Transposons in the Williams-Beuren Syndrome Critical Region are Associated with Social Behavior in Assistance Dogs.

A strong signature of selection in the domestic dog genome is found in a five-megabase region of chromosome six in which four structural variants derived from transposons have previously been associated with human-oriented social behavior, such as attentional bias to social stimuli and social interest in strangers. To explore these genetic associations in more phenotypic detail-as well as their role in training success in a specialized assistance dog program-we genotyped 1001 assistance dogs from Canine Companions for Independence®, including both successful graduates and dogs released from the training program for behaviors incompatible with their working role. We collected phenotypes on each dog using puppy-raiser questionnaires, trainer questionnaires, and both cognitive and behavioral tests. Using Bayesian mixed models, we found strong associations (95% credibility intervals excluding zero) between genotypes and certain behavioral measures, including separation-related problems, aggression when challenged or corrected, and reactivity to other dogs. Furthermore, we found moderate differences in the genotypes of dogs who graduated versus those who did not; insertions in GTF2I showed the strongest association with training success (ß = 0.23, CI95% = - 0.04, 0.49), translating to an odds-ratio of 1.25 for one insertion. Our results provide insight into the role of each of these four transposons in canine sociability and may inform breeding and training practices for working dog organizations. Furthermore, the observed importance of the gene GTF2I supports the emerging consensus that variation in GTF2I genotypes and expression have important consequences for social behavior broadly.

Basal plasma oxytocin & fecal cortisol concentrations are highly heritable and associated with individual differences in behavior & cognition in dog puppies.

Oxytocin and cortisol are hormones that can influence cognition and behavior, but the relationships between endogenous concentrations and individual differences in cognitive and behavioral phenotypes remain poorly understood. Across mammals, oxytocin has important roles in diverse social behaviors, and in dogs, it has been implicated in human-oriented behaviors such as social gaze and point-following. Cortisol, an end-product of the hypothalamic-pituitary-adrenal (HPA) axis, is often studied in relation to temperament and emotional reactivity, but it is also known to modulate executive functions. In this study, we measured basal fecal cortisol (n = 247) and plasma oxytocin (n = 249) in dog puppies from a pedigreed population (Canine Companions ®). We collected cognitive and behavioral data from these subjects (n = 247), including measures of human-oriented social cognition, memory, inhibitory control, perceptual discriminations, and temperament. Oxytocin concentrations were estimated to be very highly heritable (h2 = 0.90-0.99) and cortisol concentrations were estimated to be moderately-highly heritable (h2 = 0.43-0.47). Bayesian mixed models controlling for relatedness revealed that oxytocin concentrations were positively associated with spatial working memory and displayed a negative quadratic relationship with behavioral laterality, but no credible associations were seen for social measures. Cortisol concentrations exhibited a negative linear relationship with performance on an inhibitory control task and a negative quadratic relationship with bold behavioral reactions to a novel object. Collectively, our results suggest that individual differences in oxytocin and cortisol concentrations are under strong genetic control in dogs and are associated with phenotypic variation in aspects of temperament, behavioral laterality, and executive function.

Response to Hansen Wheat et al.: Additional analysis further supports the early emergence of cooperative communication in dogs compared to wolves raised with more human exposure.

Here, we address Hansen Wheat et al.'s commentary in this journal in response to Salomons et al. Current Biology, 31(14), 3137-3144.E11, (2021). We conduct additional analyses in response to Hansen Wheat et al.'s two main questions. First, we examine the claim that it was the move to a human home environment which enabled the dog puppies to outperform the wolf puppies in gesture comprehension tasks. We show that the youngest dog puppies who had not yet been individually placed in raisers' homes were still highly skilled, and outperformed similar-aged wolf puppies who had higher levels of human interaction. Second, we address the claim that willingness to approach a stranger can explain the difference between dog and wolf pups' ability to succeed in gesture comprehension tasks. We explain the various controls in the original study that render this explanation insufficient, and demonstrate via model comparison that the covariance of species and temperament also make this parsing impossible. Overall, our additional analyses and considerations support the domestication hypothesis as laid out by Salomons et al. Current Biology, 31(14), 3137-3144.E11, (2021).

Dog cognitive development: a longitudinal study across the first 2 years of life.

While our understanding of adult dog cognition has grown considerably over the past 20 years, relatively little is known about the ontogeny of dog cognition. To assess the development and longitudinal stability of cognitive traits in dogs, we administered a battery of tasks to 160 candidate assistance dogs at 2 timepoints. The tasks were designed to measure diverse aspects of cognition, ranging from executive function (e.g., inhibitory control, reversal learning, memory) to sensory discrimination (e.g., vision, audition, olfaction) to social interaction with humans. Subjects first participated as 8-10-week-old puppies, and then were retested on the same tasks at ~ 21 months of age. With few exceptions, task performance improved with age, with the largest effects observed for measures of executive function and social gaze. Results also indicated that individual differences were both early emerging and enduring; for example, social attention to humans, use of human communicative signals, independent persistence at a problem, odor discrimination, and inhibitory control all exhibited moderate levels of rank-order stability between the two timepoints. Using multiple regression, we found that young adult performance on many cognitive tasks could be predicted from a set of cognitive measures collected in early development. Our findings contribute to knowledge about changes in dog cognition across early development as well as the origins and developmental stability of individual differences.

Effects of maternal investment, temperament, and cognition on guide dog success.

A continuing debate in studies of social development in both humans and other animals is the extent to which early life experiences affect adult behavior. Also unclear are the relative contributions of cognitive skills ("intelligence") and temperament for successful outcomes. Guide dogs are particularly suited to research on these questions. To succeed as a guide dog, individuals must accomplish complex navigation and decision making without succumbing to distractions and unforeseen obstacles. Faced with these rigorous demands, only ∼70% of dogs that enter training ultimately achieve success. What predicts success as a guide dog? To address these questions, we followed 98 puppies from birth to adulthood. We found that high levels of overall maternal behavior were linked with a higher likelihood of program failure. Furthermore, mothers whose nursing style required greater effort by puppies were more likely to produce successful offspring, whereas mothers whose nursing style required less effort were more likely to produce offspring that failed. In young adults, an inability to solve a multistep task quickly, compounded with high levels of perseveration during the task, was associated with failure. Young adults that were released from the program also appeared more anxious, as indicated by a short latency to vocalize when faced with a novel object task. Our results suggest that both maternal nursing behavior and individual traits of cognition and temperament are associated with guide dog success.

Temperament and problem solving in a population of adolescent guide dogs.

It is often assumed that measures of temperament within individuals are more correlated to one another than to measures of problem solving. However, the exact relationship between temperament and problem-solving tasks remains unclear because large-scale studies have typically focused on each independently. To explore this relationship, we tested 119 prospective adolescent guide dogs on a battery of 11 temperament and problem-solving tasks. We then summarized the data using both confirmatory factor analysis and exploratory principal components analysis. Results of confirmatory analysis revealed that a priori separation of tests as measuring either temperament or problem solving led to weak results, poor model fit, some construct validity, and no predictive validity. In contrast, results of exploratory analysis were best summarized by principal components that mixed temperament and problem-solving traits. These components had both construct and predictive validity (i.e., association with success in the guide dog training program). We conclude that there is complex interplay between tasks of "temperament" and "problem solving" and that the study of both together will be more informative than approaches that consider either in isolation.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Increasing arousal enhances inhibitory control in calm but not excitable dogs.

The emotional-reactivity hypothesis proposes that problem-solving abilities can be constrained by temperament, within and across species. One way to test this hypothesis is with the predictions of the Yerkes-Dodson law. The law posits that arousal level, a component of temperament, affects problem solving in an inverted U-shaped relationship: Optimal performance is reached at intermediate levels of arousal and impeded by high and low levels. Thus, a powerful test of the emotional-reactivity hypothesis is to compare cognitive performance in dog populations that have been bred and trained based in part on their arousal levels. We therefore compared a group of pet dogs to a group of assistance dogs bred and trained for low arousal (N = 106) on a task of inhibitory control involving a detour response. Consistent with the Yerkes-Dodson law, assistance dogs, which began the test with lower levels of baseline arousal, showed improvements when arousal was artificially increased. In contrast, pet dogs, which began the test with higher levels of baseline arousal, were negatively affected when their arousal was increased. Furthermore, the dogs' baseline levels of arousal, as measured in their rate of tail wagging, differed by population in the expected directions. Low-arousal assistance dogs showed the most inhibition in a detour task when humans eagerly encouraged them, while more highly aroused pet dogs performed worst on the same task with strong encouragement. Our findings support the hypothesis that selection on temperament can have important implications for cognitive performance.

Context specificity of inhibitory control in dogs.

Across three experiments, we explored whether a dog's capacity for inhibitory control is stable or variable across decision-making contexts. In the social task, dogs were first exposed to the reputations of a stingy experimenter that never shared food and a generous experimenter who always shared food. In subsequent test trials, dogs were required to avoid approaching the stingy experimenter when this individual offered (but withheld) a higher-value reward than the generous experimenter did. In the A-not-B task, dogs were required to inhibit searching for food in a previously rewarded location after witnessing the food being moved from this location to a novel hiding place. In the cylinder task, dogs were required to resist approaching visible food directly (because it was behind a transparent barrier), in favor of a detour reaching response. Overall, dogs exhibited inhibitory control in all three tasks. However, individual scores were not correlated between tasks, suggesting that context has a large effect on dogs' behavior. This result mirrors studies of humans, which have highlighted intra-individual variation in inhibitory control as a function of the decision-making context. Lastly, we observed a correlation between a subject's age and performance on the cylinder task, corroborating previous observations of age-related decline in dogs' executive function.

Characterizing dog cognitive aging using spontaneous problem-solving measures: development of a battery of tests from the Dog Aging Project.

Companion dogs are a valuable model for aging research, including studies of cognitive decline and dementia. With advanced age, some dogs spontaneously develop cognitive impairments and neuropathology resembling features of Alzheimer's disease. These processes have been studied extensively in laboratory beagles, but the cognitive assays used in that context-which rely on time-consuming operant procedures-are not easily scalable to large samples of community-dwelling companion dogs. We developed a battery of five short-form tasks targeting three aspects of cognition that are impaired in Alzheimer's disease: spatial memory, executive functions, and social cognition. In Experiment 1, we tested a cross-sectional sample of dogs (N = 123) and estimated associations between age and task performance. Older dogs scored lower on measures of spatial learning, memory, and response flexibility, and spent less time near, but more time gazing at, the experimenter. We found no differences in associations between age and performance across dogs of different body masses, a proxy for expected lifespan. In Experiment 2, we demonstrated the feasibility of these measures in clinical settings (N = 35). Dogs meeting clinical criteria for moderate or severe cognitive impairment scored lower, on average, than dogs characterized as mildly impaired and healthy agers, although these distributions overlapped. However, few dogs in our study cohort met the criteria for moderate or severe impairment. The measures presented here show promise for deployment in large-scale longitudinal studies of companion dogs, such as the Dog Aging Project.

Associations between physical activity and cognitive dysfunction in older companion dogs: results from the Dog Aging Project.

Canine cognitive dysfunction (CCD) is a form of dementia that shares many similarities with Alzheimer's disease. Given that physical activity is believed to reduce risk of Alzheimer's disease in humans, we explored the association between physical activity and cognitive health in a cohort of companion dogs, aged 6-18 years. We hypothesized that higher levels of physical activity would be associated with lower (i.e., better) scores on a cognitive dysfunction rating instrument and lower prevalence of dementia, and that this association would be robust when controlling for age, comorbidities, and other potential confounders. Our sample included 11,574 companion dogs enrolled through the Dog Aging Project, of whom 287 had scores over the clinical threshold for CCD. In this observational, cross-sectional study, we used owner-reported questionnaire data to quantify dog cognitive health (via a validated scale), physical activity levels, health conditions, training history, and dietary supplements. We fit regression models with measures of cognitive health as the outcome, and physical activity-with several important covariates-as predictors. We found a significant negative relationship between physical activity and current severity of cognitive dysfunction symptoms (estimate = - 0.10, 95% CI: - 0.11 to - 0.08, p < 0.001), extent of symptom worsening over a 6-month interval (estimate = - 0.07, 95% CI: - 0.09 to - 0.05, p < 0.001), and whether a dog reached a clinical level of CCD (odds ratio = 0.53, 95% CI: 0.45 to 0.63, p < 0.001). Physical activity was robustly associated with better cognitive outcomes in dogs. Our findings illustrate the value of companion dogs as a model for investigating relationships between physical activity and cognitive aging, including aspects of dementia that may have translational potential for Alzheimer's disease. While the current study represents an important first step in identifying a relationship between physical activity and cognitive function, it cannot determine causality. Future studies are needed to rule out reverse causation by following the same dogs prospectively over time, and to evaluate causality by administering physical activity interventions.

Once-daily feeding is associated with better health in companion dogs: results from the Dog Aging Project.

A variety of diets have been studied for possible anti-aging effects. In particular, studies of intermittent fasting and time-restricted feeding in laboratory rodents have found evidence of beneficial health outcomes. Companion dogs represent a unique opportunity to study diet in a large mammal that shares human environments. The Dog Aging Project has been collecting data on thousands of companion dogs of all different ages, sizes, and breeds since 2019. We leveraged this diverse cross-sectional dataset to investigate associations between feeding frequency and cognitive function (n = 10,474) as well as nine broad categories of health conditions (n = 24,238). Controlling for sex, age, breed, and other potential confounders, we found that dogs fed once daily rather than more frequently had lower mean scores on a cognitive dysfunction scale, and lower odds of having gastrointestinal, dental, orthopedic, kidney/urinary, and liver/pancreas disorders. Therefore, we find that once-daily feeding is associated with better health in multiple domains. Future research with longitudinal data can provide stronger evidence for a possible causal effect of feeding frequency on health in companion dogs.

Early-emerging and highly heritable sensitivity to human communication in dogs.

Human cognition is believed to be unique in part because of early-emerging social skills for cooperative communication.1 Comparative studies show that at 2.5 years old, children reason about the physical world similarly to other great apes, yet already possess cognitive skills for cooperative communication far exceeding those in our closest primate relatives.2,3 A growing body of research indicates that domestic dogs exhibit functional similarities to human children in their sensitivity to cooperative-communicative acts. From early in development, dogs flexibly respond to diverse forms of cooperative gestures.4,5 Like human children, dogs are sensitive to ostensive signals marking gestures as communicative, as well as contextual factors needed for inferences about these communicative acts.6-8 However, key questions about potential biological bases for these abilities remain untested. To investigate their developmental and genetic origins, we tested 375 8-week-old dog puppies on a battery of social-cognitive measures. We hypothesized that if dogs' skills for cooperating with humans are biologically prepared, then they should emerge robustly in early development, not require extensive socialization or learning, and exhibit heritable variation. Puppies were highly skillful at using diverse human gestures, and we found no evidence that their performance required learning. Critically, over 40% of the variation in dogs' point-following abilities and attention to human faces was attributable to genetic factors. Our results suggest that these social skills in dogs emerge early in development and are under strong genetic control.

Working Dog Training for the Twenty-First Century.

Dogs are trained for a variety of working roles including assistance, protection, and detection work. Many canine working roles, in their modern iterations, were developed at the turn of the 20th century and training practices have since largely been passed down from trainer to trainer. In parallel, research in psychology has advanced our understanding of animal behavior, and specifically canine learning and cognition, over the last 20 years; however, this field has had little focus or practical impact on working dog training. The aims of this narrative review are to (1) orient the reader to key advances in animal behavior that we view as having important implications for working dog training, (2) highlight where such information is already implemented, and (3) indicate areas for future collaborative research bridging the gap between research and practice. Through a selective review of research on canine learning and behavior and training of working dogs, we hope to combine advances from scientists and practitioners to lead to better, more targeted, and functional research for working dogs.

Enhancing the Selection and Performance of Working Dogs.

Dogs perform a variety of integral roles in our society, engaging in work ranging from assistance (e.g., service dogs, guide dogs) and therapy to detection (e.g., search-and-rescue dogs, explosive detection dogs) and protection (e.g., military and law enforcement dogs). However, success in these roles, which requires dogs to meet challenging behavioral criteria and to undergo extensive training, is far from guaranteed. Therefore, enhancing the selection process is critical for the effectiveness and efficiency of working dog programs and has the potential to optimize how resources are invested in these programs, increase the number of available working dogs, and improve working dog welfare. In this paper, we review two main approaches for achieving this goal: (1) developing selection tests and criteria that can efficiently and effectively identify ideal candidates from the overall pool of candidate dogs, and (2) developing approaches to enhance performance, both at the individual and population level, via improvements in rearing, training, and breeding. We summarize key findings from the empirical literature regarding best practices for assessing, selecting, and improving working dogs, and conclude with future steps and recommendations for working dog organizations, breeders, trainers, and researchers.

Cooperative Communication with Humans Evolved to Emerge Early in Domestic Dogs.

Although we know that dogs evolved from wolves, it remains unclear how domestication affected dog cognition. One hypothesis suggests dog domestication altered social maturation by a process of selecting for an attraction to humans.1-3 Under this account, dogs became more flexible in using inherited skills to cooperatively communicate with a new social partner that was previously feared and expressed these unusual social skills early in development.4-6 Here, we comparedog (n = 44) and wolf (n = 37) puppies, 5-18 weeks old, on a battery of temperament and cognition tasks. We find that dog puppies are more attracted to humans, read human gestures more skillfully, and make more eye contact with humans than wolf puppies. The two species are similarly attracted to familiar objects and perform similarly on non-social measures of memory and inhibitory control. These results are consistent with the idea that domestication enhanced the cooperative-communicative abilities of dogs as selection for attraction to humans altered social maturation.

Cognitive characteristics of 8- to 10-week-old assistance dog puppies.

To characterize the early ontogeny of dog cognition, we tested 168 domestic dog, Canis familiaris, puppies (97 females, 71 males; mean age = 9.2 weeks) in a novel test battery based on previous tasks developed and employed with adolescent and adult dogs. Our sample consisted of Labrador retrievers, golden retrievers and Labrador × golden retriever crosses from 65 different litters at Canine Companions for Independence, an organization that breeds, trains and places assistance dogs for people with disabilities. Puppies participated in a 3-day cognitive battery that consisted of 14 tasks measuring different cognitive abilities and temperament traits such as executive function (e.g. inhibitory control, reversal learning, working memory), use of social cues, sensory discriminations and reactivity to and recovery from novel situations. At 8-10 weeks of age, and despite minimal experience with humans, puppies reliably used a variety of cooperative-communicative gestures from humans. Puppies accurately remembered the location of hidden food for delays of up to 20 s, and succeeded in a variety of visual, olfactory and auditory discrimination problems. They also showed some skill at executive function tasks requiring inhibitory control and reversal learning, although they scored lower on these tasks than is typical in adulthood. Taken together, our results confirm the early emergence of sensitivity to human communication in dogs and contextualize these skills within a broad array of other cognitive abilities measured at the same stage of ontogeny.

Predictive Models of Assistance Dog Training Outcomes Using the Canine Behavioral Assessment and Research Questionnaire and a Standardized Temperament Evaluation.

Assistance dogs can greatly improve the lives of people with disabilities. However, a large proportion of dogs bred and trained for this purpose are deemed unable to successfully fulfill the behavioral demands of this role. Often, this determination is not finalized until weeks or even months into training, when the dog is close to 2 years old. Thus, there is an urgent need to develop objective selection protocols that can identify dogs most and least likely to succeed, from early in the training process. We assessed the predictive validity of two candidate measures employed by Canine Companions for Independence (CCI), a national assistance dog organization headquartered in Santa Rosa, CA. For more than a decade, CCI has collected data on their population using the Canine Behavioral Assessment and Research Questionnaire (C-BARQ) and a standardized temperament assessment known internally as the In-For-Training (IFT) test, which is conducted at the beginning of professional training. Data from both measures were divided into independent training and test datasets, with the training data used for variable selection and cross-validation. We developed three predictive models in which we predicted success or release from the training program using C-BARQ scores (N = 3,569), IFT scores (N = 5,967), and a combination of scores from both instruments (N = 2,990). All three final models performed significantly better than the null expectation when applied to the test data, with overall accuracies ranging from 64 to 68%. Model predictions were most accurate for dogs predicted to have the lowest probability of success (ranging from 85 to 92% accurate for dogs in the lowest 10% of predicted probabilities), and moderately accurate for identifying the dogs most likely to succeed (ranging from 62 to 72% for dogs in the top 10% of predicted probabilities). Combining C-BARQ and IFT predictors into a single model did not improve overall accuracy, although it did improve accuracy for dogs in the lowest 20% of predicted probabilities. Our results suggest that both types of assessments have the potential to be used as powerful screening tools, thereby allowing more efficient allocation of resources in assistance dog selection and training.

Characterizing Early Maternal Style in a Population of Guide Dogs.

In both humans and non-humans, differences in maternal style during the first few weeks of life can be reliably characterized, and these differences affect offspring's temperament and cognition in later life. Drawing on the breeding population of dogs at The Seeing Eye, a guide dog school in Morristown, New Jersey, we conducted videotaped focal follows on 21 mothers and their litters (n = 138 puppies) over the first 3 weeks of the puppies' lives in an effort to characterize maternal style. We found that a mother's attitude and actions toward her offspring varied naturally between individuals, and that these variations could be summarized by a single principal component, which we described as Maternal behavior. This component was stable across weeks, associated with breed, litter size, and parity, but not redundant with these attributes. Furthermore, this component was significantly associated with an independent experimental measure of maternal behavior, and with maternal stress as measured by salivary cortisol. In summary, Maternal behavior captured a significant proportion of the variation in maternal style; was stable over time; and had both discriminant and predictive validity.