Phylogeny and gene function integration uncovers multiple convergences in multicellular and terrestrial transitions

In the biodiversity genomics era, vast gene catalogs have rapidly accumulated, but how gene functions map onto major evolutionary transitions remains vague. We integrated phylogenomics with functional annotations to trace the emergence of [~]4.5 million genes and their associated functions in 508 representative species across the tree of life. Using this top-down, function-centric approach, we mapped the evolutionary history of well-annotated biological functions, revealing key insights and widespread parallelism. For instance, the largest bursts of gene and function gains aligned with key evolutionary transitions, including the origins of eukaryotes, animals, land plants, and vertebrates. Independent transitions to multicellularity and terrestrial life showed convergent enrichment of semantically similar functions (involving entirely different gene families), and the presence of orthologous genes often belonging to ancient gene families. For example, terrestrialization nodes in slime molds, plants, and animals coincided with gains in stress-tolerance and developmental genes, whereas multicellularity in animals, fungi, plants, and slime molds consistently involved expansions in cell-adhesion and communication functions. Thus, our framework enables scalable interpretation of new genomes in an evolutionary context and offers a roadmap for exploring the genomic basis of biodiversity.