Correlation, causation, and the evolution of leaf teeth: A reply to Givnish and Kriebel

We are grateful to Givnish and Kriebel (2017) for providing a thorough review of the arguments that have been advanced to explain the latitudinal gradient in leaf form. Th eir paper was motivated by our recent “On Th e Nature of Th ings” essay presenting the “bud packing hypothesis” (BP) as an alternative explanation for why leaves in the temperate zone are so oft en toothed or lobed ( Edwards et al., 2016 ). Although Givnish and Kriebel (2017) added the BP hypothesis to their list of possible explanations and included it as one of many causal arrows in their synthetic model (see their fi g. 6 ), they were generally unconvinced by our arguments and instead strongly favored the “support and supply hypothesis” (SS) advanced by Givnish almost 40 years ago ( Givnish, 1979 ). Here we present new analyses that question the assumptions of the SS model and elaborate further on the possible connections between teeth and bud packing. Most importantly, we reiterate our plea for studies of bud development. But fi rst, let us note where we seem to agree. We all view leaf boundary layer dynamics, early season photosynthesis, and guttation through hydathodes as unlikely explanations for the latitudinal gradient in leaf margins. Although Givnish and Kriebel portray us as dismissing the idea that spinose teeth might sometimes defend against herbivores, we do not disagree at all. In fact, as we stressed ( Edwards et al., 2016 , p. 975), “Each of these hypotheses has some merit and might apply in particular cases.” As they rightly argued, large herbivores are especially likely to select for spinose teeth in short-statured plants in arid and semiarid environments. Our discussion focused instead on woody plants of mesic forests, where spinose leaves are rare (e.g., Ilex ). Finally, we strongly agree with Givnish and Kriebel that venation architecture deserves far more attention in relation to this problem, and we return to this topic below. However, we disagree with their other main points. Most of the Givnish and Kriebel commentary focused on demonstrating a correlation between leaf thickness and toothy margins, which they present as evidence in favor of the SS model. But, we have never doubted a relationship between leaf thickness and leaf teeth. In fact, Givnish and Kriebel used our data on Viburnum ( Schmerler et al., 2012 ; Chatelet et al., 2013 ) to show this relationship, which we were already well aware of. Because we disagree with their scoring of several species, we re-examined this relationship with a revised data set and recovered an even stronger relationship between thickness and margin type than they originally reported ( Fig. 1 ). However, it is very diffi cult to disentangle leaf thickness and leaf margins from leaf habit and longevity. In Viburnum —and we presume in many other clades—teeth and thickness are also strongly correlated with evolutionary shift s in leaf habit (evergreen vs. deciduous; Fig. 1 ), and, more importantly for our arguments, with changes in the rhythm of leaf production, leaf lifespan, and the extent of leaf development inside of resting buds. Our phylogenetic regression analyses recover a strong association between leaf thickness and margin type ( β = −3.361 ± 0.891 SE, p = 0.0002), but an equally strong relationship between leaf thickness and leaf habit ( β = 3.824 ± 0.944 SE, p = 0.0001), and, as we have shown previously ( Schmerler et al., 2012 ), another very strong relationship between leaf margin type and leaf habit ( p = 2e −12 ). Givnish and Kriebel performed two other analyses along these lines. First, they reduced a ~3500 species data set on leaf form, thickness, and habitat compiled by Royer et al. (2012) to ~600 species to repeat the original analyses in a phylogenetic context. As expected, they found a tight relationship between leaf thickness and margin type. Th ough we do not question this correlation, in general 1 Manuscript received 22 February 2017; revision accepted 30 March 2017. 2 Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman Street, Box G-W, Providence, Rhode Island 02912 USA; 3 Present address: Biomedical Imaging Unit, University of Southampton, Southampton, SO16 6YD, UK; 4 Department of Ecology and Evolutionary Biology, Yale University, P.O. Box 208106, New Haven, Connecticut 06520-8106 USA 5 Author for correspondence (e-mail: erika_edwards@brown.edu), phone: 401.863.2081 doi:10.3732/ajb.1700075 C O M M E N TA R Y