Evolutionarily conserved anterior expansion of the central nervous system promoted by a common PcG-Hox program

Abstract

A conserved feature of the central nervous system (CNS) is the prominent expansion of anterior regions (brain) when compared to posterior (nerve cord). The cellular and regulatory processes driving anterior CNS expansion are not well understood in any bilaterian species. Here, we address this expansion in Drosophila and mouse. We find that when compared to the nerve cord the brain, in both Drosophila and mouse, displays extended progenitor proliferation, more elaborate daughter cell proliferation and more rapid cell cycle speed. These features contribute to anterior CNS expansion in both species. With respect to genetic control, enhanced brain proliferation is severely reduced by ectopic Hox gene expression, by either Hox misexpression or by loss of Polycomb Group (PcG) function. Strikingly, in PcG mutants, early CNS proliferation appears unaffected, whereas subsequently, brain proliferation is severely reduced. Hence, a conserved PcG-Hox program promotes the anterior expansion of the CNS. The profound differences in proliferation and in the underlying genetic mechanisms between brain and nerve cord lend support to the emerging concept of separate evolutionary origins of these two CNS regions.