Evolutionary Properties of Neural Networks: Exploration of Robustness and Evolvability in the Genotype-Phenotype Map

Sammanfattning: Evolution is a fundamental and crucial part of life that hinges on two central properties: robustness and evolvability. Robustness is required to maintain essential traits despite mutations while evolvability produces novel traits that might prove beneficial in survival. While both robustness and evolvability are necessary, embracing them simultaneously seemingly leads to an inherent conflict due to their antagonistic goals driven by a shared mechanism, mutation. This conflict has been partially resolved by distinguishing phenotypic robustness and genotypic robustness. However, the general relationship between robustness and evolvability across various biological systems and how they are simultaneously facilitated are still unknown. Here, we study the relationship between robustness and evolvability of neural circuits using a genotype-phenotype map (GP map) which describes interactions between genes that ultimately determine the phenotype. We focus on canalization, the buffering of phenotypes against internal and external variations, to explain the relationship between robustness and evolvability. The pyloric circuit of the crustacean stomatogastric ganglion is used as the model system to study the relationship between robustness and evolvability. We use information theory to quantify robustness and evolvability and a novel simulation-based inference technique to examine the GP map which is used as an analog to a phenotype landscape. While robustness and evolvability are not directly correlated globally in the pyloric circuit, they are found to be linear with respect to collective traits of the pyloric rhythm as well as to individual traits. Robustness and evolvability are seen to be compromising around a region in the GP map, and we hypothesize that the pyloric rhythm is canalized, leading to local robustness and global evolvability. Multiple indicators of canalization and explicit calculation confirms that the pyloric rhythm is canalized in this neural circuit. Investigating the topology of the GP map reveals that the local landscape around the pyloric rhythm is flatter, facilitating robustness. Deviating from the canalized region leads to highly variable and steep landscape of the GP map, promoting evolvability. Gradient directions of the GP map at pyloric points are seen to be correlated, hinting at implicit mechanisms to preserve the biologically relevant behavior. In conclusion, this work demonstrates that the structure of the genotype-phenotype map in the stomatogastric ganglion facilitates robustness and evolvability through canalization. This study also establishes a scalable and generally applicable method to examine robustness and evolvability in any system involving mechanistic models.