A Complex Hierarchy of Avoidance Behaviors in a Single-Cell Eukaryote

Abstract

Complex behaviour is associated with animals having nervous systems but decision making and learning also occur in non-neural organisms [1], including singly-nucleated cells [2, 3, 4, 5] and multi-nucleate synctia [6, 7, 8]. Ciliates are single-cell eukaryotes, widely dispersed in aquatic habitats [9], with an extensive behavioural repertoire [10, 11, 12, 13]. In 1906, Herbert Spencer Jennings [14, 15] described in the sessile ciliate Stentor roeseli a hierarchy of responses to repeated stimulation, which are among the most complex behaviours reported for a singlynucleated cell [16, 17]. These results attracted widespread interest [18, 19] and exert continuing fascination [7, 20, 21, 22] but were discredited during the behaviourist orthodoxy by claims of non-reproducibility [23]. These claims were based on experiments with the motile ciliate Stentor coeruleus. We acquired and maintained the correct organism in laboratory culture and used micromanipulation and video microscopy to confirm Jennings' observations. Despite significant individual variation, not addressed by Jennings, S. roeseli exhibits avoidance behaviours in a characteristic hierarchy of bending, ciliary alteration, contractions and detachment, which is distinct from habituation or conditioning. Remarkably, the choice of contraction versus detachment is consistent with a fair coin toss. Such behavioural complexity may have had an evolutionary advantage in protist ecosystems and the ciliate cortex may have provided mechanisms for implement-⇤

The Single-Celled Ancestors of Animals: A History of Hypotheses

“…While the ciliate theory has now been dismissed as inconsistent with the modern eukaryotic phylogeny, it serves as a reminder of how much complexity -in morphology, patterning, and behavior -can be achieved by a single cell (Marshall 2020). The animal-like behaviors of ciliates, which fascinated scientists and philosophers at the turn of the 20 th century (Schloegel and Schmidgen 2002), are currently undergoing a renaissance as a research topic (Coyle et al 2019;Dexter, Prabakaran, and Gunawardena 2019;Mathijssen et al 2019;Wan and Jékely 2020), as are the mechanisms of their patterning and morphogenesis (Marshall 2020). Properly understood as an independent and unique evolutionary experiment in achieving levels of size and morphological complexity that rival those of small animals, ciliates remain as fascinating as ever.…”

A unicellular walker controlled by a microtubule-based finite state machine

“…Traditionally, studies of computational processes performed by cells have tended to focused on combinatorial logic, where the output of a computational process depends only on the current input, performed by networks of molecules in bacterial cells 25,32–34 . We have focused on sequential logic, where outputs depend on the system state as well, an equally important aspect of the theory of computation with notable yet less developed representation in studies of cellular and sub-cellular dynamics 16,20,79 . Behavior of eukaryotes has frequently been observed to involve stereotyped transitions between dynamical states, and our results suggest that automata theory, which includes finite state machine models and necessarily involves sequential logic, may be particularly well-suited to studying the behavior of eukaryotic cells.…”

Mirror Symmetry of Life

“…Both ciliates, motile spermatozoids and stationary epithelial cells readily change the direction of cilia movement either to navigate or alter the current of surrounding fluids [34]. Interestingly, the latter has been employed by unicellular Stentor rosei, to avoid, in quite deliberate and calculated manner, the irritating particles experimentally added to the medium [35]. The cell, however, is not always in full control over the cilia beating.…”