Effect of early experience on neuronal and behavioral responses to con- and heterospecific odors in closely related Mus taxa: epigenetic contribution in formation of precopulatory isolation

BACKGROUND: The most effective learning occurs during sensitive periods. Olfactory plasticity to main social olfactory cues is limited to a critical period to a large degree. The objective was to evaluate the influence of early olfactory experience on the behavioral and neuronal responses of males to con- and heterospecific odors of receptive females in two species, M. musculus (subspecies musculus, wagneri) and M. spicilegus, and thus to determine the potential role of epigenetic contribution in the formation of precopulatory isolation. RESULTS: Males were reciprocally cross-fostered shortly after the birth and were tested for response to con- and heterospecific urine odors of estrus females using two-choice tests at 70–85 days of age. Neuronal activity of non- and cross-fostered males was evaluated at 90–110 days of age in the MOB and AOB to con- and heterospecific female odor using fMRI (MEMRI). Non-cross-fostered males of three taxa demonstrated a strong preference for odor of conspecific females compared to odor of heterospecific ones. Spicilegus-nursed musculus preferred odor of heterospecific females. Wagneri-nursed spicilegus and spicilegus-nursed wagneri did not demonstrate significant choice of con - or heterospecific female odor. The level of MRI signal obtained from the evaluation of manganese accumulation in AOB neurons was significantly higher when the odor of conspecific estrus females was exposed, compared to urine exposure of heterospecific females. The response pattern changed to the opposite in males raised by heterospecific females. Response patterns of neuronal activity in the MOB to con- and heterospecific female odors were different in cross-fostered and control males. CONCLUSION: The maternal environment, including odor, had a greater effect on the level of MRI signal in the AOB than the genetic relationships of the recipient and the donor of the odor stimulus. Behavioral and neuronal responses to con- and heterospecific odors changed in closely related Mus taxa as a result of early experience. We demonstrated the importance of early learning in mate choice in adulthood in mice and the possibility of epigenetic contribution in the formation of precopulatory reproductive isolation.