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Abstract The history of ciliate systematics has 
been divided into fi ve periods: (1) the Age of 
 Discovery; (2) the Age of Exploitation; (3) the 
Age of Infraciliature; (4) the Age of Ultrastructure; 
and (5) the Age of Refi nement. Progress in each 
of these periods arose through an interaction of 
technology and conceptual views. For example, 
refi ned silver staining techniques revealed the law 
of desmodexy of the ciliate cortex and enabled the 
development of comparative morphogenetics in 
the Age of Infraciliature. Electron microscopy was 
essential for the conceptual notion of levels of 
organization below the cell and provided the impetus 
for the structural conservatism hypothesis in the 
Age of Ultrastructure. In this latter age, the foundations
for the current classifi cation system have been laid. 
Gene sequencing has provided the next techno-
logical innovation, which has enabled testing and 
revising our views on relationships in the current 
Age of Refi nement. Major differences between the 
scheme presented herein with its two subphyla and 
11 classes and other competing schemes are briefl y 
discussed.
Keywords Kinetid, cortex, rRNA gene, molecular
phylogeny, organic design 
 Systematics as a discipline was defined by Simpson 
(1961) as “the scientific study of the kinds and 
diversity of organisms and of any and all relation-
ships among them” (p. 7). One aim of modern 
systematics is to represent these relationships 
among organisms by natural classifications : these 
are hierarchical and reflect as closely as possible 
the true phylogeny of a group of organisms. The 
approach to establishing a hierarchical classifica-
tion is influenced by the conceptual views of how 
significant particular characters are in inferring 
relationships, and these conceptual views, in their 
turn, are influenced by the technical approaches in 
vogue. In this context, Corliss (1974a) discussed 
the historical development of ciliate systematics 
in four periods: (1) the Age of Discovery (1880–
1930), exemplified by Bütschli; (2) the Age of 
Exploitation (1930–1950), exemplified by Kahl; 
(3) the Age of the Infraciliature (1950–1970), 
exemplified by Chatton, Lwoff, and Fauré-Fremiet, 
and during which Corliss (1961) published the first 
edition of “The Ciliated Protozoa”; and (4) the Age 
of Ultrastructure , whose beginnings around 1970 
were summarized in the review chapter by Pitelka 
(1969). The zenith of the Age of Ultrastructure 
(1970–1990) was at the time of the second edition 
of “The Ciliated Protozoa” by Corliss (1979), and 
its ending might be established around 1990, at the 
appearance of the first reports on gene sequences 
of ciliates. Indeed, Greenwood, Sogin, and Lynn 
(1991a) suggested this criterion as the beginning of 
a fifth age – the Age of Refinement (1990–present), 
during which the major lines of evolution and our 
closest approach yet to a natural classification for 
the phylum might be possible. It is therefore useful 
to briefly review this history, especially empha-
sizing the last 50 years to understand how ciliate 
systematics has indeed progressed. 
 Chapter 1 
 Introduction and Progress 
in the Last Half Century 
1
2 1. Introduction and Progress in the Last Half Century
 1.1 The Ages of Discovery 
(1880–1930) and Exploitation 
(1930–1950)
 Bütschli (1887–1889) and Kahl (1930–1935), exem-
plifying the Ages of Discovery and Exploitation, 
respectively, primarily used light microscopic 
observations of living ciliates, without the use of 
sophisticated stains. From the Age of Discovery 
to the Age of Exploitation, the number of higher 
taxa doubled as our understanding of diversity 
exploded (Table 1.1). The conceptual approach 
focused on the character of the somatic and oral 
ciliature and on a consideration that evolution 
proceeded from simpler forms to more complex 
forms. This is reflected in the characterization of 
the higher taxa by Bütschli as Holotricha – evenly 
covered by somatic cilia – and Spirotricha – with a 
prominent spiralling adoral zone of membranelles 
(Table 1.1). The suctorians with their bizarre ten-
tacled appearance and absence of external ciliature 
were given equivalent stature to all other ciliates 
by both Bütschli and Kahl. Other specialized and 
“complex” sessile forms, like the chonotrichs and 
 peritrichs , were also segregated to a higher rank 
by Kahl, equivalent to Holotricha and Spirotricha 
(Table 1.1). Within these higher taxa, oral features, 
indicated by the suffix “-stomata”, were major 
characters to indicate common descent (Table 1.1). 
It is interesting to note that the opalinid “flagel-
lates” were considered “protociliates” during the 
Kahlian period based on the views of Metcalf 
(1923, 1940) among others (Table 1.1). 
 1.2 The Age of the Infraciliature 
(1950–1970)
 Five scientists – Chatton and Lwoff, Klein, von 
Gelei, and Fauré-Fremiet – stand out as the pioneers
of this period, which Corliss (1974a) suggested 
extended from about 1950 to 1970. Yet, the roots 
of this age originated earlier in the 20th century in 
descriptions of the different technical approaches 
to using silver to stain the cortex and other struc-
tures of ciliates – the dry silver method of Klein 
(1929) and the wet silver method of Chatton and 
Lwoff (1930). The observations made by these 
pioneers culminated in seminal conceptual papers 
attributing a variety of causal relationships to 
various infraciliary structures (Chatton & Lwoff, 
1935b; Klein, 1928, 1929; von Gelei, 1932, 1934b; 
von Gelei & Horváth, 1931). Chatton and Lwoff’s 
(1935b) law of desmodexy stands out as one of 
the “rules” emerging from this period that has 
stood the test of time: true kinetodesmata and/or 
kinetodesmal fibrils, when present, lie to or extend 
anteriad and/or to the organism’s right of the kinety 
with which they are associated (see Chapter 2 ).
With this rule, one can not only identify a ciliate, 
but also one can deduce the polarity of the cell. The 
developmental autonomy and “genetic” continuity 
Table 1.1. Major systems of ciliate classification popular 
prior to 1950.a
Bütschlian Erab Kahlian Era
(1880–1930)a (1930–1950)
INFUSORIA Subphylum Ciliophora
Ciliata CILIATA
Holotricha Protociliata
 Gymnostomata Opalinata
 Trichostomata Euciliata
 Astomata Holotricha
Spirotricha Gymnostomata
 Heterotricha Prostomata
 Oligotricha Pleurostomata
 Hypotricha Hypostomata
 Peritricha Trichostomata
Suctoria Apostomea
 Hymenostomata
 Thigmotricha
 Stomodea
 Rhynchodea
 Astomata
 Spirotricha
 Heterotricha
 Ctenostomata
 Oligotricha
 Tintinnoinea
 Entodiniomorpha
 Hypotricha
 Peritricha
 Mobilia
 Sessilia
 Chonotricha
SUCTORIA
a
 Classes are indicated in bold capital letters; subclasses, in ital-
ics; orders, in bold; suborders and “tribes”, further indented in 
Roman type.
b
 It should be noted that Bütschli (1887–1889) originally pro-
posed a scheme that differed slightly from that shown (see 
Corliss, 1962a; Jankowski, 1967a). Later workers in the period 
re-arranged it so that it came to resemble the form presented 
here. In all cases, the number of major groups remained essen-
tially the same.
of the infraciliature was summarized at the begin-
ning of this period by Lwoff (1950) in his book 
entitled “Problems of Morphogenesis in Ciliates”. 
 Fauré-Fremiet and his students applied these 
conceptual views of the developmental impor-
tance of infraciliary patterns to resolving phyloge-
netic problems within the phylum. Fauré-Fremiet’s 
(1950a) discussion of comparative morphogenesis 
of ciliates rested on the conceptual presumption 
that similarities in pattern of the ciliature during divi-
sion morphogenesis revealed the common ancestry 
of lineages (see Corliss, 1968). These similarities 
in division morphogenesis were particularly 
important in establishing the phylogenetic affinities 
of polymorphicforms, such as peritrichs , suctorians , 
and chonotrichs . Using similarities in division mor-
phogenesis and an imagined evolutionary trans-
formation from hymenostome to thigmotrich to 
peritrich, Fauré-Fremiet (1950a) made the case 
for the “ hymenostome ” affinities of the peritrichs 
(Fig. 1.1). His student, Guilcher (1951), argued 
that suctorians and chonotrichs ought not to be 
1.2 The Age of the Infraciliature (1950–1970) 3
Fig. 1.1. A Schematic drawings of the hymenostome Tetrahymena, the thigmotrich Boveria, and the peritrich 
Vorticella. Fauré-Fremiet (1950a) related these three groups in a transformation series, imagining that evolution of 
the peritrich form proceeded through a thigmotrich-like intermediate from an ancestral Tetrahymena-like hymenos-
tome. B Schematic drawings of the cyrtophorine Chilodonella and of the mature form and the bud of the chonotrich 
Spirochona. Guilcher (1951) argued that the similarities in pattern between the chonotrich bud and the free-living 
cyrtophorine suggested a much closer phylogenetic relationship between these two groups although the classification 
scheme of Kahl suggested otherwise (see Table 1.1)
4 1. Introduction and Progress in the Last Half Century
greatly separated from other ciliate groups, and she 
claimed that chonotrichs might in fact be highly 
derived cyrtophorine gymnostomes (Fig. 1.1). 
 Furgason (1940) in his studies of Tetrahymena
had imagined a more global evolutionary transfor-
mation of the oral apparatus of ciliates, premissed 
on the assumption that the three membranelles or 
oral polykinetids of Tetrahymena and the hymenos-
tomes preceded the evolution of the many mem-
branelles of the heterotrichs , like Stentor (Fig. 1.2).
 This view was supported by Fauré-Fremiet 
(1950a) and Corliss (1956, 1961) who envisioned 
the hymenostomes as a pivotal group in the evo-
lutionary diversification of the phylum. Corliss 
(1958a) used this concept of transformation of 
oral structures from simpler to more complex to 
argue that the hymenostomes , in their turn, had 
their ancestry in “ gymnostome ”-like forms, such as 
the nassophorean Pseudomicrothorax , which itself 
became another pivotal ancestral type. This led to 
the rearrangement of higher taxa and the proposal 
of a “Faurean” classification system by Corliss 
(1961) (Table 1.2). 
 This new view still maintained the Holotricha 
and Spirotricha , but the opalinids had now been 
removed based on the recognition that they shared 
many significant features with flagellate groups 
(Corliss, 1955, 1960a). Considering the work of 
the French ciliatologists, Corliss (1961) transferred 
the peritrichs , suctorians , and chonotrichs into the 
 Holotricha , recognizing their probable ancestry 
from groups placed in this subclass. Oral structures 
continued to play a dominant role in characterizing 
orders as indicated by the common suffix “-stomatida” 
(Table 1.2). 
 Of course, the underlying assumption of the 
transformation of oral structures proposed by Fauré-
Fremiet, Furgason, Corliss, and others was that the 
oral polykinetids or membranelles of these differ-
ent ciliates – Pseudomicrothorax , Tetrahymena , 
and Stentor – were homologous. It was the inven-
tion of the electron microscope, which was just 
beginning to demonstrate its applicability during 
the latter part of this period, that was to provide the 
evidence to refute this assumption and therefore 
undercut the general application of this concept. 
Fig. 1.2. Schematic drawings of three ciliates that have multiple oral polykinetids. The hymenostome Tetrahymena
has three oral polykinetids and a paroral while the spirotrich Protocruzia and the heterotrich Stentor have many more 
than three. Furgason (1940) imagined that evolution proceeded by proliferation of oral polykinetids or membranelles 
and so the major groups of ciliates could be ordered by this conceptual view into more ancestral-like and more 
derived
 1.3 The Age of Ultrastructure 
(1970–1990)
 As with other ages, the technological roots of 
the Age of Ultrastructure began in the 1950s and 
1960s. The silver proteinate staining technique of 
Bodian or protargol staining became established 
as the light microscopic stain of choice during this 
period, although it had its technological innova-
tors in the previous age (Kozloff, 1946; Kirby, 
1950; Tuffrau, 1967). However, it was electron 
microscopy, promoted by Pitelka (1969), that 
gained preference in resolving questions in both 
the systematics and cell biology of ciliates. These 
early results, coupled with two seminal papers by 
1.3 The Age of Ultrastructure (1970–1990) 5
Table 1.2. Faurean classification and post-Faurean system adopted by Corliss (1979).a
Faurean Era (1950–1970) Post-Faurean Era (1970–1981)
Subphylum Ciliophora Phylum Ciliophora
CILIATA KINETOFRAGMINOPHORA OLIGOHYMENOPHORA
Holotricha Gymnostomata Hymenostomata
Gymnostomatida Primociliatida Hymenostomatida
 Rhabdophorina Karyorelictida Tetrahymenina
 Cyrtophorina Prostomatida Ophryoglenina
Suctorida Archistomatina Peniculina
Chonotrichida Prostomatina Scuticociliatida
Trichostomatida Prorodontina Philasterina
Hymenostomatida Haptorida Pleuronematina
 Tetrahymenina Pleurostomatida Thigmotrichina
 Peniculina Vestibulifera Astomatida
 Pleuronematina Trichostomatida Peritricha
Astomatida Trichostomatina Peritrichida
Apostomatida Blepharocorythina Sessilina
Thigmotrichida Entodiniomorphida Mobilina
 Arhynchodina Colpodida POLYHYMENOPHORA
 Rhynchodina Hypostomata Spirotricha
Peritrichida Synhymeniida Heterotrichida
 Sessilina Nassulida Heterotrichina
 Mobilina Nassulina Clevelandellina
Spirotricha Microthoracina Armophorina
Heterotrichida Cyrtophorida Coliphorina
 Heterotrichina Chlamydodontina Plagiotomina
 Licnophorina Dysteriina Licnophorina
Oligotrichida Hypocomatina Odontostomatida
Tintinnida Chonotrichida Oligotrichida
Entodiniomorphida Exogemmina Oligotrichina
Odontostomatida Cryptogemmina Tintinnina
Hypotrichida Rhynchodida Hypotrichida
 Stichotrichina Apostomatida Stichotrichina
 Sporadotrichina Apostomatina Sporadotrichina
 Astomatophorina
 Pilisuctorina
 Suctoria
 Suctorida
 Exogenina
 Endogenina
 Evaginogenina
a
 Classes are indicated in bold capital letters; subclasses, in italics; orders, in bold with the ending 
“−ida”; suborders, further indented with the ending “−ina”.
6 1. Introduction and Progress in the Last Half Century
Jankowski (1967a, 1973c), prompted the French 
group of de Puytorac, Batisse, Bohatier, Corliss, 
Deroux, Didier, et al. (1974b) and, both with 
his French colleagues and independently, Corliss 
(1974a, 1974b) to propose revised classifications. 
Corliss (1979) used a slightly modified version in 
his third edition to “The Ciliated Protozoa” (Table 
1.2). About this time, Jankowski (1980) proposed 
a new system, which still placed major emphasis 
on oral features as indicated by the names of some 
of his classes – Apicostomata , Pleurostomata , 
 Rimostomata , Synciliostomata , Cyrtostomata , and 
 Hymenostomata . 
 The major feature of these post-Faurean schemes 
was the prominent elevation of oral features. The 
three classes in the phylum were now character-
ized by the nature of the oral apparatus: small, 
simple kinetal fragments characterized the Class 
 Kinetofragminophora ; typically three oral poly-
kinetids or membranelles characterized the Class 
 Oligohymenophora ; and many more than three mem-
branelles characterized the Class Polyhymenophora
(Table 1.2). All three names derived from the 
conceptual vision of Jankowski (1967a, 1973c, 
1975), which shared the same assumption as 
Furgason’s: homology was assumed among “oligo”-
membranelles and “poly”-membranelles. 
 Before we return to a refutation of this assump-
tion, it isimportant to set the conceptual stage, 
which was being constructed during the early 1960s. 
A seminal paper of this period was by Ehret (1960) 
and entitled “Organelle systems and biological 
organization”. Influenced by systems theory , cell 
biology , and the emerging field of molecular bio-
logy , Ehret imagined cells to be constructed of a 
series of levels of organization – from molecules to 
 macromolecular aggregates to organelles to enve-
lope systems (= cells). He concluded – 
 Within this reference frame of understanding, the cell 
ceases to occupy a central location as a fundamental unit 
of life. It appears, instead, as a special case among the 
single- and multiple-envelope systems that comprise all 
forms of life. (p. 122) 
 This perspective had a liberating effect for it 
demanded that we not constrain our view to the 
importance of cellular characters, but look “below” 
the cell at features that might be just as significant 
to an understanding of the common descent of 
protists. Ehret and McArdle (1974) then imagined 
the Paramecium cell to be constructed of levels, the 
simpler ones integrating to build more complex levels. 
In the context of the ciliate cortex, these levels 
can be imagined as macromolecule (i.e. tubulin ), 
 suborganelle or macromolecular aggregate (i.e., 
 microtubule ), unit organelle (i.e., kinetosome , 
 cilium , microtubular ribbon ), organellar complex 
(i.e., kinetid ), and organellar system (i.e., locomotory 
system or kinetome ) (Lynn, 1981; also see Chapter 
2 for definitions). 
 A number of scientists had imagined cells and 
organisms to be built in a series of increasingly com-
plex levels of organization and had concluded that 
this important property constrained morphological 
variation, especially at the lower levels of biological 
organization. In other words, if one constructs some-
thing of bricks of a certain shape that are assem-
bled in a precise sequence, changing the ultimate 
arrangement has less drastic consequences than 
changing the shape of each brick. Bronowski (1970) 
had termed this the principle of stratified stability : 
“the building up of stable configurations does have a 
direction, the more complex built on the next lower, 
which cannot be reversed in general” (pp. 242–243). 
Independently, Lynn (1976a, 1981) called it the 
 principle of structural conservatism : the conserva-
tion of structure through time is inversely related to 
the level of biological organization. Thus, if the cili-
ate cortex and infraciliature were conceived as being 
constructed of repeating and highly integrated units, 
then there should be strong selection on preserving 
this unit structure (i.e., the kinetid ) to construct the 
cortical system (Fig. 1.3). Lynn and Small (1981) 
then argued that this principle gave us an approach 
to examining the comparative ultrastructure of the 
ciliate cortex and to infer common descent: structur-
ally similar kinetids should be homologues, limited 
to vary by the “selective forces” of stratified stability 
or structural conservatism. 
 In the 21st century, this may all seem self-evident.
However, there was one major conceptual problem 
with it at the time – the idea of ‘ organic design ’. 
Pantin (1951, 1966) and Grimstone (1959) had 
argued that microtubules , basal bodies or kineto-
somes , and the cilium were of such low complex-
ity that they could conceivably have evolved many 
times, unlike “the more complex and improbable 
metazoan organs which, determined by a far more 
numerous set of genes, appear to have arisen only 
once” (p. 277, Grimstone, 1959), and “it seems 
highly improbable that the unique assemblage of 
genetic factors which ensures the development of a 
 pentadactyl limb would ever be selected independ-
ently on two separate occasions” (p. 144, Pantin, 
1951). Thus, from this view, similarities in kinetids 
would have arisen by a non-adaptive process, rather 
than as a result of natural selection . Instead, these 
structures were determined by thermodynamics 
and “by physical and spatial properties of matter 
rather than by functional needs … of a transcen-
dental rather than adaptive origin” (p. 4, Pantin, 
1966). Yet, a little over a decade later, the flagellum 
of Chlamydomonas was reported to have at least 
170 polypeptides (Huang, Piperno, & Luck, 1979) 
and the cilium of Paramecium to have at least 125 
polypeptides (Adoutte et al., 1980), and this picture 
has become even more complex in the intervening 
decades. Thus, these organelles are clearly not 
simple, but indeed are extremely highly ordered 
complexes. It is therefore reasonable to conclude 
that their structural complexity is as much a result 
of natural selection as the organs of metazoa or the 
 pentadactyl limb . 
 With this conceptual perspective, Small and 
Lynn (1981) applied structural conservatism to 
make sense of the diversity of ciliate kinetids . They 
also relied on the notion that somatic structures are 
more highly conserved than oral ones (Gerassimova 
& Seravin, 1976; Lynn, 1976a, 1976c). One reason 
lies in the development of somatic and oral regions. 
The duplication of somatic kinetids in ciliates 
usually occurs closely adjacent to pre-existing 
kinetids, called cytotaxis or structural guidance 
(Frankel, 1991), and this may place severe con-
straints on the variability of the components. On 
the other hand, the organellar complexes of the oral 
region are not as intimately linked to pre-existing 
organelles and also, as more complex structures, 
there is a higher potential for change, at least in 
size and shape. Another reason that oral structures 
Fig. 1.3. The hierarchical organization of the ciliate cortex. The fundamental component of the cortex is the dikinetid, 
an organellar complex here composed of seven unit organelles, which are the two kinetosomes, two cilia (not shown), 
transverse (T) and postciliary (Pc) microtubular ribbons, and the kinetodesmal fibril (Kd). In a patch of cortex, the 
microtubular ribbons and kinetodesmal fibrils of adjacent kinetids are closely interrelated. The interrelated kinetids 
comprise the components of the next higher level in the hierarchy, the organellar system called the kinetome. Two 
major cortical organellar systems are the somatic region or kinetome and the oral region, functioning in locomotion 
and feeding, respectively. (from Lynn & Small, 1981.)
1.3 The Age of Ultrastructure (1970–1990) 7
8 1. Introduction and Progress in the Last Half Century
are more variable is that even slight structural 
alterations, if they resulted in increased capture 
and ingestion rates, would directly affect growth 
and reproductive rates, enhancing relative fitness and 
fixation of new variants. Thus, Lynn (1979b) 
concluded “somatic over oral”, meaning that 
somatic structures have in general a “deeper” 
phylogenetic signal than oral ones. 
 The consistent application of these principles 
(i.e., structural conservatism and somatic over oral) 
resulted in the proposal of eight major classes by 
Small and Lynn (1981) (Table 1.3). During the Age 
of Ultrastructure , the classification was refined by 
Small and Lynn (1985) and Lynn and Small (1990), 
the latter revision beginning to consider the early 
results of molecular genetic research. Overall, 
 somatic kinetids were used to identify mono-
phyletic clades, called classes, and this approach 
often placed genera that had been assigned to dif-
ferent, older higher taxa together. The colpodeans 
provide a most dramatic example: Sorogena was 
a gymnostome ; Colpoda was a vestibuliferan ; 
Cyrtolophosis was a hymenostome ; and Bursaria
was a heterotrich (Fig. 1.4)! 
 Small and Lynn (1981, 1985) divided the phylum 
into three subphyla, based on ultrastructural features 
of the cortex: for the somatic cortex – the overlap-
ping postciliary microtubular ribbons – for the 
Subphylum Postciliodesmatophora (Gerassimova& Seravin, 1976; Seravin & Gerassimova, 1978); 
and for the oral cortex – the presence of transverse 
microtubular ribbons supporting the cytopharynx 
in the Subphylum Rhabdophora and the presence 
of postciliary microtubular ribbons supporting the 
cytopharynx in the Subphylum Cyrtophora (Small, 
1976) (Table 1.3). However, Huttenlauch and 
Bardele (1987) demonstrated in an ultrastructural 
study of oral development that the supposed oral 
transverse ribbons of the prostomate rhabdophoran 
Coleps were in fact postciliary microtubules that 
Table 1.3. Classifications systems proposed by Small and Lynn (1981, 1985).a
Small & Lynn (1981) Small & Lynn (1985)
Phylum Ciliophora Phylum Ciliophora
Postciliodesmatophora Postciliodesmatophora
KARYORELICTEA KARYORELICTEA
SPIROTRICHEA SPIROTRICHEA
Rhabdophora Heterotrichia
PROSTOMEA Stichotrichia
LITOSTOMEA Choreotrichia
Haptoria Rhabdophora
Vestibuliferia PROSTOMATEA
Cyrtophora LITOSTOMATEA
PHYLLOPHARYNGEA Haptoria
Phyllopharyngia Trichostomatia
Chonotrichia Cyrtophora
Suctoria PHYLLOPHARYNGEA
NASSOPHOREA Phyllopharyngia
Hypostomia Chonotrichia
Polyhymenophoria Suctoria
COLPODEA NASSOPHOREA
 OLIGOHYMENOPHOREA Nassophoria
Hymenostomia Hypotrichia
Peritrichia COLPODEA
Astomia OLIGOHYMENOPHOREA
Apostomia Hymenostomatia
 Peritrichia
 Astomatia
 Apostomatia
 Plagiopylia
a
 Classes are indicated in bold capital letters; subclasses, in italics.
became twisted during division morphogenesis, 
making them appear to be transverse microtubules. 
So, this rhabdophoran was really a cyrtophoran ! 
This undercut our confidence that these characters
had deep phylogenetic significance, and led Lynn 
and Corliss (1991) to abandon the subphyla, 
retaining only the eight classes of Small and 
Lynn. Later, de Puytorac et al. (1993) suggested 
three different subphyla, also based on signifi-
cant cortical ultrastructural features proposed by 
Fleury, Delgado, Iftode, and Adoutte (1992): the 
Subphylum Tubulicorticata – a microtubular cor-
tex; the Subphylum Filicorticata – a micro fibrillar 
cortex; and the Subphylum Epiplasmata – an epi-
plasmic cortex (Table 1.4). Fleury et al. (1992) 
had used molecular phylogenies derived from large 
subunit rRNA gene sequences to support these 
morphology-based subdivisions. Nevertheless, 
Lynn and Small (1997) argued that given the 
variability of cortical ultrastructures in ciliates 
it was extremely difficult to circumscribe the 
 limits of these subphyla. For example, virtually 
Fig. 1.4. Colpodeans and their somatic kinetids as a demonstration of the more conservative nature of the somatic 
kinetid and its “deeper” phylogenetic signal over the oral structures and general morphology of a group of ciliates. 
Sorogena was a gymnostome; Colpoda was a vestibuliferan; Cyrtolophosis was a hymenostome; and Bursaria was 
a spirotrich
1.3 The Age of Ultrastructure (1970–1990) 9
10 1. Introduction and Progress in the Last Half Century
all ciliates could be described as having a “corti-
cal cytoskeleton of superficial microtubules associ 
ated, or not, with cortical kinetosomes” – the major 
feature distinguishing ciliates in the Subphylum 
 Tubulicorticata (de Puytorac et al., 1993). 
 This reduced emphasis on oral structures as being 
of great phylogenetic significance extended to the 
homology of “ membranelles ” or oral polykinetids , 
used to establish the Classes Kinetofragminophora , 
 Oligohymenophora , and Polyhymenophora . De 
Puytorac and Grain (1976) and Grain (1984) had 
demonstrated the variety of “membranelles” or 
oral polykinetids in their reviews of the diversity 
of cortical ultrastructures of ciliates. This variety 
Table 1.4. A comparison of the macrosystems of the Phylum Ciliophora of de Puytorac (1994a) 
and the system proposed herein. Authorships for names will be found in Chapter 17.a
de Puytorac (1994a) Proposed system
Phylum Ciliophora Phylum Ciliophora
 Tubulicorticata Postciliodesmatophora
 POSTCILIODESMATOPHORA KARYORELICTEA
KARYORELICTEA HETEROTRICHEA
Trachelocercia Intramacronucleata
Loxodia SPIROTRICHEA
Protocruziidia Protocruziidia
Protoheterotrichia Phacodiniidia
HETEROTRICHEA Hypotrichia
Heterotrichia Oligotrichia
Clevelandellidia Choreotrichia
 SPIROTRICHA Stichotrichia
HYPOTRICHEA Licnophoria
Euplotia ARMOPHOREA
Oxytrichia LITOSTOMATEA
OLIGOTRICHEA Haptoria
Oligotrichia Trichostomatia
Strobilia PHYLLOPHARYNGEA
 TRANSVERSALA Cyrtophoria
COLPODEA Rhynchodia
Colpodia Chonotrichia
Bryometopia Suctoria
PLAGIOPYLEA NASSOPHOREA
 Filicorticata COLPODEA
LITOSTOMATEA PROSTOMATEA
VESTIBULIFEREA PLAGIOPYLEA
 Epiplasmata OLIGOHYMENOPHOREA
 CILIOSTOMATOPHORA Peniculia
PHYLLOPHARYNGEA Scuticociliatia
Cyrtophoria Hymenostomatia
Chonotrichia Apostomatia
Rhynchodia Peritrichia
Suctoria Astomatia
 MEMBRANELLOPHORA
NASSOPHOREA
Prostomatia
Nassulia
OLIGOHYMENOPHOREA
 Peniculia
 Scuticociliatia
 Peritrichia
 Hysterocinetia
 Astomatia
 Hymenostomatia
 Apostomatia
*Superclasses are indicated in capital letters; classes, in bold capital letters; subclasses, in italics.
lead to a proliferation of names to capture some 
of these differences. Oral polykinetids in kinetof-
ragminophorans could be pseudomembranelles , 
in oligohymenophorans could be membranoids or 
 membranelles , and in polyhymenophorans could 
be paramembranelles or heteromembranelles (see 
definitions in Chapter 2 ). This diversity suggested 
that these different complex oral structures were 
probably not homologues. In fact, what they 
undoubtedly illustrate are diverse solutions to the 
“problem” of filter feeding that had arisen through 
convergent evolution in a much larger number than 
three independent lineages or classes. Small and 
Lynn (1981, 1985) recognized these lineages as 
eight classes, established primarily on the basis of 
the ultrastructure of the somatic cortex, applying 
the principles of “structural conservatism” and 
“somatic over oral” (Fig. 1.4). 
 1.4 The Age of Refinement 
(1990–Present)
 Greenwood et al. (1991a) suggested that 1990 
might be designated as the beginning of the next 
age in ciliate systematics , the Age of Refinement , 
for it is in this period that tremendous advances 
have been made in confirming our basic notions 
derived from research on ciliate ultrastructure. As 
with the other ages, the technological roots of this 
age precede its formal beginning, and are based in 
the molecular phylogenetic work of Sogin’s lab 
on small subunit rRNA gene sequences (Elwood, 
Olsen, & Sogin, 1985; Lynn & Sogin, 1988) 
and Adoutte’s lab on large subunit rRNA gene 
sequences (Adoutte, Baroin, & Perasso, 1989; 
Baroin, Perasso, Qu, Brugerolle, Bachellerie, & 
Adoutte, 1988). Thus, it might also be called the 
 Age of Genetic Diversity , since the sequences of 
these highly conserved genes (see Chapter 16 ),
enabled us to test the structural conservatism of the 
ciliate somatic cortex , using the “molecular skel-
etons” of the ribosomal subunits – the small and 
large subunit rRNAs. 
 These early papers demonstrated tremendous 
genetic diversity within the phylum, a level 
of genetic diversity similar to differences among 
the “kingdoms” of multicellular organisms, like 
the plants , animals , and fungi . Further, the major 
clades established on the basis of ultrastructural 
research were generally confirmed, indicating that 
the somatic kinetid was a generally reliable feature 
to establish common descent (Lynn, 1991, 1996a; 
Lynn & Small, 1997). However, the molecular 
data suggested the need for further separation of 
clades, both at the “class” level and higher (Lynn, 
1996b; Lynn & Small). De Puytorac (1994a) 
had presaged this by elevating to class rank two 
groups that molecular genetic data confirmed to 
be distinct – the Class PLAGIOPYLEA and the 
Class HETEROTRICHEA, removing heterotrichs 
from the spirotrich assemblage (cf. Table 1.3, 
1.4). However, de Puytorac (1994a) elevated sev-
eral groups to class rank (e.g., HYPOTRICHEA , 
 OLIGOTRICHEA , VESTIBULIFEREA ) for which 
there is as yet no strong molecular genetic evidence 
(see Chapter 16 ). Two new clades differentiated by 
 small subunit rRNA gene sequences and now rec-
ognized as classes are the Class ARMOPHOREA 
(see Affa’a, Hickey, Strüder-Kypke, & Lynn, 2004; 
van Hoek, Akhmanova, Huynen, & Hackstein, 
2000a) and the Class PLAGIOPYLEA (see Embley 
& Finlay, 1994; Lynn & Strüder-Kypke, 2002) (Fig. 
1.5, Table 1.4). Lynn (2004) highlighted a diffi-
culty with each of these so-called “ riboclasses ”: the 
Class ARMOPHOREA associated genera, such as 
Metopus and Nyctotherus , whose somatic kinetids 
were dissimilar, while the Class PLAGIOPYLEA 
separated some genera, such as Plagiopyla and 
Trimyema , whose kinetids were quite similar to 
those of the Class OLIGOHYMENOPHOREA to 
which the plagiopyleans had been transferred as 
a subclass by Small and Lynn (1985) (Table 1.3). 
Thus, somatic kinetid structure seems not to be highly 
conserved in armophoreans and to be more highly 
conserved in some plagiopyleans! We have appar-
ently reached the limits of structural conservatism 
of the somatic cortex as a principle, and we can 
only say that these are the exceptions that prove 
the rule! 
 By the mid-1990s there was ample evidence 
from a variety of independent phylogenetic analy-
ses of both small subunit and large subunit rRNA 
gene sequences to demonstrate a fundamental 
bifurcation in the phylum (Baroin-Tourancheau, 
Tsao, Klobutcher, Pearlman, & Adoutte, 1995; 
Hammerschmidt, Schlegel, Lynn, Leipe, Sogin, 
& Raikov, 1996; Hirt et al., 1995) (Fig. 1.5). 
One branch, which separates the ciliates with 
 postciliodesmata sensu stricto , corresponds to 
1.4 The Age of Refinement (1990–Present) 11
Fig. 1.5. A molecular phylogeny of the Phylum Ciliophora based on small subunit rRNA gene sequences. Several 
representatives of each class have been chosen to demonstrate the genetic diversity within the phylum and the dis-
tinctness of the different clades that are considered to be of class rank in the classification proposed herein (see Table 
1.4) (see Chapter 16 for further discussion of molecular phylogenetics)
the Subphylum POSTCILIODESMATOPHORA , 
a concept proposed by Gerassimova and Seravin 
(1976). This subphylum now includes only the Classes 
 KARYORELICTEA and HETEROTRICHEA ; it 
excludes the spirotrich clade, which was included by 
Small and Lynn (1985) (cf. Tables 1.3, 1.4). While 
 karyorelicteans do not have dividing macronuclei, 
the heterotrichs do, apparently relying primarily 
on extramacronuclear microtubules for this proc-
ess (Diener, Burchill, & Burton, 1983; Jenkins, 
1973). Lynn (1996a) named the other branch, the 
Subphylum INTRAMACRONUCLEATA , because 
all ciliates in this clade have a dividing macronu-
cleus that relies predominantly on intramacronu-
clear microtubules for completion of division. The 
suggestion that macronuclear division has arisen 
separately twice during the evolution of ciliates is 
not unreasonable, considering that at least two kinds 
of nuclear division, using both extranuclear and 
intranuclear microtubules also occur in the dinoflag-
ellates (Perret, Albert, Bordes, & Soyer-Gobillard, 
1991), the sister clade to the ciliates (Leander & 
Keeling, 2003; Van de Peer, Van der Auwera, & De 
Wachter, 1996). 
 1.5 Major Differences in the New 
Scheme
 Corliss (1979) noted in his discussion of the major 
differences of schemes that an obvious trend has 
been the inflation of taxa as our discovery and 
understanding of diversity have changed from 
the 1880s until the present. As discussed above, 
approaches have been influenced both by techno-
logical advances – light microscopy , cytological 
staining, electron microscopy , molecular biology 
– and by new conceptual views. With respect to 
the latter, the emphasis on the somatic cortex by 
Small and Lynn (1981) caused a major revision 
in our understanding of relationships between the 
mid-1970s and the mid-1980s. Currently, there are 
two recent classification systems of ciliates seeking 
adherents; one proposed by de Puytorac (1994a) and 
his colleagues in the second volume of the Traité 
de Zoologie and the other proposed most recently 
by Lynn (2004) and presented in a slightly revised 
version herein (Table 1.4). Since various differences 
between these views have been discussed above, this 
section will serve to summarize these. 
 1. The subphyletic divisions in the two systems 
are different: three by de Puytorac (1994a) and 
two here (Table 1.4). Data on genetic diversity 
support a major division into two subphyla, the 
Subphylum POSTCILIODESMATOPHORA and 
the Subphylum INTRAMACRONUCLEATA . 
 2. De Puytorac (1994a) recognizes five super-
classes, one essentially equivalent to our 
Subphylum POSTCILIODESMATOPHORA , 
while we provide no such subdivisions (Table 
1.4). It is the case in molecular phylogenies 
that there is substructure within the Subphylum 
 INTRAMACRONUCLEATA . For example, 
six classes (i.e., PHYLLOPHARYNGEA , 
 NASSOPHOREA , COLPODEA , PLAGIO-
PYLEA , PROSTOMATEA , and OLIGOHYM-
ENOPHOREA ) are often consistently supported 
as a clade (Fig. 1.5). This grouping may repre-
sent a natural assemblage, and therefore repre-
sent a superclass assemblage. However, there 
is no obvious shared derived morphological 
feature uniting these taxa, and at this time we 
do not recognize it as a taxonomic category. 
 3. De Puytorac (1994a) recognizes 11 classes 
as does the system proposed here (Table 
1.4). However, the classes are different. De 
Puytorac (1994a) includes the prostomates 
in the Class NASSOPHOREA . Differences 
in the somatic kinetid (Eisler, 1989; Lynn, 
1991), stomatogenesis (Eisler; Huttenlauch & 
Bardele, 1987), and small subunit rRNA gene 
sequences (Stechmann, Schlegel, & Lynn, 
1998) between nassophoreans and prostomate-
ans argue against uniting them in the same class 
(Fig. 1.5). While both systems recognize the 
 spirotrichs as a larger assemblage, the eleva-
tion of the oligotrichs to class rank, equivalent 
to hypotrichs , is not justified by the molecular 
data, which suggest at least seven separate 
lineages in the Class SPIROTRICHEA , here 
recognized as subclasses (Strüder-Kypke & 
Lynn, 2003). 
 Finally, we cannot agree with de Puytorac 
(1994a) that elevation of the vestibuliferians to 
class rank is warranted. We prefer to refer to this 
clade by the Bütschlian moniker, Trichostomatia 
(Table 1.4). The trichostomatians in this sense and 
the haptorians share virtually identical somatic 
kinetid patterns (Lynn, 1981, 1991). This varies only
in the entodiniomorphids where Lynn (1991) has 
1.5 Major Differences in the New Scheme 13
14 1. Introduction and Progress in the Last Half Century
interpreted the appearance of a transient micro-
tubule during kinetid replication (see Furness 
& Butler, 1986) to be the homologue of the 
T2 transverse microtubular ribbon of litostomes . 
Moreover, extensive analyses of litostome small 
subunit rRNA gene sequences consistently group 
the haptorians and trichostomes (Wright & 
Lynn, 1997b; Strüder-Kypke, Wright, Foissner, 
Chatzinotas, & Lynn, 2006). 
 De Puytorac (1994a) elevated a considerable 
number of taxa to subclass and ordinal ranks, 
totalling 25 subclasses and 70 orders. Comparison 
with the scheme presented here will demonstrate 
considerable agreement in the basic groups or 
clades, despite possible differences in rank (Table 
1.4 and the original references). While Small and 
Lynn (1981, 1985) established 15 subclasses and 
48 orders, our revised scheme has 19 subclasses 
and 59 orders. Many of these changes have been 
influenced by genetic data obtained in the last 
few years, and these are discussed both by Lynn 
(1996b,2004) and in the chapters devoted to each 
class (see Chapters 5–15 ).
 1.6 Guide to Remaining Chapters 
 This book takes its basic form from the 3rd edi-
tion of “The Ciliated Protozoa” by Corliss (1979). 
Following this Introduction, we have revised 
Chapter 2, but used Corliss as the solid grounding 
for the glossary of terms. Whenever appropriate, 
cross-reference has been made to terms, and the 
plural of non-English words has been included. 
Figures are explicitly referred to by number so that 
it should be easy to find illustrative support for 
many of the definitions. 
 Chapter 3 provides a discussion of the approach to 
constructing our macrosystem. The important charac-
ters used to establish different ranks in the hierarchy 
are described and justification is provided for their 
use. Some of this is a repetition of the material in this 
chapter, but in a different context. 
 Chapters 4 through 15 are structured along 
the lines of the Traité de Zoologie edited by de 
Puytorac (1994a). The phylum (Chapter 4) and 
each class (Chapters 5–15) are treated under the 
following topics: overview of the group; taxonomic 
structure of the group and its diversity; life history 
and ecology, including symbioses; somatic struc-
tures, cortical and cytoplasmic; oral structures; 
division and morphogenesis; sexuality and life 
cycle, including nuclear features; and other, a final 
section that may include aspects of the applied 
relevance of a group. 
 Chapter 16, a preamble to Chapter 17, deals 
particularly with important research papers on the 
genetic diversity of the phylum, especially as these 
results impact on refining the relationships of taxa. 
There is also some discussion of character evolu-
tion within the phylum, particularly as it relates to 
the classes and subphyla, and as revealed by the 
topologies of gene trees. 
 Chapter 17 is the taxonomic chapter, again 
relying heavily on Corliss (1979) for the basic 
characterization of groups from the family level 
and higher. As in Corliss, genera are assigned to 
families, but there is rarely any discussion of these 
assignments. Valid genera primarily follow the rec-
ommendations of Aescht (2001), whose important 
work should be referred to for the detailed nomen-
clatural background to problematic names. While 
not considered valid by the International Code of 
Zoological Nomenclature, nomina nuda have been 
included and are clearly indicated as such. 
 The References section includes an extensive 
literature cited section. In this, we have been con-
scious of including reference to the classic litera-
ture as both Corliss (1961) and Corliss (1979) are 
now out of print. However, we have also included, 
as appropriate, citation to important works bearing 
on the topics of Chapters 4 through Chapters 16. 
We do regret that we have often been unable to 
include all relevant literature on a topic, and trust 
that expert readers will understand and agree with 
our selection of references.