Stability in gene expression and body-plan development leads to evolutionary conservation

Abstract

Abstract Background: Phenotypic evolution is mainly explained by selection for phenotypic variation arising from factors including mutation and environmental noise. Recent theoretical and experimental studies in the medaka fish Oryzias latipes suggest that greater developmental stability in phenotype and gene expression level, observed under conditions of minimal mutation and environmental noise, is positively correlated with intra-specific evolutionary conservation. Therefore, stability would be a novel intrinsic factor that potentially limits phenotypic variation, promoting evolutionary conservation. However, while these prior studies have revealed correlative relationships between stability and evolutionary conservation, the issue of causality has remained unclear. Here, in Japanese medaka, we tested experimentally whether greater stability in phenotype and gene expression leads to evolutionary conservation. Results: Experimental evolution was performed by crossing distantly related Japanese medaka lines, followed by two rounds of intra-generational crossing. We then analyzed whether more stable developmental stages and genes with more stable expression in the F0 generation were more conserved in the F3 generation. The results indicated that greater stability in the F0 generation led to less diversity in the F3 generation. Conclusions: These findings reveal that stability in phenotype and gene expression leads to theirevolutionary conservation, most likely by reducing the potential for phenotypic variation. Further, among the developmental stages, the body-plan-establishment stage exhibited the greatest stability and conservation, potentially contributing to the strict conservation of animal body plan.