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Pair-bonding allows for division of labor across behavioral tasks such as protecting a territory, caring for pups or foraging for food. However, how these labor divisions are determined, whether they are simply intrinsic differences in the individual’s behavior or a coordinated behavioral response by the pair, remains unknown. We used the monogamous, biparental and territorial California mouse ( Peromyscus californicus ) to study how behavioral approach to an aggressive vocal stimulus in a novel environment was affected by pair-bonding. Using a three-chambered vocal playback paradigm, we first measured the amount of time individuals spent in close proximity to aggressive bark vocalizations. We found that animals could be categorized as either approachers or avoiders. We then paired individuals based on their initial approach behavior to an opposite sex individual who displayed either similar or different approach behaviors. These pairs were then retested for approach behavior as a dyad 10–11 days post-pairing. This test found that pairs showed convergence in their behavioral responses, such that pairs who were mismatched in their approach behaviors became more similar, and pairs that were matched remained so. Finally, we analyzed the ultrasonic vocalizations (USV) produced and found that pairs produced significantly more USVs than individuals. Importantly, increased USV production correlated with increasing behavioral convergence of pairs. Taken together, this study shows that pair-bonded animals alter their approach behaviors to coordinate their response with their partner and that vocal communication may play a role in coordinating these behavioral responses. Overall, our findings indicate that pair-bonding generates an emergent property in pairs, adjusting their combined approach behavior towards a new aggressive stimulus representing a potential challenge to the bonded pair. Such findings may be broadly important for social bonding in other social systems. 

Maternal-offspring communication and care are essential for offspring survival. Oxytocin (OXT) is known for its role in initiation of maternal care, but whether OXT can rapidly influence maternal behavior or ultrasonic vocalizations (USVs; above 50 kHz) has not been examined. To test for rapid effects of OXT, California mouse mothers were administered an acute intranasal (IN) dose of OXT (0.8 IU/kg) or saline followed by a separation test with three phases: habituation with pups in a new testing chamber, separation via a wire mesh, and finally reunion with pups. We measured maternal care, maternal USVs, and pup USVs. In mothers, we primarily observed simple sweep USVs, a short downward sweeping call around 50 kHz, and in pups we only observed pup whines, a long call with multiple harmonics ranging from 20 kHz to 50 kHz. We found that IN OXT rapidly and selectively enhanced the normal increase in maternal simple sweep USVs when mothers had physical access to pups (habituation and reunion), but not when mothers were physically separated from pups. Frequency of mothers’ and pups’ USVs were correlated upon reunion, but IN OXT did not influence this correlation. Finally, mothers given IN OXT showed more efficient pup retrieval/carrying and greater total maternal care upon reunion. Behavioral changes were specific to maternal behaviors (e.g. retrievals) as mothers given IN OXT did not differ from controls in stress-related behaviors (e.g. freezing). Overall, these findings highlight the rapid effects and context-dependent effect a single treatment with IN OXT has on both maternal USV production and offspring care.