Myxozoa, Polypodium, and the origin of the Bilateria: The phylogenetic position of “Endocnidozoa” in light of the rediscovery of Buddenbrockia

Since their discovery, endoparasitic Myxozoa have been considered protozoans; however, a century ago, Stolc (1899) remarked that they should be classified as reduced cnidarians because of the nematocyst-like architecture of their spores. Later on, the multicellular nature of Myxozoa and the structural and developmental similarity of their polar capsules to cnidarian nematocysts were recognized repeatedly (recently by Lom and Dykov a, 1997; Siddall et al., 1995, and references therein). In the past few years, the topic of myxozoan relationships has become further complicated. A new clade, the ectoproct–parasitic (possibly ectoproct–fish–parasitic) Malacosporea (Canning et al., 2000), was discovered and identified as a sister group of the rest of the Myxozoa. In 2002, one of the most enigmatic metazoan species, Buddenbrockia plumatellae Schr€ oder, 1910, was rediscovered and reinterpreted phylogenetically (for its pre-2002 interpretation see Nielsen, 2001, p. 497, and references therein). Buddenbrockia is a motile worm-like animal inhabiting body cavities of freshwater ectoprocts. It possesses four nematode-like bands of longitudinal muscular cords, cnidarian-like complement of numerous polar capsules in its ‘‘mural cells’’ (1⁄4 epidermis? ), and myxozoan-like infective spores (including polar capsules) that are formed inside the body cavity. Surprisingly, Buddenbrockia has been shown to be conspecific with the malacosporean species Tetracapsula bryozoides Canning, Okamura & Curry, 1996, a conclusion based on morphology (Canning et al., 2002; Okamura et al., 2002) and small-subunit (1⁄4 18S) ribosomal RNA (‘‘SSU’’ hereinafter; Monteiro et al., 2002). The molecular data, viz. SSU and Hox genes, clearly indicate a metazoan origin of Myxozoa but those data are as yet unable to reveal their specific relationships. Two conflicting hypotheses concerning the position of the Myxozoa within Metazoa have so far been formulated, one treating the Myxozoa as modified cnidarians and the other placing them within bilaterians. According to the former, more traditional point of view, supported by several SSU analyses, myxozoans probably represent a sister group of Polypodium hydriforme Ussov, 1885 (Siddall et al., 1995; Siddall and Whiting, 1999; Zrzav y et al., 1998), an aberrant cnidarian with a life cycle including both free-living medusoid stages and stages adapted to intracellular parasitism in oocytes of fishes (Raikova, 1994). Traditionally, Polypodium is regarded a member of the hydrozoan group of Narcomedusae, but Raikova (1994) has suggested (with no cladistic analysis) to elevate Polypodium to the level of a new cnidarian class, Polypodiozoa. The comprehensive phylogenetic analysis of the cnidarian SSU sequences (Collins, 2002) indeed retrieves monophyletic Cnidaria and Hydrozoa (1⁄4Hydroidolina and Trachylina, the latter including the Narcomedusae) but an uncertain position of Polypodium and Myxozoa outside the Hydrozoa (A.G. Collins, pers. comm.). In most other SSU studies (which usually do not include Polypodium s sequence at all), the Myxozoa group within Bilateria, close to basal clades such as Mesozoa and Nematoda (Hanelt et al., 1996; Pawlowski et al., 1996; Schlegel et al., 1996; Smothers et al., 1994). Application of different tree-building methods shows that the clade consisting of Polypodium and Myxozoa (1⁄4 ‘‘Endocnidozoa,’’ a name informally proposed by P. Schuchert; see de Meeûs and Renaud, 2002, p. 247, who misspelled the name as ‘‘Endocnydozoa’’ and attributed it erroneously to Siddall et al., 1995) is not likely an artifact caused by the ‘‘longbranch attraction’’ of aberrant SSU sequences (Siddall and Whiting, 1999). However, most of their experimental trees tend to show the Endocnidozoa as basal bilaterians rather than derived cnidarians. In their distance tree, Kim et al. (1999) found a weakly supported Polypodium–Myxozoa clade branching as a sister group of Bilateria; in the maximum-likelihood tree, Myxozoa remained a sister group of bilaterians while Polypodium branched off an unresolved base of the tree (with Placozoa and several cnidarian subclades). The analysis of myxozoan Hox genes suggests that Myxozoa is more closely related to bilaterians Cladistics 19 (2003) 164–169