Mycorrhizal evolution restructures forest ecosystems

Akira Yamawo , Naoto Shinohara, Kohmei Kadowaki, Yuuya Tachiki, Shunsuke Utsumi

Mutualisms are key drivers of species diversification and biodiversity, yet their comprehensive role in shaping contemporary ecosystems remains poorly understood. Mycorrhizal symbioses (Arbuscular mycorrhiza [AM] and Ectomycorrhizal [EcM]) are among the most ecologically important interactions on Earth, driving the origin and maintenance of terrestrial biodiversity. Nearly all tree species associate with these fungi; AM symbiosis, the ancient form, dominates tropical forests, while the later-emerging EcM symbiosis, though taxonomically narrow, primarily influences temperate forests. Previous studies have shown that mycorrhizal type is associated with both tree population density and forest spatial organization. At the population level, EcM trees tend to attain higher local densities than AM trees. At the forest-community level, EcM-rich forests exhibit stronger spatial structuring, characterized by greater conspecific aggregation than the dispersed distributions typically observed in AM-dominated forests. In this paper, we propose the Ecosystem Regime Restructuring by Mycorrhizal Symbiosis (ERRM) hypothesis. Here, we defome am ecosystem regime as the large-scale organization of ecosystems characterized by dominant spatial structures, trophic interactions, and trait syndromes. This hypothesis posits that the evolutionary shifts in mycorrhizal type from AM to EcM have widely altered ecosystem spatial structure, thereby reshaping tree macroevolutionary patterns, driving large-scale ecosystem reorganization, and creating distinct ecological and evolutionary contexts. Dispersed AM trees typically favor long-range biotic seed dispersal and biotic pollination. Clustered EcM trees, conversely, favor wind pollination and short-range wind dispersal. This suggests joint evolution between mycorrhizal type and reproductive/dispersal modes. Spatial structure also influences plant defense strategies: clustered EcM trees may tend to display a higher carbon-to-nitrogen ratio and carbon-based quantitative defenses. AM trees may be associated with higher nutrient content and qualitative chemical defenses like alkaloids. These contrasting defense strategies may reflect differences in herbivore encounter rates determined by the spatial structure of AM and EcM communities. Furthermore, the dense, stable resource environment provided by EcM clusters facilitates the evolution of specialized herbivores. We present this novel hypothesis with an empirical dataset partially supporting it. Finally, we argue that the ERRM hypothesis provides the fundamental framework toward a new understanding of the present ecosystem regime with an integrative approach combining phylogenetic analysis, macroecology, and experimental studies.