A Global Assessment of Plant-Mite Mutualism and its Ecological Drivers

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Abstract

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 the first 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 previously undescribed pattern of evolutionary convergence in domatia morphology, with tuft-form domatia more likely to evolve in dry temperate habitats and pit domatia were 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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