Volume 106, Issue 12
News & Views
Free Access

Endless forms most functional: uncovering the role of natural selection in the evolution of leaf shape

Kathleen G. Ferris

Corresponding Author

E-mail address: kferris@tulane.edu

Department of Ecology and Evolutionary Biology, Tulane University, 6823 St. Charles Avenue, Lindy Boggs Building, Room 400, New Orleans, LA, 70118 USA

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kferris@tulane.edu

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First published: 03 December 2019

“There is grandeur in this view of life, with its several powers, having been originally breathed into a few forms or into one; and that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved.” —Charles Darwin, On the Origin of Species, p. 429

LEAF FORM AND FUNCTION

As the major photosynthetic organ of most plants, leaves are critical to plant fitness. For optimal photosynthetic function, leaves must maintain a tight balance between gas, water, and heat exchange with the surrounding air while maximizing light capture. An organ's form is of paramount functional importance, and leaf shape directly affects the physiological properties of the leaf (Vogel, 1970; Givnish, 1979; Nobel, 1999; Nicotra et al., 2011). The striking diversity of leaf shape across seed plants has long been hypothesized to be adaptive (Nicotra et al., 2011). Yet few studies have detected signatures of natural selection on leaf form, elucidated its adaptive function, or uncovered the environmental variables driving its diversification (but see Bright and Rausher, 2008; Campitelli and Stinchcombe, 2013; Ferris and Willis, 2018; Richards et al., 2019). Uncovering the adaptive significance of leaf shape is difficult because phenotypic variation among plants may have stochastic rather than selective causes. However, combining quantitative genetics, population genomics, and common garden studies can untangle adaptive from neutral processes.

Adaptive hypotheses about leaf shape have proposed both abiotic and biotic factors as potential selective pressures. Leaf shape affects the boundary layer, with lobed and narrow leaves having a thinner boundary layer than rounded entire leaves (Givnish, 1979; Schuepp, 1993). The boundary layer affects the rates of gas, heat, and water exchange between the leaf and atmosphere. Leaves with a thinner boundary layer are cooled or heated more efficiently by convection and closely track ambient air temperature (Vogel, 1970; Schuepp, 1993). Therefore, lobed and narrow leaves are less prone to overheating during the day or freezing on clear nights when leaves radiate heat to the sky (Nobel, 1999). Lobed and dissected leaves also have lower hydraulic resistance than entire leaves because they have fewer minor veins, which could be advantageous in dry environments (Brodribb et al., 2010; Nicotra et al., 2011). Given these physiological effects, complex or elongated leaves are likely adaptive in particularly cold, hot, or dry habitats. Leaf shape may also affect resistance to pathogens and herbivores. Leaves of palatable plant species may mimic leaves of less‐palatable species to deter herbivores (Bright and Rausher, 2008). Another theory is that deeply divided leaves decrease insect feeding efficiency, causing herbivores to prefer plants with entire leaves (Brown and Lawton, 1991). No universal relationship between leaf shape and broad‐scale environmental variation has been found across taxa (Nicotra et al., 2011). This lack suggests that leaf shape may be more critical at the microhabitat level.

IS LEAF SHAPE ADAPTIVE?

Whether leaf shape is under selection has been investigated using phylogenetic comparative methods, within‐species clinal variation, and phenotypic selection analysis. In Pelargonuim and Viburnum, phylogenetically controlled comparisons have found that the evolution of lobed leaves is associated with xeric habitats, while in the Poaceae narrower leaved‐species occupy more open habitats (Jones et al., 2009; Schmerler et al., 2012; Mitchell et al., 2015; Gallaher et al., 2019). Contrary to theoretical predictions, narrow leaves are associated with higher mean annual precipitation in Protea (Mitchell et al., 2015). Several factors may account for results not consistently aligning with predictions. First, the geographic scale of environmental measurements used in comparative analyses is broad, but natural selection acts on individuals experiencing their local environment. Therefore, there is a discordance between the scale of environmental data used in comparative analyses (macroclimatic) and the microclimatic scale at which adaptation occurs. Second, most phylogenetic comparisons have been based on field‐collected leaves whose shape is influenced by both genetic and environmental variation. Environmentally induced phenotypic plasticity may create noise in comparative leaf shape analyses, making a universal trend hard to detect.

While the comparative method identifies patterns at a broad evolutionary scale, population and quantitative genetics approaches identify signatures of selection on within‐species variation in leaf shape. Clinal analysis, the coincidence of phenotypic and environmental clines, is a classic test for natural selection. Many clines in leaf shape have been identified along environmental gradients in natural populations (Wyatt and Antonovics, 1981; Gurevitch, 1988; Bright, 1998; Brennan et al., 2009). However, without genetic data, it is impossible to discern whether these clines are due to neutral population structure or selection. Clinal analysis with genetic and phenotypic data and QSTFST analysis are methods that compare patterns of phenotypic to neutral genetic variation in natural populations. If phenotypic patterns are explained by environmental variation rather than neutral population structure, then selection is likely at work. These approaches have detected selection on leaf form in a latitudinal cline of Ipomea hederaceae across eastern North America (Campitelli and Stinchcombe, 2013), and an altitudinal cline in a Senecio‐hybrid zone on Mt. Etna (Brennan et al., 2009). In I. hederaceae, northern populations are fixed for lobed leaf shape, while in Senecio plants with dissected leaves occur at low, warmer elevations. One issue with these methods is that while controlling for neutral genetic structure reduces the likelihood of false positives, the probability of a false negative is increased since patterns of locally varying selection may correlate with neutral population structure (e.g., in local adaptation between discreet populations). Additionally, if leaves are field‐collected for clinal methods, then as in comparative analyses, plastic variation may obscure or falsely enhance signals of selection.

Phenotypic selection analysis uses multiple linear regression to detect signatures of selection on quantitative traits (Lande and Arnold, 1983). Combining phenotypic selection analysis with controlled crosses in a common garden is particularly powerful since crosses break up existing trait correlations in parental populations and common gardens control for environmental variation (Lexer et al., 2003). Therefore, the fitness effects of leaf shape can be measured against a randomized genetic background. In studies of reciprocal transplants using experimental hybrids, spatially varying selection on leaf shape was found within populations of Ipomea hederaceae (Bright, 1998; Bright and Rausher, 2008), the Mimulus guttatus species complex (Ferris and Willis, 2018), and the Senecio lautus species complex (Richards et al., 2019). Through experimental manipulation in the field, Bright (1998) further discovered that lobed‐leaved plants of I. hederaceae were more resistant to fungal pathogens. Limitations of this approach relate to feasibility. Transplants can only measure selection at a handful of discrete locations and are best suited to studies of annuals or short‐lived perennials. Leaf‐shape variation in long‐lived plants or over macrogeographic ecological gradients will be difficult to study using these methods. Furthermore, while these studies demonstrated that leaf‐shape variation is under natural selection, few have elucidated causal links between environmental variables and leaf shape or delimited its adaptive function (but see Bright, 1998).

WHERE DO WE GO FROM HERE?

It is clear from the contemporary literature that leaf shape is frequently under natural selection. Therefore, consistent with theoretical predictions, variation in leaf shape does affect fitness, but why and how are still unclear. Is leaf‐shape variation adaptive due to its effect on the boundary layer? Or hydraulic resistance? Are water and temperature the driving selective variables? Or do biotic interactions or uninvestigated factors (e.g., soil chemistry) drive patterns of shape variation? In comparative and clinal analyses that test for adaptation across broader geographic scales, the direction of selection seems to differ across taxa. Different shapes are seemingly selected for in similar habitats in different genera (Brennan et al., 2009; Jones et al., 2009; Schmerler et al., 2012; Campitelli and Stinchcombe, 2013; Mitchell et al., 2015; Gallaher et al., 2019), indicating that multiple shapes may be adaptive in the same environment. Another explanation for these conflicting results is that we do not know what drives leaf‐shape evolution, and we are therefore measuring the wrong environmental factors or the right factors at the wrong geographic scale. For example, different ecological variables may be controlling macro‐ vs. microevolution in leaf shape. In addition, while the influence of spatially varying selection has been tested, the affects of temporally fluctuating or periodic selection on the evolution of leaf shape are virtually unknown.

Each approach used to determine the adaptive significance of leaf shape has strengths and weaknesses. However, let us start small, for when we zoom out too far, we may miss many interesting patterns. Adaptive evolution begins with the generation and maintenance of genetic variation within a single population. Quantitative genetic techniques can test whether leaf‐shape polymorphisms are under selection within a population (e.g., Bright and Rausher, 2008). These approaches control for environmentally induced phenotypic variation and neutral genetic population structure and focus on local ecological factors that directly impact plant fitness. Experimental manipulations can be added to determine which environmental variables are driving selection and to identify the functional consequences of leaf‐shape variation (Wade and Kalisz, 1990; Bright, 1998). Once the botanical community understands within‐population variation in leaf shape, then we can progress to studying divergent selection on leaf shape between populations and species. A comprehensive picture of the adaptive significance of leaf shape will be best painted by integrating broad‐scale comparative analyses, population and quantitative genetics approaches, and experimental manipulation of biotic and abiotic variables all in the same genus (Fig. 1).

image
Leaf‐shape variation in the Mimulus guttatus species complex at all evolutionary levels within the same genus. Mimulus provides an ideal opportunity to examine selection on leaf shape within a single population, across populations within a single species, and between species. (A) Leaf‐shape variation within the Black Diamond Road (BDR) population of M. guttatus from a serpentine outcrop in Mendocino County, California (K. Ferris, unpublished data). (B) Leaf‐shape variation across populations of Mimulus laciniatus from along an altitudinal gradient in the Sierra Nevada, California (K. Ferris, unpublished data). (C) Variation in leaf shape across species in the M. guttatus species complex. From left to right leaf images are from two populations of M. guttatus, M. filicifolius, M. nudatus, and M. laciniatus (Ferris et al., 2015). Leaves in Figure 1 were collected from plants grown in a common environment, indicating that shape differences are due to genetic and not environmental differences.

ACKNOWLEDGMENTS

I thank the Editor‐in‐Chief, Pamela Diggle, and two anonymous reviewers for their time and thoughtful feedback on earlier versions of this manuscript. Their insightful comments were incorporated and resulted in a greatly improved final version.