Ultrasonic vocalization production and playback predicts intrapair and extrapair social behaviour in a monogamous mouse

Most studies examining rodent ultrasonic vocalizations (USVs) have investigated pericopulatory vocal behaviour in polygynous rodents, while vocalizations related to pair bond maintenance in monogamous rodents remain unexplored. In the monogamous California mouse, Peromyscus californicus, we used ultrasonic playbacks and post-playback social interactions to assess possible functions of USVs. We found that females responded with approach towards USVs of an unfamiliar male (bonded male from another pair) compared to a noise control, but displayed no difference in response to calls of their partner versus noise. Responsiveness to unfamiliar males does not appear to reflect an interest in extrapair copulations because during post-playback social interactions, females displayed more agonistic behaviours and fewer affiliative behaviours towards unfamiliar, sexually naïve 'stranger' males than towards their partners. We speculate that approach to unfamiliar male USVs instead may be related to territorial defence. We further explored associations within the data set. Interestingly, female affiliation with her partner was predicted by USV output, particularly a higher number and proportion of complex call types, produced during the male partner USV elicitation phase. Female approach towards USVs was related to syllable duration of one call type in partner USVs (not in unfamiliar USVs) but no other features, and sufficient variation exists in syllable duration to allow females to theoretically distinguish between individuals based on this measure. Similarly, while pregnancy state did not influence female social behaviour, it decreased approach to playback of partner USVs but not to that of unfamiliar USVs. Overall, our results illuminate concepts about vocal communication in monogamous rodent species with strong pair bonds and suggest that functions of USVs in rodents can extend beyond mate choice.