The evolution of gene expression in seasonal environments

The biological activities of organisms are closely linked to seasonality. Phenology, the temporal orchestration of biological activities, is governed by gene expression, yet the evolutionary dynamics shaping seasonal gene expression remain unclear. To investigate the evolutionary patterns of gene expression in seasonal environments, we compared genome-wide expression dynamics (molecular phenology) in four dominant evergreen Fagaceae species in Asia ( Quercus glauca , Q. acuta , Lithocarpus edulis , and L. glaber ), using leaf and bud tissues over two seasonal cycles. We assembled high-quality reference genomes for Q. glauca and L. edulis , identifying 11749 single-copy orthologous genes. Seasonal transcriptomic profiling of these orthologous genes revealed highly conserved gene expression across species in winter when temperatures fall below ~10°C. Rhythmic gene expression with significant periodic oscillations was more prevalent in buds (51.9%) than in leaves (40.6%), with most rhythmic genes (78.4 - 92.0%) exhibiting annual periodicity, while a smaller fraction (1.2 - 11.9%) followed half-annual cycles. The seasonal peaks of rhythmic genes were synchronized across species in winter but diverged during the growing season, aligning with phenological events such as leaf flushing and flowering. Genes with conserved seasonal peaks exhibited slower evolutionary rates, suggesting weak selective pressures maintaining seasonal gene expression. However, the evolutionary rates were similarly slow regardless of whether genes were expressed in winter or the growing season. These findings suggest that winter gene expression is more conserved than that in the growing season, imposing a seasonal constraint on gene expression evolution. This constraint may limit temporal niche partitioning and slow species divergence rates in seasonal environments.