Phylogenomics meets neuroscience: How many times might complex brains have evolved?

Abstract

The origin of complex centralized brains is one of the major evolutionary transitions in the history of animals. Monophyly (i.e. presence of a centralized nervous system in urbilateria) vs polyphyly (i.e. multiple origins by parallel centralization of nervous systems within several lineages) are two historically conflicting scenarios to explain such transitions. However, recent phylogenomic and cladistic analysis suggests that complex brains may have independently evolved at least 9 times within different animal lineages. Indeed, even within the phylum Mollusca cephalization might have occurred at least 5 times. Emerging molecular data further suggest that at the genomic level such transitions might have been achieved by changes in expression of just a few transcriptional factors – not surprising since such events might happen multiple times over 700 million years of animal evolution. Both cladistic and genomic analyses also imply that neurons themselves evolved more than once. Ancestral polarized secretory cells were likely involved in coordination of ciliated locomotion in early animals, and these cells can be considered as evolutionary precursors of neurons within different lineages. Under this scenario, the origins of neurons can be linked to adaptations to stress/injury factors in the form of integrated regeneration-type cellular response with secretory signaling peptides as early neurotransmitters. To further reconstruct the parallel evolution of nervous systems genomic approaches are essential to probe enigmatic neurons of basal metazoans, selected lophotrochozoans (e.g. phoronids, brachiopods) and deuterostomes.

Convergent evolution of neural systems in ctenophores

“…2E), but it is probably a subset of complex distributed networks controlling both stereotyped and learned behaviors (Hernandez-Nicaise, 1991; Horridge, 1974;Tamm, 1982). (Moroz, 2009;Moroz, 2012;Moroz et al, 2014)]. Choanoflagellates are placed at the base of the tree as a sister group for Metazoa (King et al, 2008) followed by Ctenophora (represented by the photo of Pleurobrachia bachei) as the sister group to all other animals.…”

“…Red numbers indicate that at least nine independent events of neuronal centralization have occurred during evolution. Even in Mollusca, this centralization of the nervous system might occur 4-5 times in parallel (Kocot et al, 2011;Moroz, 2012). Only representative groups of the 34-36 recognized animal phyla are shown in the diagram (Nielsen, 2012).…”

“…(1) Classical Eumetazoans (i.e animals with nervous systems, Cnidaria, Ctenophora and Bilateria) are the polyphyletic clade (Moroz, 2012;Moroz et al, 2014). This hypothesis implies either massive loss of complex animal traits in sponges and placozoans (such as mesoderm, muscles and neurons) or massive homoplasies (molecular innovations) in ctenophores.…”

“…The comparative data suggest that at least some neuronal cell types and complex integrative structures (such as the aboral organ) evolved independently in the ctenophore lineage (Moroz, 2012;Moroz et al, 2014). The process could employ a subset of evolutionarily conserved gene modules that existed in the common ancestor of all animals to control directional propagation of electrical signals and polarized secretion, as well as novel neurogenic and signal molecules.…”

“…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.…”