Gene network simulations provide testable predictions for the molecular domestication syndrome

Area of Science:

• Evolutionary biology
• Genetics
• Computational biology

Background:

• Plant domestication causes repeatable morphological evolution (phenotypic domestication syndrome).
• Domestication involves genomic changes like reduced genetic diversity and altered gene expression.
• Gene regulatory networks (GRNs) are crucial for development and adaptation.

Purpose of the Study:

• To theoretically explore the impact of domestication on the evolution of gene regulatory networks.
• To investigate how domestication scenarios, including bottlenecks and specific selection pressures, affect GRN evolution and gene expression.

Main Methods:

• Population genetics simulations modeling genotype (GRN) and gene expression.
• Simulated domestication scenarios with population bottlenecks and directional/canalizing selection.
• Analysis of genetic diversity, gene expression variance, plasticity, GRN rewiring, and genetic correlations.

Main Results:

• Domestication significantly alters genetic architectures, predicting a drop in neutral allelic diversity.
• Gene expression variance changes depend on the specific domestication scenario, with transient maladaptive plasticity observed.
• GRNs undergo deep rewiring, showing a trend toward gaining regulatory interactions.
• Global increase in genetic correlations among gene expressions, leading to loss of modularity in coexpression patterns and networks.

Conclusions:

• Domestication profoundly impacts the genetic architecture of traits, leading to a 'molecular domestication syndrome'.
• Simulations provide empirically testable predictions for distinguishing wild and domesticated plant genetic architectures.
• Understanding these evolutionary changes in GRNs is key to defining the molecular basis of domestication.