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Abstract

How does biology innovate? Ever since Darwin’s famous visit of the Galapagos Islands and his studies beak shapes and food preferences of finches has this question been asked, addressed, and revisited. The study of biological innovation is at the core of all our attempts to explain morphological differences throughout different stages of animal development. Today, the availability of modern molecular techniques makes it possible to study biological innovations in great depth at the organismal, cellular, or genomic level. And still, it remains unclear how these different levels are linked to eventually produce something entirely new. In my thesis I identified two ways of how biology can create something new in the early stages of fly development, one at the cellular level and one at the tissue level. My discoveries are based on a comparison of the first hours of embryo development in the midge Chironomus riparius and the fruit fly Drosophila melanogaster. This comparison allowed me to identify and characterize cause and consequence of biological innovation, from new genes to new cell biology and putative adaptive benefits. The first part of the results section comprises my comparative work on the formation of the first epithelium in insect embryos, the blastoderm. Here I identified tall blastoderm cells as a feature of presumably higher fly species and small blastoderm cells as a feature of more basal flies. To characterize the function of tall cells and how they emerged I used a comparative approach to distinguish tall from small blastoderm cells and their formation using the fruit fly Drosophila melanogaster as a representative of tall cells and the midge Chironomus riparius as a representative of small cells. By moving from tissue- to cell-level organization, I identified slam, as the first of a set of new genes, that act as headmaster of blastoderm columnarization in flies. By experimental engineering the blastoderm of Chironomus from a cuboidal to a columnar blastoderm I show that this novel Rho/F-actin regulator controls epithelial cell lengthening by an extension of E-cadherin based adhesion along the basolateral membrane. These experimentally columnized cells were less affected by desiccation suggesting an advantage by an increased barrier function of the epithelium. The second part of my thesis focused on a previously identified diversity in extraembryonic tissue development within Diptera, where higher flies show a reduction in extraembryonic tissue development. More basal flies develop extraembryonic tissues that spreads over and covers the entire embryo. By studying interactions of yolk sac membrane with overlaying extraembryonic serosa cells in the scuttle fly Megaselia abdita I revealed decoupling of both tissues was necessary to ensure free spreading of the serosa to cover and protect the embryo. When interfering with the mechanism for decoupling, by interfering with yolk cortical actin or kock-down of Megaselia-Matrix metalloprotease 1 (Mab-Mmp1), coupling of both tissues was prolonged and serosa stayed at a dorsal domain similar to a reduced extraembryonic tissue. The reduction of extraembryonic tissue here pretty much coincides with the transition from small to tall cells.