Evolution after whole-genome duplication (WGD) drives phenotypic and transcriptomic divergence more than WGD in an autopolyploid herb.

Abstract

Whole-genome duplication (WGD) is a major driver of plant speciation and often hypothesized to promote rapid adaptation to new or changing environmental conditions. However, the extent to which WGD per se fosters phenotypic and transcriptional novelties, and the relative contribution of WGD-induced changes vs post-WGD evolution to trait differentiation between cytotypes remains poorly understood. Here, we investigated the phenotypic and transcriptomic consequences of WGD and subsequent evolution in the Biscutella laevigata diploid-autotetraploid complex by comparing replicated diploid, synthetic autotetraploids, and natural autotetraploids (originated some 24,000 to 7,000 generations ago) under moderate daily temperature fluctuations (stable) vs. daily heat stress (changing) conditions. WGD led to reduced specific leaf area and slower rosette growth but had no significant effect on biomass. Post-WGD evolution acted in contrasting directions on WGD-induced changes, either reverting traits to diploid-like values or maintaining them in natural autotetraploids. Overall, WGD induced a decrease in fitness that was mitigated by post-WGD evolution, resulting in natural autotetraploids with similar or higher fitness under changing conditions than diploids. While the genetic background modulates the effects of WGD, cytotype-level transcriptomic analyses revealed limited immediate effects of WGD under stable conditions, although heat stress induced different responses across cytotypes. Altogether, our results highlight a complex interplay between immediate WGD-induced and subsequent evolution at the phenotypic and transcriptomic levels, supporting a predominant role of post-WGD evolution in the differentiation of current cytotypes and the adaptive evolution of autotetraploids of B. laevigata.