Tudor genes of Holozoa: Early evolution and within Metazoa diversification of a multifaceted protein family

Early metazoan evolution was characterized by the expansion of many gene families involved in novel multicellularity-related functions, like the Tudor family. In eukaryotes, Tudor genes are numerous and heterogeneous, mostly associated with gene expression regulation. However, the family underwent a lineage-specific expansion in animals, with novel elements almost exclusively involved in the germline-specific regulation of retrotransposons through piRNAs (as spatiotemporal regulators of the key-element Piwi, another previously supposedly animal-specific gene). In the present analysis, we used online-available proteomes for a total of 25 major taxonomic groups to characterize the Tudor gene family at a holozoan-wide level, and we confirmed the apomorphic expansion of piRNA-related Tudor genes in animals. However, we could also interestingly observe the presence of elements of the piRNA pathway, both Tudor and Piwi genes, in some Ichthyosporea species, suggesting that some elements of the pathway were already present in the last common ancestor of Holozoa. Moreover, we observed an outstanding variability (34-fold) of Tudor gene number both 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, possibly leading to the expansion of retrotransposon silencing pathways. Reductions were instead mostly associated with overall phenotypic and genomic simplifications, like almost all endoparasites of our dataset. Lastly, we phylogenetically tested a previously proposed model for the evolution of the three possible secondary structures of the Tudor domains and we could mostly (but not completely) confirm the model.