Multiple independent losses of cell mouth in phylogenetically distant endosymbiotic lineages of oligohymenophorean ciliates: A lesson from Clausilocola

Abstract

The cell mouth is a property of the vast majority of free-living and endosymbiotic/epibiotic ciliates of the class Oligohymenophorea. Cytostome, however, naturally absents in the whole endosymbiotic subclass Astomatia and was naturally or experimentally lost in a few members of the subclass Hymenostomatia. This poses a question of how homoplastic might be the lack of oral structures in the oligohymenophorean evolution. To address this question, we used two mitochondrial genes, five nuclear markers, and detailed morphological data from an enigmatic mouthless ciliate, Clausilocola apostropha, which we re-discovered after more than half of a century. According to the present phylogenetic analyses, astomy evolved at least three times independently and in different time frames of the oligohymenophorean phylogeny, ranging from the Paleozoic to the Cenozoic period. Mouthless endosymbionts inhabiting mollusks (represented by Clausilocola), planarians (Haptophrya), and annelids ('core' astomes) never clustered together. Haptophrya grouped with the scuticociliate genus Conchophthirus, 'core' astomes were placed in a sister position to the scuticociliate orders Philasterida and Pleuronematida, and Clausilocola was robustly nested within the hymenostome family Tetrahymenidae. The tetrahymenid origin of Clausilocola is further corroborated by the existence of mouthless Tetrahymena mutants and the huge phenotypic plasticity in the cytostome size in tetrahymenids.

Keywords: Astomatia; Clausilocola; Haptophrya; Hymenostomatia; Molecular clock; Multigene phylogeny.