Macroevolutionary constraints to tolerance: trade‐offs with drought tolerance and phenology, but not resistance

Abstract

Plant tolerance of herbivory, i.e., the ability to recover after damage, is an important component of how plants cope with herbivores. Tolerance has long been hypothesized to be constrained evolutionarily by plant resistance to herbivores, traits that allow plants to cope with stressful growing conditions, and traits that influence the timing of damage in relation to reproduction. Variation in tolerance and resistance can be caused by differences in the identity of the plant (e.g., genotype, species, clade) and by the context of the herbivore threat (e.g., identity of the herbivore, type of damage it causes, abiotic conditions in which the plant is growing). To date, the vast majority of studies have explored trade-offs with tolerance within species. Here, we test hypotheses of constraints on tolerance using comparative approaches in a clade of mustards, emphasizing the variety of contexts in which damage is realistically tolerated. We estimated tolerance to leaf damage, tolerance to apical clipping at the bolting stage - simulating browsing -, and resistance to a specialist and generalist lepidopteran herbivore for a group of native mustards, grown in field soils unique to each population and in a common potting soil. Resistance to herbivores was soil dependent, while surprisingly, tolerance was not. Phylogenetic signal in resistance to specialist and generalist lepidopteran herbivores was present, but only when plants were grown in field soils. Tolerance had low phylogenetic signal. Tolerance to leaf damage was unrelated to tolerance to simulated browse. We found no evidence for a resistance-tolerance trade-off, and some evidence for a soil-dependent positive correlation between tolerance and resistance to both herbivores. Drought-tolerant species had poorer ability to tolerate browse damage, and earlier flowering species tended to be less tolerant to leaf damage. Our results suggest that tolerance trades off with traits that allow mostly annual, monocarpic Streptanthus (s.l.) to persist in drought-prone conditions but is largely unrelated to resistance to herbivores. Our study highlights a need for a new framework for tolerance to herbivory that explicitly acknowledges that the relationship among tolerance, resistance, and traits that ameliorate abiotic stress.

Resistance and Tolerance to Root Herbivory in Maize Were Mediated by Domestication, Spread, and Breeding

“…Our results addressing the effects of maize domestication and spread on defense strategy evolution were consistent with theoretical predictions concerning resistance and tolerance evolution in the contexts of plant productivity-resistance trade-offs and plant resistance-tolerance trade-offs, respectively (Agrawal et al, 2010;Pearse et al, 2017;Zust and Agrawal, 2017).…”

Resistance and Tolerance to Root Herbivory in Maize were Mediated by Domestication, Spread, and Breeding

“…Our results addressing the effects of maize domestication and spread on defense strategy evolution were consistent with theoretical predictions concerning resistance and tolerance evolution in the contexts of plant productivity-resistance trade-offs and plant resistance-tolerance trade-offs, respectively (Agrawal et al, 2010;Pearse et al, 2017;Zust and Agrawal, 2017). Namely, our results showed that resistance to WCR decreased with both maize domestication and spread, and tolerance increased as resistance decreased, as expected.…”

Overcompensation: a 30‐year perspective

“…In this Special Feature, Pearse et al. () estimated tolerance to folivory, tolerance to “browsing” (through clipping), and resistance to two lepidopteran herbivores for a number of species in the Streptanthus clade. Using phylogenetically informed analyses, they found that tolerance was not constrained by phylogeny.…”

“…The ecological context is known to affect the magnitude and even the direction of plant tolerance (Abrams 1987, Chamberlain et al 2014, Garcia and Eubanks 2019, Pearse et al 2017, Poveda et al 2018. As an example, the indirect positive effects of herbivores on plant performance are mediated by improved soil nutrient pools or by the removal of competitors (de Mazancourt et al 2001).…”

“…To date, nearly all comparisons of tolerance among species rely on meta-analysis of tolerance studies and comparisons between plants from disparate plant families (but see Agrawal and Fishbein 2008). In this Special Feature, Pearse et al (2017) estimated tolerance to folivory, tolerance to "browsing" (through clipping), and resistance to two lepidopteran herbivores for a number of species in the Streptanthus clade. Using phylogenetically informed analyses, they found that tolerance was not constrained by phylogeny.…”