Abstract
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.Electronic supplementary materialThe online version of this article (doi:10.1007/s00427-016-0541-8) contains supplementary material, which is available to authorized users.
Highlights
The evolution of animals has resulted in a staggering diversity of forms
The early patterning of the ocellar region entails the generation of basically two cell fates (OC and interocellar cuticle size (IOC)), the control of their respective size, and their spacing into an BOC–IOC–ocellar size (OC)^ pattern
We have studied the ocellar gene regulatory networks (GRNs), as an example of gene network regulated by the Hh morphogen, to predict the range of available phenotypic space for morphological variation and tried to predict parameters within this network with a major effect in controlling that morphological variation
Summary
The answer to this question requires considering that the shape of body parts is controlled by complex genetic programs operating during embryonic development. These programs integrate the action of many genes across growing fields of cells forming extensive developmental gene regulatory networks (BGRN^) (Arnone and Davidson 1997). If form is determined to a large extent by gene networks, it follows that these networks should restrict the potential evolutionary routes to morphological variation (Oster et al 1988; Kauffman 1993; Arthur 2006; Davidson and Erwin 2006; Felix 2012; Jaeger and Monk 2014), an idea first formulated by C. Determining the potential range of phenotypes allowed by a particular GRN, is not straightforward, because gene networks are complex
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