Domain-Shuffling in the Evolution of Cyclostomes and Gnathostomes.

Vertebrates acquired various novel traits that were pivotal in their morphological evolution. Domain shuffling, rearrangements of functional domains between genes, is a key molecular mechanism in deuterostome evolution. However, comprehensive studies focusing on early vertebrates are lacking. With advancements in genomic studies, the genomes of early vertebrate groups and cyclostomes are now accessible, enabling detailed comparative analysis while considering the timing of gene acquisition during evolution. Here, we compared 22 metazoans, including four cyclostomes, to identify genes containing novel domain architectures acquired via domain-shuffling (DSO-Gs), in the common ancestor of vertebrates, gnathostomes, and cyclostomes. We found that DSO-Gs in the common ancestor of vertebrates were associated with novel vertebrate characteristics and those in the common ancestor of gnathostomes correlated with gnathostome-specific traits. Notably, several DSO-Gs acquired in common ancestors of vertebrates have been linked to myelination, a distinct characteristic of gnathostomes. Additionally, in situ hybridization revealed specific expression patterns for the three vertebrate DSO-Gs in cyclostomes, supporting their potential functions. Our findings highlight the significance of DSO-Gs in the emergence of novel traits in the common ancestors of vertebrates, gnathostomes, and cyclostomes.