Reconciling classical and molecular phylogenies in the stichotrichines (Ciliophora, Spirotrichea), including new sequences from some rare species

doi:10.1016/j.ejop.2004.05.004

European Journal of Protistology

Volume 40, Issue 4, 9 December 2004, Pages 265-281

https://doi.org/10.1016/j.ejop.2004.05.004 Get rights and content

Abstract

We performed a comparative morphological and molecular study on oxytrichid and urostylid stichotrichs (=part of the former hypotrichs). Included are new small subunit (18S) ribosomal RNA (rRNA) gene sequences from five rare oxytrichids (Gonostomum namibiense, Cyrtohymena citrina, Hemiurosoma terricola, Onychodromopsis flexilis, Orthoamphisiella breviseries) and published sequences, based on cultures provided by the senior author, of two key stichotrichid genera, viz., Gastrostyla and Engelmanniella. These and other sequences, altogether 27 species representing 23 genera, were used to analyze how 18S rRNA-based phylogenetic trees can be reconciled with the morphological and ontogenetical data. In 18S rRNA trees, the oligotrichine family Halteriidae invariably clusters within the oxytrichid clade, usually near Oxytricha granulifera, type species of the genus. This position is hardly supported by morphological and ecological evidence and, especially, it contradicts the current ontogenetic findings; possibly, it is an artifact caused by taxa undersampling and/or special molecular evolutionary events. In contrast, most morphological and DNA sequence data of the stichotrichs can be harmonized with the CEUU (Convergent Evolution of Urostylids and Uroleptids) hypothesis which suggests that the urostylid midventral pattern evolved from an oxytrichine ancestor, developing a second time within the Oxytrichidae. The systematic position of one of the two key genera could be clarified with the 18S rRNA sequences: Gastrostyla is a stylonychine oxytrichid. Based on the molecular data and a reassessment of ontogenesis, a new genus, Styxophrya nov. gen., is established for Onychodromus quadricornutus Foissner, Schlegel & Prescott, 1987.

Introduction

The spirotrichs are a large group of ciliates consisting of about 2000 described species. The majority of these species have recently been classified into two main lineages, i.e., the oligotrichs and hypotrichs s.l. (Petz and Foissner 1992; Lynn and Small 1997). The heterotrichs, which were considered as typical spirotrichs for a long time (Bütschli 1889; Kahl 1932; Corliss 1979), are now regarded as a separate class within the subphylum Postciliodesmatophora due to their special somatic ultrastructure (postciliodesmata) and the macronucleus, which divides by extramacronuclear microtubules (Lynn and Small 1997). A large part of the remaining spirotrichs are hypotrichs s.l., which were split, mainly according to DNA sequence data (Lynn and Small (1997), Lynn and Small (2002)), into hypotrichs s.str. (the former euplotids) and stichotrichs (all other former hypotrichs). However, this classification is still in discussion (Chen and Song 2002).

Our paper has three main aims. First, we will discuss the classification of the oligotrichine halteriids which molecular phylogenies (Hoffman and Prescott 1997; Strüder-Kypke and Lynn 2003) assign to the stichotrichine hypotrichs, neglecting the highly conflicting ontogenetic evidence (Petz and Foissner 1992). The second aim of our study concerns the classification of some groups of stichotrichs for which sufficient morphological, ontogenetical, and DNA sequence data are available to investigate as to whether morphological and sequence data can be reconciled. We shall pay special attention to the oxytrichids and urostylids, two distinct lineages recognized already by Bütschli (1889), Kahl (1932) and Borror (1972). The former are characterized by the 18 fronto-ventral-transverse (FVT) cirral pattern (Berger 1999), while the latter have a so-called midventral row composed of two rows of cirri arranged in a highly characteristic zigzag (=midventral) pattern (Borror 1972). We will show that this pattern probably evolved twice from the 18 FVT cirral pattern by anlagen multiplication.

Finally, we will investigate the subfamilial and generic classification of the oxytrichid stichotrichs, a difficult enterprise not only for morphologists (see the opposing views of Berger and Foissner 1997 and Eigner 1997), but also for molecular systematists, who usually discuss this matter only marginally. For this reason, we sequenced 18S rRNA genes of several uncommon stichotrichs and evaluated published sequences. The majority of these sequences had been retrieved from rare and interesting species sent to or identified for Prof. Prescott by the senior author. The sequences of these species, especially Gastrostyla steinii and Engelmanniella mobilis, were published recently, but not discussed from a morphological point of view (Croft et al. 2003; Hewitt et al. 2003).

Our study tries to reconcile classical and molecular taxonomy of the stichotrichs by reconsidering the morphological axioms and emphasizing the frequently ignored hiatus between various molecular classifications. A detailed discussion of this matter is urgently needed because the increasing complexity of the data makes it difficult to discuss them properly. It is likely that most problems are caused by undersampling of taxa and parallel evolution, which is much more common than usually assumed and difficult to recognize with any method.

Section snippets

Materials and methods, terminology

Species investigated: Relevant data for the species investigated are compiled in Table 1. Most of the new sequences are from terrestrial stichotrichs cultivated with the non-flooded Petri dish method, as described in Foissner et al. (2002). About 50 specimens from each culture were collected with a fine pipette, washed in Eau de Volvic (French table water), immersed in a solution of 8 M guanidine chloride, and stored at room temperature until DNA extraction.

All other sequences are retrieved from

The puzzling classification of halteriids

Halteria has been considered as a typical oligotrich ciliate for a long time (Kahl 1932; Corliss 1979). However, in 1988 doubts arose when Lynn and Sogin (1988) showed that 18S rRNA sequences locate Halteria within the stichotrichine spirotrichs (formerly, hypotrichs). Subsequently, this classification has been confirmed by other working groups and for several Halteria populations (Hoffman and Prescott 1997; Snoeyenbos-West et al. 2002; Hewitt et al. 2003; Strüder-Kypke and Lynn 2003) and even

Contrasting morphological and molecular classifications of two major stichotrichine lineages: oxytrichids and urostylids/holostichids

Berger and Foissner (1997) and/or Berger (1999) should be consulted for terminology and synonymy and for a detailed discussion of oxytrichid morphology and characters.

The distinction of oxytrichids from urostylids (composed of urostylid and holostichid stichotrichs) dates back to Bütschli (1889). Later, Borror (1972) refined terminology by introducing the term midventral row, that is, two narrowly spaced, median cirral rows, whose paired cirri form a highly characteristic zigzag (= midventral)

The CEUU hypothesis: an attempt to reconcile morphological and molecular classifications of oxytrichid and urostylid stichotrichs

There is increasing evidence for convergent evolution of many of the characteristic stichotrichine cirral patterns (Berger and Foissner 1997; Eigner (1994), Eigner (1997); Berger 1999; Shi et al. 1999; Foissner et al. 2002). The CEUU (Convergent Evolution of Urostylids and Uroleptids) hypothesis, which tries to combine classical and molecular data, proposes that even one of the most distinct features, viz., the midventral pattern, evolved convergently in at least two lineages (Fig. 4). The CEUU

Classification of lower categories

Although 18S rRNA gene sequences are probably not the ideal marker for distinguishing ciliate genera and species, they are frequently used for this purpose, e.g., by Lynn et al. (2000), Strüder-Kypke et al. (2000), Modeo et al. (2003), and Shang et al. (2003). Indeed, morphologically related species often cluster together in 18S rRNA gene trees, as also evident from our data, for instance, the three Uroleptus species. However, in stichotrichs the matter is more complicated because the

Styxophrya nov. gen

Diagnosis: Oxytrichidae (Stylonychinae) with oral apparatus in Stylonychia pattern. Many (>30) fronto-ventral-transverse cirri in several distinct rows. More than 6 dorsal kineties. Caudal cirri present. Cytoplasmic processes (horns) on dorsal surface. Distinctly more than 6 fronto-ventral-transverse cirral primordia, each producing many cirri and originating independently in proter and opisthe. Dorsal kineties with multiple fragmentation, dorsomarginal kineties present.

Type species:

Acknowledgements

We thank Prof. Dr. Martin Schlegel (Leipzig University) and Dr. Sabine Agatha for helpful comments. The technical assistance of Dr. Eva Herzog is greatly acknowledged. The study was supported by the Austrian Science Foundation (FWF), projects P-15017 and P-14778.

References (70)

H. Berger et al.
Cladistic relationships and generic characterization of oxytrichid hypotrichs (Protozoa, Ciliophora)
Arch. Protistenk
(1997)
D. Bernhard et al.
Phylogenetic relationships within the class Spirotrichea (Ciliophora) inferred from small subunit rRNA gene sequences
Molec. Phylogen. Evol
(2001)
M.R. Duvall et al.
18S gene trees are positively misleading for monocot/dicot phylogenetics
Molec. Phylogen. Evol
(2004)
P. Eigner
Divisional morphogenesis and reorganization in Eschaneustyla brachytona Stokes, 1886 and revision of the Bakuellinae (Ciliophora, Hypotrichida)
Europ. J. Protistol
(1994)
P. Eigner
Comparison of divisional morphogenesis in four morphologically different clones of the genus Gonostomum and update of the natural hypotrich system (Ciliophora, Hypotrichida)
Europ. J. Protistol
(1999)
P. Eigner et al.
Divisional morphogenesis in Bakuella pampinaria nov. spec. and reevaluation of the classification of the urostylids (Ciliophora, Hypotrichida)
Europ. J. Protistol
(1992)
E.A. Hewitt et al.
Phylogenetic relationships among 28 spirotrichous ciliates documented by rDNA
Molec. Phylogen. Evol
(2003)
R.P. Hirt et al.
Phylogenetic relationships among karyorelictids and heterotrichs inferred from small subunit rRNA sequencesresolution at the base of the ciliate tree
Molec. Phylogen. Evol
(1995)
F. Jeanmougin et al.
Multiple sequence alignment with Clustal X
Trends Biochem. Sci
(1998)
K. Kelminson et al.
Histone H4 genes in some stichotrichous ciliates
Europ. J. Protistol
(2002)

D.H. Lynn et al.

Assessment of phylogenetic relationships among ciliated protists using partial ribosomal RNA sequences derived from reverse transcripts

BioSystems

(1988)

M.K. Shin et al.

Phylogenetic position of the ciliates Phacodinium (order Phacodiniida) and Protocruzia (subclass Protocruziidia) and systematics of the spirotrich ciliates examined by small subunit ribosomal RNA gene sequences

Europ. J. Protistol

(2000)

M.C. Strüder-Kypke et al.

Phylogenetic relationships of the genus Paramecium inferred from small subunit rRNA gene sequences

Molec. Phylogen. Evol

(2000)

A. Warren et al.

The morphology of the poorly known freshwater urostylid ciliate Neokeronopsis spectabilis (Kahl, 1932) nov. gen., nov. comb., (Ciliophora, Urostylidae), with notes on its morphogenesis

Europ. J. Protistol

(2002)

E. Wirnsberger-Aescht et al.

Morphogenesis and ultrastructure of the soil ciliate Engelmanniella mobilis (Ciliophora, Hypotrichida)

Europ. J. Protistol

(1989)

E. Wirnsberger-Aescht et al.

Natural and cultured variability of Engelmanniella mobilis (Ciliophora, Hypotrichida); with notes on the ultrastructure of its resting cyst

Arch. Protistenk

(1990)

Berger, H., 1999. Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae biol., 78, i–xii,...

H. Berger

Catalogue of Ciliate Names 1

(2001)

H. Berger et al.

Morphology and biometry of some soil hypotrichs (Protozoa, Ciliophora) from Europe and Japan

Bull. Br. Mus. nat. Hist. (Zool.)

(1989)

A.C. Borror

Revision of the order Hypotrichida (Ciliophora, Protozoa)

J. Protozool

(1972)

A.C. Borror et al.

The suborder Urostylina Jankowski (Ciliophora, Hypotrichida)morphology, systematics and identification of species

Acta Protozool

(1983)

O. Bütschli

Protozoa. III. AbtheilungInfusoria und system der Radiolaria

Z. Chen et al.

Phylogenetic positions of Aspidisca steini and Euplotes vannus within the order Euplotida (Hypotrichia: Ciliophora) inferred from complete small subunit ribosomal RNA gene sequences

Acta Protozool

(2002)

J.O. Corliss

The ciliated protozoa. Characterization, classification and guide to the literature

(1979)

K.E. Croft et al.

Macronuclear molecules encoding actins in spirotrichs

J. Molec. Evol

(2003)

C.R. Curds

A guide to the species of the genus Euplotes (Hypotrichida, Ciliatea)

Bull. Br. Mus. nat. Hist. (Zool.)

(1975)

J. Dragesco et al.

Ciliés libres de l’Afrique intertropicale. Introduction à la connaissance et à l’étude des ciliés

Faune tropicale

(1986)

P. Eigner

Evolution of morphogenetic processes in the Orthoamphisiellidae n. fam., Oxytrichidae, and Parakahliellidae n. fam., and their depiction using a computer method (Ciliophora, Hypotrichida)

J. Euk. Microbiol

(1997)

P. Eigner

Divisional morphogenesis in Uroleptus caudatus (Stokes, 1886), and the relationship between the Urostylidae and the Parakahliellidae, Oxytrichidae, and Orthoamphisiellidae on the basis of morphogenetic processes (Ciliophora, Hypotrichida)

J. Euk. Microbiol

(2001)

P. Eigner et al.

Divisional morphogenesis in Amphisiellides illuvialis n. sp., Paramphisiella caudata (Hemberger) and Hemiamphisiella terricola Foissner, and redefinition of the Amphisiellidae (Ciliophora, Hypotrichida)

J. Euk. Microbiol

(1994)

Fauré-Fremiet, E., 1961. Remarques sur la morphologie comparée et la systématique des ciliata Hypotrichida. C. r. hebd....

J. Felsenstein

PHYLIP (Phylogenetic Inference Package) version 3.6a3. Distributed by the author

(2002)

T. Fenchel et al.

A purple protist

Nature

(1993)

W. Foissner

Ontogenesis in ciliated protozoa, with emphasis on stomatogenesis

W. Foissner et al.

Identification and ontogenesis of the nomen nudum hypotrichs (Protozoa: Ciliophora) Oxytricha nova (= Sterkiella nova sp. n.) and O. trifallax (= S. histriomuscorum)

Acta Protozool

(1999)

Cited by (108)

Morphology and molecular phylogeny of two new soil ciliates, Hemiurosomoida warreni nov. spec. and Hemiurosoma clampi nov. spec. (Ciliophora, Hypotrichia) from Tibet
2021, European Journal of Protistology
Citation Excerpt :
There are over 1000 species distributed throughout approximately 200 genera (Berger 1999, 2001, 2006, 2008, 2011; Foissner 2016; Foissner et al. 2002; Shao et al. 2015; Song and Shao 2017). Morphogenetic data are increasingly used to discriminate morphologically similar species (Bai et al. 2018; Berger 1999, 2006, 2008, 2011; Borror 1972; Chen et al. 2018; Deng et al. 2018; Foissner 1999, 2016; Foissner and Adam 1983; Foissner et al. 2002; Jerka-Dziadosz 1963, 1965; Jung and Berger 2019; Li F.C. et al. 2017; Lynn 2008; Shao et al. 2013; Wang et al. 2017a,b, 2019; Xu et al. 2019, 2020; Zhang et al. 2018, 2020) and phylogenetic analyses have led to a better understanding of the systematics and evolutionary relationships of hypotrichs (Dong et al. 2020; Foissner et al. 2004; Gao et al. 2016, 2017; Li Y.B. et al. 2018; Luo et al. 2018; Lyu et al. 2018b, c; Schmidt et al. 2007; Shao et al. 2007; Sheng et al. 2018; Wang Y. et al. 2019). The genus Hemiurosomoida was established by Singh and Kamra (2015) with H. longa (original combination: Oxytricha longa Gelei and Szabados, 1950) designated as the type species.
Two novel hypotrichous ciliates, Hemiurosomoida warreni nov. spec. and Hemiurosoma clampi nov. spec., isolated from soil in the Lhalu Wetland and Motuo Virgin Forest in Tibet, respectively, were investigated using live observation and protargol staining. Hemiurosomoida warreni nov. spec. strongly resembles the type species H. longa but can be distinguished by its body size in vivo (110–145 × 30–40 μm vs. 50–100 × 18–40 μm), number of adoral membranelles (25–38 vs. 15–22), and numbers of right (29–39 vs. 14–23) and left (26–35 vs. 13–23) marginal cirri, transverse cirri (3 vs. 4 or 5) and macronuclear nodules (4–8 vs. 2). Hemiurosoma clampi nov. spec. is characterized by its vermiform body shape, colourless cortical granules distributed in irregular rows, two macronuclear nodules, three frontal cirri, one buccal cirrus, four frontoventral cirri ranged in a line, two transverse cirri, lacking postoral ventral and pretransverse ventral cirri, and marginal rows that are not posteriorly confluent. Phylogenetic analyses based on SSU rDNA gene sequences suggest that Hemiurosomoida is not monophyletic. A close relationship is revealed between Hemiurosomoida warreni nov. spec., Parakahilella macrostoma, Hemiurosoma clampi nov. spec., and the type species Hemiurosoma terricola. As expected, all these species are classified within the “non-oxytrichid Dorsomarginalia”.
Wilhelm Foissner and the European Journal of Protistology
2020, European Journal of Protistology
Systematic Redefinition of the Hypotricha (Alveolata, Ciliophora) Based on Combined Analyses of Morphological and Molecular Characters
2020, Protist
Citation Excerpt :
Separate analyses: Trees resulting from the 18S matrix under ML and parsimony (Supplementary Material Figs S2, S4) are in conformity with the array of phylogenetic patterns found in previous studies (e.g. Chen L. et al. 2017; Foissner et al. 2014; Gao et al. 2016; Heber et al. 2014; Park et al. 2017, 2020; Shao et al. 2014c; Singh and Kamra 2013, 2015a), thus, warrant no further discussion in the present context. Interestingly enough, the ML and parsimony morphological trees (Supplementary Material Figs S1, S3) independently corroborated some major findings from earlier molecular analyses, namely that neither traditional urostylids nor the 18-FVT oxytrichids are monophyletic, and uroleptids are more closely related to the latter than to the former (Foissner et al. 2004; Paiva et al. 2009; Schmidt et al. 2007). In addition, other notable molecular-based discoveries on the affinities of hypotrich genera were represented by the results of the morphological analyses, as for instance: the non-monophyly of genera such as Anteholosticha (Berger 2003, 2006b; Huang et al. 2014; Zhao et al. 2015), Oxytricha s. l. (Méndez-Sánchez et al. 2018; Paiva et al. 2009; Schmidt et al. 2007), and Sterkiella (Bharti et al. 2018; Hewitt et al. 2003); the placement of the midventral complex-bearing Neokeronopsis and Pattersoniella among Dorsomarginalia (Bernhard et al. 2001; Foissner and Stoeck 2008); a monophylum formed by Hemiamphisiella, Pseudouroleptus and Strongylidium (Bharti et al. 2014; Chen et al. 2013a; Jung et al. 2014; Paiva et al. 2009), viz. the strongylidiids, and their affinity to or within Dorsomarginalia (Luo et al. 2018); the separation of marine amphisiellids from other amphisiellid ventral row-bearing hypotrichs, such as Gastrostyla and strongylidiids (Berger 2008; Chen et al. 2013a; Huang et al. 2016).
The systematics of Hypotricha is one of the most puzzling problems in ciliate biology, having spanned numerous conflicting hypotheses with unstable relationships at various levels in molecular trees, for which the constant addition of newly discovered species has only increased the confusion. The hypotrichs comprise a remarkable morphologically diversified group of ciliates, and the phylogenetic potential of morphological traits is generally recognized. However, such characters were rarely used in phylogenetic reconstructions, and congruence with molecular data never assessed from simultaneous analyses. To properly reconciliate morphological and molecular information, maximum-likelihood and parsimony analyses of 79 morphological characters and 18S rDNA sequences were performed for 130 ingroup terminals, broadly sampled to represent the known hypotrich diversity. As result, well-supported and relatively stable clades were recovered, based on which the redefined Hypotricha comprises at least six higher taxa: The “arcuseriids”, Holostichida, Parabirojimida, and the “amphisiellids”, plus the two large clades Kentrurostylida nov. tax. (Hispidotergida nov. tax. and Simplicitergida nov. tax.) and Diatirostomata nov. tax. (“bistichellids”, “kahliellids”, Gonostomatida and Dorsomarginalia [Postoralida nov. tax. and Uroleptida]). Each taxon was circumscribed by synapomorphies, of which most were homoplastic, as the natural history of hypotrichs is portrayed by an outstanding quantity of convergences and reversions.
Description of a new species of Tetmemena (Ciliophora, Oxytrichidae) using classical and molecular markers
2020, Journal of King Saud University - Science
Tetmemena saprai n. sp. was isolated from fresh-water samples collected from Okhla Bird Sanctuary, Delhi, India and described based on its morphology, morphogenesis and molecular markers, namely the small-subunit (SSU) rRNA gene and internal transcribed spacers (ITS1-5.8S-ITS2). The morphological features of T. saprai n. sp. are as follows: colourless; rigid body with no cortical granules; water expelling vesicle about 15 µm in size, located below the adoral zone of membranelles near the left body margin; body size about 125–140 × 50–60 μm in live and about 100 × 45 μm in protargol preparations, with body length : width ratio should be 2:1; undulating membranes in a Stylonychia-pattern; adoral zone about 44 μm in length with (on average) 45 adoral membranelles; 18 frontal-ventral-transverse cirri; one right and one left marginal row; six dorsal rows including two dorsomarginals, of which the fourth row is shortened anteriorly; three caudal cirri which are not equidistant; two macronuclear nodules; 2–4 micronuclei. A detailed morphogenetic study revealed the oral primordium to originate near the leftmost transverse cirrus, and the involvement of five parental cirri (three frontals and two ventrals) in the formation of streaks I–VI for the proter and opisthe. The genetic distance between T. saprai n. sp. and its congeners T. pustulata and T. vorax (S. vorax) varied from between 1% and 2% in the SSU rRNA gene and 1% and 6% in the ITS1-5.8S-ITS2 sequence. The secondary structures of the ITS1 and ITS2 RNA transcripts of four different species of genus Tetmemena (T. saprai n. sp., T. pustulata, T. vorax and T. bifaria) were also compared, revealing that the ITS1 region was more variable than ITS2. The morphological and morphogenetic characterisation, and phylogenetic analyses based on the molecular markers, confirm that the present species is a distinct species of the genus Tetmemena belonging to the subfamily Stylonychinae. This study also reveals that the macronuclear ITS region can be a suitable candidate for species identification.
Two Urosoma species (Ciliophora, Hypotrichia): A multidisciplinary approach provides new insights into their ultrastructure and systematics
2020, European Journal of Protistology
The general morphology and ultrastructure of two soil hypotrichous ciliates, Urosoma emarginata and U. salmastra, were investigated using light microscopy, scanning electron microscopy and transmission electron microscopy. Phylogenetic analyses, based on the newly sequenced small subunit ribosomal (SSU) rRNA genes, were conducted on three U. emarginata populations and one U. salmastra population. Our findings support for the validity of Perilemmaphora Berger, 2008, a rankless taxon comprising spirotrich ciliates having a perilemma. The cortical granules of both species are extrusomes representing a new type of mucocyst in U. emarginata and possibly a new type of pigmentocyst in U. salmastra. Additionally, the lithosomes were revealed as subglobose structures composed of a low electron-dense, homogeneous inner part and an electron-dense outer part. The ultrastructural features of the cortical granules, together with ontogenetic and molecular phylogenetic data, suggest that the genus Urosoma might need to be divided. It is posited that ultrastructural features of hypotrichous ciliates in general may have important taxonomic value warranting further investigation.
A huge diversity of metopids (Ciliophora, Armophorea) in soil from the Murray River floodplain, Australia. III. Morphology, ontogenesis and conjugation of Metopus boletus nov. spec., with implications for the phylogeny of the SAL supercluster
2019, European Journal of Protistology
The morphology, ontogenesis, conjugation, and phylogenetic position of Metopus boletus nov. spec. were studied using live observation, various silver impregnation methods, scanning electron microscopy, morphometry, and the 18S rRNA gene sequence. The new species is outstanding in having a mushroom-like appearance; a globular to broadly ellipsoid macronucleus in anterior body half; 5–10 elongated caudal cilia; 4–6 dikinetids curved rightwards in the anterior portion of the first postoral kinety; and an adoral zone composed of an average of 28 small polykinetids. Ontogenesis of M. boletus follows the metopid mode and the species-specific vegetative morphology is obtained after division. Its conjugation is temporary, isogamic and the partners unite ventral-to-dorsal, forming strongly arched to almost rod-like pairs, which indicates a heteropolar arrangement. There are only two maturation divisions and a single synkaryon division in exconjugants. The conjugation data corroborate a sister group relationship of the classes Armophorea and Litostomatea within the SAL (Spirotrichea + Armophorea + Litostomatea) supercluster in that the partners unite ventral-to-dorsal and the main body axes are antiparallel. On the other hand, the last common ancestor of the spirotricheans very likely had a ventral-to-ventral and homopolar conjugation mode with the main body axes oriented in parallel.

View all citing articles on Scopus

View full text

Reconciling classical and molecular phylogenies in the stichotrichines (Ciliophora, Spirotrichea), including new sequences from some rare species

Abstract

Introduction

Section snippets

Materials and methods, terminology

The puzzling classification of halteriids

Contrasting morphological and molecular classifications of two major stichotrichine lineages: oxytrichids and urostylids/holostichids

The CEUU hypothesis: an attempt to reconcile morphological and molecular classifications of oxytrichid and urostylid stichotrichs

Classification of lower categories

Styxophrya nov. gen

Acknowledgements

Arch. Protistenk

Molec. Phylogen. Evol

Molec. Phylogen. Evol

Europ. J. Protistol

Europ. J. Protistol

Europ. J. Protistol

Molec. Phylogen. Evol

Molec. Phylogen. Evol

Trends Biochem. Sci

Europ. J. Protistol

BioSystems

Europ. J. Protistol

Molec. Phylogen. Evol

Europ. J. Protistol

Europ. J. Protistol

Arch. Protistenk

Catalogue of Ciliate Names 1

Morphology and biometry of some soil hypotrichs (Protozoa, Ciliophora) from Europe and Japan

Bull. Br. Mus. nat. Hist. (Zool.)

Revision of the order Hypotrichida (Ciliophora, Protozoa)

J. Protozool

The suborder Urostylina Jankowski (Ciliophora, Hypotrichida)morphology, systematics and identification of species

Acta Protozool

Protozoa. III. AbtheilungInfusoria und system der Radiolaria

Phylogenetic positions of Aspidisca steini and Euplotes vannus within the order Euplotida (Hypotrichia: Ciliophora) inferred from complete small subunit ribosomal RNA gene sequences

Acta Protozool

The ciliated protozoa. Characterization, classification and guide to the literature

Macronuclear molecules encoding actins in spirotrichs

J. Molec. Evol

A guide to the species of the genus Euplotes (Hypotrichida, Ciliatea)

Bull. Br. Mus. nat. Hist. (Zool.)

Ciliés libres de l’Afrique intertropicale. Introduction à la connaissance et à l’étude des ciliés

Faune tropicale

Evolution of morphogenetic processes in the Orthoamphisiellidae n. fam., Oxytrichidae, and Parakahliellidae n. fam., and their depiction using a computer method (Ciliophora, Hypotrichida)

J. Euk. Microbiol

Divisional morphogenesis in Uroleptus caudatus (Stokes, 1886), and the relationship between the Urostylidae and the Parakahliellidae, Oxytrichidae, and Orthoamphisiellidae on the basis of morphogenetic processes (Ciliophora, Hypotrichida)

J. Euk. Microbiol

Divisional morphogenesis in Amphisiellides illuvialis n. sp., Paramphisiella caudata (Hemberger) and Hemiamphisiella terricola Foissner, and redefinition of the Amphisiellidae (Ciliophora, Hypotrichida)

J. Euk. Microbiol

PHYLIP (Phylogenetic Inference Package) version 3.6a3. Distributed by the author

A purple protist

Nature

Ontogenesis in ciliated protozoa, with emphasis on stomatogenesis

Identification and ontogenesis of the nomen nudum hypotrichs (Protozoa: Ciliophora) Oxytricha nova (= Sterkiella nova sp. n.) and O. trifallax (= S. histriomuscorum)

Acta Protozool