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1. Playback of broadband vocalizations of female mice suppresses male ultrasonic calls

   https://doi.org/10.1371/journal.pone.0273742  

   Hood, Kayleigh E.; Long, Eden; Navarro, Eric; Hurley, Laura M. (January 2023, PLOS ONE)

   Coleman, Melissa J. (Ed.)

   Although male vocalizations during opposite- sex interaction have been heavily studied as sexually selected signals, the understanding of the roles of female vocal signals produced in this context is more limited. During intersexual interactions between mice, males produce a majority of ultrasonic vocalizations (USVs), while females produce a majority of human-audible squeaks, also called broadband vocalizations (BBVs). BBVs may be produced in conjunction with defensive aggression, making it difficult to assess whether males respond to BBVs themselves. To assess the direct effect of BBVs on male behavior, we used a split-cage paradigm in which high rates of male USVs were elicited by female presence on the other side of a barrier, but which precluded extensive male-female contact and the spontaneous production of BBVs. In this paradigm, playback of female BBVs decreased USV production, which recovered after the playback period. Trials in which female vocalizations were prevented by the use of female bedding alone or of anesthetized females as stimuli also showed a decrease in response to BBV playback. No non-vocal behaviors declined during playback, although digging behavior increased. Similar to BBVs, WNs also robustly suppressed USV production, albeit to a significantly larger extent. USVs suppression had two distinct temporal components. When grouped in 5-second bins, USVs interleaved with bursts of stimulus BBVs. USV suppression also adapted to BBV playback on the order of minutes. Adaptation occurred more rapidly in males that were housed individually as opposed to socially for a week prior to testing, suggesting that the adaptation trajectory is sensitive to social experience. These findings suggest the possibility that vocal interaction between male and female mice, with males suppressing USVs in response to BBVs, may influence the dynamics of communicative behavior. 

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2. Pygmy mouse songs reveal anatomical innovations underlying acoustic signal elaboration in rodents

   https://doi.org/10.1242/jeb.223925  

   Riede, Tobias; Pasch, Bret (May 2020, The Journal of Experimental Biology)

   Elaborate animal communication displays are often accompanied by morphological and physiological innovations. In rodents, acoustic signals used in reproductive contexts are produced by two distinct mechanisms, but the underlying anatomy that facilitates such divergence is poorly understood. ‘Audible’ vocalizations with spectral properties between 500 Hz and 16 kHz are thought to be produced by flow-induced vocal fold vibrations, whereas ‘ultrasonic’ vocalizations with fundamental frequencies above 19 kHz are produced by an aerodynamic whistle mechanism. Baiomyine mice (genus Baiomys and Scotinomys) produce complex frequency modulated songs that span these traditional distinctions and represent important models to understand the evolution of signal elaboration. We combined acoustic analyses of spontaneously vocalizing northern pygmy mice (B. taylori) mice in air and light gas atmosphere with morphometric analyses of their vocal apparatus to infer the mechanism of vocal production. Increased fundamental frequencies in heliox indicated that pygmy mouse songs are produced by an aerodynamic whistle mechanism supported by the presence of a ventral pouch and alar cartilage. Comparative analyses of the larynx and ventral pouch size among four additional ultrasonic whistle-producing rodents indicate that the unusually low ‘ultrasonic’ frequencies (relative to body size) of pygmy mice songs are associated with an enlarged ventral pouch. Additionally, mice produced shorter syllables while maintaining intersyllable interval duration, thereby increasing syllable repetition rates. We conclude that while laryngeal anatomy sets the foundation for vocal frequency range, variation and adjustment of central vocal motor control programs fine tunes spectral and temporal characters to promote acoustic diversity within and between species. 

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3. Pair-bonding leads to convergence in approach behavior to conspecific vocalizations in California mice (Peromyscus californicus)

   https://doi.org/10.1371/journal.pone.0255295  

   Rieger, Nathaniel S.; Monari, Patrick K.; Hartfield, Kamryn; Schefelker, Juliette; Marler, Catherine A. (August 2021, PLOS ONE)

   Rosenfeld, Cheryl S. (Ed.)

   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. 

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4. Glucocorticoid-Mediated Changes in Male Green Treefrog Vocalizations Alter Attractiveness to Females

   https://doi.org/10.1093/icb/icab053  

   Leary, Christopher J; Crocker-Buta, Sarah; Holloway, Ashli; Kennedy, Joseph G (May 2021, Integrative and Comparative Biology)

   Synopsis Adrenal glucocorticoids (GCs) are increasingly recognized as important modulators of male courtship signals, suggesting that circulating levels of these steroids can play a central role in sexual selection. However, few studies have examined whether GC-mediated effects on male sexual signals actually impact mate choice by females. Here, we examine how corticosterone (CORT)-mediated changes in the vocalizations of male green treefrogs, Dryophytes cinereus, influence attractiveness to females. In this species, agonistic acoustic signaling between rival males competing for mates increases circulating CORT levels in contest losers. Acute elevations in CORT, in turn, decrease the duration of male advertisement calls and increase the latency between successive calls, resulting in a net reduction in vocal effort (the amount of signaling per unit time) that occurs independently of changes in circulating androgens. Based on known preferences for acoustic features in D. cinereus, and other anuran species, the direction of CORT-mediated effects on temporal call characteristics is expected to compromise attractiveness to females, but whether they are of sufficient magnitude to impact female mate choice decisions is unclear. To examine whether CORT-mediated effects on male advertisement calls reduce attractiveness to females, we broadcast vocalizations in dual speaker playback experiments approximating the mean and 1 SD above and below the mean call duration and vocal effort values (the two primary vocal features impacted by elevated CORT) of males with low and high CORT levels. Results revealed strong preferences by females for the calls characteristic of males with low CORT in tests using the approximate mean and 1 SD above the mean call duration and vocal effort values, but females did not show a preference for calls of males with low CORT in trials using call values approximating 1 SD below the mean. Overall, females preferred males with signal traits predictive of low CORT, however this effect was nonlinear with attenuated preferences when signal alternatives differed only marginally indicating a possible thresholding effect. Specifically, females appeared to discriminate between males with low versus high CORT based primarily on differences in call rates associated with CORT-mediated changes in call duration and vocal effort. Our results highlight that changes in circulating CORT during male–male vocal interactions can decrease attractiveness to females, suggesting that circulating levels of CORT can play a critical role in both intra- and intersexual selection. 

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5. Reproductive state modulates utricular auditory sensitivity in a vocal fish

   https://doi.org/10.1152/jn.00315.2022  

   Rogers, Loranzie S.; Coffin, Allison B.; Sisneros, Joseph A. (November 2022, Journal of Neurophysiology)

   The plainfin midshipman, Porichthys notatus, is a seasonally breeding vocal fish that relies on acoustic communication to mediate nocturnal reproductive behaviors. Reproductive females use their auditory senses to detect and localize “singing” males that produce multiharmonic advertisement (mate) calls during the breeding season. Previous work showed that the midshipman saccule, which is considered the primary end organ used for hearing in midshipman and most other fishes, exhibits reproductive state and hormone-dependent changes that enhance saccular auditory sensitivity. In contrast, the utricle was previously posited to serve primarily a vestibular function, but recent evidence in midshipman and related toadfish suggests that it may also serve an auditory function and aid in the detection of behaviorally relevant acoustic stimuli. Here, we characterized the auditory-evoked potentials recorded from utricular hair cells in reproductive and nonreproductive female midshipman in response to underwater sound to test the hypothesis that variation in reproductive state affects utricular auditory sensitivity. We show that utricular hair cells in reproductive females exhibit up to a sixfold increase in the utricular potential magnitude and have thresholds based on measures of particle acceleration (re: 1 ms −2 ) that are 7–10 dB lower than nonreproductive females across a broad range of frequencies, which include the dominant harmonics of male advertisement calls. This enhanced auditory sensitivity of the utricle likely plays an essential role in facilitating midshipman social and reproductive acoustic communication. NEW & NOTEWORTHY In many animals, vocal-acoustic communication is fundamental for facilitating social behaviors. For the vocal plainfin midshipman fish, the detection and localization of social acoustic signals are critical to the species’ reproductive success. Here, we show that the utricle, an inner ear end organ often thought to primarily serve a vestibular function, serves an auditory function that is seasonally plastic and modulated by the animal’s reproductive state effectively enhancing auditory sensitivity to courting male advertisement calls. 

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