Evolutionary divergence of potential drought adaptations between two subspecies of an annual plant: Are trait combinations facilitated, independent, or constrained?

Premise: Whether drought-adaptation mechanisms tend to evolve together, evolve independently, or evolve constrained by genetic architecture is incompletely resolved, particularly for water-relations traits besides gas exchange. We addressed this issue in two subspecies of Clarkia xantiana (Onagraceae), California winter annuals that separated approximately 65,000 years ago and are adapted, partly by differences in flowering time, to native ranges differing in precipitation.

Methods: In these subspecies and in recombinant inbred lines (RILs) from a cross between them, we scored traits related to drought adaptation (timing of seed germination and of flowering, succulence, pressure-volume curve variables) in common environments.

Results: The subspecies native to more arid environments (parviflora) exhibited slower seed germination in saturated conditions, earlier flowering, and greater succulence, likely indicating superior drought avoidance, drought escape, and dehydration resistance via water storage. The other subspecies (xantiana) had lower osmotic potential at full turgor and lower water potential at turgor loss, implying superior dehydration tolerance. Genetic correlations among RILs suggest facilitated evolution of some trait combinations and independence of others. Where genetic correlations exist, subspecies differences fell along them, with the exception of differences in succulence and turgor loss point. In that case, subspecies difference overcame genetic correlations, possibly reflecting strong selection and/or antagonistic genetic correlations with other traits.

Conclusions: Clarkia xantiana subspecies' differ in multiple mechanisms of drought adaptation. Genetic architecture generally does not seem to have constrained the evolution of these mechanisms, and it may have facilitated the evolution of some of trait combinations.