Ecological and evolutionary responses of earthworm holobionts to environmental changes

Abstract

Global environmental change substantially affects soil detritivores, including earthworms, impacting host-microbiota interactions and altering key soil biogeochemical processes such as litter decomposition. As microbial communities are inherently capable of rapid evolution, responses of earthworms and associated microbiota (i.e., earthworm holobionts) to global environmental change may likely involve the interplay of ecological and evolutionary processes and feedbacks. Although species-level responses of earthworms to global environmental change are well-studied, the potential ecological and evolutionary responses of earthworm holobionts to environmental change remain unexplored. Here, we provide a conceptual framework to elaborate on the complex network of earthworm host−microbiota interactions that modify their traits in response to global environmental change, jointly shaping their ecology and evolution. Based on literature, we synthesize evidence of global environmental change impacts on earthworm host-microbiota and discuss evidence of their ecological and evolutionary responses to environmental change. Lastly, we highlight the agro- and eco-system level consequences of environmental change-mediated shift in earthworm host-microbiota functions. Soil legacies of environmental change have cascading detrimental impacts on the abundance, diversity, and functional dynamics of earthworm host-microbiota interactions in agriculture and ecosystems. The primary mechanisms driving such responses of earthworm hosts and associated microbial communities to environmental change include altered litter quality and host dietary preferences, competitive interactions and exclusion, habitat homogenization, and a shift in soil physicochemical and biological processes. Therefore, advancing knowledge of the intricate animal-microorganism interactions is crucial for belowground biodiversity management in a changing global environment.