Toward a study of gene regulatory constraints to morphological evolution of the Drosophila ocellar region

The morphology and function of organs depend on coordinated changes in gene expression during development. These changes are controlled by transcription factors, signaling pathways, and their regulatory interactions, which are represented by gene regulatory networks (GRNs). Therefore, the structure of an organ GRN restricts the morphological and functional variations that the organ can experience—its potential morphospace. Therefore, two important questions arise when studying any GRN: what is the predicted available morphospace and what are the regulatory linkages that contribute the most to control morphological variation within this space. Here, we explore these questions by analyzing a small “three-node” GRN model that captures the Hh-driven regulatory interactions controlling a simple visual structure: the ocellar region of Drosophila. Analysis of the model predicts that random variation of model parameters results in a specific non-random distribution of morphological variants. Study of a limited sample of drosophilids and other dipterans finds a correspondence between the predicted phenotypic range and that found in nature. As an alternative to simulations, we apply Bayesian networks methods in order to identify the set of parameters with the largest contribution to morphological variation. Our results predict the potential morphological space of the ocellar complex and identify likely candidate processes to be responsible for ocellar morphological evolution using Bayesian networks. We further discuss the assumptions that the approach we have taken entails and their validity.Open access funding provided by Max Planck Society (Max Planck Institute for the Physics of Complex Systems). Research at the Casares laboratory is funded by the Spanish Ministry for Economy and Innovation (MINECO) and Feder Funds through grant BFU2012-34324 to FC. DGM is a MINECO PhD Fellow. DBA was supported in part by the Spanish Inter-Ministerial Commission of Science and Technology under Project TIN2014-54583-C2-1-R, the European Regional Development fund, and the “Junta de Andalucía” (Spain), under Project P2011-TIC-7508.Peer reviewe