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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.
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