Convergent evolution of neural systems in ctenophores

Abstract

Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers -features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Multiple origins of neurons and synapses from different classes of ancestral secretory cells might have occurred more than once during ~600 million years of animal evolution with independent events of nervous system centralization from a common bilaterian/cnidarian ancestor without the bona fide central nervous system. Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. First, recent genome analyses place ctenophores as a sister group to other animals. Second, ctenophores have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localized in muscles and presumed bilaterian neuronspecific RNA-binding protein Elav is found in non-neuronal cells). Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamineconsistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Nevertheless, it is expected that other classes of signal and neurogenic molecules would be discovered in ctenophores as the next step to decipher one of the most distinct types of neural organization in the animal kingdom.

Genomic data do not support comb jellies as the sister group to all other animals

“…In light of the Ctenophora-sister hypothesis, this result has been interpreted as evidence for convergent evolution, especially for nervous systems (5,11). However, other authors have interpreted the same data differently, concluding they actually are consistent with a single origin of nervous systems (9,10).…”

“…The Ctenophora-sister hypothesis, if correct, would require a major revision of our understanding of animal evolution because it would imply a more complicated evolutionary history, dominated by multiple independent gains and/or losses, of key metazoan characters (7,8). Indeed, this hypothesis has already stirred a controversial discussion about multiple origins of nervous systems (9)(10)(11).…”

Evolution of brain elaboration

“…A largely conserved battery of transcription factors and signalling molecules pattern elements of the nervous system in Bilateria (reviewed by [1,2]), while a number of genes involved in neuron differentiation and function are also shared with the Cnidaria [3,4]. By this criterion, the use of a different array of developmental genes in the Ctenophora suggests that their nervous systems evolved independently from those of Cnidaria þ Bilateria [5]. In the latter grouping, however, the molecular developmental evidence suggests that neurons arose in a common ancestor of Cnidaria þ Bilateria, while mechanisms for patterning subcompartments along the anterior-posterior and dorsal-ventral axes were present in the ancestral bilaterian.…”

Electrogenesis in the lower Metazoa and implications for neuronal integration

“…Analysis of the genomes of Mnemiopsis leidyi (Ryan et al, 2013) and Pleurobrachia bachei (Moroz et al, 2014) supports the possibility that ctenophore neurons evolved independently of other nervous systems (see Moroz, 2015). Electron microscopy shows synapse-like and neuron-like structures (Hernandez-Nicaise, 1973; Hernandez-Nicaise, 1991) while immunofluorescence studies demonstrate the existence of two distinctly separate nerve nets (Jager et al, 2011).…”

“…That being so, comparisons between different neural systems should increase our understanding of the factors that determine their form and function. Moroz (Moroz, 2015) has compared the transmitter make-up predicted by the ctenophore genome with that of other nervous systems. Here, I discuss the performance of the hydrozoan nervous system, in particular the contribution of its electrical properties to neural integration.…”