Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development

Abstract

Recent molecular genetic analyses of Drosophila melanogaster and mouse central nervous system (CNS) development revealed strikingly similar genetic patterning mechanisms in the formation of the insect and vertebrate brain. Thus, in both insects and vertebrates, the correct regionalization and neuronal identity of the anterior brain anlage is controlled by the cephalic gap genes otd/Otx and ems/Emx, whereas members of the Hox genes are involved in patterning of the posterior brain. A third intermediate domain on the anteroposterior axis of the vertebrate and insect brain is characterized by the expression of the Pax2/5/8 orthologues, suggesting that the tripartite ground plans of the protostome and deuterostome brains share a common evolutionary origin. Furthermore, cross-phylum rescue experiments demonstrate that insect and mammalian members of the otd/Otx and ems/Emx gene families can functionally replace each other in embryonic brain patterning. Homologous genes involved in dorsoventral regionalization of the CNS in vertebrates and insects show remarkably similar patterning and orientation with respect to the neurogenic region (ventral in insects and dorsal in vertebrates). This supports the notion that a dorsoventral body axis inversion occurred after the separation of protostome and deuterostome lineages in evolution. Taken together, these findings demonstrate conserved genetic patterning mechanisms in insect and vertebrate brain development and suggest a monophyletic origin of the brain in protostome and deuterostome bilaterians.

Molecular genetic insights into deuterostome evolution from the direct-developing hemichordateSaccoglossus kowalevskii

“…More recent interpretations of the molecular genetic data based on model systems with the central nervous systems lead to quite different conclusions and propose a protostome-deuterostome ancestor with a complex, centralized nervous system with a regionalized brain. The homologous suites of genes involved in the patterning of the central nervous systems of model systems are very similarly deployed spatially during development (Arendt & Nü bler-Jung 1994, 1996Finkelstein & Boncinelli 1994;Sharman & Brand 1998;Hirth et al 2003;Lichtneckert & Reichert 2005). Along the anteroposterior axis, the hox genes are involved in patterning the nerve cords of both arthropods and chordates.…”

“…Most studies have focused on similarities in nervous system patterning along both dorsoventral and anteroposterior axes (Acampora et Lichtneckert & Reichert 2005). Classical morphological comparisons have generally converged on the hypothesis that the central nervous systems of arthropods and chordates evolved independently and that early bilaterian nervous systems were generally quite simple (Holland 2003).…”

“…Although it is now widely accepted that many of the developmental regulatory cascades controlling anteroposterior and dorsoventral axial patterning are probably homologous as regulatory modules (Gerhart & Kirschner 1997;Carroll 2005;Davidson 2006), the extent to which the comparative expression and functional studies involving regulatory genes are effective for testing hypotheses of morphological homology remains controversial De Robertis & Sasai 1996;Lowe et al 2003Lowe et al , 2006Lichtneckert & Reichert 2005;Denes et al 2007). Most studies have focused on similarities in nervous system patterning along both dorsoventral and anteroposterior axes (Acampora et Lichtneckert & Reichert 2005).…”

Conservation of gene function in behaviour

“…Flames & Hobert [91] recently found that the function of a dopamine cis regulatory motif called DA is conserved (and interchangeable) in C. elegans and M. musculus. These and other findings will open the door towards understanding the evolution of structures and neural circuits in animal brains [92].…”

Expression pattern of annelid Zic in embryonic development of the oligochaete Tubifex tubifex

“…Emx homologues are expressed in early embryonic brains in both Drosophila and the mouse (Lichtneckert and Reichert 2005).…”