The reference genome of the freshwater snail Lymnaea stagnalis reveals evolutionary and molecular implications of simultaneous hermaphroditism

The great pond snail Lymnaea stagnalis has served as a model organism to disciplines such as neurophysiology, evolution, ecotoxicology and developmental biology for more than a hundred years. We generated a highly homozygous line by alternating selfing and full-sib mating of this simultaneous hermaphrodite gastropod over multiple generations. Whole genome sequencing (~176 x depth), assembly and annotation resulted in a final assembly of 943 Mb (L50:257; N50 957,215) with a total of 22,499 predicted gene models. Because of the unusual reproductive biology of L. stagnalis, we used this resource to focus on the identification of receptors potentially involved in cell-type specification, presumably required for the establishment and maintenance of simultaneously active male and female reproductive systems. We focused on nuclear receptors (NRs, including newly discovered 2DBD-NRs), G protein-coupled receptors (GPCRs), and receptor tyrosine kinases (RTKs). We found that significant gene family expansions have resulted in abundant GPCRs of a specific family, Rhodopsin neuropeptide FMRFamide-receptor like, throughout the L. stagnalis genome. Phylogenetic analyses and spatial gene expression profiling reveals that the GPCR expansion coincides with the occurrence of simultaneous hermaphroditism in gastropods, consistent with the observation that male and female reproductive processes need to be regulated mutually exclusively in the same body. These findings will support receptor de-orphanisation efforts, and provide deeper insight into the mechanisms that underlie the modes of action of compounds involved in neuroendocrine regulation of reproduction, induced toxicity, and development in L. stagnalis and molluscs in general.