Specificity of California mouse pup vocalizations in response to olfactory cues

In rodents, young pups communicate with their parents through harmonic calls and ultrasonic vocalizations (USVs). These forms of communication can improve chances of survival, since pups rely on their parents for thermoregulation, nutrition and protection. The extent to which pups modulate calls in response to their surroundings remains unclear. In this study we examined whether olfactory stimuli influence characteristics of pup calls, and how these calls may be affected by pup sex and litter size, in the California mouse (Peromyscus californicus). Pups were isolated and audio recorded during an initial, 3-minute control period, after which they were exposed for 5 minutes to bedding containing one of 4 olfactory cues: scent from their home cage, scent from the home cage of an unfamiliar family, coyote urine, or no scent. Latency to call, call rate, call duration and call characteristics (e.g. frequency and amplitude) were compared between the control period and olfactory-exposure period as well as among olfactory conditions. Pups from 2-pup litters called more quietly (lower amplitude) when exposed to odor from a predator while pups from 3-pup litters called louder (higher amplitude). Additionally, pups tended to reduce their call rates in response to odors from their home cage, consistent with contact quieting. However, pups tended to increase their rate of calling when exposed to predator urine, in contrast to the expectations of predator-induced vocal suppression. Lastly, male pups produced higher-frequency calls and more USVs than females. These results indicate that a number of pup call characteristics in this species can be influenced by acute olfactory stimuli as well as factors such as litter size and sex. The value of these pup call variations for offspring-parent communication is unclear: whether they elicit different parental responses is unknown and would be an interesting/valuable/informative avenue for future studies.

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

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.

Intranasal oxytocin reduces pre-courtship aggression and increases paternal response in California mice (Peromyscus californicus)

Oxytocin (OXT) is a neuropeptide that can facilitate prosocial behavior and decrease social stress and anxiety. We investigated whether acute pulses of intranasal (IN) OXT influenced social behavior during social challenges that are likely to occur throughout the lifespan of a wild mouse. To test this, we examined the acute effects of IN OXT in the male California mouse (Peromyscus californicus), a monogamous, biparental, and territorial rodent, using a within-subjects longitudinal design. Social challenges included a pre-courtship male-female encounter conducted during the initial aggressive and not the following affiliative phase of courtship, same-sex resident intruder test, and parental care test, with each test and dose separated by at least two weeks. Males were treated with intranasal infusions of 0.8 IU/kg OXT or saline controls 5-min before each behavioral test, receiving a total of three treatments of either IN OXT or saline control. We predicted that IN OXT would 1) decrease aggression and increase affiliation during the pre-courtship aggression phase, 2) increase aggression during resident intruder paradigms and 3) increase paternal care and vocalizations during a paternal care test. As predicted, during pre-courtship aggression with a novel female, IN OXT males displayed less contact aggression than control males, although with no change in affiliative behavior. However, post-pairing, during the resident intruder test, IN OXT males did not differ from control males in contact aggression. During the paternal care test, IN OXT males were quicker to approach their pups than control males but did not differ in vocalizations produced, unlike our previous research demonstrating an effect on vocalizations in females. In summary, during pre-courtship aggression and the paternal care test, IN OXT promoted prosocial approach; however, during the resident intruder test IN OXT did not alter social approach. These data suggest that IN OXT promotes prosocial approach specifically in social contexts that can lead to affiliation.

Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus

Epidemiological evidence suggests that social interactions and especially bonding between couples influence tumorigenesis, yet whether this is due to lifestyle changes, homogamy (likelihood of individuals to marry people of similar health), or directly associated with host-induced effects in tumors remains debatable. In the present study, we explored if tumorigenesis is associated with the bonding experience in monogamous rodents at which disruption of pair bonds is linked to anxiety and stress. Comparison of lung cancer cell spheroids that formed in the presence of sera from bonded and bond-disrupted deer mice showed that in monogamous Peromyscus polionotus and Peromyscus californicus, but not in polygamous Peromyscus maniculatus, the disruption of pair bonds altered the size and morphology of spheroids in a manner that is consistent with the acquisition of increased oncogenic potential. In vivo, consecutive transplantation of human lung cancer cells between P. californicus, differing in bonding experiences (n = 9 for bonded and n = 7 for bond-disrupted), and nude mice showed that bonding suppressed tumorigenicity in nude mice (p<0.05), suggesting that the protective effects of pair bonds persisted even after bonding ceased. Unsupervised hierarchical clustering indicated that the transcriptomes of lung cancer cells clustered according to the serum donors’ bonding history while differential gene expression analysis pointed to changes in cell adhesion and migration. The results highlight the pro-oncogenic effects of pair-bond disruption, point to the acquisition of expression signatures in cancer cells that are relevant to the bonding experiences of serum donors, and question the ability of conventional mouse models to capture the whole spectrum of the impact of the host in tumorigenesis.

Impacts of Timber Harvest on Communities of Small Mammals, Ticks, and Tick-Borne Pathogens in a High-Risk Landscape in Northern California

Timber harvest may impact tick-borne disease by affecting small mammal and tick community structures. We assessed tick and small mammal populations in older second-growth redwood (Sequoia sempervirens (D. Don) Endl) habitat at two harvested sites in Santa Cruz County, California, where local risk of tick-borne disease is high and determined the prevalence of tick-borne pathogens in ticks. After single-tree removal harvest in 2014, there was a modest reduction in canopy, primarily toward the end of the study. Harvested sites showed strong reductions in California mouse (Peromyscus californicus, (Gambel)) captures 2-yr after harvest, resolving such that treatments and controls were comparable by the end of the study. Following harvest, treated sites experienced a transient decreased tick infestation while control plots experienced an increase. Ixodes angustus (Neumann) infestation probability on harvested plots decreased immediately after harvest, increasing with time but remaining lower than control plots, whereas I. pacificus (Cooley and Kohls) prevalence was higher shortly after the harvest on harvested plots, and continued to increase. Mean abundance of ticks on vegetation increased on control plots. We detected Borrelia burgdorferi ((Johnson et al.) Baranton) and Anaplasma phagocytophilum ((Foggie 1949) Dumler) in 3.8 and 3.1% of ticks on rodents, but no differences were associated with harvest. Impacts of forest harvest on tick-borne disease depend on removal practice and intensity, whether or not hosts are habitat specialists, and whether or not ticks are host specialists.