New contributions to the phylogeny of the ciliate class Heterotrichea (Protista, Ciliophora): analyses at family-genus level and new evolutionary hypotheses

Abstract

Heterotrichous ciliates play an important role in aquatic ecosystem energy flow processes and many are model organisms for research in cytology, regenerative biology, and toxicology. In the present study, we combine both morphological and molecular data to infer phylogenetic relationships at family-genus level and propose new evolutionary hypotheses for the class Heterotrichea. The main results include: (1) 96 new ribosomal DNA sequences from 36 populations, representing eight families and 13 genera, including three poorly annotated genera, Folliculinopsis, Ampullofolliculina and Linostomella; (2) the earliest-branching families are Spirostomidae in single-gene trees and Peritromidae in the concatenated tree, but the family Peritromidae probably represents the basal lineage based on its possession of many "primitive" morphological characters; (3) some findings in molecular trees are not supported by morphological evidence, such as the family Blepharismidae is one of the most recent branches and the relationship between Fabreidae and Folliculinidae is very close; (4) the systematic positions of Condylostomatidae, Climacostomidae, and Gruberiidae remain uncertain based either on morphological or molecular data; and (5) the monophyly of each genus included in the present study is supported by the molecular phylogenetic trees, except for Blepharisma in the SSU rDNA tree and Folliculina in the ITS1-5.8S-ITS2 tree.

Taxonomy and SSU rDNA-Based Phylogeny of Two Heterotrich Ciliates (Ciliophora, Heterotrichea) Collected From Subtropical Wetlands of China, Including the Description of a New Species, Linostomella pseudovorticella n. sp.

“…Stentoridae, Blepharismidae, Fabreidae, Folliculinidae, Maristentoridae, and Gruberiidae are closely related in our SSU rDNA tree, which is consistent with previous analyses ( Shazib et al, 2014 , 2016 , 2019 ; Fernandes et al, 2016 ; Chen et al, 2017 , 2018 ; Luo et al, 2019 ; Chi et al, 2020 , 2021 ). The monophyletic family Condylostomatidae is divided into two subclades, Condylostomides + Linostomella (freshwater habitat) and Chattonidium + Condylostentor + Condylostoma (marine water habitat).…”

“…The monophyletic family Condylostomatidae is divided into two subclades, Condylostomides + Linostomella (freshwater habitat) and Chattonidium + Condylostentor + Condylostoma (marine water habitat). The genus Linostomella is monophyletic and is closely related with Condylostomides, which is consistent with previous studies (Rossi et al, 2016;Chi et al, 2020Chi et al, , 2021. The findings of the present study support the assertion that habitat preference is a phylogenetically informative character among these taxa (Chi et al, 2021).…”

“…Phylogenetic relationships among families in the class Heterotrichea remain unresolved, as previous studies have concluded that either Peritromidae or Spirostomidae could be the basal group in SSU rDNA trees ( Shazib et al, 2014 ; Fernandes et al, 2016 ; Yan et al, 2016 ; Chen et al, 2017 ; Chi et al, 2021 ). In the present study, Spirostomidae branches before Peritromidae, which is supported by the morphological data and is consistent with the findings of Fernandes et al (2016) and Chi et al (2020) .…”

“…Although 16 nominal species of Peritromus have been reported, detailed morphological information and molecular data are available for only two, i.e., Peritromus faurei Kahl, 1932 andPeritromus kahli Villeneuve-Brachon, 1940 (Song and Wilbert, 1997;Rosati et al, 2004;Miao et al, 2009). It has been hypothesized that Peritromidae (Peritromus) is the ancestral taxon of Heterotrichea (Chi et al, 2021), although this finding is inconsistent with most other molecular phylogenetic trees (Yan et al, 2015;Fernandes et al, 2016;Chen et al, 2017). Therefore, the phylogenetic position of Peritromidae remains ambiguous.…”

“…The Heterotrichea contains 10 families and about 60 genera, several of which are well-known, e.g., Stentor Oken, 1815 and Spirostomum Ehrenberg, 1834. In contrast, some genera are not familiar because they have few species and/or they are difficult to collect, e.g., Linostomella Aescht in Foissner et al, 1999 , Chattonidium Villeneuve, 1937, and Peritromus Stein, 1863 ( Rosati et al, 2004 ; Modeo et al, 2006 ; Chi et al, 2020 , 2021 ).…”