Quantitative Relationships Between Growth, Differentiation, and Shape That Control Drosophila Eye Development and Its Variation.

Francisco Javier Lobo-Cabrera,Tomás Navarro,Antonella Iannini,Fernando Casares,Alejandro Cuetos

doi:10.3389/fcell.2021.681933

Francisco Javier Lobo-Cabrera, Tomás Navarro + Show 3 more

Open Access

https://doi.org/10.3389/fcell.2021.681933

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Abstract

The size of organs is critical for their function and often a defining trait of a species. Still, how organs reach a species-specific size or how this size varies during evolution are problems not yet solved. Here, we have investigated the conditions that ensure growth termination, variation of final size and the stability of the process for developmental systems that grow and differentiate simultaneously. Specifically, we present a theoretical model for the development of the Drosophila eye, a system where a wave of differentiation sweeps across a growing primordium. This model, which describes the system in a simplified form, predicts universal relationships linking final eye size and developmental time to a single parameter which integrates genetically-controlled variables, the rates of cell proliferation and differentiation, with geometrical factors. We find that the predictions of the theoretical model show good agreement with previously published experimental results. We also develop a new computational model that recapitulates the process more realistically and find concordance between this model and theory as well, but only when the primordium is circular. However, when the primordium is elliptical both models show discrepancies. We explain this difference by the mechanical interactions between cells, an aspect that is not included in the theoretical model. Globally, our work defines the quantitative relationships between rates of growth and differentiation and organ primordium size that ensure growth termination (and, thereby, specify final eye size) and determine the duration of the process; identifies geometrical dependencies of both size and developmental time; and uncovers potential instabilities of the system which might constraint developmental strategies to evolve eyes of different size.

Highlights

The control of organ size and shape in animals constitutes a fundamental process that is still not very well understood (Hafen and Stocker, 2003; Eder et al, 2017)
Previous quantitative data support that this analogy is valid (Vollmer et al, 2016). Another fundamental aspect is the movement of a differentiation wave, known as the morphogenetic furrow (MF), that starts at the posterior pole of the primordium and sweeps toward anterior
In this article we have presented a theoretical model in an attempt to shed light on the dynamics and geometrical constrains of Drosophila eye growth, used here as a model for any developing system where growth and differentiation are coupled through a moving wave

Summary

Introduction

The control of organ size and shape (i.e., the organ’s morphology) in animals constitutes a fundamental process that is still not very well understood (Hafen and Stocker, 2003; Eder et al, 2017). Organ growth is coordinated with the overall growth of the individual, it is often the case that the size of an organ is largely controlled in an organ-autonomous manner That is, it depends on its own genetic constitution. The grafted limb grew just to the small size typical of the small species (Twitty and Schwind, 1931) despite its having developed in the context of a larger individual. This experiment highlights the two major questions behind organ growth control: how organs grow to a species-specific size and how organ size varies in different species. We try to contribute to addressing these questions by studying a simple model, the eye of the vinegar fly Drosophila melanogaster

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