Abstract

Molecular biology has provided a rich dataset to develop hypotheses of nervous system evolution. The startling patterning similarities between distantly related animals during the development of their central nervous system (CNS) have resulted in the hypothesis that a CNS with a single centralized medullary cord and a partitioned brain is homologous across bilaterians. However, the ability to precisely reconstruct ancestral neural architectures from molecular genetic information requires that these gene networks specifically map with particular neural anatomies. A growing body of literature representing the development of a wider range of metazoan neural architectures demonstrates that patterning gene network complexity is maintained in animals with more modest levels of neural complexity. Furthermore, a robust phylogenetic framework that provides the basis for testing the congruence of these homology hypotheses has been lacking since the advent of the field of ‘evo-devo’. Recent progress in molecular phylogenetics is refining the necessary framework to test previous homology statements that span large evolutionary distances. In this review, we describe recent advances in animal phylogeny and exemplify for two neural characters—the partitioned brain of arthropods and the ventral centralized nerve cords of annelids—a test for congruence using this framework. The sequential sister taxa at the base of Ecdysozoa and Spiralia comprise small, interstitial groups. This topology is not consistent with the hypothesis of homology of tripartitioned brain of arthropods and vertebrates as well as the ventral arthropod and rope-like ladder nervous system of annelids. There can be exquisite conservation of gene regulatory networks between distantly related groups with contrasting levels of nervous system centralization and complexity. Consequently, the utility of molecular characters to reconstruct ancestral neural organization in deep time is limited.

Highlights

  • Molecular biology has provided a rich dataset to develop hypotheses of nervous system evolution

  • The advent of molecular biology and developmental genetic tools has ushered in a new set of comparative data with great potential to impact our understanding of body plan evolution

  • In flies and vertebrates, similarities in the mechanisms that define the position of the central nervous system (CNS) on either the dorsal or ventral side of the body plan, respectively, revealed some fundamental patterning similarities: bone morphogenic protein (BMP)/chordin signalling is involved in defining the region of the ectoderm that will give rise to the CNS [28]

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Summary

Nervous system diversity and its molecular patterning

Any reconstruction of the deep ancestry of morphology requires a comprehensive comparative approach [40,41]. Transcription factors that pattern the forebrain of chordates such as retinal homeobox (rx), six, foxG, nk and dlx are expressed broadly in the proboscis ectoderm of hemichordates reflecting the organization of the basiepithelial neural plexus (figure 1c) Markers of midbrain such as emx, otx, Pax and lim1/5 are largely localized in the same circumferential epithelial domain, but further posteriorly into the collar ectoderm, and markers of hindbrain engrailed (en) and gbx are localized in the anterior trunk (figure 1c). Some questions still remain open—e.g. the placement of the Acoela and the internal phylogeny of Lophotrochozoa—an emerging phylogenetic framework is allowing zoologists and evolutionary biologists to map morphological and molecular characters to test long-standing rstb.royalsocietypublishing.org Phil. It is an exciting time to be a comparative biologist, and it is clear that the improved resolution of animal relationships gained from phylogenomics will help resolve many of the current debates of morphologists and evo-devo researchers, and open up new horizons for future research

The phylogenetic framework and testing hypotheses of homology
Conclusion and outlook
68. Bourlat SJ et al 2006 Deuterostome phylogeny
93. Marletaz F et al 2006 Chaetognath phylogenomics

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