Human-like modes of communication, including mutual gaze, in dogs may have been acquired during domestication with humans. We show that gazing behavior from dogs, but not wolves, increased urinary oxytocin concentrations in owners, which consequently facilitated owners' affiliation and increased oxytocin concentration in dogs. Further, nasally administered oxytocin increased gazing behavior in dogs, which in turn increased urinary oxytocin concentrations in owners. These findings support the existence of an interspecies oxytocin-mediated positive loop facilitated and modulated by gazing, which may have supported the coevolution of human-dog bonding by engaging common modes of communicating social attachment.

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Recent evidence suggests that enduring social bonds have fitness benefits. However, very little is known about the neural circuitry and neurochemistry underlying the formation and maintenance of stable social bonds outside reproductive contexts. Oxytocin (OT), a neuropeptide synthetized by the hypothalamus in mammals, regulates many complex forms of social behavior and cognition in both human and nonhuman animals. Animal research, however, has concentrated on monogamous mammals, and it remains unknown whether OT also modulates social bonds in nonreproductive contexts. In this study we provide behavioral evidence that exogenous OT promotes positive social behaviors in the domestic dog toward not only conspecifics but also human partners. Specifically, when sprayed with OT, dogs showed higher social orientation and affiliation toward their owners and higher affiliation and approach behaviors toward dog partners than when sprayed with placebo. Additionally, the exchange of sociopositive behaviors with dog partners triggered the release of endogenous OT, highlighting the involvement of OT in the development of social relationships in the domestic dog. These data provide new insight into the mechanisms that facilitate the maintenance of close social bonds beyond immediate reproductive interest or genetic ties and complement a growing body of evidence that identifies OT as one of the neurochemical foundations of sociality in mammalian species.cooperative bonds | cooperative mechanisms A ccording to behavioral ecology theory, sociability evolved either to reduce individuals' risk from predation or to increase individuals' ability to find and defend food (1). New evidence from a range of mammalian species, however, shows that competitive success and reproductive performance of social individuals are affected by the nature and quality of the social bonds they form, suggesting that sociability is adaptive in its own right (2, 3). The impact of social bonds on individuals' fitness extends beyond the benefits derived from associations directly related to mating and parental care (4). For example, in baboons (Papio hamadryas ursinus) (2, 3), house mice (Mus musculus) (5), rats (Rattus norvegicus) (6), horses (Equus equus) (7), and bottlenose dolphins (Tursiops truncatus) (8), individuals that maintain strong, enduring same-sex bonds experience a higher longevity or offspring survival than individuals with weaker bonds. These data parallel evidence from human studies that show that the quality and quantity of individuals' social relationships is associated not only with better mental health but also with reduced mortality (9).Beside the above-mentioned fitness benefits of social integration, very little is known about the neural circuitry and neurochemistry underlying the formation and maintenance of social bonds outside reproductive contexts. Although it is likely that brain systems that motivate animals to establish individualized relationships with other group members first evolved to mobilize the maternal care necessary f...

Mutual gaze is the most fundamental manifestation of social bonding in humans between mothers and infants and between sexual partners in monogamous species. Dog-to-owner gaze probably evolved as a form of social communication during domestication with humans, leading to the establishment of a human-dog bond that is similar to a mother-infant relationship. Urinary oxytocin increases in mothers following mutual gaze in both mothers and infants. A rise in urinary oxytocin occurs in dogs following mutual gaze, but it is unclear whether the increase also occurs in dog owners.This study investigated the effect of mutual gaze in both dogs and their owners on levels of urinary oxytocin. A primary aim was to determine whether there is a causal relationship between mutual gaze and the release of oxytocin. The authors tested the hypothesis that an oxytocin-mediated positive loop (as has been postulated between mother and infants) exists between humans and dogs that is mediated by gaze. To show that the hormone was a cause not just an effect of the interaction, oxytocin was administered intranasally to dogs, and the gazing interaction between dogs and their owners as well as unfamiliar humans was assessed.Gazing behavior increased urinary oxytocin in dogs as well as their owners. Owners and dogs sharing a long mutual gaze had higher levels of oxytocin in their urine than did owners and dogs with shorter eye contact. Although a prolonged gaze increased oxytocin in dogs, it did not increase levels of oxytoxin in hand-raised pet wolves, suggesting that mutual gaze is not used in wolves as a form of social communication with humans. Female dogs receiving intranasal oxytocin gazed longer at their owners than did those given saline. Moreover, oxytocin levels were increased by intranasal oxytocin in dog owners (who had not been given this hormone). These mutual effects were not seen between dogs and unfamiliar humans or between male dogs and their owners.These findings indicate that oxytocin is the cause, not the effect, of the interaction and support of the existence of an interspecies self-perpetuating oxytocin-mediated positive loop facilitated and modulated by mutual gazing. Gazing behavior may have supported the coevolution of human-dog bonding as a common mode of communicating social attachment.

BackgroundVocal learning is a central functional constituent of human speech, and recent studies showing that adult male mice emit ultrasonic sound sequences characterized as “songs” have suggested that the ultrasonic courtship sounds of mice provide a mammalian model of vocal learning.ObjectivesWe tested whether mouse songs are learned, by examining the relative role of rearing environment in a cross-fostering experiment.Methods and FindingsWe found that C57BL/6 and BALB/c males emit a clearly different pattern of songs with different frequency and syllable compositions; C57BL/6 males showed a higher peak frequency of syllables, shorter intervals between syllables, and more upward frequency modulations with jumps, whereas BALB/c males produced more “chevron” and “harmonics” syllables. To establish the degree of environmental influences in mouse song development, sons of these two strains were cross-fostered to another strain of parents. Songs were recorded when these cross-fostered pups were fully developed and their songs were compared with those of male mice reared by the genetic parents. The cross-fostered animals sang songs with acoustic characteristics - including syllable interval, peak frequency, and modulation patterns - similar to those of their genetic parents. In addition their song elements retained sequential characteristics similar to those of their genetic parents' songs.ConclusionThese results do not support the hypothesis that mouse “song” is learned; we found no evidence for vocal learning of any sort under the conditions of this experiment. Our observation that the strain-specific character of the song profile persisted even after changing the developmental auditory environment suggests that the structure of these courtship sound sequences is under strong genetic control. Thus, the usefulness of mouse “song” as a model of mammalian vocal learning is limited, but mouse song has the potential to be an indispensable model to study genetic mechanisms for vocal patterning and behavioral sequences.

Dogs have a unique ability to understand visual cues from humans. We investigated whether dogs can discriminate between human facial expressions. Photographs of human faces were used to test nine pet dogs in two-choice discrimination tasks. The training phases involved each dog learning to discriminate between a set of photographs of their owner's smiling and blank face. Of the nine dogs, five fulfilled these criteria and were selected for test sessions. In the test phase, 10 sets of photographs of the owner's smiling and blank face, which had previously not been seen by the dog, were presented. The dogs selected the owner's smiling face significantly more often than expected by chance. In subsequent tests, 10 sets of smiling and blank face photographs of 20 persons unfamiliar to the dogs were presented (10 males and 10 females). There was no statistical difference between the accuracy in the case of the owners and that in the case of unfamiliar persons with the same gender as the owner. However, the accuracy was significantly lower in the case of unfamiliar persons of the opposite gender to that of the owner, than with the owners themselves. These results suggest that dogs can learn to discriminate human smiling faces from blank faces by looking at photographs. Although it remains unclear whether dogs have human-like systems for visual processing of human facial expressions, the ability to learn to discriminate human facial expressions may have helped dogs adapt to human society.

BackgroundSexual imprinting is important for kin recognition and for promoting outbreeding, and has been a driving force for evolution; however, little is known about sexual imprinting by auditory cues in mammals. Male mice emit song-like ultrasonic vocalizations that possess strain-specific characteristics.ObjectivesIn this study, we asked whether female mice imprint and prefer specific characteristics in male songs.Methods and FindingsWe used the two-choice test to determine the song preference of female C57BL/6 and BALB/c mice. By assessing the time engaged in searching behavior towards songs played back to females, we found that female mice displayed an innate preference for the songs of males from different strains. Moreover, this song preference was regulated by female reproductive status and by male sexual cues such as the pheromone ESP1. Finally, we revealed that this preference was reversed by cross-fostering and disappeared under fatherless conditions, indicating that the behavior was learned by exposure to the father's song.ConclusionsOur results suggest that female mice can discriminate among male song characteristics and prefer songs of mice from strains that are different from their parents, and that these preferences are based on their early social experiences. This is the first study in mammals to demonstrate that male songs contribute to kin recognition and mate choice by females, thus helping to avoid inbreeding and to facilitate offspring heterozygosity.

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