The All-Data-Based Evolutionary Hypothesis of Ciliated Protists with a Revised Classification of the Phylum Ciliophora (Eukaryota, Alveolata)

Abstract

The phylum Ciliophora plays important roles in a wide range of biological studies. However, the evolutionary relationships of many groups remain unclear due to a lack of sufficient molecular data. In this study, molecular dataset was expanded with representatives from 55 orders and all major lineages. The main findings are: (1) 14 classes were recovered including one new class, Protocruziea n. cl.; (2) in addition to the two main branches, Postciliodesmatophora and Intramacronucleata, a third branch, the Mesodiniea, is identified as being basal to the other two subphyla; (3) the newly defined order Discocephalida is revealed to be a sister clade to the euplotids, strongly suggesting the separation of discocephalids from the hypotrichs; (4) the separation of mobilids from the peritrichs is not supported; (5) Loxocephalida is basal to the main scuticociliate assemblage, whereas the thigmotrichs are placed within the order Pleuronematida; (6) the monophyly of classes Phyllopharyngea, Karyorelictea, Armophorea, Prostomatea, Plagiopylea, Colpodea and Heterotrichea are confirmed; (7) ambiguous genera Askenasia, CyclotrichiumParaspathidium and Plagiocampa show close affiliation to the well known plagiopyleans; (8) validity of the subclass Rhynchostomatia is supported, and (9) the systematic positions of Halteriida and Linconophoria remain unresolved and are thus regarded as incertae sedis within Spirotrichea.

Figure 1

Phylogenetic tree (A) and classification (B) of the phylum Ciliophora. (A) Maximum likelihood (ML) tree reconstructed using 152 ciliates and concatenated genes (the SSU rDNA sequence is available for all the taxa whereas the 5.8S rDNA, LSU rDNA and alpha-tubulin gene sequences are available for only a subset of these taxa, Additional file 1: Table S2). Numbers at nodes represent the bootstrap values of maximum likelihood (ML) out of 1000 replicates and the posterior probability of Bayesian analysis (BI). Only bootstraps above 50% are shown. Fully supported (100%/1.00) branches are marked with solid circles. Asterisk (*) indicates disagreement between ML and BI analyses. The three main branches of ciliates are in bold. The scale bar corresponds to 10 substitutions per 100 nucleotide positions. (B) Classification scheme of phylum Ciliophora according to Lynn and Adl et al..

Figure 2

Maximum likelihood (ML) trees of the phylum Ciliophora based on the SSU rDNA ((A), 152 taxa) and LSU rDNA ((B), 118 taxa). Numbers at nodes represent the bootstrap values of maximum likelihood (ML) out of 1000 replicates and the posterior probability of Bayesian analysis (BI). Only bootstraps above 50% are shown. Fully supported (100%/1.00) branches are marked with solid circles. Asterisk (*) indicates disagreement between ML and BI analyses. The three main branches of ciliates are in bold. The scale bar corresponds to 10 substitutions per 100 nucleotide positions.

Figure 3. Systematic scheme for the phylum Ciliophora suggested by the present and previous works.

The order Discocephalida was established by Wicklow, and revised to contain two suborders Discocephalina and Pseudoamphisiellina by Miao et al.. The order Discotrichida was established in Fan et al.. The order Loxocephalida was originally proposed by Jankowski and was confirmed by Li et al., Gao et al., Zhang et al., etc. The order Lynnellida was established by Liu et al.. The class Cariacotrichea was established by Orsi et al.. The order Mesodiniida was resurrected and the class Mesodiniea was established by Chen et al.. The classes Protocruziea and Licnophoriea are defined in the present study.

Figure 4. Hypothetical evolution of ciliated protozoa based on both morphological and molecular data to show the relationship and the positions of the taxa at order level.

(1–8), (14–17), (21), (24–26), (29–32), (36), (38), (39), (42–54), (58), (61), and (63–78) are from the present authors. (9) is from Bardele et al.. (10–13), (19), (22–23), (27–28), (33–35), (37), (40–41), (55–56), (59), and (62) are from Corliss. (18) is from Foissner et al., (20) is from Foissner et al.. (57) is from Dehority. (60) is from Orsi et al..