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Stomata regulate the supply of CO2for photosynthesis and the rate of water loss out of the leaf. The presence of stomata on both leaf surfaces, termed amphistomy, increases photosynthetic rate, is common in plants from high light habitats, and rare otherwise. In this study I use optimality models based on leaf energy budget and photosynthetic models to ask why amphistomy is common in high light habitats. I developed an R packageleafoptimizerto solve for stomatal traits that optimally balance carbon gain with water loss in a given environment. The model predicts that amphistomy is common in high light because its marginal effect on carbon gain is greater than in the shade, but only if the costs of amphistomy are also lower under high light than in the shade. More generally, covariation between costs and benefits may explain why stomatal and other traits form discrete phenotypic clusters.

Stomatal pores control both leaf gas exchange and are an entry for many plant pathogens, setting up the potential for tradeoffs between photosynthesis and defense. To prevent colonization and limit infection, plants close their stomata after recognizing pathogens. In addition to closing stomata, anatmoical shifts to lower stomatal density and/or size may also limit pathogen colonization, but such developmental changes would permanently reduce the gas exchange capacity for the life of the leaf. I developed and analyzed a spatially explicit model of pathogen colonization on the leaf as a function of stomatal size and density, anatomical traits which determine maximum rates of gas exchange. The model predicts greater stomatal size or density increases colonization, but the effect is most pronounced when stomatal cover is low. I also derived scaling relationships between stomatal size and density that preserves a given probability of colonization. These scaling relationships set up a potential conflict between maximizing defense and minimizing stomatal cover. To my knowledge, this is the first mathematical model connecting gas exchange and pathogen defense via stomatal anatomy. It makes predictions that can be tested with experiments and may explain variation in stomatal anatomy among plants. The model is generalizable to many types of pathogens, but lacks significant biological realism that may be needed for accurate predictions.

SummaryIn most plants, stomata are located only on the abaxial leaf surface (hypostomy), but many plants have stomata on both surfaces (amphistomy). High light and herbaceous growth form have been hypothesized to favor amphistomy, but these hypotheses have not been rigourously tested together using phylogenetic comparative methods.I leveraged a large dataset including stomatal ratio, Ellenberg light indicator value, growth form, and phylogenetic relationships for 372 species of British angiosperms. I used phylogenetic comparative methods to test how light and/or growth form influence stomatal ratio and density.High light and herbaceous growth form are correlated with amphistomy, as predicted, but they also interact; the effect of light is pronounced in therophytes (annuals) and perennial herbs, but muted in phanerophytes (shrubs and trees). Furthermore, amphistomy and stomatal density evolve together in response to light.Comparative analyses of British angiosperms reveal two major insights into physiological evolution. First, light and growth form interact to shape variation in stomatal ratio; amphistomy is common under high light, but mostly for herbs. Second, coordinated evolution of adaxial stomatal density and light tolerance indicates that amphistomy is an important adaptation to optimally balance light acquisition with gas exchange. These results advance our understanding of why stomatal ratio evolves and its potential as a functional trait for paleoecology and crop improvement.

Although traditionally separated by different aims and methodologies, research on agricultural and evolutionary problems shares a common goal of understanding the mechanisms underlying functionally important traits. As such, research in both fields offers potential complementary and reciprocal insights. Here, we discuss adaptive stress responses (specifically to water stress) as an example of potentially fruitful research reciprocity, where agricultural research has clearly produced advances that could benefit evolutionary studies, while evolutionary studies offer approaches and insights underexplored in crop studies. We focus on research on Solanum species that include the domesticated tomato and its wild relatives. Integrated approaches to understanding ecological adaptation are particularly attractive in tomato and its wild relatives: many presumptively adaptive phenotypic differences characterize wild species, and the physiological and mechanistic basis of many relevant traits and environmental responses has already been examined in the context of cultivated tomato and some wild species. We highlight four specific instances where these reciprocal insights can be combined to better address questions that are fundamental both to agriculture and evolution.

A long-standing idea is that the macroevolutionary adaptive landscape -- a `map' of phenotype to fitness -- constrains evolution because certain phenotypes are fit, while others are universally unfit. Such constraints should be evident in traits that, across many species, cluster around particular modal values, with few intermediates between modes. Here, I compile a new global database of 599 species from 94 plant families showing that stomatal ratio, an important functional trait affecting photosynthesis, is multimodal, hinting at distinct peaks in the adaptive landscape. The dataset confirms that most plants have all their stomata on the lower leaf surface (hypostomy), but shows for the first time that species with roughly half their stomata on each leaf surface (amphistomy) form a distinct mode in the trait distribution. Based on a new evolutionary process model, this multimodal pattern is unlikely without constraint. Further, multimodality has evolved repeatedly across disparate families, evincing long-term constraint on the adaptive landscape. A simple cost-benefit model of stomatal ratio demonstrates that selection alone is sufficient to generate an adaptive landscape with multiple peaks. Finally, phylogenetic comparative methods indicate that life history evolution drives shifts between peaks. This implies that the adaptive benefit conferred by amphistomy -- increased photosynthesis -- is most important in plants with fast life histories, challenging existing ideas that amphistomy is an adaptation to thick leaves and open habitats. I conclude that peaks in the adaptive landscape have been constrained by selection over much of land plant evolution, leading to predictable, repeatable patterns of evolution.