Below-ground plant-fungus network topology is not congruent with above-ground plant-animal network topology

Abstract

In nature, plants and their pollinating and/or seed-dispersing animals form complex interaction networks. The commonly observed pattern of links between specialists and generalists in these networks has been predicted to promote species coexistence. Plants also build highly species-rich mutualistic networks below ground with root-associated fungi, and the structure of these plant–fungus networks may also affect terrestrial community processes. By compiling high-throughput DNA sequencing data sets of the symbiosis of plants and their root-associated fungi from three localities along a latitudinal gradient, we uncovered the entire network architecture of these interactions under contrasting environmental conditions. Each network included more than 30 plant species and hundreds of mycorrhizal and endophytic fungi belonging to diverse phylogenetic groups. The results were consistent with the notion that processes shaping host-plant specialization of fungal species generate a unique linkage pattern that strongly contrasts with the pattern of above-ground plant–partner networks. Specifically, plant–fungus networks lacked a “nested” architecture, which has been considered to promote species coexistence in plant–partner networks. Rather, the below-ground networks had a conspicuous “antinested” topology. Our findings lead to the working hypothesis that terrestrial plant community dynamics are likely determined by the balance between above-ground and below-ground webs of interspecific interactions.