Making pore choices: repeated regime shifts in stomatal ratio

Abstract

Ecologically important traits do not evolve without limits. Instead, evolution is constrained by the set of available and viable phenotypes. In particular, natural selection may only favour a narrow range of adaptive optima constrained within selective regimes. Here, I integrate data with theory to test whether selection explains phenotypic constraint. A global database of 599 plant species from 94 families shows that stomatal ratio, a trait affecting photosynthesis and defence against pathogens, is highly constrained. Most plants have their stomata on the lower leaf surface (hypostomy), but species with half their stomata on each surface (amphistomy) form a distinct mode in the trait distribution. A model based on a trade-off between maximizing photosynthesis and a fitness cost of upper stomata predicts a limited number of adaptive solutions, leading to a multimodal trait distribution. Phylogenetic comparisons show that amphistomy is the most common among fast-growing species, supporting the view that CO 2 diffusion is under strong selection. These results indicate that selective optima stay within a relatively stable set of selective regimes over macroevolutionary time.

Paleoecology, Ploidy, Paleoatmospheric Composition, and Developmental Biology: A Review of the Multiple Uses of Fossil Stomata

“…Instead, we advocate the use of quantitative traits that provide comparative estimates of water use efficiency, maximum gas exchange capacity, and leaf level transpiration of co-occurring fossil taxa within a fossil assemblage. Finally, of all the possible stomatalbased traits that can be observed in fossils, it appears that quantitative assessment of stomatal distribution across both leaf surfaces (Muir's stomatal distribution ratio; Muir, 2015) together with estimated genome size (Beaulieu et al, 2008) will yield meaningful inferences on relative growth rate and plant habit and help to assess hypotheses on the likely growth form of extinct taxa.…”

“…In Proteaceae, amphistomaty is strongly associated with open vegetation (Jordan et al, 2014), leading to the suggestion that amphistomaty may be a good proxy for an open habitat. However, Muir (2015) argues that the adaptive significance of this relatively rare stomatal distribution (,10% of modern global flora are amphistomatic) relates most strongly to life history traits such as relative growth rate. Annuals, biennials, and perennials were shown to have a much greater frequency of species that were amphistomatous than shrubs and trees across 599 species and 94 families (Muir, 2015).…”

“…However, other aspects of stomatal development, such as amphistomaty or specifically the ratio of abaxial to adaxial stomatal density (sensu; Muir, 2015), look more promising for broader application to the fossil record to interpret paleoecology, including habit and habitat. Herbaceous taxa are believed to be very poorly represented in the fossil record yet many fossil plant assemblages over the past 400 million years are characterized by an unusually high proportion of amphistomatous taxa compared with the modern flora (e.g.…”

“…Could these differences observed within Medullosales stomatal complex type reflect changes in the relative growth rate of the fronds belonging to different species? It certainly appears as though detailed assessment of fossil stomatal complex developmental pathways (Rudall et al, 2013) together with quantitative paleoecological traits such as the ratio of amphistomaty (SD adaxial surface/SD abaxial surface; Muir, 2015) have the potential to yield important insights on plant habit in the future.…”

Examining plant physiological responses to climate change through an evolutionary lens

“…These general themes may be true for other plant physiological traits that mediate plant responses to environmental change. For example, recent work using a phylogenetic approach suggests that adaptation in leaf stomatal ratio is associated with environmental conditions and selection for fast growth rate, yet it is also subject to constraints mediated by tradeoffs between photosynthetic rate and biotic interactions (Muir, 2015). As studies on evolutionary patterns in plant physiology accumulate, an important goal will be to synthesize mechanistic and phylogenetic studies and fossil evidence in order to characterize and predict macroevolutionary responses to climate change (Rothwell et al, 2014).…”