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1. 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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2. Testosterone pulses paired with a location induce a place preference to the nest of a monogamous mouse under field conditions

   https://doi.org/10.7554/eLife.65820  

   Petric, Radmila ; Kalcounis-Rueppell, Matina ; Marler, Catherine A ( March 2022 , eLife)

   Changing social environments such as the birth of young or aggressive encounters present a need to adjust behavior. Previous research examined how long-term changes in steroid hormones mediate these adjustments. We tested the novel concept that the rewarding effects of transient testosterone pulses (T-pulses) in males after social encounters alter their spatial distribution on a territory. In free-living monogamous California mice ( Peromyscus californicus ), males administered three T-injections at the nest spent more time at the nest than males treated with placebo injections. This mimics T-induced place preferences in the laboratory. Female mates of T-treated males spent less time at the nest but the pair produced more vocalizations and call types than controls. Traditionally, transient T-changes were thought to have transient behavioral effects. Our work demonstrates that in the wild, when T-pulses occur in a salient context such as a territory, the behavioral effects last days after T-levels return to baseline. 

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3. 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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4. Acute intranasal oxytocin dose enhances social preference for parents over peers in male but not female peri-adolescent California mice (Peromyscus californicus)

   https://doi.org/10.1016/j.ygcen.2023.114230  

   Guoynes, Caleigh D. ; Marler, Catherine A. ( May 2023 , General and Comparative Endocrinology)

   Peri-adolescence is a critical developmental stage marked by profound changes in the valence of social interactions with parents and peers. We hypothesized that the oxytocin (OXT) and vasopressin (AVP) systems, known for influencing social behavior, would be involved in the maintenance and breaking of bonding behavior expressed by very early peri-adolescent males and females. In rodents, OXT is associated with mother–pup bonding and may promote social attachment to members of the natal territory. AVP, on the other hand, can act in contrasting ways to OXT and has been associated with aggression and territoriality. Specifically, we predicted that in peri-adolescent male and female juveniles of the biparental and territorial California mouse (Peromyscus californicus), a) OXT would increase the social preferences for the parents over unfamiliar age-matched peers (one male and one female), and b) AVP would break the parent-offspring bond and either increase time in the neutral chamber and/or approach to their unfamiliar and novel peers. We examined anxiety and exploratory behavior using an elevated plus maze and a novel object task as a control. Peri-adolescent mice were administered an acute intranasal (IN) treatment of 0.5 IU/kg IN AVP, 0.5 IU/kg IN OXT, or saline control; five minutes later, the behavioral tests were conducted. As predicted, we found that IN OXT enhanced social preference for parents; however, this was only in male and not female peri-adolescent mice. IN AVP did not influence social preference in either sex. These effects appear specific to social behavior and not anxiety, as neither IN OXT nor AVP influenced behavior during the elevated plus maze or novel object tasks. To our knowledge, this is the first evidence indicating that OXT may play a role in promoting peri-adolescent social preferences for parents and delaying weaning in males. 

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5. 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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