Evolution of the extraembryonic tissue in flies: from Megaselia abdita to Drosophila melanogaster

2017 
Embryonic development establishes the body plan, organs, and the shape of the adult animal organism. This process involves cells and tissues that eventually will not be part of the growing embryo, so-called extraembryonic tissues. In insects, extraembryonic tissues contribute to embryonic development by fulfilling important roles during specific morphogenetic movements, such as blastokinesis, germband retraction and dorsal closure, but also in the protection of the embryo against egg desiccation and pathogens. Within insects, extraembryonic tissues differ in number and topology, they may display diverse morphologies even between closely related species, and it is currently not yet clear which specific function each extraembryonic tissue fulfills and how its development is genetically regulated. Most of our current understanding of extraembryonic development and function in insects stems from studies in Tribolium castaneum and Drosophila melanogaster. The two species show several morphological differences, not only at the extraembryonic level but also in the morphology of the embryo. Specifically, T. castaneum has two extraembryonic tissues called amnion and serosa: the serosa separates from the embryo, grows over it, and eventually encloses the embryo, the amnion stays attached to the embryo and covers its ventral side. D. melanogaster, by contrast, develops only one single extraembryonic tissue called amnioserosa that remains in constant contact with the embryo and stays on its dorsal side. The diversity in form, development, and function of extraembryonic tissues in insect species provides an outstanding model to address how form and function of specific epithelia evolved, and how these changes were genetically encoded. In my thesis, I have taken advantage of intermediate characters in extraembryonic development of Megaselia abdita (Diptera, Phoridae), which features a similar embryonic development as D. melanogaster but maintained two extraembryonic tissues and thus part of the ancestral extraembryonic development described in T. castaneum. I have focused my attention on a detailed in vivo analysis of extraembryonic development at a morphogenetic and cellular level by establishing and using light-sheet microscopy. I acquired evidence that links extraembryonic tissues behavior in M. abdita to orthologues of the T-box transcription factor Dorsocross and the tumor necrosis factor Eiger, which in D. melanogaster are key genes that contribute to specification and morphogenesis of the amnioserosa. In vivo observations and functional studies suggest an important interaction of the extraembryonic tissues of M. abdita with the extracellular matrix that seems to be finely regulated. In conclusion, the results of this study increase our knowledge on morphology and development of extraembryonic tissues in M. abdita and provided an in vivo technique for non-model organisms to study in toto dynamics of early development.
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