Shaped by context: Evolutionary trajectories of desiccation tolerance in land plants.

Desiccation tolerance (DT), the ability to survive near-complete cellular dehydration, is widespread in diaspores but rare in the vegetative tissues of land plants. The patchy and punctuated phylogenetic distribution of vegetative desiccation tolerance (VDT) suggests that the trait is both ancient and recurrent, yet the evolutionary trajectories remain unresolved. Here, we synthesize evidence across land plants to propose a framework for the evolution of VDT in embryophytes. We build on the current understanding of VDT as an ancestral trait, present in the gametophyte of early land plants. The transition to sporophyte dominance and resulting homiohydry in vascular plants coincides with the widespread loss of VDT, likely driven by relaxed selection for VDT, coupled with new structural constraints and anatomical innovations that facilitated water acquisition, transport, and retention. The core molecular modules of DT were retained in the diaspores of most land plants, where they served as evolutionary refugia for the essential building blocks of the trait. Some species later reestablished VDT by co-opting deeply conserved diaspore modules and evolving key anatomical innovations to support them. We argue that such reestablishments of VDT are dependent on both anatomical predispositions as well as exposure to key selective pressures and ecological filters. We conclude that VDT is not a simple presence-absence trait, but rather a modular system, subject to anatomical constraints and contingent on the ecological context. Ultimately, we suggest that VDT serves as an elegant example of how complex traits emerge, persist, and shift across time.