An ancestral apical brain region contributes to the central complex under the control of <i>foxQ2</i> in the beetle <i>Tribolium</i>.

Abstract

The genetic control of anterior brain development is highly conserved throughout animals. For instance, a conserved anterior gene regulatory network specifies the ancestral neuroendocrine center of animals and the apical organ of marine organisms. However, its contribution to the brain in non-marine animals has remained elusive. Here, we study the function of the <i>Tc-foxQ2</i> forkhead transcription factor, a key regulator of the anterior gene regulatory network of insects. We characterized four distinct types of <i>Tc-foxQ2</i> positive neural progenitor cells based on differential co-expression with <i>Tc-six3</i>/<i>optix</i>, <i>Tc-six4</i>, <i>Tc-chx</i>/<i>vsx</i>, <i>Tc-nkx2.1</i>/<i>scro</i>, <i>Tc-ey</i>, <i>Tc-rx</i> and <i>Tc-fez1</i>. An enhancer trap line built by genome editing marked <i>Tc-foxQ2</i> positive neurons, which projected through the primary brain commissure and later through a subset of commissural fascicles. Eventually, they contributed to the central complex. Strikingly, in <i>Tc-foxQ2</i> RNAi knock-down embryos the primary brain commissure did not split and subsequent development of midline brain structures stalled. Our work establishes <i>foxQ2</i> as a key regulator of brain midline structures, which distinguish the protocerebrum from segmental ganglia. Unexpectedly, our data suggest that the central complex evolved by integrating neural cells from an ancestral anterior neuroendocrine center.