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.

Keywords: Basal cognition; Choanoflagellates; Multicellularity; Origin of animals; Sensation.

Fig. 1

Phylogenetic position and cellular features of choanoflagellates. A Choanoflagellates (Choanoflagellatea) are the sister group to animals (Metazoa), forming a monophyletic clade named Choanozoa (pink). Animals, choanoflagellates and other unicellular relatives form the Holozoa clade (blue) within the Opisthokonta eukaryotic supergroup (gray). Topology based on King et al. (2008), Fairclough et al. (2013), Torruella et al. (2015), Hehenberger et al. (2017), and Grau-Bové et al. (2017). Uncertain relationships are depicted as polytomies. B Diagnostic features of a choanoflagellate cell. C Transmission electron micrograph of a Salpingoeca rosetta cell showcasing the generic cellular architecture of a choanoflagellate. Colored labels refer to the nearby cellular structure of the same color, including the apical flagella and collar (which together form the collar complex), organelles, and basal filopodia. ER: endoplasmic reticulum. Image modified from Booth et al. (2018). D Life stages of the colonial S. rosetta (Dayel et al. ; Levin and King 2013). The single-celled slow-swimmer stage can transition to fast swimmers and to clonal multicellular forms (chain and rosette colonies), where neighboring cells are linked by intercellular bridges. Fast swimmers can also transition to a sessile thecate stage through a process named “filopodial walking”. In this process, basal filopodia contact the substrate and allow the cell to adhere, move and settle at a given spot, where it then secretes an organic covering known as theca. Arrows indicate directionality of each transition (loop arrows indicate cell division)

Fig. 2

External stimuli and choanoflagellate cellular responses by chemosensation, photosensation and mechanosensation. (A–H) Choanoflagellate responses to various external stimuli, involving chemosensation (A, aerotaxis (Kirkegaard et al. 2016a); B, pH-taxis (Miño et al. 2017); C–D, bacterial cues (Alegado et al. ; Woznica et al. 2016, 2017); E, NO signaling ((Reyes-Rivera et al. 2022)), photosensation (F, light-to-dark transitions (Brunet et al. 2019)) and mechanosensation (G, flow (Leadbeater 1983a); H, confinement (Brunet et al. 2021)). A’–H’ Conversion of stimuli to cellular responses, including, when known, sensory receptors. A’’–H’’ Behavioral outputs resulting from chemosensation, photosensation and mechanosensation

Fig. 3

Phylogenetic distribution of putative molecular sensors and sensory transducers in choanozoans. Presence or absence of key chemosensory, photosensory and mechanosensory receptors as well as components of signal transduction pathways are represented in columns and color-coded (see key in figure). Numbers inside each box represent number of ortholog sequences either previously reported in literature or predicted by ourselves. Note that experimental evidence of these molecules in the sensory categories listed requires further investigation. See Table S1 for methods of ortholog identification and accession numbers. The phylogenetic relationships of selected taxa are based on Brunet et al. (2019)