Duplication of spiralian-specific TALE genes and evolution of the blastomere specification mechanism in the bivalve lineage

BACKGROUND: Despite the conserved pattern of the cell-fate map among spiralians, bivalves display several modified characteristics during their early development, including early specification of the D blastomere by the cytoplasmic content, as well as the distinctive fate of the 2d blastomere. However, it is unclear what changes in gene regulatory mechanisms led to such changes in cell specification patterns. Spiralian-TALE (SPILE) genes are a group of spiralian-specific transcription factors that play a role in specifying blastomere cell fates during early development in limpets. We hypothesised that the expansion of SPILE gene repertoires influenced the evolution of the specification pattern of blastomere cell fates. RESULTS: We performed a transcriptome analysis of early development in the purplish bifurcate mussel and identified 13 SPILE genes. Phylogenetic analysis of the SPILE gene in molluscs suggested that duplications of SPILE genes occurred in the bivalve lineage. We examined the expression patterns of the SPILE gene in mussels and found that some SPILE genes were expressed in quartet-specific patterns, as observed in limpets. Furthermore, we found that several SPILE genes that had undergone gene duplication were specifically expressed in the D quadrant, C and D quadrants or the 2d blastomere. These expression patterns were distinct from the expression patterns of SPILE in their limpet counterparts. CONCLUSIONS: These results suggest that, in addition to their ancestral role in quartet specification, certain SPILE genes in mussels contribute to the specification of the C and D quadrants. We suggest that the expansion of SPILE genes in the bivalve lineage contributed to the evolution of a unique cell fate specification pattern in bivalves. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13227-021-00181-2.