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Ciliophora, Spirotricha, Oligotrichida) Based on Somatic Ciliary Patterns and Ontogenetic Data Sabine Agatha∗

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Ciliophora, Spirotricha, Oligotrichida) Based on Somatic Ciliary Patterns and Ontogenetic Data Sabine Agatha∗ European Journal of Protistology 47 (2011) 51–56 Updated hypothesis on the evolution of oligotrichid ciliates (Ciliophora, Spirotricha, Oligotrichida) based on somatic ciliary patterns and ontogenetic data Sabine Agatha∗ University of Salzburg, Department of Organismic Biology, Hellbrunnerstrasse 34, A-5020 Salzburg, Austria Received 23 January 2010; received in revised form 24 August 2010; accepted 6 September 2010 Abstract The two recently established genera Apostrombidium Xu et al., 2009 and Varistrombidium Xu et al., 2009 and the analysis of ontogenetic data in Strombidium constrictum, S. montagnesi, S. wilberti, Omegastrombidium elegans, and Paratontonia gracillima necessitated a revision of the hypothesis about the somatic ciliary pattern evolution in oligotrichid ciliates. As a consequence, the species-rich genus Strombidium was split, establishing two genera for species with a horizontal girdle kinety posterior to the oral primordium: Opisthostrombidium nov. gen. with the extrusome attachment sites along the anterior margin of the girdle kinety and posterior to the oral primordium and Foissneridium nov. gen. with the extrusome attachment sites distinctly apart from the girdle kinety and anterior to the oral primordium. The ontogenetic data revealed that the -shaped girdle kinety pattern evolved convergently from the Pseudotontonia pattern with its horizontal girdle kinety in the tailed genus Paratontonia and from the Novistrombidium pattern with its dextrally spiralled girdle kinety in the tailless genus Omegastrombidium. The somatic ciliary pattern of the latter genus probably gave rise to the patterns of Apostrombidium and Varistrombidium. © 2010 Elsevier GmbH. All rights reserved. Keywords: Ciliophora; New genera; Oligotrichida; Somatic ciliary pattern; Taxonomy Introduction of somatic ciliary patterns suggested by Agatha (2004a),by including the genera and the ontogenetic data on Strombidium Although the somatic ciliature of the Oligotrichida (Cil- constrictum, S. montagnesi, S. wilberti, Omegastrombid- iophora, Spirotricha) typically comprises only a girdle and ium elegans, and Paratontonia gracillima. Thus, this study a ventral kinety, the diversity of ciliary patterns created by provides a better understanding of the diversity within the these two rows is considerable. Recently, Xu et al. (2009) Oligotrichida. published descriptions of two strombidiid genera with unique somatic ciliary patterns: Varistrombidium possessing five somatic kineties and Apostrombidium having two inverted U- shaped kinety fragments in the right and left cell halves. The Material and Methods present paper assigns positions for these two genera within the Strombidiidae and expands on the hypothesized evolution The original literature was used (references in Agatha 2004a; Agatha 2004c; Agatha et al. 2005; Liu et al. 2009; Skovgaard and Legrand 2005; Song 2005; Wilbert and Song ∗Fax: +43 662 8044 5698. 2005; Xu and Song 2006; Xu et al. 2005, 2006a,b,c, 2007, E-mail address: [email protected]. 2008, 2009) and the following genera were considered: 0932-4739/$ – see front matter © 2010 Elsevier GmbH. All rights reserved. doi:10.1016/j.ejop.2010.09.001 52 S. Agatha / European Journal of Protistology 47 (2011) 51–56 Apostrombidium Xu, Warren and Song, 2009; Cyrtostrom- Agatha (2004a) assumed a single origin of the -shaped bidium Lynn and Gilron, 1993; Laboea Lohmann, 1908; girdle kinety pattern derived from the Type II pattern. How- Limnostrombidium Krainer, 1995; Novistrombidium Song ever, ontogenetic data indicate that this only occurred in the and Bradbury, 1998; Omegastrombidium Agatha, 2004; Par- Type IV pattern of Omegastrombidium (Fig. 1), while the - allelostrombidium Agatha, 2004; Paratontonia Jankowski, shaped pattern of Paratontonia (Type VI pattern) probably 1978; Pelagostrombidium Krainer, 1991; Pseudotontonia evolved from the Type V pattern by the posterior migration Agatha, 2004; Spirostrombidium Jankowski, 1978; Spiroton- of both girdle kinety ends, as indicated by the position of tonia Agatha, 2004; Strombidium Claparède and Lachmann, the oral primordium posterior to the girdle kinety (Fig. 1). 1859; Tontonia Fauré-Fremiet, 1914; and Varistrombidium Accordingly, the -shaped girdle kinety pattern developed Xu, Warren and Song, 2009. Note, a description and diagno- not only convergently in the tailed (tontoniid) and tailless sis of Varistrombidium were given by Xu, Warren, and Song (strombidiid) taxa, as suggested by Agatha (2004b), but also (2009), referring to an original description by Xu, Yi, Song from different patterns. and others in press, but this latter publication does not exist; The Type X pattern of Apostrombidium and the Type XII hence, Xu, Warren, and Song (2009) were considered the pattern of Varistrombidium probably developed from such a authorities on this genus. -shaped girdle kinety pattern. It is more parsimonious to By regarding the somatic kineties in the Oligotrichida assume that these tailless genera originated from the Type IV as homologs of the dorsal kineties in the hypotrich and pattern of the tailless genus Omegastrombidium than from the stichotrich spirotrichs (Agatha 2004a,b; Agatha and Strüder- Type VI pattern of the tailed genus Paratontonia; however, Kypke 2007; Foissner et al. 2007), the evolution of the ciliary ontogenetic and/or molecular data are required to support this patterns can be inferred from the orientation of the somatic conjecture for Apostrombidium. While the Type X pattern of dikinetids (based on which basal body bears the cilium) Apostrombidium probably evolved from the Type IV pattern and the location of the oral primordium. The orientation by a dorsal split of the girdle kinety and an extension of the of the somatic dikinetids was inferred from a line drawing new kinety ends to the posterior cell pole, the development of of the ventral side in Apostrombidium and a micrograph of the Type XII pattern in Varistrombidium was more complex. the posterior ventral cell portion in Varistrombidium; both First, a hypothetical intermediate Type XI pattern was gen- patterns were verified by D. Xu (Department of Biology, erated by an elongation and sinistral torsion of the parallel North Carolina Central University, NC, USA) and W. Song girdle kinety ends, while the ventral kinety disappeared. Next, (Laboratory of Protozoology, Ocean University of China, the dorsal portion of the first whorl broke, and the new kinety Qingdao, China), using the type slides of A. pseudokielum ends extended to the posterior cell pole, cutting through the and the protargol slides of V. kielum. kinety spirals and producing the several ciliary row fragments Data on the ontogenesis of Strombidium montagnesi and characteristic of the Type XII pattern. A similar, but conver- S. wilberti were published by Xu et al. (2006c) and Song gent dorsal split of the girdle kinety occurred not only in the (2005), respectively. The position of the oral primordium Type X pattern of Apostrombidium, but also in the Type VIII was studied in S. constrictum, using protargol slides from pattern of Cyrtostrombidium. the type locality kindly provided by D.H. Lynn (Depart- Besides the Type VI pattern of Paratontonia (see above) ment of Integrative Biology, University of Guelph, Canada), and the Type VII pattern of Laboea and Spirotontonia,two and in Paratontonia gracillima, using protargol-impregnated further somatic ciliary patterns probably developed from the specimens from the North Pacific kindly provided by the Type V pattern: the Type VIII pattern of Cyrtostrombidium Tohoku University Museum (Sendai, Japan). In Omegastrom- (the pre-equatorial position of the girdle kinety suggests this bidium elegans, however, the position of the oral primordium origin) and the Type IX pattern of Strombidium constrictum, could only be inferred from micrographs, because of the two S. montagnesi, and S. wilberti. In contrast to the Type V pat- slides stated to be deposited in the Natural History Museum in tern, e.g., found in the type species Strombidium sulcatum London, one was inadequate to evaluate the target structures (Fauré-Fremiet 1912, 1953), the formation of the oral pri- and the other was not included into the collection. Hence, the mordium commences anteriorly to the girdle kinety in the information was taken from Figures 41 and 42 in Song et al. latter pattern (refer to Fig. 1; own data; Song 2005; Xu et al. (2000; p. 340). 2006c). Since the extrusome attachment sites usually form a stripe along the anterior margin of the girdle kinety in the olig- otrichids, the insertion of the extrusomes distinctly separate Results and Discussion from the girdle kinety and anterior to the oral primordium in S. constrictum (Fig. 7) suggests the former position and Evolution of the Somatic Ciliary Patterns course of the girdle kinety. Thus, it seems likely that the Type IX pattern evolved from the Type V pattern by a migration In Agatha (2004a), the hypothetical evolution of the of the horizontal girdle kinety below the oral primordium, oligotrichid somatic ciliature comprised six patterns: the as proposed by Agatha (2004b). However, this arrangement Types I–V, and VII. Below, five further patterns are recog- of the girdle kinety developed twice independently: in S. nized, viz., the Types VI, VIII–X, and XII (Fig. 1). montagnesi and S. wilberti, both the girdle kinety and the S. Agatha / European Journal of Protistology 47 (2011) 51–56 53 Fig. 1. Hypothetical evolution of oligotrichid somatic ciliary patterns. Small arrows mark the orientation
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