Whole-genome duplication promotes phenotypic and genetic adaptation to elevation.

Abstract

Whole-genome duplication (WGD) is often considered as either an adaptive dead-end or a facilitator of rapid adaptation under changing environments. How diploids vs tetraploids out of WGD respond to selection remains, however, poorly understood. Using whole-genome sequence data and phenotypic evidence from transplant experiments of diploid and autotetraploid populations of Biscutella laevigata (Brassicaceae) sampled at low and high elevation in a factorial design, we here assessed how genomic and phenotypic variation responded to selection across elevation in each ploidal level. While all populations showed similar decay of linkage disequilibrium and synonymous genetic variation, tetraploids showed higher nonsynonymous genetic variation, consistent with relaxed purifying selection following WGD and a higher proportion of candidate loci supportive of adaptation to elevation than diploids. Despite the strong plasticity of most phenotypes in both ploidal levels, diploids maintained high fitness homeostasis across elevation, whereas genetically variable tetraploids exhibited contrasted fitness consistent with adaptation to elevation. As compared to diploids of B. laevigata that evolved adaptive phenotypic plasticity, genomic variation accumulated in tetraploids promoted a strong response to selection, refuting the prediction that WGD is an adaptive dead-end and indicating that it promotes post-WGD adaptation across heterogenous environments.