Expanded Expression of Pro-Neurogenic Factor SoxB1 during Larval Development of Gastropod Lymnaea stagnalis Suggests Preadaptation to Prolonged Neurogenesis in Mollusca

Abstract

The diversity in the organization of the nervous system in mollusks raises intriguing questions about its development and evolution. Our study aims to gain a deeper understanding of how the nervous system forms in Mollusca by examining the involvement of SoxB-family transcription factors in the early development of neurogenic zones. Specifically, we explore the expression patterns of two SoxB genes in the gastropod Lymnaea stagnalis, namely Ls-SoxB1 and Ls-SoxB2, across various developmental stages. Through a combination of in situ hybridization chain reaction, immunohistochemistry, and proliferation assays, we examine the dynamic spatial distribution of Ls- SoxB1 and Ls-SoxB2, with a particular emphasis on the formation of central ring ganglia and the identification of active proliferative zones. Our findings reveal that Ls-SoxB1 exhibits expanded ectodermal expression from the gastrula to the postmetamorphic stage, evident at both transcriptional and translational levels. Throughout larval development, Ls-SoxB1 is expressed in the ectoderm of the head, foot, and visceral complex, as well as in ganglia anlagen and sensory cells. In contrast, the expression of Ls-SoxB2 in the ectoderm is observed until the veliger stage, after which it persists in subepithelial layer cells and ganglia rudiments. Proliferation assay reveals a uniform distribution of dividing cells in the ectoderm at all developmental stages, indicating the absence of distinct neurogenic zones with increased proliferation in gastropods. Our findings highlight that Ls-SoxB1 exhibit widespread expression patterns in both location and time compared to other Lophotrochozoa species. This prolonged expression of SoxB genes in gastropods can be interpreted as a form of transcriptional neoteny, playing a crucial role in the diversification of nervous systems. Thus, it serves as a preadaptation to prolonged neurogenesis and an increase in the central nervous system complexity in Mollusca.