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

Abstract

Complex behavior is associated with animals with 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 behavioral 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 behaviors reported for a singly nucleated cell [16, 17]. These results attracted widespread interest [18, 19] and exert continuing fascination [7, 20, 21, 22] but were discredited during the behaviorist 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 behaviors 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 behavioral complexity may have had an evolutionary advantage in protist ecosystems, and the ciliate cortex may have provided mechanisms for implementing such behavior prior to the emergence of multicellularity. Our work resurrects Jennings- pioneering insights and adds to the list of exceptional features, including regeneration [24], genome rearrangement [25], codon reassignment [26], and cortical inheritance [27], for which the ciliate clade is renowned.