Origin and early evolution of neural circuits for the control of ciliary locomotion

Abstract

Behaviour evolved before nervous systems. Various single-celled eukaryotes (protists) and the ciliated larvae of sponges devoid of neurons can display sophisticated behaviours, including phototaxis, gravitaxis or chemotaxis. In single-celled eukaryotes, sensory inputs directly influence the motor behaviour of the cell. In swimming sponge larvae, sensory cells influence the activity of cilia on the same cell, thereby steering the multicellular larva. In these organisms, the efficiency of sensory-to-motor transformation (defined as the ratio of sensory cells to total cell number) is low. With the advent of neurons, signal amplification and fast, long-range communication between sensory and motor cells became possible. This may have first occurred in a ciliated swimming stage of the first eumetazoans. The first axons may have had en passant synaptic contacts to several ciliated cells to improve the efficiency of sensory-to-motor transformation, thereby allowing a reduction in the number of sensory cells tuned for the same input. This could have allowed the diversification of sensory modalities and of the behavioural repertoire. I propose that the first nervous systems consisted of combined sensory-motor neurons, directly translating sensory input into motor output on locomotor ciliated cells and steering muscle cells. Neuronal circuitry with low levels of integration has been retained in cnidarians and in the ciliated larvae of some marine invertebrates. This parallel processing stage could have been the starting point for the evolution of more integrated circuits performing the first complex computations such as persistence or coincidence detection. The sensory-motor nervous systems of cnidarians and ciliated larvae of diverse phyla show that brains, like all biological structures, are not irreducibly complex.

Early eukaryotic origins for cilia-associated bioactive peptide-amidating activity

“…In addition, the G-proteincoupled receptors for neuropeptide Y, somatostatin and kisspeptin localize to neuronal cilia (Loktev and Jackson, 2013). Interestingly, neuropeptide precursors have been identified in ciliated metazoans lacking a nervous system, suggesting that regulation of ciliary motility was an ancestral function of peptide-based signaling (Jekely, 2011(Jekely, , 2013.…”

Convergent evolution of neural systems in ctenophores

“…to distant neural processes. The first neural circuits could reasonably have evolved from undifferentiated secretory-like cells (perhaps without recognized bona fide neurons as in Trichoplax) to control cilia and coordinate primary (ciliated) locomotion (Jékely, 2011) recruiting small peptides as early signal molecules. The first proto-neurons could mediate their action via volume transmission without structurally differentiated synapses.…”

“…Our understanding of the origins and early evolution of nervous systems is vague and highly controversial (Bullock and Horridge, 1965;Horridge, 1968;Jékely, 2011;Lentz, 1968;Mackie, 1970;Mackie, 1990;Miller, 2009;Moroz, 2009;Moroz, 2012;Moroz, 2014;Parker, 1919;Pennisi, 2013;Sakharov, 1974 obstacles in the field are the lack of molecular and physiological information about signaling systems from representatives of the basal animals. The phylum Ctenophora, or comb jellies, is of particular interest for two reasons.…”

A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development

“…It accounts for the common orientation of epidermis-derived structures such as hairs, scales and feathers, and is also crucial for coordinating ciliary beating direction in many vertebrate epithelia, for example in airways and the kidney. The larval forms of most animal groups also bear ciliated ectodermal cells, the coordinated beating of which is responsible for directional swimming and/or feeding behaviour with respect to the main body axis (Jékely, 2011). For instance, cnidarian planula larvae are extensively covered by ciliated ectodermal cells aligned along the single oralaboral axis (Fig.…”