Divergent genomic trajectories predate the origin of animals and fungi

Animals and fungi have radically distinct morphologies, yet both evolved within the same eukaryotic supergroup: Opisthokonta(1)(,2). Here we reconstructed the trajectory ofgenetic changesthat accompanied the origin of Metazoa and Fungi since the divergence of Opisthokonta with a dataset that includes four novel genomes from crucial positions in the Opisthokonta phylogeny. We showthat animals arose only after the accumulation ofgenes functionally important for their multicellularity, a tendency that began in the pre-metazoan ancestors and later accelerated in the metazoan root. By contrast, the pre-fungal ancestors experienced net losses of most functional categories, including those gained in the path to Metazoa. On a broad-scale functional level, fungal genomes contain a higher proportion of metabolic genes and diverged less from the last common ancestor of Opisthokonta than did the gene repertoires of Metazoa. Metazoa and Fungi also show differences regardinggene gain mechanisms. Gene fusions are more prevalent in Metazoa, whereas a larger fraction of gene gains were detected as horizontal gene transfers in Fungi and protists, in agreement with the long-standing idea that transfers would be less relevant in Metazoa due to germline isolation(3-)(5). Together, our results indicate that animals and fungi evolved undertwo contrasting trajectories ofgenetic change that predated the origin of both groups. The gradual establishment oftwo clearly differentiated genomic contexts thus set the stage for the emergence of Metazoa and Fungi.

Automated summary

Animals and fungi have distinct morphologies and genetic changes. Animals gained important genes from pre-metazoan ancestors, while fungi experienced net losses in functional categories. Fungal genomes have more metabolic genes and show less divergence from the Opisthokonta ancestor compared to animals. Gene fusions are more prevalent in animals, while horizontal gene transfers are more common in fungi and protists.