Transcriptome characterization of three main ganglia in Patinopecten yessoensis provides novel insights into a monophyletic origin of the bilaterian central nervous system

Abstract

The question of whether the central nervous system (CNS) of bilaterians arose independently or has a monophyletic origin has been hotly debated. Increasing evidence supports the monophyletic origin of CNS across the three major bilaterian groups. However, in Mollusca, the second largest animal phylum, evolutional information of CNS was mainly obtained from cephalopods, of which the ganglionated cephalic neural system is under controversy to be homolog to vertebrate brain. Yesso scallop (Patinopecten yessoensis), a bivalve mollusk stands out with its slow-evolving genome and differential preservation of ganglia fusion trace. Here, we systematically analyzed the transcriptome of three main ganglia in Yesso scallop. We identified a ganglia-related module using gene co-expression network, and discovered the expansion of neurotransmitter receptors and hypothalamic hormone receptors, suggesting a complex CNS in scallops than we thought. Our analysis revealed predominant expression of expanded hypothalamic hormone receptors in ganglia. Furthermore, the repertoire of fundamental markers for vertebrate pituitary development was largely conserved in scallop ganglia, suggesting a shared evolutionary origin of the pituitary. Our investigation of specific ganglia characteristics demonstrated that ganglia fusion promotes both structural and functional complexity. Particularly, gene-set enrichment analysis (GSEA) demonstrated that gene sets of vertebrate pituitary or brain development are enriched by genes expressed in scallop ganglia, indicating the homolog between ganglionated neural system and vertebrate brain, which supporting the monophyletic origin of brain. Our findings provide new evidences to understand the monophyletic origin of the brain and pituitary in bilaterians.