The Early Evolution of Tudor Genes in Holozoa and How Their Distribution Was Influenced by Life History Traits in Metazoa

Early metazoan evolution was characterized by the expansion of multiple gene families, such as the Tudor family, involved in novel multicellularity-related functions. In eukaryotes, Tudor genes (i.e. genes including at least one Tudor domain) are numerous, heterogeneous, and mostly associated with gene expression regulation. However, they underwent an animal-specific expansion, with novel elements almost exclusively involved in retrotransposon regulation through Piwi-interacting RNAs, as spatiotemporal regulators of the key-element Piwi, another previously considered animal-specific gene. Here, we used online-Available proteomes covering 25 major taxonomic groups to characterize the Tudor gene family at a holozoan-wide level, confirming the apomorphic metazoan expansion of Piwi-interacting RNA-related Tudor genes. However, we also annotated elements of the Piwi-interacting RNA pathway (Tudor and Piwi genes) in Ichthyosporea species, suggesting that elements of the Piwi-interacting RNA pathway were already present in the holozoan common ancestors. We observed an outstanding variability (34-fold) of Tudor gene number between and within metazoan phyla that could be associated with convergent genomic and phenotypic evolutions: expansions were usually sided by whole-genome duplications and/or life history traits such as parthenogenesis; reductions were mostly associated to overall phenotypic and genomic simplifications, like in almost all considered endoparasites. Lastly, we phylogenetically tested, and mostly (but not completely) confirmed, a previously proposed model for the evolution of the Tudor domain secondary structures.