Central complex circuit assembly in the beetle Tribolium castaneum and the fruitfly Drososphila melanogaster, an evolutionary developmental comparison at the anatomical and the molecular level.

• Applicant: Dr. Marita Buescher, Ph.D.
• Subject Area: Developmental Neurobiology ; Evolutionary Cell and Developmental Biology (Zoology)
• Term: since 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 500617048

Insect brains have a modular structure. Each module is an anatomically distinct compartment and forms an information processing unit. The central complex (CX) is a compartment within the brain, common to all insect species. It functions as a ‘command center’ that directs motor actions in response to visual stimuli. The CX is an ensemble of several individual neuropils. While the overall architecture of the CX is conserved across insect species, the size and shape of its neuropils vary greatly reflecting an evolutionary adaptation to different habitats. What are the molecular mechanisms that drive CX evolution? It was suggested that evolutionary adaptations of the brain anatomy may occur at the level of core transcription factors: small changes in their expression patterns and/or in their repertoire of target genes can drive evolution without compromising the functional constraints that act on neural circuits. Probing this hypothesis with respect to the CX requires the identification of at least one transcription factor that is expressed and has a functional role in CX neurons in at least two insect species. In contrast to the well-studied CX anatomy, little is known about the gene-regulatory programs which effect the morphological and physiological properties of CX neurons. Recently, I have described a transcription factor, Shaking hands (Skh), that is a highly suitable candidate to examine the role of core transcription factors in brain evolution. In the flour beetle Tribolium, the developmental dynamics of skh expression are characteristic of core transcription factors that specify neuronal subtype identity. In the embryonic brain, skh expression is restricted to a subset of differentiation neurons, many of which survive to adulthood and contribute to the mature CX. skh knockdown results in axon outgrowth defects, thus preventing the formation of an embryonic CX primordium. The previously unstudied Drosophila skh shows a similar embryonic expression pattern and is also required for axon outgrowth, suggesting that subtype specification of CX neurons by skh may be conserved. My proposal addresses the following issues: 1.The identification and characterization of skh expressing neurons and their axonal and dendritic elaborations within the CX, to obtain an accurate and complete picture of the contributions of skh expressing neurons to the CX. 2. What are the direct targets of Skh and which role do these targets play in CX circuit assembly? 3. Does Skh coordinately directs the expression of a battery of subtype-specific effector genes; if so, what do we learn about gene-regulatory programs that determine the properties of neuronal subtypes? 4. Are differences in the Skh expression patterns and/or differences among the Skh target genes causal to species-specific variations of the CX anatomies in Tribolium and Drosophila? If so, what do we learn about the molecular mechanisms underlying the evolutionary adaptations of insect brains in general?

• DFG Programme: Research Grants