Variation and constraint on stomatal evolution

A major unresolved goal in macroevolution is to understand the physical, developmental, and functional constraints on phenotypic variation. Stomatal anatomy is a fantastic system to address these questions. Stomata are the microscopic pores on the leaf surface of most vascular land plants. Despite their diminutive dimensions, they play an outsized role in plant ecology because they allow plants to tightly regulate the exchange of two key resources: water lost through transpiration and CO$_2$ gained through photosynthesis. Extensive biophysical theory makes quantitative predictions for how stomatal traits should vary and we can test theory using a combination of experimental and powerful phylogenetic comparative studies. We have focused on what drives variation and constraint on stomatal size, density, and distribution. Below, I briefly summarize our contributions.

1. Our work has revived interest in the perplexing problem of why most leaves only develop stomata on the lower surface, which is called hypostomy. Amphistomatous leaves (stomata on upper and lower leaf surfaces) photosynthesize more without transpiring much more water, which means they should be common, but they are not. We discovered there are two distinct modes of leaves: woody plants and shade-loving herbs are hypostomatous; sun-loving, fast-growing herbs are typically amphistomatous ( Muir 2015; 2018). We are developing testable hypotheses for why the fitness benefit of amphistomy is maximized under high light and/or why the fitness cost is highest in the shade ( Muir 2019; 2020).

2. Biologists have known for over a century that stomatal sizes negatively covaries with density. As part of an international collaboration, I used biophysical and macroevolutionary quantitative genetic theory to show that a common statistical approach has been leading to incorrect inferences. Applying an alternative method supported by our theory and simulations, we overturn the prevailing view that stomatal size and density are constrained by limited epidermal space. Instead, the pattern of covariation is consistent with lack of selection for toward extremely low or high capacity for gas exchange ( Liu et al. In review).