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Abstract PremiseCalcium oxalate biomineralization in plants is phylogenetically widespread and morphologically diverse, but the function of these inorganic crystals is an area of active debate. The variety of environmental conditions that produce the crystals, as well as the inconsistent evidence that they provide antiherbivore defense across plant and herbivore species, suggests that different crystal morphologies might have different functions. MethodsUsingVitis riparia, or riverbank grape, we experimentally investigated the environmental influence of excess calcium and simulated herbivory on the formation of calcium oxalate druse and raphide crystals in leaves. We also investigated the putative defensive function of these crystals by using a no‐choice herbivore bioassay manipulating herbivore diet composition to test for impacts of crystal shape on herbivore growth, both on its own and with plant chemistry. ResultsWe found that the addition of calcium to soil increased the density of both raphide and druse crystals inV. riparialeaves. Contrary to expectations, the herbivory treatment decreased the density of raphides in leaves, andV. riparia‐derived crystals did not impact weight gain, time to pupation, or survival of moth larvae. ConclusionsOur multifaceted test of the formation and function of calcium oxalate crystals in riverbank grape demonstrates that an abiotic factor (i.e., soil calcium) is a relatively stronger determinant of crystal production and that, contrary to hundreds of years of speculation on their function, these crystals do not seem to mediate plant‐insect herbivory in all plant taxa. Instead, the alternative hypothesis of calcium regulation was supported by our experimental evidence. 

Abstract Mite domatia — small structures on plant leaves that house mutualistic mites — are widespread across plants yet remain relatively understudied. Here we investigate the chemistry and micromorphology of mite domatia across sympatric species of broadleaf deciduous woody species that have convergently evolved tuft-form mite domatia. Specifically, we test whether domatia display similar micromorphological and chemical properties using metabolomics and scanning electron microscopy across multiple independent sympatric lineages. To identify domatia-specific phenotypes, we also compare tissue within domatia to that of nearby leaf tissue on each of the four domatium-bearing species, and test whether species with domatia exhibit reduced chemical defense relative to species that lack domatia using four additional species that lack prominent domatia as a control. We found that domatium-bearing species had significantly lower total phenolic concentrations and lower total defense compound abundance compared to control species, consistent with an evolutionary trade-off between chemical and mutualistic defense. However, within leaves, domatium tissue chemical defense did not differ from surrounding laminar tissue. In contrast, trichome morphology showed clear convergent modification: domatium trichomes were 24–31% longer than trichomes elsewhere on the leaf, a pattern reversed in control species. Together, our findings shed light on the degree of phenotypic convergence in a widespread, ecologically important trait. 

Abstract Fossilized organisms only represent a small fraction of Earth’s evolutionary history, motivating “ancestral state reconstruction” techniques for inferring unobserved phenotypes of evolving lineages based on measurements of their relatives. Stochastic character mapping has emerged as a particularly powerful approach in this regard, allowing researchers to sample histories of discrete variables on phylogenies and better account for the inherent uncertainty of reconstructed ancestral states. Here, we generalize stochastic character mapping to work with continuous variables by developing an efficient algorithm for sampling evolutionary histories under Brownian motion models with the flexibility to include multiple correlated phenotypes, measurement error, and/or among-lineage variation in evolutionary rates/trends. We implement this “continuous stochastic character mapping” procedure in a new R package called contsimmap and demonstrate potential applications of this technique by developing a novel pipeline for inferring relationships between rates of continuous trait evolution and continuously varying factors (e.g., body size, generation time)—a difficult statistical problem for which relatively few methods are available. After verifying this pipeline’s performance on simulated data, we use it to show that smaller eucalypt trees tend to exhibit higher rates of flower and leaf trait evolution overall, aligning with well-established predictions based on life history theory as well as empirical patterns in other systems. Ultimately, continuous stochastic character mapping is a valuable new tool for analyzing macroevolutionary data, enabling rigorous yet flexible investigation of complex evolutionary dynamics involving continuous traits and/or continuous variables hypothesized to affect evolutionary processes. 

ABSTRACT Many plants engage in indirect defense via tri‐trophic interactions whereby plants provide resources such as food or shelter to mutualists in exchange for protection against herbivores and pathogens, increasing plant fitness. As temperature regimes shift under climate change, understanding the influence of temperature on tri‐trophic defensive interactions is increasingly important. However, where plant species host multiple tri‐trophic defensive interactions, we still lack an understanding of if each interaction, even within the same system, responds in the same way to temperature. In this study, we monitored black cherry (Prunus serotina)seedlings for 10 weeks under ambient and increased temperatures to explore the effects of temperature on two different tri‐trophic defensive interactions between black cherry and: (1) mutualistic leaf domatia‐dwelling mites and leaf fungi; and (2) arthropod predators and herbivores. We found that the positive association between mite abundance and domatia size increased by 8.7% on warmed plants, while warming weakened the positive relationship between mite abundance and the abundance of foliar fungi by 14%, though warmer conditions alone did not affect the abundances of any of these groups. Further, warming increased the abundance of arthropod predators by 116% and decreased the amount of herbivory plants experienced by 42%, but did not modify the impact predators had on herbivory. Ultimately, the differences among interacting species with warming did not translate to differences in plant growth, indicating black cherry can be robust to at least some of the variation in species interactions caused by changing temperatures in the short term. These findings illustrate that warming can modify the abundance of, and relationships between, some but not all tri‐trophic defensive interactions in a given system, further confirming that temperature does not impact plant interactions uniformly. 

ABSTRACT Mite–plant defense mutualisms are among the most common defense mutualisms in the world—yet studies providing basic information on their prevalence in plant communities remain rare. Here, we systematically surveyed common woody plants in a North American deciduous forest for the presence of plant–mite mutualistic interactions. We scored 16 common woody species in a wooded natural area for the presence and number of mite domatia—small structures on the underside of plant leaves that are known to house mutualistic mites. We found that 80% of common woody species in the forest had mite domatia, the highest reported percentage of mite domatia in any survey conducted thus far. We paired our survey with a quantification of the number of mites found on each leaf and investigated the relationship between mite domatia and mite abundance within and across species. We found that plants with mite domatia had significantly more mites on their leaves than species that lacked mite domatia, and that plants with more domatia had more mites. Together, our study provides much needed systematic survey data on plant–mite mutualism prevalence in an important plant community and points to northern temperate forests as a promising system to study plant–mite mutualisms in high densities in the future. 

The processes driving defense trait correlations may vary within and between species based on ecological or environmental contexts. However, most studies of plant defense theory fail to address this potential for shifts in trait correlations across scales. In this work, we tested for correlations between multiple defensive traits (secondary chemistry, carbon to nitrogen ratio, domatia, leaf toughness, trichomes, and pearl bodies) across a common garden of 21Vitisspecies and eighteen genotypes of the speciesVitis ripariato identify when and where patterns of defense trait evolution persist or break down across biological scales. Additionally, we asked whetherVitisdefense trait investment correlates with environmental variables as predicted by plant defense theory, using environmental metrics for eachVitisspecies andV. ripariagenotype from the GBIF and WorldClim databases. We tested for correlations between defense trait investment, herbivore palatability, and environmental variables using phylogenetically informed models. Beyond a few likely physiological exceptions, we observed a lack of significant correlations between defense traits at both intra‐ and interspecific scales, indicating that these traits evolve independently of each other inVitisrather than forming predictable defense syndromes. We did find that investment in carbon:nitrogen (at both scales) and pearl bodies increases with proximity to the equator, demonstrating support for plant defense theory's prediction of higher investment in defenses at more equatorial environments for some, but not all, defense traits. Overall, our results challenge commonly held hypotheses about plant defense evolution, namely the concept of syndromes, by demonstrating that strong correlations between defense traits are not the prevailing pattern both across and withinVitisspecies. Our work also provides the first comprehensive evaluation of the evolutionary divergence in approaches thatVitis, a genus with significant agricultural value, have evolved to defend themselves against herbivores. 

Mutualisms are mediated by adaptive traits of interacting organisms and play a central role in the ecology and evolution of species. Thousands of plant species possess tiny structures called “domatia” that house mites which protect plants from pests, yet these traits remain woefully understudied. Here, we release a worldwide database of species with mite domatia and provide an evaluation of the phylogenetic and geographic distribution of this mutualistic trait. With >2,500 additions based on digital herbarium scans and published reports, we increased the number of known species with domatia by 27% and, importantly, documented their absence in >4,000 species. We show that mite domatia likely evolved hundreds of times among flowering plants, occurring in an estimated ~10% of woody species representing over a quarter of all angiosperm families. Contrary to classic hypotheses about the evolutionary drivers of mutualism, we find that mite domatia evolved more frequently in temperate regions and in deciduous lineages; this pattern is concordant with a large-scale geographic transition from predominantly ant-based plant defense mutualisms in the tropics to mite-based defense mutualisms in temperate climates. Our data also reveal a pattern of evolutionary convergence in domatia morphology, with tuft-form domatia more likely to evolve in dry temperate habitats and pit domatia more likely to evolve in wet tropical environments. We have shown climate-associated drivers of mite domatia evolution, demonstrating their utility and power as an evolutionarily replicated system for the study of plant defense mutualisms.