Conserved and derived expression patterns and positive selection on dental genes reveal complex evolutionary context of ever-growing rodent molars

Abstract

ABSTRACTBackgroundContinuously growing teeth are an important innovation in mammalian evolution, yet genetic regulation of continuous growth by stem cells remains incompletely understood. Dental stem cells are lost at the onset of tooth root formation, but this loss of continuous crown growth is difficult to study in the mouse because regulatory signaling overlaps with signals that pattern tooth size and shape. Within the voles (Cricetidae, Rodentia, Glires), species have evolved both rooted and unrooted molars that have similar size and shape. We assembled ade novogenome ofMyodes glareolus, a vole with high-crowned, rooted molars, and performed genomic and transcriptomic analyses in a broad phylogenetic context of Glires (rodents and lagomorphs) to assess differential selection and evolution in tooth forming genes.ResultsOurde novogenome recovered 91% of single-copy orthologs for Euarchontoglires and had a total length of 2.44 Gigabases, enabling genomic and transcriptomic analyses. We identified six dental genes undergoing positive selection across Glires and two genes undergoing positive selection in species with unrooted molars,DsppandAqp1. Transcriptomics analyses demonstrated conserved patterns of dental gene expression with species-specific variation likely related to developmental timing and morphological differences between mouse and vole molars.ConclusionsOur results support ongoing dental gene evolution in rodents with unrooted molars. We identify candidate genes for further functional analyses, particularlyDspp, which plays an important role in mineralizing tissues. Our expression results support conservation of dental genes between voles and model species like mice, while revealing significant effects of overall tooth morphology on gene expression.