American Society of Naturalists

Ian S. Pearse, Jessica M. Aguilar, and Sharon Y. Strauss (Apr 2020)

Mustards live in drought; having trait plasticity keeps their fitness high

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Water limits the success and the distribution of plants in many parts of the world. The availability of water is rapidly changing the environment. Longer, more severe droughts are predicted to become the norm in places where they were once uncommon. Drought-resistant plants are those that thrive and produce high fitness in the low water conditions. Drought resistance is caused by numerous aspects of a plant’s biology, such as the timing of its life cycle, its traits that limit water loss, and its traits that allow it to persist despite water loss. Drought resistance is fundamentally a plastic trait, describing the relationship between water and plant fitness. As plants evolve, are there tradeoffs to drought resistance, such as the ability to capitalize on high water environments? And what mechanisms cause these tradeoffs?

Ian Pearse and colleagues explore the evolution of drought resistance in a clade of mustards, the jewelflowers. Many jewelflower species, native to the western USA, grow in extreme, water-limited habitats, such as scree slopes, deserts, and serpentine barrens. Species that were the most drought-resistant were unable to capitalize on high water environments. These species tended to live in the most drought-prone environments. They coped with drought by having a short and fixed life span, producing seeds before the harshest summer conditions. In contrast, less drought-resistant species could extend their flowering late into the summer and achieve high fitness in high water environments. Thus, flowering phenology and annual lifespan underlie a fundamental tradeoff between fitness at high and low water in these short-lived plants. By exploring how plants produce fitness over water conditions, we will better understand how drought resistance evolves, what traits underlie it, and how plants will cope with drier environments.

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Abstract

Water limitation is a primary driver of plant geographic distributions and individual plant fitness. Drought resistance is the ability to survive and reproduce despite limited water, and numerous studies have explored its physiological basis in plants. However, it is unclear how drought resistance and trade-offs associated with drought resistance evolve within plant clades. We quantified the relationship between water availability and fitness for 13 short-lived plant taxa in the Streptanthus clade that vary in their phenology and the availability of water in the environments where they occur. We derived two parameters from these relationships: plant fitness when water is not limiting, and the water inflection point (WIF), the watering level at which additional water is most efficiently turned into fitness. We used phylogenetic comparative methods to explore trade-offs related to drought resistance and trait plasticity, and the degree to which water relationship parameters are conserved. Taxa from drier climates produced fruits at the lowest water levels, had a lower WIF, flowered earlier, had shorter lifespans, more plastic water use efficiency (WUE), and lower fitness at non-limiting water. In contrast, later-flowering Streptanthus taxa from less xeric climates experienced high fitness at non-limiting water but had no fitness at the lowest water levels. Across the clade, we found a trade-off between drought resistance and fitness at high water, though a single ruderal species was an outlier in this relationship. Our results suggest that drought escape trades off with maximal fitness under non-limiting water, and both are tied to phenology. We also found that variation in trait plasticity determines how different plant species produce fitness over a water gradient.