Evolutionary trade-offs under stochastic water stress shape xylem vulnerability to drought

Abstract

Damage to the water supply system in plants (xylem) during water stress is a major cause of plant mortality under drought. However, theory is lacking for the evolutionary emergence of, and variation in, the ability of xylem to resist damage when the maximum water stress experienced each year is stochastic. We determine optimal xylem vulnerability to water stress that balances trade-offs among water transport for photosynthetic carbon gains, carbon costs of constructing xylem that is resistant to damage, and the likelihood of experiencing water stress. Higher water stress optimally selects for higher resistance to water stress, loss of functional xylem over a larger range of water stress, greater water use efficiency, and, counterintuitively, higher chances of complete loss of xylem function despite larger hydraulic safety margins. The greater hydraulic safety observed in gymnosperms over angiosperms is most likely because of less severe increases in the cost of xylem that can withstand higher water stress. Species with longer-lived xylem are predicted to be especially vulnerable to increased mortality if transitions to a drier climate occur faster than adaptation. Our stochastic water stress theory shows that a relative metric of hydraulic safety, the hydraulic safety index, coupled with climate variability, better reflects the likelihood of hydraulic failure than does the widely used hydraulic safety margin. By placing water stress in a stochastic framework, our theory provides insights into adaptive xylem vulnerability and the risk of hydraulic failure.