What is it like to be a choanoflagellate? Sensation, processing and behavior in the closest unicellular relatives of animals

Abstract

All animals evolved from a single lineage of unicellular precursors more than 600 million years ago. Thus, the biological and genetic foundations for animal sensation, cognition and behavior must necessarily have arisen by modifications of pre-existing features in their unicellular ancestors. Given that the single-celled ancestors of the animal kingdom are extinct, the only way to reconstruct how these features evolved is by comparing the biology and genomic content of extant animals to their closest living relatives. Here, we reconstruct the Umwelt (the subjective, perceptive world) inhabited by choanoflagellates, a group of unicellular (or facultatively multicellular) aquatic microeukaryotes that are the closest living relatives of animals. Although behavioral research on choanoflagellates remains patchy, existing evidence shows that they are capable of chemosensation, photosensation and mechanosensation. These processes often involve specialized sensorimotor cellular appendages (cilia, microvilli, and/or filopodia) that resemble those that underlie perception in most animal sensory cells. Furthermore, comparative genomics predicts an extensive “sensory molecular toolkit” in choanoflagellates, which both provides a potential basis for known behaviors and suggests the existence of a largely undescribed behavioral complexity that presents exciting avenues for future research. Finally, we discuss how facultative multicellularity in choanoflagellates might help us understand how evolution displaced the locus of decision-making from a single cell to a collective, and how a new space of behavioral complexity might have become accessible in the process.

Behavioral plasticity in aneural organisms.

“…There is extensive molecular similarity in proteins present in vesicles storing peptides (and neurotransmitters) between those in animal neurons and in unicellular choanoflagellates. Some choanoflagellates form colonies in which communication between adjacent cells may depend on the release of peptides to the surrounding environment, rather than through specific contact sites, such as in synapses (Ros-Rocher & Brunet, 2023). The implication is that the evolution of these proteins sets the conditions for the emergence of neurons in the earliest animals.…”

Leveraging Cancer Phenotypic Plasticity for Novel Treatment Strategies

“…Thus, a living cell may be perceived as being analogous to a perceptron (or McCulloch–Pitts neuron), a single-layer neural network that integrates input assigned with a weighted matrix and computes an output such as a decision to switch phenotypes. These tantalizing revelations have not only put phenotypic plasticity in perspective but have also put scientists at the vanguard of a new field called basal cognition, which embodies fundamental processes and mechanisms that enabled protists to monitor or track environmental states and act appropriately to ensure survival and reproduction long before the metazoan nervous systems developed during evolution [ 18 , 19 , 20 , 21 , 22 , 23 , 24 ].…”

Functional fibrillar interfaces: Biological hair as inspiration across scales

“…They drive fluid flow through a conical filter consisting of microvilli with diameters of 100–200 nm, spaced 200–700 nm apart [ 121 – 122 ]. While the microvilli contain actin and myosin, which together enable motility during escapes and help to transport trapped organic matter for consumption [ 123 ], they function passively when filtering organic matter. The structure driving the fluid flow through the filter remains elusive.…”