An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium

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 Tc-foxQ2 forkhead transcription factor, a key regulator of the anterior gene regulatory network of insects. We characterized four distinct types of Tc-foxQ2 positive neural progenitor cells based on differential co-expression with Tc-six3/optix, Tc-six4, Tc-chx/vsx, Tc-nkx2.1/scro, Tc-ey, Tc-rx and Tc-fez1. An enhancer trap line built by genome editing marked Tc-foxQ2 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 Tc-foxQ2 RNAi knock-down embryos the primary brain commissure did not split and subsequent development of midline brain structures stalled. Our work establishes foxQ2 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.

Sequence heterochrony led to a gain of functionality in an immature stage of the central complex: A fly–beetle insight

“…However, one should be aware that a genetic neural lineage is not equivalent to a neural lineage (i.e., one neuroblast and all of its offspring). Rather, we find that several neural lineages are marked both by rx (this work) and foxQ2 expression [41]. In the latter work, we even found indication that both type I and type II neuroblasts may be marked by one genetic neural lineage, likely also valid for rx (see tentative lineage assignments in SI).…”

“…Actually, recent technical advances have opened the possibility to study the genetic and cellular basis of brain development not only in the classic model organism D. melanogaster but also in other insects in order to reveal conserved and divergent aspects. The red flour beetle T. castaneum is spearheading comparative functional genetic work in neurogenesis because of its welldeveloped genetic toolkit and advances in neurobiological methods [9,[37][38][39][40][41][42][43][44][45][46][47]. Recently, we suggested to compare homologous cells in different taxa by marking what we called genetic neural lineages, i.e., cells that express the same conserved transcription factor [9].…”

“…It should be noted, however, that the actual identity of a given neuroblast lineage is not determined by a single transcription factor but by a cocktail of several factors [ 48 ]. Genetic neural lineages can be labeled either by classic enhancer trapping or a targeted genome editing approach, both available in Tribolium [ 39 , 41 , 47 ].…”

six3 acts upstream of foxQ2 in labrum and neural development in the spider Parasteatoda tepidariorum

“…Both these transcription factors pattern anterior neurogenic domains during the embryonic development of the brachiopod T. transversa (Santagata et al 2012). In the red flour beetle, Tc-foxQ2positive cells contribute to the central complex and the gene is required for central brain development (He et al 2019). In T. castaneum, an extended GRN for anterior head development has been proposed in which Tc-six3 and Tc-foxQ2 hold upstream positions (Kitzmann et al 2017).…”

Shaking hands is a putative terminal selector and controls axon outgrowth of central complex neurons in the insect modelTribolium

“…To gain an overview of G10011-GFP expression, we crossed G10011 to Ten-a--RFP expressing beetles and examined the adult brains of the resulting progeny. Ten-a--RFP is a derivative of the enhancer trap line Tenascin-a (also called Teneurin-a)-GFP (He et al, 2019). Figure 1A), the FB and the EB ( Figure 1B; for a schematic depiction of CX neuropils and coordinates of the axes refer to panels E and G, respectively).…”