Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution

Abstract

A remarkable diversity of life history strategies, geographic distributions, and morphological characters provide a rich substrate for investigating the evolutionary relationships of arhynchobdellid leeches. The phylogenetic relationships, using parsimony analysis, of the order Arhynchobdellida were investigated using nuclear 18S and 28S rDNA, mitochondrial 12S rDNA, and cytochrome c oxidase subunit I sequence data, as well as 24 morphological characters. Thirty-nine arhynchobdellid species were selected to represent the seven currently recognized families. Sixteen rhynchobdellid leeches from the families Glossiphoniidae and Piscicolidae were included as outgroup taxa. Analysis of all available data resolved a single most-parsimonious tree. The cladogram conflicted with most of the traditional classification schemes of the Arhynchobdellida. Monophyly of the Erpobdelliformes and Hirudiniformes was supported, whereas the families Haemadipsidae, Haemopidae, and Hirudinidae, as well as the genera Hirudo or Aliolimnatis, were found not to be monophyletic. The results provide insight on the phylogenetic positions for the taxonomically problematic families Americobdellidae and Cylicobdellidae, the genera Semiscolex, Patagoniobdella, and Mesobdella, as well as genera traditionally classified under Hirudinidae. The evolution of dietary and habitat preferences is examined.

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.