skip to main content


Title: Testosterone pulses at the nest site modify ultrasonic vocalization types in a monogamous and territorial mouse
Abstract

Modulation of baseline testosterone (T) via long‐lasting T implants alters territorial, sexual, and social behavior of animals in the field. Transient T increases occur in numerous species after social interactions, but these transient increases in T have not been manipulated in the field. In the laboratory, these T increases can influence future behavior for days, causing changes in social behavior and inducing preferences for specific locations. We manipulated transient increases in T in the field at the nests of the monogamous and territorial California mouse (Peromyscus californicus) to examine long‐term (>24 hr) changes in ultrasonic vocalizations (USVs). Males of bonded male–female dyads (=pair) were administered a T injection (vs. saline) three times over seven days and USVs of the male–female dyad were measured for three days after the last injection. At T nests, the male–female dyad produced significantly more 1SV (one call SV: an SV is a sustained vocalization that is long in duration and low in modulation) and 4SV (four call SV) type USVs than controls, but no significant changes in aggressive barks. Overall, male–female dyad mice at T nests produced a greater diversity in call types such that 1SV, 4SV, 5SV, and a complex sweep were produced at T nests but not control nests. There were significantly more USVs produced at T nests on night 2 after the final injection. There were no differences in spectral characteristics of SV calls or aggressive barks between T and control nests. The function of the changes that occurred is unknown, but is consistent with increased long‐term changes in behavioral interactions with nest mates and may reflect T‐induced conditioned place preferences to the nest site. Significantly, transient increases in T influence future acoustic communication under field conditions with competing biotic and abiotic stimuli.

 
more » « less
NSF-PAR ID:
10244011
Author(s) / Creator(s):
 ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Ethology
Volume:
124
Issue:
11
ISSN:
0179-1613
Page Range / eLocation ID:
p. 804-815
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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. 
    more » « less
  2. 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. 
    more » « less
  3. Abstract

    Defending offspring incurs temporal and energetic costs and can be dangerous for the parents. Accordingly, the intensity of this costly behavior should reflect the perceived risk to the reproductive output. When facing costly brood parasitism by brown‐headed cowbirds (Molothrus ater), where cowbirds lay eggs in heterospecific nests and cause the hosts to care for their young, yellow warblers (Setophaga petechia) use referential “seet” calls to warn their mates of the parasitic danger. Yellow warblers of both sexes produce this call only in response to cowbirds or seet‐calling conspecifics. Seet calls are mainly produced during the laying and incubation stages of breeding, when risk of brood parasitism is highest, rather than during the nestling stage. On the other hand, general alarm calls (chips) are produced throughout the nesting cycle and are also used in conspecific interactions unrelated to nesting. We hypothesized that context shapes responses prior to breeding as well, such that yellow warblers without a mate and active nest would be less likely to respond to playbacks that simulate brood parasitism risk. To test this hypothesis, we presented playbacks of two nest threats, cowbirds (brood parasite) and blue jays (Cyanocitta cristata; nest predator), on territories of unmated male warblers (unpaired) and male warblers with a known mate (paired). We found that unpaired males were unresponsive toward playbacks indicating nest threats, whereas paired males were significantly more aggressive and vocal toward these playbacks compared to control playbacks. However, both paired and unpaired males were vocally responsive toward chip calls, which are informative for males regardless of pairing status. Male yellow warblers appear to adjust their responses during the earliest stages of breeding depending on the contextual relevance of specific threat stimuli, and together with prior studies, our work further supports that referential seet calls are associated with stage‐specific risk of brood parasitism.

     
    more » « less
  4. 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. 
    more » « less
  5. 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. 
    more » « less