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Abstract

Background: The emergence of new genes is an important driver of evolutionary novelty. Yet, we lack a conceptual and computational approach that accurately traces gene-family founder events and effectively associates them with trait innovation and major radiation events.
Results: We present GenEra (https://github.com/josuebarrera/GenEra), a DIAMOND-fuelled gene-family founder inference framework that addresses previously raised limitations and biases of founder gene detection in genomic phylostratigraphy by accounting for homology detection failure (HDF), accelerating gene-family founder computations from several months to a few days for any query genome of interest. We analyzed 30 genomes to explore the emergence of new gene families during the major evolutionary transitions in plants, animals, and fungi. The detection of highly conserved protein domains in these gene families indicate that the neofunctionalization of pre-existing protein domains is a richer source of gene-family founder events compared to de novo gene birth. We report vastly different patterns of gene-family founder events in animals and fungi before and after accounting for HDF, while only plants show a consistent pattern of gene-family emergence after accounting for HDF. We show that the transition to multicellularity in streptophytes, the terrestrialization of land plants and the origin of angiosperms are associated with gene-family founder bursts; as well as the evolution of bilateral symmetry in animals.
Conclusions: Our results indicate that the impact of HDF on the inferred patterns of gene emergence is lineage-dependent, suggesting that plants are more likely to evolve novelty through the emergence of new genes compared to animals and fungi.