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.

Fig. 1

Parallel evolution of neuronal centralization in Deuterostomes and Protostomes. The diagram shows types of neural organization among all major Deuterostome lineages. The presented reconstruction of phylogenetic relationships is based upon recent large-scale phylogenomic analysis among all bilaterians [63]. Filled circles indicate possible events of neural centralization from diffuse Nerve Net type of organization in a common ancestor of all Deuterostomes and Protostomes (open circles). Note that nerve nets in Deuterostomes have only superficial similarities and might not be genealogically related to each other. See text for details. Two major superclades of Protostomes (Ecdysozoa and Lophotrochozoa) might also have evolved complex brains independently from Chordates

Fig. 2

The polygenesis of neuronal centralization. The hypothetical scenario outlining multiple origins of neuronal centralization in Bilateria. The ancestral urbilateria had diffuse, possibly only epidermal nerve nets and did not possess central nervous systems. Centralization of neuronal elements and the formation of CNSs and complex brains occurred independently several times in the course of animal evolution (see also Figs 1, 4 and 5). The inversion of the ventral to dorsal axis took place during earlier stages of Chordate evolution. Ctenophore and Cnidaria nervous systems may have evolved in parallel and, at least in part, may not necessarily be related to bilaterian neural organization. Red, orange and green colors schematically illustrate different neuronal structures. Open white circles indicate the position of the mouth. the author supports this hypothesis of neuronal evolution; see text and [54] for details

Fig. 3

The hypothesis of monophyletic origin of the central nervous system in Bilateria. This is an alternative scenario of the neuronal evolution in animals as outlined in Fig. 2. Here, the ancestral urbilateria had a well-defined central nervous system in the form of a ventral cord. However, multiple animal lineages both within Deuterostomes, Ecdysozoa and Lophotrochozoa independently lost their central nervous system (yet many representatives of these groups are still free living organisms, sometimes with complex behavioral repertoires). Ctenophore and Cnidaria nervous systems might be related/homologous to bilaterian neural organization (although at least some parts of them may have evolved independently). Red, orange and green colors schematically illustrate different neuronal structures. Open white circles indicate the position of the mouth. See text and [54] for details

Fig. 4

The molluscan phylogeny and their neuronal organization. The relationships among major molluscan classes is based on recent phylogenomic analysis [47]. The phylum mollusca has a very broad spectrum of types of neuronal organization. It is based on tetraneury with multiple events of neuronal centralization that are most notable in cephalopods and selected gastropods. See text for details

Fig. 5

Parallel evolution of neuronal centralization in the animal kingdom. The diagram summarizes the current view of evolutionary relationships in the animal kingdom and indicates the presence or absence of a central nervous system (CNS) or brain. From this tree it is possible to see at least 9 possible events of multiple origins of complex brains – shown as red numbers. Circles indicate possible events of multiple origins of neurons. See text for details. This reconstruction of phylogenetic relationships among phyla is a combined view based upon recent large-scale molecular/phylogenomic analyses of several dozen proteins from representatives of more than 15 animal phyla [20, 24, 31, 34, 47, 63, 64, 78, 82, 87]. Only representative groups of the 36 known animal phyla are shown in the diagram. The origin of animals can be traced back to more than 700 Million years ago (Mya) [24]. However, the extant animal phyla might have a more recent evolutionary history and the diversification of the modern bilaterian phyla might be linked to the cambrian explosion. As a result the accurate evolutionary relationships among basal lineages and major bilaterian phyla are not well resolved (dotted lines). Possible timing of the divergence in the diagram is indicated as Mya

Fig. 6

Phylogeny of basal metazoa and independent origin of neurons in Ctenophora. The relationships among five basal metazoan groups (Ctenophora, Porifera, Placozoa, Cnidaria and Bilateria) is based upon [20, 34]. Although the exact placement of Ctenophora and Porifera is not currently resolved (dotted lines), these two lineages were branched before Placozoa, Cnidaria and Bilateria (a clade that was named ParaHoxozoa [72]). The topology of this tree and our recent analysis of Ctenophore gene complements suggest that neurons evolved independently in ctenophores. Sponges either primarily lack neurons or they might have lost them secondarily. Placozoa might also be viewed as a secondarily simplified group