Farnworth, M. S. | bioRxiv Science

bioRxiv2019

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

Animal behavior is guided by the brain. Therefore, adaptations of brain structure and function are essential for animal survival, and each species differs in such adaptations. The brain of one individual may even differ between life stages, for instance as adaptation to the divergent needs of larval and adult life of holometabolous insects. All such differences emerge during development but the cellular mechanisms behind the diversification of brains between taxa and life stages remain enigmatic. In this study, we investigated holometabolous insects, where larvae differ dramatically from the adult in both behavior and morphology. As consequence, the central complex, mainly responsible for spatial orientation, is conserved between species at the adult stage, but differs between larvae and adults as well as between larvae of different taxa. We used genome editing and established transgenic lines to visualize cells expressing the conserved transcription factor retinal homeobox, thereby marking homologous genetic neural lineages in both the fly Drosophila melanogaster and the beetle Tribolium castaneum. This approach allowed us for the first time to compare the development of homologous neural cells between taxa from embryo to the adult. We found complex heterochronic changes including shifts of developmental events between embryonic and pupal stages. Further, we provide, to our knowledge, the first example of sequence heterochrony in brain development, where certain developmental steps changed their position within the ontogenetic progression. We show that through this sequence heterochrony, an immature developmental stage of the central complex gains functionality in Tribolium larvae. We discuss the bearing of our results on the evolution of holometabolous larval central complexes by regression to a form present in an ancestor.

evolutionary biology↗

bioRxiv2019

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

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.\n\nSummary statementAn ancestral neuroendocrine center contributes to the evolution of the central complex. foxQ2 is a gene required for the development of midline structures of the insect brain, which distinguish protocerebrum from segmental ganglia.

developmental biology↗