, Julian Favovich, Meir Rigby, Annie Torres, and Patricio Torres for their assistance in obtaining several of the species newly included here. This research was supported by the National Science Foundation
References (68)
- et al.
Higher-level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences
Mol. Phylogenet. Evol.
(1999) - et al.
The status of the medicinal leech Hirudo medicinalis in Europe and especially in the British Isles
Biol. Cons.
(1984) - et al.
Phylogeny of leeches (Hirudinea) based on mitochondrial cytochrome c oxidase subunit I
Mol. Phylogenet. Evol.
(1998) - et al.
Validating Livanow: Molecular data agrees that leeches, branchiobdellidans, and Acanthobdella peledina form a monophyletic group of oligochaetes
Mol. Phylogenet. Evol.
(2001) - et al.
On the isolation of the thrombin inhibitor hirudin
Thromb. Res.
(1985) - et al.
Netrin signal is produced in leech embryos by segmentally iterated sets of central neurons and longitudinal muscle cells
Dev. Genes Evol.
(2001) - et al.
Mechanisms of inhibition of vascular-platelet homeostasis by salivary gland secretion of the medicinal leech Hirudo medicinalis
Biokhimiya
(1987) Annelides
- Blanchard, R., 1893. Sur une sangsue terrestre du Chili. Compt. Rend. Acad. Sci., Paris 116,...
Hirudinées
Boll. Mus. Torino
(1896)
Monographie des Hémadipsines (Sangsues terrestres)
Bull. Soc. Path. Exot.
The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction
Evolution
Did the lumbriculids provide the ancestors of the branchiobdellidans, acanthobdellidans and leeches?
Hydrobiologia
Progressive recovery of learning during regeneration of a single synapse in the medicinal leech
J. Comp. Neuro.
Nuevo genero y especie de Hirudı́neos perteneciente a la subfamilia Haemadipsinae
XV. Ann. Inst. Biol. México
Hirudı́neos de México XX: Taxa y nomenclatura de la clase Hirudinea hasta generos
An. Inst. Biol. México
Los Hirudı́neos del Nordeste del Brasil, I
Ann. Acad. Brasil. Sci.
The ecology of the littoral leech fauna (Hirudinea) in Lake Esrom, Denmark
Archiv. Hydrobiol. Suppl.
Phenology of the medicinal leech, Hirudo medicinalis L., in north-western Turkey
Hydrobiologia
The medicinal leech
Biologist
Ein neuer Landegel aus Osterreich, Verh
K.K. Zool.-bot. Gesell. Wein
Essai sur les Hirudinées
Arch. Soc. Med. Biol. Montpellier
Comments on the classification of the Clitellata
Hydrobiologia
Prolonged bleeding from the bite of the Asian medicinal leech Hirudo nipponia
Comp. Haem. Int.
Hirudineen aus dem Sudan
Res. Swed. Zool. Exped. Egypt
Phenology of the medicinal leech, Hirudo medicinalis L., in Turkey
Hydrobiologia
New medicinal and scientific uses of the leech
Nature
Phylogeny of the leech family Glossiphoniidae based on mitochondrial gene sequences and morphological data
J. Parasitol.
The anatomy and systematic position of the Chilean terrestrial leech, Cardea valdiviana (Philippi)
Proc. Acad. Natl. Sci. Philadelphia
The segmentation (metamerism and annulation) of the Hirudinea; Arhynchobdellae
Leeches (Hirudinea) from the Hawaiian Islands, and two new species from the Pacific region in the Bishop Museum collection
Occas. Pap. Bernice P. Bishop Mus.
Cited by (125)
Cryptic carnivores: Intercontinental sampling reveals extensive novel diversity in a genus of freshwater annelids
2023, Molecular Phylogenetics and EvolutionPhylogenetic relationships and species delimitation in Haemopis (Annelida: Hirudinea: Haemopidae)
2023, Molecular Phylogenetics and EvolutionCitation Excerpt :One of the most striking results of our analyses is that we only find weak support for a monophyletic group of Palearctic taxa. This contrasts previous results from phylogenetic analyses that robustly infer a well-supported split between Palearctic and Nearctic taxa (see Borda and Siddall, 2004). Notwithstanding the support values in this part of our tree, the Palearctic taxa do place as the sister group to the remaining species in our ML analysis.
Leeches in the extreme: Morphological, physiological, and behavioral adaptations to inhospitable habitats
2020, International Journal for Parasitology: Parasites and WildlifeCitation Excerpt :While this thought is undeniably true, it is not representative of the morphological, physiological, and behavioral diversity that enables leeches to survive and even thrive in extreme habitats. There are more than 700 species of leeches, with many notable examples of diversity and interesting evolutionary transitions in habitat preference, feeding behavior, and morphological adaptations (Borda and Siddall, 2004; Sket and Trontelj, 2008; Phillips and Siddall, 2009; Phillips et al., 2010; Oceguera-Figueroa, 2012; Oceguera-Figueroa et al., 2011; Govedich and Moser, 2015; Tessler et al., 2018). Leeches are found on all continents and seas, except terrestrial Antarctica, and they can be found in freshwater, estuarine, and marine aquatic ecosystems, as well as moist terrestrial ecosystems.