Investigating the Evolutionary Origins and Modification of Novel Morphologies and their Developmental Networks

The nature of the origin of morphological characters has long been a central subject of interest in the field of evolutionary developmental biology. Currently, many morphologies are known to be underscored by vast gene regulatory networks (GRNs) such that GRNs are anticipated for any feature of anatomy. Hence, if networks drive anatomical development, how do they evolve? The co-option of networks, a phenomenon in which cohorts of pre-existing transcriptional circuits are redeployed to new developmental settings, has been proposed to facilitate the rapid evolution of GRNs. Although several examples suggest the contribution of network co-option to the evolution of novel structures, examples that demonstrate and explore this process in molecular detail are currently lacking. In this dissertation I investigate the posterior lobe as a model of network co-option. A cuticular outgrowth on the genitalia of male fruit flies, this morphology is unique to the Drosophila melanogaster clade. By studying the ancestry of one gene’s posterior lobe activity, I discovered that it existed before the evolution of the posterior lobe, and had been redeployed from a network active during embryonic life. I next investigate the origin of the posterior lobe by studying the intercellular signaling pathways that contribute to its specification, discovering that a drastically altered pattern of the Notch ligand Delta is necessary for the development and evolution of the posterior lobe. I then explore how an embryonic circuit that was co-opted to the posterior lobe was subsequently modified to alter its shape. Finally, I study the origins of novelty at the level of an individual transcriptional circuit, analyzing all possible intermediate states along its evolutionary path. These studies demonstrate the value of an approach focused on understanding the co-option and origination of regulatory circuitry for the study of the evolution of novel characters