A Cladistic Approach for the Classification of Oligotrichid Ciliates (Ciliophora: Spirotricha)

Abstract

Currently, gene sequence genealogies of the Oligotrichea Bütschli, 1889 comprise only few species. Therefore, a cladistic approach, especially to the Oligotrichida, was made, applying Hennig's method and computer programs. Twenty-three characters were selected and discussed, i.e., the morphology of the oral apparatus (five characters), the somatic ciliature (eight characters), special organelles (four characters), and ontogenetic particulars (six characters). Nine of these characters developed convergently twice. Although several new features were included into the analyses, the cladograms match other morphological trees in the monophyly of the Oligotrichea, Halteriia, Oligotrichia, Oligotrichida, and Choreotrichida. The main synapomorphies of the Oligotrichea are the enantiotropic division mode and the de novo-origin of the undulating membranes. Although the sister group relationship of the Halteriia and the Oligotrichia contradicts results obtained by gene sequence analyses, no morphologic, ontogenetic or ultrastructural features were found, which support a branching of Halteria grandinella within the Stichotrichida. The cladistic approaches suggest paraphyly of the family Strombidiidae probably due to the scarce knowledge. A revised classification of the Oligotrichea is suggested, including all sufficiently known families and genera.

Figs 1a-c

Cladograms showing different models of the phylogenetic relationships within the Spirotricha. a - according to Petz and Foissner (1992); b - according to Lynn and Small (2002); c - according to Strüder-Kypke and Lynn (2003).

Figs 2a-d

Generalized ventral (a-c) and dorsal (d) views, illustrating some diagnostic features of the halteriid genera Meseres (a - modified from Petz and Foissner 1992) and Halteria (b - modified from Song 1993) as well as the oligotrichid genus Strombidium (c - from Agatha 2004) and the choreotrichid genus Rimostrombidium (d). The halteriids Meseres and Halteria have two undulating membranes, i.e., an outer paroral and an inner endoral, while the Oligotrichida and Choreotrichida possess only an endoral. AM - anterior polykinetids/membranelles, B - bristle complexes, E - endoral, EM - external polykinetids/membranelles, GK - girdle kinety, IM - internal polykinetids/membranelles; P - paroral, SK - somatic kineties, VK - ventral kinety, VM - ventral polykinetids/membranelles.

Figs 3a-g

Evolution of the ciliary patterns in the Oligotrichida (from Agatha 2004). a - ancestor with many longitudinal somatic kineties, whose dikinetids bear a distinct cilium only at each anterior basal body (see detail); b - reduction in kinety number to two. The clockwise torsion of the proximal end of the membranellar zone and the cell proper caused the dextrally spiralled pattern of the girdle and ventral kinety; c - the ventral kinety orientated longitudinally; d - the right portion of the girdle kinety migrated posteriorly; both kinety ends are thus close to the cell's posterior on ventral side; e - the posterior portion of the girdle kinety curved anteriorly and is thus inversely orientated to the parallel ventral kinety; f - the left portion of the dextrally spiralled girdle kinety migrated anteriorly, causing a horizontal orientation; g - the right portion of the horizontal girdle kinety spiralled sinistrally to the rear end. The number of whorls performed by the girdle kinety is possibly positively correlated with the cell size because Tontonia turbinata with a length of 50-80 μm after protargol impregnation has ~ 1.5 whorls, while T. grandis with a size of up to 180 μm has 3-3.5 whorls (Song and Bradbury 1998, Suzuki and Han 2000, Agatha et al. 2004). Arrows indicate orientation of kineties. GK - girdle kinety, VK - ventral kinety.

Fig. 4

Cladistic scheme generated by Hennig's argumentation method. For character coding, see Table 1 and section on character states. Apomorphies are marked by black squares, convergences are starred. a - Meseres corlissi Petz and Foissner, 1992 (modified from Petz and Foissner 1992); b - Halteria grandinella (Müller, 1773) Dujardin, 1841 (modified from Song 1993); c - Parallelostrombidium rhyticollare (Corliss and Snyder, 1986) Agatha, 2004 (modified from Petz et al. 1995); d - Tontonia appendiculariformis Fauré-Fremiet, 1914 (from FauréFremiet 1924); e - Paratontonia gracillima (Fauré-Fremiet, 1924) Jankowski, 1978 (from Lynn et al. 1988); f - Pseudotontonia cornuta (Leegaard, 1915) Agatha, 2004 (modified from Suzuki and Song 2001); g - Spirotontonia grandis (Suzuki and Han, 2000) Agatha, 2004 (from Suzuki and Han 2000); h - Omegastrombidium elegans (Florentin, 1901) Agatha, 2004 (from Song et al. 2000); i - Spirostrombidium urceolare (Stein, 1867) Lei et al., 1999 (from Lei et al. 1999); j - Novistrombidium apsheronicum (Alekperov and Asadullayeva, 1997) Agatha, 2003 (from Agatha 2003a); k - Laboea strobila Lohmann, 1908 (from Montagnes et al. 1988); l - Strombidium sulcatum Claparède and Lachmann, 1859 (from Song et al. 2000); m - Limnostrombidium pelagicum (Kahl, 1932) Krainer, 1995 (from Krainer 1991); n - Pelagostrombidium mirabile (Penard, 1916) Krainer, 1991 (from Krainer 1991); o - Cyrtostrombidium longisomum Lynn and Gilron, 1993 (from Lynn and Gilron 1993).

Fig. 5

50% majority-rule consensus tree (tree length = 74, retention index = 0.85, rescale consistency index = 0.68) computed with the maximum parsimony analysis of PAUP* version 4.0b10 (Swofford 2002), using the Hypotrichea, i.e., the hypotrichs and stichotrichs, as out-group (for feature matrix, see Table 2). The numbers represent the bootstrap values out of 100 re-samplings of the data set. The main apomorphies are marked by black squares; convergences are starred.