Dynamic evolutionary history of spiralian-specific TALE homeobox genes in mollusks

Homeobox genes play essential roles in the early development of many animals. Although the repertoire of most homeobox genes, including three amino acid loop extension (TALE)-type homeobox genes, is conserved in animals, spiralian-TALE (SPILE) genes are a notable exception. In this study, SPILE genes were extracted from the genomic data of 22 mollusk species and classified into four clades (-A/C, -B, -D, and -E) to determine which SPILE genes exhibit dynamic repertoire changes. While SPILE-D and -E duplications were rarely observed, SPILE-B duplication was observed in the bivalve lineage and SPILE-A/C duplication was observed in multiple clades. Conversely, most or all SPILE genes were lost in cephalopods and in some gastropod lineages. SPILE gene expression patterns were also analyzed in multiple mollusk species using publicly available RNA-seq data. The majority of SPILE genes examined, particularly those in the A/C- and B-clades, were specifically expressed during early development, suggesting that most SPILE genes exert specific roles in early development. This comprehensive cataloging and characterization revealed a dynamic evolutionary history, including SPILE-A/C and -B gene duplications and the loss of SPILE genes in several lineages. Furthermore, this study provides a useful resource for studying the molecular mechanism of spiralian early development and the evolution of young and lineage-specific transcription factors.