It's all in the timing: vegetative phase change alters selection under drought and contributes to local adaptation

Abstract

The timing of developmental transitions is critical for adaptation, aligning stress-tolerant and sensitive stages with harsh and benign periods. At the same time, tradeoffs can promote diversity in development within populations. While geographic clines in developmental timing are often documented, there are few documented genetic tradeoffs in stress tolerance across developmental stages. Here, we study the juvenile-to-adult vegetative phase change (VPC), a conserved transition marked by changes in leaf morphology and physiology. In Arabidopsis, we found strong rank-changing genotype-by-environment interactions for fitness depending on the stage of drought exposure, indicating tradeoffs and stage-specific mechanisms of drought adaptation. Adult plants significantly increased water-use efficiency under drought, while juveniles did not, indicating lower juvenile plasticity. VPC timing varied with climate in Iberia, where genotypes from warm, dry climates transitioned earlier than those from cool, moist climates. However, SNPs associated with VPC timing and drought fitness showed little global geographic variation, suggesting tradeoffs maintain diversity across the species range. Genome-wide association mapping revealed candidate loci for VPC timing and stage-specific drought responses, several validated in T-DNA lines. Our results show that VPC timing contributes to drought adaptation and that genetic tradeoffs across developmental stages help maintain natural diversity.