New considerations on the phylogeny of Sessilida (Protista: Ciliophora: Peritrichia) based on multiple-gene information, with emphasis on colonial taxa

Abstract

The subclass Peritrichia, containing two orders Sessilida and Mobilida, is a major group of ciliates with worldwide distribution and high species diversity. Several studies have investigated the phylogeny of peritrichs; however, the evolutionary relationships and classification of some families and genera within the Sessilida remain unclear. In the present study, we isolated and identified 22 peritrich populations representing four families and six genera and obtained 64 rDNA sequences to perform phylogenetic analyses and assess their systematic relationships. Ancestral character reconstruction was also carried out to infer evolutionary routes within the Sessilida. The results indicate: (1) family Vaginicolidae is monophyletic and acquisition of the typical peritrich lorica represents a single evolutionary divergence; (2) core epistylidids evolved from a Zoothamnium-like ancestor and experienced spasmoneme loss during evolution; (3) Campanella clusters with species in the basal clade and shows stable morphological differences with other epistylidids, supporting its assignment to a separate family; (4) the structure of the peristomial lip may be a genus-level character rather than a diagnostic character for discriminating Epistylididae and Operculariidae, thus a redefinition of Operculariidae should be carried out when more species have been investigated; (5) some characters, such as lifestyle (solitary or colonial), spasmoneme and living habit (sessile or free-swimming), evolved repeatedly among sessilids indicating that species with non-contractile stalks or that are free-swimming have multiple evolutionary routes and might derive from any sessilid lineage without a lorica. The close phylogenetic relationships of some morphologically distinct sessilids imply that the diagnoses of some genera and families should be improved.

Keywords: Ancestral state reconstruction; Ciliates; Morphology; Peritrichs; Phylogenetic analyses.

Fig. 1

Phylogenetic tree based on SSU rDNA sequences. Sequences from the present study are in red. Numbers given at nodes of branches are Ultrafast bootstrap value (%) for ML analysis and posterior probabilities for BI analysis. The insert figure in the top left corner shows the major clades of sessilids. The scale bar corresponds to five substitutions per 100 nucleotide positions. The question marks in red denote the validity and/or the assignment of the sequence need to be verified

Fig. 2

Phylogenetic tree based on ITS1-5.8 rDNA-ITS2 sequences. Sequences from the present study are in red. Numbers given at nodes of branches are Ultrafast bootstrap value (%) for ML analysis and posterior probabilities for BI analysis. The insert figure in the top left corner shows the major clades of sessilids. The scale bar corresponds to 20 substitutions per 100 nucleotide positions. The question marks in red denote that the validity and/or the assignment of the sequence need to be verified

Fig. 3

Phylogenetic tree based on LSU rDNA sequences. Sequences from the present study are in red. Numbers given at nodes of branches are Ultrafast bootstrap value (%) for ML analysis and posterior probabilities for BI analysis. The insert figure in the top left corner shows the major clades of sessilids. The scale bar corresponds to five substitutions per 100 nucleotide positions. The question marks in red denote that the validity and/or the assignment of the sequence need to be verified

Fig. 4

Phylogenetic tree based on concatenated sequences. Sequences from the present study are in red. Numbers given at nodes of branches are Ultrafast bootstrap value (%) for ML analysis and posterior probabilities for BI analysis. The insert figure in the top left corner shows the major clades of sessilids. The scale bar corresponds to five substitutions per 100 nucleotide positions. The question marks in red denote that the validity and/or the assignment of the sequence need to be verified

Fig. 5

Ancestral reconstruction for sessilid species based on the SSU rDNA ML tree. Ancestral lifestyle (solitary or colonial) (A), spasmoneme (present or absent) (B), living habit (sessile or free-swimming) (C), and lorica (present or absent) (D). Pie charts show the marginal probability of the ancestral state at each node. The compressed visualizations are shown in the bottom panel