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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.
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Mite Domatia and Associated Mite Density in a North American Eastern Deciduous Forest in Michigan
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.
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- Award ID(s):
- 2236747
- PAR ID:
- 10603869
- Publisher / Repository:
- Ecology and Evolution
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 15
- Issue:
- 4
- ISSN:
- 2045-7758
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Abstract Context Habitat fragmentation is a leading threat to biodiversity, yet the impacts of fragmentation on most taxa, let alone interactions among those taxa, remain largely unknown. Objectives We studied how three consequences of fragmentation—reduced patch connectivity, altered patch shape, and edge proximity—impact plant-dwelling mite communities and mite-plant-fungus interactions within a large-scale habitat fragmentation experiment. Methods We sampled mite communities from the leaves of Quercus nigra (a plant species that has foliar domatia which harbor fungivorous and predacious mites) near and far from edge within fragments of varying edge-to-area ratio (shape) and connectivity via corridors. We also performed a mite-exclusion experiment across these fragmentation treatments to test the effects of mite presence and fungal hyphal abundance on leaf surfaces. Results Habitat edges influenced the abundance and richness of leaf-dwelling mites; plants closer to the edge had higher mite abundance and species richness. Likewise, hyphal counts were higher on leaves near patch edges. Despite both mite and fungal abundance being higher at patch edges, leaf hyphal counts were not impacted by mite abundance on those leaves. Neither patch shape nor connectivity influenced mite abundance, mite species richness, or the influence of mites on leaf surface fungal abundance. Conclusion Our results suggest that mites and foliar fungi may be independently affected by edge-structured environmental gradients, like temperature, rather than trophic effects. We demonstrate that large-scale habitat fragmentation and particularly edge effects can have impacts on multiple levels of microscopic communities, even in the absence of cascading trophic effects.more » « less
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Summary Here, we investigated the molecular genetic basis of mite domatia, structures on the underside of leaves that house mutualistic mites, and intraspecific variation in domatia size inVitis riparia(riverbank grape).Domatia and leaf traits were measured, and the transcriptomes of mite domatia from two genotypes ofV. ripariawith distinct domatia sizes were sequenced to investigate the molecular genetic pathways that regulate domatia development and intraspecific variation in domatia traits.Key trichome regulators as well as auxin and jasmonic acid are involved in domatia development. Genes involved in cell wall biosynthesis, biotic interactions, and molecule transport/metabolism are upregulated in domatia, consistent with their role in domatia development and function.This work is one of the first to date that provides insight into the molecular genetic bases of mite domatia. We identified key genetic pathways involved in domatia development and function, and uncovered unexpected pathways that provide an avenue for future investigation. We also found that intraspecific variation in domatia size inV. ripariaseems to be driven by differences in overall leaf development between genotypes.more » « less
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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.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1002/ece3.71379
