The following is a précis of the article:Lynn, D.H. and E.B. Small. 1997. A Revised Classification of the Phylum Ciliophora Doflein, 1901. Rev. Soc. Mex. Hist. Nat. 47: 65-78.
Introduction
Lynn (unpubl.) has revised the classification of the Phylum Ciliophora Doflein, 1901. His latest revision is the culmination of several years of research by Lynn and various colleagues (see, Lynn and Corliss (1991), Lynn and Small (1997, 2002), Small and Lynn (1981, 1985)).
Small and Lynn (1981) placed greater weight on structural conservatism of the kinetidal components in the somatic cortex. The stability of somatic kinetid patterns, reviewed by Lynn (1981, 1991), was used to recognise major clades within the phylum. Small and Lynn (1981) also considered the importance that division morphogenesis played in recognising diversity within major ciliate clades. They proposed that there was more stability in the dikinetid structures of the oral region than the polykinetid structures. Moreover, Small and Lynn (1981) favoured Raikov’s hypothesis (Raikov, 1969), which explained the evolution of nuclear dualism within the phylum.
How many Subphyla?
Small and Lynn (1985) proposed three subphyla and eleven classes. Three of the classes (LITOSTOMATEA, NASSOPHOREA, and COLPODEA) and ten of the orders were new. De Puytorac et al. (1974) have published two revisions of their classification: (1) de Puytorac et al. (1987) and (2) de Puytorac et al. (1993). The early dichotomy between the French and the Small and Lynn classifications is based upon, in part, Small and Lynn’s strong emphasis of somatic kinetid ultrastructure. Lynn and collaborators have recently used the analysis of gene sequences, particularly the small subunit ribosomal RNA (SSrRNA). There is now ample evidence from a variety of independent phylogenetic analyses of rRNA genes that there is a fundamental bifurcation in the ciliates (Fig. 1).
This bifurcation separates the ciliates with postciliodesmata from all other ciliates. This branch corresponds to the subphylum POSTCILIODESMATOPHORA Gerassimova & Seravin, 1976 sensu Small & Lynn, 1985 (Lynn, 1996). In the current classification this subphylum includes the classes KARYORELICTEA and HETEROTRICHEA (Lynn, unpubl.). Karyorelictean ciliates do not have dividing macronuclei (Raikov, 1969) whereas heterotrichs and all other ciliates do. Heterotrichs, however, divide their macronucleus using extramacronuclear microtubules while all other ciliates seemingly divide the macronucleus by intramacronuclear microtubules (Lynn, 1996). Lynn (1996) used the character of intramacronuclear microtubules to define the subphylum INTRAMACRONUCLEATA Lynn, 1996 (Lynn, unpubl.).
How many Superclasses?
Small and Lynn (1981, 1985) and Lynn (Lynn, unpubl.) did not establish superclasses. However, de Puytorac et al. (1994) recognized five superclasses: POSTCILIODESMATOPHORA Gerassimova & Seravin 1976, SPIROTRICHA Bütschli, 1889, and TRANSVERSALA de Puytorac et al., 1993 in the subphylum TUBULICORTICATA; and the superclasses CILIOSTOMATOPHORA de Puytorac et al., 1993 and MEMBRANELLOPHORA Jankowski, 1975 in the subphylum EPIPLASMATA (de Puytorac, 1994).
The superclass POSTCILIODESMATOPHORA sensu de Puytorac et al., 1993 includes essentially the same taxa as my current system. However, on the basis of SSrRNA gene sequences (Hammerschmidt et al., 1996), I have removed the monotypic subclass Protocruziidia to the class SPIROTRICHEA. The superclass SPIROTRICHA sensu de Puytorac et al., 1993 includes the same taxa as my revised class SPIROTRICHEA. The superclass TRANSVERSALA sensu de Puytorac et al., 1993 unites two classes: the PLAGIOPYLEA and the COLPODEA. De Puytorac et al. (1993) characterized this superclass as having transverse microtubular ribbons that are always longitudinally oriented along the length of kineties (de Puytorac et al., 1993). This ignores, however, the very different origins within the kinetid of the transverse microtubular ribbons in the two classes. Furthermore, it simplifies the complexity of interactions among the sets of transverse microtubular ribbons in the cortex of members of the COLPODEA (Lynn, 1976), and it ignores the more or less longitudinal orientation of the T1 set of transverse microtubules of the members of the LITOSTOMATEA (Lynn, 1991). Finally, SSrRNA gene sequences strongly suggest that members of the classes COLPODEA and PLAGIOPYLEA (although being members of the same major clade) are not sister taxa (Fig. 1).
The superclass CILIOSTOMATOPHORA sensu de Puytorac et al., 1993 only includes the class PHYLLOPHARYNGEA, which is composed of the same taxa in the classification of de Puytorac et al. (1993) and my revised classification (Lynn, unpubl.). Finally, the superclass MEMBRANELLOPHORA sensu de Puytorac et al., 1993 includes the classes NASSOPHOREA and OLIGOHYMENOPHOREA. This superclass includes ciliates with oral structures that include adoral polykinetids that can be as few as three in number and a paroral on the right side, which can be circular when the oral region is apical. This last character of the class is necessary because de Puytorac et al. (1993) included the prostomate ciliates as a subclass within the class NASSOPHOREA (de Puytorac, 1994). Phylogenies derived from SSrRNA gene sequences clearly demonstrate a relationship between the classes NASSOPHOREA and OLIGOHYMENOPHOREA (Fig. 1). However, they are rarely sister taxa, and typically members of the class PLAGIOPYLEA are more closely related to the oligohymenophoreans than are the nassophoreans. Thus, I am not convinced that these superclasses are meaningful conceptions.
I do not believe that it is necessary to establish superclasses within the subphylum POSTCILIODESMATOPHORA. Nevertheless, the phylogenies derived from the distance analysis of SSrRNA gene sequences clearly demonstrate substructure within the subphylum INTRAMACRONUCLEATA (Fig. 1). Often, the classes LITOSTOMATEA, SPIROTRICHEA, and ARMOPHOREA are in one clade (Fig. 1) while the classes PHYLLOPHARYNGEA, NASSOPHOREA, COLPODEA, PROSTOMATEA, PLAGIOPYLEA, and OLIGOHYMENOPHOREA are in the other clade (Fig. 1). However, this topology is not supported by parsimony analysis (Wright et al., 1997). Thus, it is premature at this time to recognize any superclasses within the subphylum INTRAMACRONUCLEATA.
How many Classes?
The classification of Small and Lynn (1981, 1985) increased the number of classes of ciliates from the three proposed by de Puytorac et al. (1974) to eight. De Puytorac et al. (1993) increased this number to eleven by recognizing the heterotrichs, oligotrichs, plagiopylians, and vestibuliferians as classes and submerging the prostomates within the class NASSOPHOREA (de Puytorac, 1994). Differences in the somatic kinetid pattern (Lynn, 1981, 1991), stomatogenesis (Eisler, 1989), and SSrRNA gene sequences (Stechmann et al., 1997) between nassophoreans and prostomateans argue against uniting them within the same class. Thus, I cannot accept reducing the rank of the class PROSTOMATEA sensu Small and Lynn, 1985.
I concur with de Puytorac et al. (1993) that the heterotrichs should be elevated to class rank. The sequence divergence between heterotrichs and spirotrichs is very great (Fig. 1), and their modes of stomatogenesis are very different. Current research in my laboratory on the oligotrichs and choreotrichs place the two within the class SPIROTRICHEA.
Small and Lynn (1985) recognized the subclass Plagiopylia as a new one within the class OLIGOHYMENOPHOREA. I agree that the plagiopylians should be elevated to class rank as suggested by de Puytorac et al. (1993). However, a careful analysis of the stomatogenesis of plagiopyleans may reveal oligohymenophorean affinities that could argue for placing them again as a subclass within the class OLIGOHYMENOPHOREA.
I cannot agree with de Puytorac et al. (1993) that elevation of the vestibuliferians to class rank is warranted. I prefer to refer to this clade by the old Bütschlian moniker, Trichostomatia. The trichostomatians and haptorians share virtually identical somatic kinetid patterns (Lynn 1981, 1991). This varies only slightly in the entodiniomorphids for which Lynn (1991) has interpreted the appearance of a transient microtubule during somatic kinetid replication to be the homologue of the T2 transverse microtubular ribbon of other litostomes. Moreover, extensive analysis of litostome SSrRNA gene sequences consistently group the haptorians and trichostomes whose genetic divergence, at least on this marker, is significantly less than genetic divergences within the classes SPIROTRICHEA and OLIGOHYMENOPHOREA (Fig. 1).
Subclasses and Orders
De Puytorac et al. (1993) have elevated a number of taxa to subclass and ordinal rank. Their scheme currently has 25 subclasses and 70 orders (de Puytorac, 1994). Comparison of my scheme (Lynn, unpubl.) with that of de Puytorac et al. (de Puytorac, 1994) demonstrates considerable agreement in the basic clades despite differences in rank.
Conclusions
Ciliatologists in France and North American are converging on similar schemes of classification for this important phylum of protists. Major differences between schemes rest mainly at the levels of higher taxonomic ranks (subphyla and superclasses) and lower taxonomic ranks (orders). As additional data are obtained, I am confident that a global consensus will emerge.