Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

ABSTRACT Complex multicellularity represents the most advanced level of biological organization and it has evolved only a few times: in metazoans, green plants, brown and red algae and fungi. Compared to other lineages, the evolution of multicellularity in fungi follows different principles; both simple and complex multicellularity evolved via unique mechanisms not found in other lineages. Herein we review ecological, palaeontological, developmental and genomic aspects of complex multicellularity in fungi and discuss general principles of the evolution of complex multicellularity in light of its fungal manifestations. Fungi represent the only lineage in which complex multicellularity shows signatures of convergent evolution: it appears 8–11 times in distinct fungal lineages, which show a patchy phylogenetic distribution yet share some of the genetic mechanisms underlying complex multicellular development. To explain the patchy distribution of complex multicellularity across the fungal phylogeny we identify four key observations: the large number of apparently independent complex multicellular clades; the lack of documented phenotypic homology between these clades; the conservation of gene circuits regulating the onset of complex multicellular development; and the existence of clades in which the evolution of complex multicellularity is coupled with limited gene family diversification. We discuss how these patterns and known genetic aspects of fungal development can be reconciled with the genetic theory of convergent evolution to explain the pervasive occurrence of complex multicellularity across the fungal tree of life.