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The protection of vulnerable developing structures evolved repeatedly in terrestrial organisms and includes, among others, viviparity in animals and the seed in land plants. In mushroom-forming fungi (Agaricomycetes), sexual spores are born on fruiting bodies, the growth of which is a complex developmental process that is exposed to environmental factors (e.g., desiccation, fungivorous animals). Mushroom-forming fungi evolved a series of innovations in fruiting body protection, however, how these emerged is obscure, leaving the evolutionary principles of fruiting body development poorly known. Here, we show that developmental innovations that lead to the spore-producing surface (hymenophore) being enclosed in a protected environment display asymmetry in their evolution and are associated with increased diversification rates. 'Enclosed' development evolved convergently and became a dominant developmental type in several clades of mushrooms. This probably mirrors spore production benefits for species with protected fruiting body initials, by better coping with environmental factors. Our observations highlight new morphological traits associated with mushroom diversification that parallel the evolution of protection strategies in other organisms, such as viviparity or the seed in animals or plants, respectively, but in the context of spore development, highlighting the general importance of protecting vulnerable progeny across the tree of life.

Multicellularity has been one of the most important innovations in the history of life. The role of gene regulatory changes in driving transitions to multicellularity is being increasingly recognized; however, factors influencing gene expression patterns are poorly known in many clades. Here, we compared the developmental transcriptomes of complex multicellular fruiting bodies of eight Agaricomycetes and Cryptococcus neoformans, a closely related human pathogen with a simple morphology. In-depth analysis in Pleurotus ostreatus revealed that allele-specific expression, natural antisense transcripts, and developmental gene expression, but not RNA editing or a ‘developmental hourglass,’ act in concert to shape its transcriptome during fruiting body development. We found that transcriptional patterns of genes strongly depend on their evolutionary ages. Young genes showed more developmental and allele-specific expression variation, possibly because of weaker evolutionary constraint, suggestive of nonadaptive expression variance in fruiting bodies. These results prompted us to define a set of conserved genes specifically regulated only during complex morphogenesis by excluding young genes and accounting for deeply conserved ones shared with species showing simple sexual development. Analysis of the resulting gene set revealed evolutionary and functional associations with complex multicellularity, which allowed us to speculate they are involved in complex multicellular morphogenesis of mushroom fruiting bodies.