Evolution of centralized nervous systems: two schools of evolutionary thought

Abstract

Understanding the evolution of centralized nervous systems requires an understanding of metazoan phylogenetic interrelationships, their fossil record, the variation in their cephalic neural characters, and the development of these characters. Each of these topics involves comparative approaches, and both cladistic and phenetic methodologies have been applied. Our understanding of metazoan phylogeny has increased greatly with the cladistic analysis of molecular data, and relaxed molecular clocks generally date the origin of bilaterians at 600-700 Mya (during the Ediacaran). Although the taxonomic affinities of the Ediacaran biota remain uncertain, a conservative interpretation suggests that a number of these taxa form clades that are closely related, if not stem clades of bilaterian crown clades. Analysis of brain-body complexity among extant bilaterians indicates that diffuse nerve nets and possibly, ganglionated cephalic neural systems existed in Ediacaran organisms. An outgroup analysis of cephalic neural characters among extant metazoans also indicates that the last common bilaterian ancestor possessed a diffuse nerve plexus and that brains evolved independently at least four times. In contrast, the hypothesis of a tripartite brain, based primarily on phenetic analysis of developmental genetic data, indicates that the brain arose in the last common bilaterian ancestor. Hopefully, this debate will be resolved by cladistic analysis of the genomes of additional taxa and an increased understanding of character identity genetic networks.

Fig. 1.

Reconstruction of the Ediacaran (A) and Burgess Shale (B) biotas. The Ediacaran biota is reconstructed to convey maximal morphological complexity. (A) 1, Eoporpita; 2, Charniodiscus; 3, Dickinsonia; 4, Arkarua; 5, Spriggina; 6, Praecambridium; 7, soft-bodied “trilobite”; 8, Kimberella. (B) 1, Burgessochaeta; 2, Lingulella; 3, Ottoia; 4, Marrella; 5, Olenoides; 6, Naraoia; 7, Canadaspis; 8, Sidneyia, 9, Opabinia; 10, Anomalocaris; 11, Gogia; 12, Eldonia; 13, Pikaia; 14, Aysheaia; 15, Hallucigenia; 16, Odontogriphus; 17, Dinomischus.

Fig. 2.

Outgroup analysis of cephalic neural characters across extant metazoans. The cladogram is modified from the work by Glenner et al. (104), with the inclusion of xenacoelmorphs as the sister taxon to other deuterostomes (106). The analysis indicates that the last bilaterian common ancestor possessed a diffuse nerve plexus and that brains independently evolved at least four times among bilaterians.