Selection for distinct gene expression properties favours the evolution of mutational robustness in gene regulatory networks

Abstract

Mutational robustness is a genotype's tendency to keep a phenotypic trait with little and few changes in the face of mutations. Mutational robustness is both ubiquitous and evolutionarily important as it affects in different ways the probability that new phenotypic variation arises. Understanding the origins of robustness is specially relevant for systems of development that are phylogenetically widespread and that construct phenotypic traits with a strong impact on fitness. Gene regulatory networks are examples of this class of systems. They comprise sets of genes that, through cross-regulation, build the gene activity patterns that define cellular responses, different tissues or distinct cell types. Several empirical observations, such as a greater robustness of wild-type phenotypes, suggest that stabilizing selection underlies the evolution of mutational robustness. However, the role of selection in the evolution of robustness is still under debate. Computer simulations of the dynamics and evolution of gene regulatory networks have shown that selection for any gene activity pattern that is steady and self-sustaining is sufficient to promote the evolution of mutational robustness. Here, I generalize this scenario using a computational model to show that selection for different aspects of a gene activity phenotype increases mutational robustness. Mutational robustness evolves even when selection favours properties that conflict with the stationarity of a gene activity pattern. The results that I present support an important role for stabilizing selection in the evolution of robustness in gene regulatory networks.

Genotype by environment interaction for gene expression in Drosophila melanogaster

“…5a, b and Supplementary Data 6 ). Previous theoretical work has suggested that stabilizing selection was important in promoting the evolution of network robustness 36 . Our result is one of the few 37 that provides empirical support for the role of stabilizing selection in evolving network robustness.…”

La Ecología Evolutiva del Desarrollo en México

“…Esta última propuesta fue verificada empíricamente a través del análisis genómico de la conservación de la red regulatoria del desarrollo floral en diferentes angiospermas (Dávila-Velderrain, Servin-Márquez y Álvarez-Buylla, 2013). También se han realizado contribuciones importantes sobre el papel de la plasticidad fenotípica (y la variabilidad no genética en general) en la adaptación y consistencia de sistemas biológicos en el contexto de la evolución de la modularidad de las plantas (Espinosa-Soto, 2016;Espinosa-Soto y Wagner, 2010;Espinosa-Soto et al, 2011a, b). Estos últimos estudios han generado predicciones interesantes sobre el papel que puede desempeñar la plasticidad de los genotipos en la evolución adaptativa (Espinosa-Soto et al, 2011a, b).…”

“…También explora cómo emergen la plasticidad fenotípica (i.e., variación fenotípica de un mismo genotipo en distintos ambientes) y las normas de reacción de un genotipo (i.e., patrón de cambio fenotípico de un genotipo ante variaciones de un factor ambiental). Finalmente, se investiga cuál es el papel de la plasticidad en la evolución fenotípica adaptativa y no adaptativa (Espinosa-Soto, 2016;Espinosa-Soto, Martin y Wagner, 2011a, b).…”

“…En particular, algunos de los autores del presente artículo han estudiado las consecuencias fenotípicas de la retroalimentación entre mecanismos genéticos y epigenéticos con la ecología de los organismos y sus consecuencias para la evolución fenotípica Álvarez-Buylla et al, 2008Álvarez-Buylla et al, , 2013Álvarez-Buylla et al, , 2016Chaos et al, 2006;Espinosa-Soto, Padilla-Longoria y Álvarez-Buylla, 2004). Otros grupos en México han abordado enfoques bioinformáticos y experimentales que son relevantes para el estudio Eco-Evo-Devo en plantas (Rosas et al, 2013), animales (e.g., Santacruz, Tinoco-Cuellar, Rangel-Huerta y Maldonado, 2015) y en desarrollo de exploraciones teóricas (Espinosa-Soto, 2016;Espinosa-Soto et al, 2011a, b). A continuación presentamos los avances en varios temas abordados en México a través de la Eco-Evo-Devo.…”

Convergence Analysis and Network Properties of Wagner's Artificial Gene Regulatory Network Model

“…This mechanism is crucial for evolutionary innovations, because genotypes which control gene-gene interactions can change profoundly without affecting phenotypes which represent gene activities or expression concentrations [2]. Wagner's GRN model motivates research on the evolution of genetic networks, and has been successfully employed to study many fundamental evolutionary and ecological questions [15,16,17,18,19,20,21,22,23,11,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52] (See [12] for an in-depth review).…”