The macroevolutionary dynamics of symbiotic and phenotypic diversification in lichens

Abstract

Symbioses are evolutionarily pervasive and play fundamental roles in structuring ecosystems, yet our understanding of their macroevolutionary origins, persistence, and consequences is incomplete. We traced the macroevolutionary history of symbiotic and phenotypic diversification in an iconic symbiosis, lichens. By inferring the most comprehensive time-scaled phylogeny of lichen-forming fungi (LFF) to date (over 3,300 species), we identified shifts among symbiont classes that broadly coincided with the convergent evolution of phylogenetically or functionally similar associations in diverse lineages (plants, fungi, bacteria). While a relatively recent loss of lichenization in Lecanoromycetes was previously identified, our work instead suggests lichenization was abandoned far earlier, interrupting what had previously been considered a direct switch between trebouxiophycean and trentepohlialean algal symbionts. Consequently, some of the most diverse clades of LFF are instead derived from nonlichenized ancestors and re-evolved lichenization with Trentepohliales algae, a clade that also facilitated lichenization in unrelated lineages of LFF. Furthermore, while symbiont identity and symbiotic phenotype influence the ecology and physiology of lichens, they are not correlated with rates of lineage birth and death, suggesting more complex dynamics underly lichen diversification. Finally, diversification patterns of LFF differed from those of wood-rotting and ectomycorrhizal taxa, likely reflecting contrasts in their fundamental biological properties. Together, our work provides a timeline for the ecological contributions of lichens, and reshapes our understanding of symbiotic persistence in a classic model of symbiosis.