Many plant species harbour stable within-population polymorphisms in leaf colour, with red (anthocyanic) and green individuals coexisting despite divergent herbivory and carbon gain. Menzies et al. (2016) proposed that in Pseudowintera colorata this polymorphism is maintained by a balance between resistance and tolerance: red leaves are better chemically defended (higher polygodial, an insect antifeedant) and signal this defence visually, suffering less herbivory, while green leaves have substantially higher photosynthetic capacity that may compensate for damage. Because fitness was equal between morphs and photosynthesis was measured only constitutively, the tolerance arm of this balance remains an untested inference. The open problem is to establish directly whether such a resistance–tolerance trade-off maintains leaf colour polymorphism: manipulate and quantify tolerance (compensatory photosynthesis and resource reallocation after herbivory) in red versus green morphs, test the defence–photosynthesis trade-off's generality across other leaf colour polymorphisms, identify the environmental conditions under which the balance equalizes morph fitness, and build evolutionary models integrating resistance and tolerance that predict the distribution of red and green morphs among populations and species.

Background

Leaf colour polymorphism means the coexistence of individuals with differently coloured leaves within a single plant population; the red variants owe their colour to anthocyanins, water-soluble vacuolar pigments that absorb green-yellow light before it reaches the chloroplasts. Why such polymorphisms persist is a classic balancing-selection puzzle: if red leaves were simply better defended, green morphs should be eliminated, and vice versa. Plant-herbivore theory distinguishes resistance, i.e. traits that reduce the amount of damage (chemical defences such as toxins or antifeedants, and visual signals of them), from tolerance, i.e. traits that reduce the fitness impact of a given amount of damage, notably compensatory photosynthesis (an increase in the photosynthetic rate of remaining tissue after herbivory) and reallocation of stored resources to regrowth. A trade-off between investing in resistance and investing in tolerance is expected because both are costly. The warning signal (aposematic signalling) hypothesis predicts that red pigmentation deters herbivores by honestly advertising chemical defence. In the New Zealand shrub Pseudowintera colorata (horopito), whose principal antifeedant is polygodial, a sesquiterpene dialdehyde biosynthesized through the terpenoid pathway independently of anthocyanins, earlier work had shown that leaves with wider red margins contain more polygodial and suffer less herbivory (Cooney et al. 2012). Menzies et al. (2016) extended this to whole-plant colour morphs: redder foliage contained more polygodial and received less insect damage, redder plants hosted 22% fewer lepidopteran leafroller larvae, yet seed production and seed mass did not differ between red and green plants. The likely equalizing force they identified was photosynthesis: green leaves showed about 47% higher light-saturated CO2 assimilation (AsatA_{\text{sat}}) than matched red leaves from neighbouring plants, together with higher chlorophyll concentrations. They therefore proposed that a balance between defence signalling and photosynthesis maintains the polymorphism — a novel mechanism for leaf colour polymorphism — while explicitly noting its limits: the tolerance interpretation was inferred from constitutive photosynthetic differences, not from measurements of damage responses; fitness was compared at a single site in a single season; and no model existed to predict when such a balance would maintain polymorphism rather than drive one morph extinct.

Problem Statement

Determine whether, and under what conditions, a resistance–tolerance trade-off maintains within-species leaf colour polymorphism, as proposed for Pseudowintera colorata by Menzies et al. (2016). The open problem comprises four interconnected components: (1) a direct test of the tolerance arm — experimentally imposing herbivore (or equivalent mechanical) damage on matched red and green morphs and quantifying compensatory photosynthesis and resource reallocation after damage, so that tolerance is measured as a damage response rather than inferred from constitutive assimilation rates, together with the resulting fitness consequences; (2) a test of the generality of the photosynthesis–defence trade-off in at least one other naturally leaf-colour-polymorphic species, measuring defence chemistry, damage, photosynthetic capacity, and fitness in both morphs; (3) an analysis of the environmental conditions (e.g. light, temperature, herbivore pressure gradients) under which the balance equalizes morph fitness and can maintain polymorphism versus driving one morph extinct; and (4) an evolutionary model integrating resistance and tolerance strategies that predicts the distribution of red and green leaf morphs among populations and species. These components share one scientific objective — establishing the mechanism and the conditions for maintenance of leaf colour polymorphism — with the empirical components supplying the parameterization and validation for the model, and the model in turn generalizing the single-system results. A resolution requires components (1)–(4) jointly: the empirical studies (1) and (2) are addressed by specifying and justifying the experimental design, manipulations, and measurements to be taken, and the analytical components (3) and (4) by analysis and modelling.

References

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