On the Heterochrony and Evolution of Oral Structures in Phyllopharyngean Ciliates (Protista: Ciliophora)

ABSTRACT Heterochronic shifts in developmental sequences of unicellular organisms are rarely considered as mechanisms behind their morphological evolution. Among eukaryotic microbes, ciliates represent a key model group, exhibiting diverse morphologies and developmental trajectories. To explore the morphological evolution of oral structures in connection with modifications in the relative timing of developmental events, we focused on the orally diverse ciliate class Phyllopharyngea. Two of its subclasses (Rhynchodia and Cyrtophoria) follow the “standard” ontogenetic sequence (stomatogenesis–karyokinesis–cytokinesis), while two subclasses (Suctoria and Chonotrichia) have convergently deviated from the ancestral mode regarding the timing of stomatogenesis. Daughter cells of suctorians and chonotrichs bud from their mother cells, causing juveniles (so‐called swarmers) to differ strikingly from adults. The transformation of free‐swimming swarmers into sessile adults represents a newly inserted step in the ontogeny of suctorians and chonotrichs. The elongated juvenile phase enabled further extrapolation beyond the terminal morphology of their ancestors (i.e., peramorphosis), allowing a transition from a mobile to a sessile lifestyle in the adult stage. On the other hand, the interrupted and/or postponed stomatogenesis is a neotenic shift (i.e., paedomorphosis). Thus, the adult morphologies of suctorians and chonotrichs are the result of mosaic heterochrony, in which various traits are affected by different types of heterochronic processes. Modifications in the rank order of developmental events and the relative elongation of the ontogenetic timeline are correlated with shifts in the feeding strategies of suctorians and chonotrichs. This review also compiles current knowledge about the morphological evolution of oral structures in the four phyllopharyngean subclasses.