Selection constrains phenotypic evolution in a functionally important plant trait

Selection constrains phenotypic evolution in a functionally important plant trait
Christopher D Muir

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.


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