Sex differences in vocal communication of freely interacting adult mice depend upon behavioral context

Abstract

Ultrasonic vocalizations (USVs) are believed to play a critical role in mouse communication. Although mice produce USVs in multiple contexts, signals emitted in reproductive contexts are typically attributed solely to the male mouse. Only recently has evidence emerged showing that female mice are also vocally active during mixed-sex interactions. Therefore, this study aimed to systematically quantify and compare vocalizations emitted by female and male mice as the animals freely interacted. Using an eight-channel microphone array to determine which mouse emitted specific vocalizations during unrestrained social interaction, we recorded 13 mixed-sex pairs of mice. We report here that females vocalized significantly less often than males during dyadic interactions, with females accounting for approximately one sixth of all emitted signals. Moreover, the acoustic features of female and male signals differed. We found that the bandwidths (i.e., the range of frequencies that a signal spanned) of female-emitted signals were smaller than signals produced by males. When examining how the frequency of each signal changed over time, the slopes of male-emitted signals decreased more rapidly than female signals. Further, we revealed notable differences between male and female vocal signals when the animals were performing the same behaviors. Our study provides evidence that a female mouse does in fact vocalize during interactions with a male and that the acoustic features of female and male vocalizations differ during specific behavioral contexts.

Ultrasonic vocalizations in house mice depend upon genetic relatedness of mating partners and correlate with subsequent reproductive success

“…For this reason, studies on USV emission recorded during sexual interactions often assume that only males vocalize [14,26]. More recently, however, female mice have been shown to vocalize during direct opposite-sex interactions [27][28][29]. However, females in these studies contributed only up to 18% of the total USVs emitted, and this is insufficient to explain the 5x increase during direct interactions that we detected in our study.…”

“…Playback studies are now needed to manipulate the amount, types and order of USVs that females perceive during opposite-sex interactions over the stages of courtship, and to examine female responses to differences in the rate and other features of male USVs. Determining the function of dynamic modulation of male courtship USVs will be a challenge, especially since courtship vocalizations appear to be an interactive exchange between the sexes (duetting) [27][28][29].…”

Spontaneous social communication in laboratory mice - placing ultrasonic vocalizations in their behavioral context

“…In the vast majority of previous studies investigating mouse social communication, USVs were triggered by social deprivation (e.g., two weeks of isolation) and recorded in the first minutes or hours of interaction (Neunuebel et al, 2015;Sangiamo et al, 2020;Warren et al, 2018bWarren et al, , 2020). The USV types were either classified in a pre-determined repertoire (Scattoni et al, 2010) or simplified for modeling to reduce the complexity of the signals (e.g., ignoring harmonic components or frequency jumps or normalizing over duration; (Neunuebel et al, 2015;Sangiamo et al, 2020;Warren et al, 2018bWarren et al, , 2020). In our study, we provide a complementary approach by determining a large set of acoustic variables to avoid masking the complexity of the signals and leave the door open for any user to design their own classification.…”

“…In paired interactions, USVs trigger no behavioral variations in female-female interactions, but males accelerate when the females accelerate while vocalizing in male-female interactions (Warren et al, 2018b(Warren et al, , 2020).…”

Male mice adjust courtship behavior in response to female multimodal signals

“…Male mice can unequivocally differentiate between female and male urine [18], but there is mixed evidence on whether males and females produce different USVs [33,[63][64][65][66] and even less is known about whether males and females produce different squeaks. Within a single sex we know that female squeaks elicited during an intersexual encounter are similar to those elicited during restraint [34] but there is still a lack of understanding about male squeaks and propensity.…”