A dog's life: Early life histories influence methylation of glucocorticoid (NR3C1) and oxytocin (OXTR) receptor genes, cortisol levels, and attachment styles.

Early life deprivation and stress can contribute to life-long, problematic consequences, including epigenetic variations related to behavior and health. Domestic dogs share human environments and social-cognitive traits, making them a promising comparative model to examine developmental plasticity. We examined 47 owner-dog dyads, including dogs rescued from abusive or neglectful environments, and matched control dogs for changes in DNA methylation of glucocorticoid (NR3C1) and oxytocin (OXTR) receptor genes previously shown to be affected by early life stress in other species including humans. We used an attachment paradigm, which included a separation event to examine cortisol levels and owner-dog attachment styles. Overall, dogs with adverse histories had different NR3C1 methylation patterns as a function of age and less OXTR methylation than comparison dogs. Dogs with adverse histories did not differ in their cortisol change from baseline to poststressor from comparison dogs, but the change in cortisol was associated with NR3C1 methylation. In addition, dogs with a history of early life stress had more insecure attachment styles; for every unit increase of OXTR methylation, the odds increased for insecure attachment style. This study demonstrates that adverse life histories lead to methylation differences, resulting in the hypothalamic-pituitary-adrenal (HPA) axis's dysregulation and differences in behavioral phenotypes.

Ruff Morning? The Use of Environmental Enrichment during an Acute Stressor in Kenneled Shelter Dogs.

The length of stay for some animals has increased with the recent reduction of animals euthanized in US shelters and animal control facilities. Research examining the effectiveness of different types of enrichment on buffering the effects of acute daily stressors in the shelter environment, such as kennel cleaning, is lacking. In addition, daily known stressors can result in undesirable behaviors that could lead to a need for euthanasia. Ways to effectively reduce the effects of daily stressors while optimizing strained resources is currently a high priority. In this study, we presented shelter dogs with food, tactile, and scent enrichment items to increase (arousing) or decrease (calming) activity during the daily stressor of morning kennel cleaning. We found that calming, rather than arousing, enrichment items were associated with body position scores indicative of lower stress in dogs, with calming scent enrichment (lavender) producing the most significant benefit. In contrast, items that showed the greatest reduction in vocalization were arousing (ball) compared to other arousing conditions. Our findings suggest that different unwanted behaviors in the kennel environment often associated with stress can be reduced using specific types of enrichment during a daily stressful event. Further, the results illustrate that enrichment items other than food might be more effective at decreasing certain undesirable behaviors. Overall, this study provides insight into how shelter workers might effectively use enrichment items during an unavoidable acute stressor. With many shelters keeping dogs longer, addressing events that might cause repeated stress in this population may indirectly help with adopting and lowering euthanasia rates due to unwanted behavior that develops due to repeated exposure to this necessary but acute stressor of morning cleaning.

Early life adversity in dogs produces altered physiological and behavioral responses during a social stress-buffering paradigm.

Although owners can act as stress buffers for their dogs, whether dogs with poor early life histories with humans will respond similarly is unknown. We tested 45 dogs, 23 of which were rescued from adverse conditions, in a social paradigm in which a threatening stranger confronted them with either their owner or an unfamiliar human present. Salivary cortisol levels were assessed at three points, and the dogs' behavior and owners' responses to questionnaires were evaluated. Dogs from adverse backgrounds engaged in greater contact and exhibited more relaxed behaviors and social referencing when their owners were present. Dogs from the comparison group explored more when accompanied by their owners. Dogs from adverse backgrounds experienced greater decreases in cortisol levels from the first to third samples relative to dogs in the comparison group. Dogs from adverse backgrounds were also more likely to respond fearfully to a threatening stranger. Their owners rated them as having higher levels of stranger-directed fear, nonsocial fear, separation-related problems, attention seeking, and lower levels of chasing and trainability. These findings from this study suggest that early adverse environments may have lasting effects on dogs' social behavior.

Evidence for a synchronization of hormonal states between humans and dogs during competition.

Social interactions with humans have been shown to influence hormonal processes in dogs, but it is unclear how the hormonal states of humans factor into this relationship. In this study, we explored the associations between changes in the cortisol levels of dogs with humans' hormonal changes, behavior, and perceptions of their performance at an agility competition. A total of 58 dogs and their handlers (44 women, 14 men) provided saliva samples before and after competing. Dogs' saliva samples were later assayed for cortisol and humans' samples for cortisol and testosterone. Following the competition, handler-dog interactions were observed for affiliative and punitive behavior towards their dogs, and handlers completed questionnaires that included personal ratings of their performance. Structural equation modeling revealed that elevations in handlers' cortisol levels were associated with increases in their dogs' cortisol levels. Handlers' affiliative and punitive behaviors towards their dogs following competition were associated with their ratings of their performance, but these variables were unrelated to changes in their own cortisol levels and their dogs', implying their behavior did not mediate the relationship. These findings suggest that changes in the hormonal states were reflected between humans and their dogs, and this relationship was not due to handlers' perceptions of their performance or the behaviors we observed during post-competition social interactions. This study is one of the first to provide evidence for a synchronization of hormonal changes between species.

Contagious yawning, social cognition, and arousal: an investigation of the processes underlying shelter dogs' responses to human yawns.

Studies of contagious yawning have reported inconsistent findings regarding whether dogs exhibit this behavior and whether it is mediated by social-cognitive processes or the result of physiological arousal. We investigated why some dogs yawn in response to human yawns; particularly, whether these dogs are exceptional in their ability to understand human social cues or whether they were more physiologically aroused. Sixty shelter dogs were exposed to yawning and nonyawning control stimuli demonstrated by an unfamiliar human. We took salivary cortisol samples before and after testing to determine the role of arousal in yawn contagion. Dogs were tested on the object-choice task to assess their sensitivity for interpreting human social cues. We found that 12 dogs yawned only in response to human yawns (i.e., appeared to exhibit yawn contagion), though contagious yawning at the population level was not observed. Dogs that exhibited yawn contagion did not perform better on the object-choice task than other dogs, but their cortisol levels remained elevated after exposure to human yawning, whereas other dogs had reduced cortisol levels following yawning stimuli relative to their baseline levels. We interpret these findings as showing that human yawning, when presented in a stressful context, can further influence arousal in dogs, which then causes some to yawn. Although the precise social-cognitive mechanisms that underlie contagious yawning in dogs are still unclear, yawning between humans and dogs may involve some communicative function that is modulated by context and arousal.

Embryonic exposure to maternal testosterone influences age-specific mortality patterns in a captive passerine bird.

Hormones are potent mediators of developmental programming and maternal epigenetic effects. In vertebrates, developmental exposure to maternal androgen hormones has been shown to impact multiple behavioral and physiological traits of progeny, but the possible consequences of this early exposure in terms of aging-related changes in mortality and fitness remain largely unexplored. Avian eggs naturally contain variable doses of maternal hormones-in particular, androgens-which have documented effects on embryo growth and differentiation as well as adult behavior and physiology. Here, we report that injections of a physiological dose of testosterone (T) into yolks of freshly laid eggs of a small, seasonally breeding songbird, the house sparrow (Passer domesticus), increased survivorship in a semi-natural aviary environment. In addition, survival effects of developmental T exposure were sex-dependent, with males generally having a higher risk of death. Separate analyses for young birds in their first year of life (from hatching up to the first reproductive period the following calendar year) and in adulthood (after the first breeding season) showed similar effects. For first-year birds, mortality risk was higher during the winter than during the period after fledging; for adults, mortality risk was higher during the reproductive than the non-reproductive phase (post-breeding molt and winter). T treatment did not affect nestling body mass, but resulted in higher body mass at 3-4 months of age; T and body mass at this age interacted to influence mortality risk. Embryonic exposure to maternal testosterone may result in lower adult mortality by modifying intrinsic physiological processes involved in health or aging over the lifespan of adult birds.

Transitive behavior in hippocampal-lesioned pigeons.

The hippocampus of birds and mammals is critical for the learning of map-like memory representations of environmental space. It has been suggested that the hippocampus of rats also participates in non-spatial relational learning, including the learning of non-spatial transitive relationships among odor stimuli [Bunsey and Eichenbaum, Nature 1996]. Although transitive-like learning has been demonstrated in a variety of vertebrate species, from a comparative perspective the role of the hippocampus in this form of learning has not been tested in other amniote groups. We trained control and hippocampal-lesioned homing pigeons on a series of visual, non-spatial, go/no-go conditional discriminations and then tested them on novel transitivity probe trials. The hippocampal-lesioned pigeons were as successful as control pigeons in responding appropriately to correct and incorrect transitivity pairs. The finding that the homing pigeon hippocampal formation is not necessary for solving this serial, conditional discrimination task is important for further understanding hippocampal function across species, and represents one of the few studies that have attempted to localize a brain region responsible for the phenomenon of transitive behavior learning.

Hippocampus lesions impair landmark array spatial learning in homing pigeons: a laboratory study.

Hippocampal (HF)-lesioned pigeons display impaired homing ability when flying over familiar terrain, where they are presumably relying on a map-like representation of familiar landmarks to navigate. However, research carried out in the field precludes a direct test of whether hippocampal lesions compromise the ability of homing pigeons to navigate by familiar landmarks. To examine more thoroughly the relationship between hippocampus and landmark spatial learning, control, neostriatum-lesioned, and HF-lesioned homing pigeons were trained on two open field, laboratory, conditional discrimination tasks. One was a visual landmark array task, and the other was a room color discrimination task. For the tasks, the correct of three differently colored food bowls was determined by the spatial relationship among a group of five landmarks and room color, respectively. Intact control birds successfully learned both tasks, while neostriatum-lesioned birds successfully learned the landmark array task-the only task on which they were trained. By contrast, HF-lesioned birds successfully learned the room color task but were unable to learn the landmark array task. The data support the hypothesis that homing performance deficits observed in the field following hippocampal lesions are in part a consequence of an impairment in the ability of lesioned pigeons to use familiar visual landmarks for navigation.