Development of the Olfactory and Vomeronasal Systems in the Fossorial Water Vole (Arvicola scherman). I. The Late Prenatal Stages

Chemical communication is essential for mammalian survival from the earliest stages of life, yet most of what is known about the prenatal development of the olfactory and vomeronasal systems comes from laboratory rodents. These models, while invaluable, may not fully represent the developmental trajectories of wild species living under natural ecological pressures. Here we investigated the fetal development of the nasal chemosensory systems in the fossorial water vole (Arvicola scherman), a free-living arvicoline rodent with a highly subterranean lifestyle. We analyzed fetuses at embryonic days E17 and E21 (term) using classical histology, immunohistochemistry (markers: Gi2, Go, G{gamma}8, CB, CR, PGP 9.5, GAP-43, {beta}-tubulin, MAP2), and lectin histochemistry (UEA, LEA, SBA, STA, DBA). This combined approach enabled us to assess structural maturation, neuronal differentiation, and the temporal dynamics of glycoconjugate expression in the vomeronasal organ (VNO), olfactory epithelium (OE), and the main (MOB) and accessory olfactory bulbs (AOB). By E21, the MOB displayed a six-layered adult-like organization with well-defined glomeruli and interneuronal populations, whereas the AOB showed delayed morphological maturation but already exhibited selective molecular signatures in its nerve and superficial layers. Prenatally, the VNO underwent conspicuous structural differentiation, including stratification of the sensory epithelium, robust axonal fasciculation, and early development of vomeronasal glands. Immunohistochemical analysis revealed early expression of G-protein subunits and calcium-binding proteins, indicating premature pathway specification and interneuronal circuit formation. Lectin labeling provided additional insights: SBA emerged as a highly selective marker of the vomeronasal pathway; UEA highlighted early compartmentalization of vomeronasal projections; LEA showed a conserved, pan-chemosensory binding pattern across systems; and DBA, despite its lower specificity, revealed late-onset reactivity in postmitotic neurons. Together, these findings demonstrate that A. scherman exhibits a remarkably accelerated prenatal maturation of its chemosensory systems compared with laboratory rodents. This early functional readiness likely reflects adaptive pressures of a fossorial lifestyle, emphasizing the importance of incorporating wild species into developmental neurobiology to refine our understanding of mammalian chemosensory evolution.