Around the clock: gradient shape and noise impact the evolution of oscillatory segmentation dynamics

Area of Science:

• Evolutionary developmental biology
• Computational modeling of biological systems

Background:

• Segmentation is a key evolutionary innovation in bilaterian animals, primarily occurring via sequential segmentation.
• This process, generating segments sequentially from a posterior zone, is often driven by a clock-and-wavefront mechanism.
• The complexity of oscillator networks and their slowing in vertebrates remain incompletely understood, particularly regarding evolutionary origins.

Purpose of the Study:

• To investigate the evolutionary conditions favoring oscillator complexity and slowing in sequential segmentation.
• To explore the relationship between oscillator properties and factors like morphogen gradient steepness and gene expression noise.
• To understand the potential for parallel evolution of segmentation mechanisms across different animal clades.

Main Methods:

• Extension of a pre-existing computational model for the evolution of segmentation.
• Systematic variation of the posterior morphogen gradient slope and gene expression noise levels.
• Analysis of evolved oscillator network properties, including complexity, damping, and the presence of travelling waves.

Main Results:

• Steeper morphogen gradients accelerate evolution and lead to simpler oscillator networks compared to shallow gradients.
• Steep gradients favor damped oscillators, while shallow gradients necessitate persistent oscillators and travelling waves.
• Gene expression noise promotes persistent oscillators under steep gradients and frequency gradients under shallow gradients.
• Oscillator complexity and travelling wave evolution were found to be uncorrelated.

Conclusions:

• Travelling waves in segmentation may evolve as a response to shallow morphogen gradients and gene expression noise.
• These factors could explain variations in segmentation mechanisms observed across arthropod and chordate species.
• The independent evolution of oscillator complexity and travelling waves suggests distinct selective pressures for each property.