Divergent Mechanisms of Head-Trunk Separation in Dipteran Flies

Abstract

Evolution has led to an immense diversity in the form and shape of animals that we can observe today. As a result of an evolutionary trend called cephalization, most animals develop a head as a separate entity than the trunk. Foundations of head as an isolated body part become evident while the animal body plan is established during the early development. Mechanisms of head and trunk separation, however, are poorly understood. Studying how and which developmental programs contribute to the divergence of head-trunk separation mechanism is, therefore, essential. As our understanding of morphogenesis, the making of morphology, has drastically changed over the years, we can now tackle such phenomenon in greater detail. In my thesis, I interrogated the head-trunk separation mechanisms during early gastrulation among dipteran flies as a model. Dipteran tree of flies present a valuable diversity in head-trunk separation strategies. While derived cyclorrhaphan fruit fly Drosophila melanogaster and basal cyclorrhaphan scuttle fly Megaselia abdita embryos employ a head fold called the cephalic furrow, which physically separates embryonic head from trunk; basal non-cyclorrhaphan midge fly C. riparius embryos, like most insects, do not form a head fold. In D. melanogaster, the cephalic furrow formation is a deep epithelial infolding event, that invariably appears in the same position, critically requires the overlapping expression of two transcription factors, even-skipped and buttonhead. My findings suggested that the absence of a head fold in C. riparius coincides with non-overlapping expression patterns these two genes, while M. abdita has a similar overlap with some differences. I further identified that in the absence of such a visible separator, differential arrangement of subcellular contractile actomyosin networks in the anteroposterior axis has a pivotal role in head- trunk separation in C. riparius. Furthermore, uncovering prominent out-of-plane divisions in the C. riparius’ head development allowed me to speculate a putatively analogous function to the cephalic furrow in higher flies, as a number of cells sink below the embryo surface in both cases. Taken together, my thesis shed light onto the variation of head-trunk separation strategies, underlying genetics, and its implementation at the cellular, tissue and embryonic level in dipteran flies.