Rapid evolutionary changes in gene expression in response to climate fluctuations

There is now abundant evidence of rapid evolution in natural populations, but the genetic mechanisms of these changes remain unclear. One possible route to rapid evolution is through changes in the expression of genes that influence traits under selection. We examined contemporary evolutionary gene expression changes in plant populations responding to environmental fluctuations. We compared genome-wide gene expression, using RNA-seq, in two populations of Brassica rapa collected over four time points between 1997 and 2014, during which precipitation in southern California fluctuated dramatically and phenotypic and genotypic changes occurred. By combining transcriptome profiling with the resurrection approach, we directly examined evolutionary changes in gene expression over time. For both populations, we found a substantial number of differentially expressed genes between generations, indicating rapid evolution in the expression of many genes. Using existing gene annotations, we found that many changes occurred in genes involved in regulating stress responses and flowering time. These appeared related to the fluctuations in precipitation and were potentially adaptive. However, the evolutionary changes in gene expression differed across generations within and between populations, indicating largely independent evolutionary trajectories across populations and over time. Our study provides strong evidence for rapid evolution in gene expression, and indicates that changes in gene expression can be one mechanism of rapid evolutionary responses to selection episodes. This study also illustrates that combining resurrection studies with transcriptomics is a powerful approach for investigating evolutionary changes at the gene regulatory level, and will provide new insights into the genetic basis of contemporary evolution.