Evan MacLean

Interests

Research

https://scholar.google.com/citations?user=uB6cpSUAAAAJ&hl=en&oi=ao

Courses

Scholarly Contributions

Chapters

• MacLean, E. (2018). Comparative methods in the study of animal cognition. In Field and laboratory methods in animal cognition: A comparative guide(pp 420-422). Cambridge University Press.
• MacLean, E., & Nunn, C. (2017). Phylogenetic approaches for research in comparative cognition. In APA handbook of comparative psychology(pp 201-215). American Psychological Association.
• MacNamara, M., & MacLean, E. (2017). Selecting animals for education environments. In How animals help students learn: Research and practice for educators and mental health professionals(pp 182-196). Routledge, Taylor Francis Group.
• MacLean, E., & Hare, B. (2016). Comparative perspectives on lemur cognition. In The missing lemur link: An ancestral step in human evolution. Cambridge University Press.

Journals/Publications

• Bray, E. E., Raichlen, D. A., Forsyth, K. K., Promislow, D. E., Alexander, G. E., MacLean, E. L., & , D. A. (2022). Associations between physical activity and cognitive dysfunction in older companion dogs: results from the Dog Aging Project. GeroScience.
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  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 
• Bryer, M. A., Koopman, S. E., Cantlon, J. F., Piantadosi, S. T., MacLean, E. L., Baker, J. M., Beran, M. J., Jones, S. M., Jordan, K. E., Mahamane, S., Nieder, A., Perdue, B. M., Range, F., Stevens, J. R., Tomonaga, M., Ujfalussy, D. J., & Vonk, J. (2022). The evolution of quantitative sensitivity. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 377(1844), 20200529.
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  The ability to represent approximate quantities appears to be phylogenetically widespread, but the selective pressures and proximate mechanisms favouring this ability remain unknown. We analysed quantity discrimination data from 672 subjects across 33 bird and mammal species, using a novel Bayesian model that combined phylogenetic regression with a model of number psychophysics and random effect components. This allowed us to combine data from 49 studies and calculate the Weber fraction (a measure of quantity representation precision) for each species. We then examined which cognitive, socioecological and biological factors were related to variance in Weber fraction. We found contributions of phylogeny to quantity discrimination performance across taxa. Of the neural, socioecological and general cognitive factors we tested, cortical neuron density and domain-general cognition were the strongest predictors of Weber fraction, controlling for phylogeny. Our study is a new demonstration of evolutionary constraints on cognition, as well as of a relation between species-specific neuron density and a particular cognitive ability. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.
• Gnanadesikan, G. E., Hammock, E. A., Tecot, S. R., Lewis, R. J., Hart, R., Carter, C. S., & MacLean, E. L. (2022). What are oxytocin assays measuring? Epitope mapping, metabolites, and comparisons of wildtype & knockout mouse urine. Psychoneuroendocrinology, 143, 105827.
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  Oxytocin has become a popular analyte in behavioral endocrinology in recent years, due in part to its roles in social behavior, stress physiology, and cognition. Urine samples have the advantage of being non-invasive and minimally disruptive to collect, allowing for oxytocin measurements even in some wild populations. However, methods for urinary oxytocin immunoassay have not been sufficiently optimized and rigorously assessed for their potential limitations. Using samples from oxytocin knockout (KO) and wildtype (WT) mice, we find evidence of considerable interference in unextracted urine samples, with similar distributions of measured oxytocin in both genotypes. Importantly, although this interference can be reduced by a reversed-phase solid-phase extraction (SPE), this common approach is not sufficient for eliminating false-positive signal on three immunoassay kits. To better understand the source of the observed interference, we conducted epitope mapping of the Arbor Assays antibody and assessed its cross-reactivity with known, biologically active fragments of oxytocin. We found considerable cross-reactivity (0.5-52% by-molarity) for three fragments of oxytocin that share the core epitope, with more cross-reactivity for longer fragments. Given the presence of some cross-reactivity for even the tripeptide MIF-1, it is likely that many small protein metabolites might be sufficiently similar to the epitope that at high concentrations they interfere with immunoassays. We present a new mixed-mode cation-exchange SPE method that minimizes interference-with knockout samples measuring below the assay's limit of detection-while effectively retaining oxytocin from the urine of wildtype mice. This method demonstrates good parallelism and spike recovery across multiple species (mice, dogs, sifakas, humans). Our results suggest that immunoassays of urine samples may be particularly susceptible to interference, even when using common extraction protocols, but that this interference can be successfully managed using a novel mixed-mode cation exchange extraction. These findings imply that previous conclusions based on urinary oxytocin measurements-especially those involving unextracted samples-may need to be reassessed.
• Herbeck, Y. E., Eliava, M., Grinevich, V., & MacLean, E. L. (2022). Fear, love, and the origins of canid domestication: An oxytocin hypothesis. Comprehensive psychoneuroendocrinology, 9, 100100.
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  The process of dog domestication likely involved at least two functional stages. The initial stage occurred when subpopulations of wolves became synanthropes, benefiting from life nearby or in human environments. The second phase was characterized by the evolution of novel forms of interspecific cooperation and social relationships between humans and dogs. Here, we discuss possible roles of the oxytocin system across these functional stages of domestication. We hypothesize that in early domestication, oxytocin played important roles in attenuating fear and stress associated with human contact. In later domestication, we hypothesize that oxytocin's most critical functions were those associated with affiliative social behavior, social engagement, and cooperation with humans. We outline possible neurobiological changes associated with these processes and present a Siberian fox model of canid domestication in which these predictions can be tested. Lastly, we identify limitations of current studies on the neuroendocrinology of domestication and discuss challenges and opportunities for future research.
• Jensen, C. L., Rodriguez, K. E., MacLean, E. L., Abdul Wahab, A. H., Sabbaghi, A., & O'Haire, M. E. (2022). Characterizing veteran and PTSD service dog teams: Exploring potential mechanisms of symptom change and canine predictors of efficacy. PloS one, 17(7), e0269186.
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  Psychiatric service dogs are an emerging complementary intervention for posttraumatic stress disorder (PTSD). Initial evidence suggests that partnership with a service dog may be related to less PTSD symptom severity. However, it remains unclear how or why this might occur. To address this gap, we conducted a longitudinal investigation of 82 post-9/11 military members or veterans and their PTSD service dogs to (1) evaluate service dog characteristics as potential predictors of efficacy, (2) assess dog and human characteristics as potential predictors of veteran-dog bond, and (3) explore potential mechanisms for mental health outcomes. Aim 1 results demonstrated that most service dog characteristics did not predict veterans' mental health outcomes, but lower service dog excitability was associated with less PTSD symptom severity at follow-up. Aim 2 results showed that closer dog-veteran relationships were associated with less excitable dog temperament. Aim 3 results indicated that worse mental health at follow-up was associated with greater use of the specifically trained PTSD service dog task to initiate a social greeting ("make a friend"), whereas better mental health was related to less use of dominance-based training methods, lower perceived emotional/logistical costs of service dog partnership, and closer veteran-dog relationships. More frequent use of the trained service dog task to signal when someone approaches from behind (cover/watch back) was associated with greater anxiety, but less PTSD symptom severity. Overall, veterans spent an average of 82% of their time with service dogs (assessed via Bluetooth proximity between dog collar and veteran smartphone), and most frequently asked their service dogs to perform the trained task for calming their anxiety (calm/comfort anxiety). The present study provides subjective and objective metrics of the heterogeneity among veteran-service dog dyads while also suggesting which of the assessed metrics might be potential mechanisms involved in the intervention.
• Ruple, A., MacLean, E., Snyder-Mackler, N., Creevy, K. E., & Promislow, D. (2022). Dog Models of Aging. Annual review of animal biosciences, 10, 419-439.
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  As the most phenotypically diverse mammalian species that shares human environments and access to sophisticated healthcare, domestic dogs have unique potential to inform our understanding of the determinants of aging. Here we outline key concepts in the study of aging and illustrate the value of research with dogs, which can improve dog health and support translational discoveries. We consider similarities and differences in aging and age-related diseases in dogs and humans and summarize key advances in our understanding of genetic and environmental risk factors for morbidity and mortality in dogs. We address health outcomes ranging from cancer to cognitive function and highlight emerging research opportunities from large-scale cohort studies in companion dogs. We conclude that studying aging in dogs could overcome many limitations of laboratory models, most notably, the ability to assess how aging-associated pathways influence aging in real-world environments similar to those experienced by humans.
• Applebaum, J. W., MacLean, E. L., & McDonald, S. E. (2021). Love, fear, and the human-animal bond: On adversity and multispecies relationships. Comprehensive psychoneuroendocrinology, 7.
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  Love and strong social bonds are known buffers in the experience of adversity. Humans often form strong bonds with non-human animals. The human-animal bond refers to a mutually beneficial and dynamic relationship between humans and non-human animals. Previous research suggests that strong bonds with pets may promote resilience in the experience of adversity, but a strong bond with a pet can also complicate this very experience of adversity, particularly among low-resourced and disadvantaged populations. What is the role of the human-animal bond in adversity, and what is the role of adversity in the bond between a human and a non-human animal? In this article we outline the state of research on the role of various types and sources of adversities in multispecies households (i.e., families, relationships) to consider this overarching question. We focus specifically on intimate partner violence, housing discrimination, LGBTQ+ identity-based discrimination, racism, neighborhood disadvantage, and economic inequality. We then outline an agenda for future research about love, adversity, and multispecies relationships, and discuss implications for public policy and community-based interventions.
• Bray, E. E., Gnanadesikan, G. E., Horschler, D. J., Levy, K. M., Kennedy, B. S., Famula, T. R., & MacLean, E. L. (2021). Early-emerging and highly heritable sensitivity to human communication in dogs. Current biology : CB, 31(14), 3132-3136.e5.
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  Human cognition is believed to be unique in part because of early-emerging social skills for cooperative communication. 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. 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. 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. 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.
• Bray, E. E., Gruen, M. E., Gnanadesikan, G. E., Horschler, D. J., Levy, K. M., Kennedy, B. S., Hare, B. A., & MacLean, E. L. (2021). Dog cognitive development: a longitudinal study across the first 2 years of life. Animal cognition, 24(2), 311-328.
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  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.
• Bray, E. E., Otto, C. M., Udell, M. A., Hall, N. J., Johnston, A. M., & MacLean, E. L. (2021). Enhancing the Selection and Performance of Working Dogs. Frontiers in veterinary science, 8, 644431.
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  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.
• Gnanadesikan, G. E., Hammock, E. A., Tecot, S. R., Carter, C. S., & MacLean, E. L. (2021). Specificity of plasma oxytocin immunoassays: A comparison of commercial assays and sample preparation techniques using oxytocin knockout and wildtype mice. Psychoneuroendocrinology, 132, 105368.
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  Oxytocin has garnered much interest due to its role in affective states, social behaviors, and diverse physiological functions. However, approaches for measuring endogenous oxytocin concentrations have generated considerable controversy and debate. Common procedures for measuring oxytocin often produce uncorrelated results, and the detected concentrations frequently vary across two orders of magnitude. These findings have led some researchers to argue that immunoassays of plasma oxytocin may be unreliable and nonspecific, particularly when samples are not first processed using an extraction procedure. Here, we assess the specificity of oxytocin immunoassays using plasma samples from wildtype (WT) and oxytocin knockout (KO) mice. Plasma samples from both genotypes were measured using immunoassay and were measured with or without a solid-phase extraction. Using a commercially available kit from Arbor Assays, we demonstrate that both techniques generate a clear contrast between genotypes, with wildtype samples containing high concentrations of oxytocin (unextracted mean = 468 pg/ml; extracted mean = 381 pg/ml), while knockout samples measured below the lower limit of detection. Analytical validations demonstrated good parallelism and spike recovery for both methods. Furthermore, the same wildtype samples measured with both procedures were highly correlated (r = 0.95), although unextracted samples measured at significantly higher concentrations (p = 2.0 ×10, Cohen's d = 2.65). To test the generalizability of these results across immunoassay kits, we performed additional assays with kits from Cayman Chemical and Enzo Life Sciences. The Cayman Chemical kit produced results similar to Arbor Assays with a clean signal differentiating WT and KO plasma, both with and without an extraction step. The Enzo kit also differentiated the genotypes, with correlation between extracted and unextracted samples, but was considerably more susceptible to interference without the extraction, as evidenced by false positive signal in KO plasma samples. The extent to which these results generalize to other species remains unknown and challenging to assess.
• Hall, N. J., Johnston, A. M., Bray, E. E., Otto, C. M., MacLean, E. L., & Udell, M. A. (2021). Working Dog Training for the Twenty-First Century. Frontiers in veterinary science, 8, 646022.
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  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.
• Horschler, D. J., Santos, L. R., & MacLean, E. L. (2021). How do non-human primates represent others' awareness of where objects are hidden?. Cognition, 212, 104658.
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  Although non-human primates (NHPs) generally appear to predict how knowledgeable agents use knowledge to guide their behavior, the cognitive mechanisms that enable this remain poorly understood. We assessed the conditions under which NHPs' representations of an agent's awareness break down. Free-ranging rhesus macaques (Macaca mulatta) watched as an agent observed a target object being hidden in one of two boxes. While the agent could no longer see the boxes, the box containing the object flipped open and the object either changed in size/shape (Experiment 1) or color (Experiment 2). Monkeys looked longer when the agent searched for the object incorrectly rather than correctly following the color change (a non-geometric manipulation), but not the size/shape change (a geometric manipulation). Even though the agent maintained knowledge of the object's location in both cases, monkeys no longer expected the agent to search correctly after it had been geometrically (but not non-geometrically) manipulated. Experiment 3 confirmed that monkeys were sensitive to the color manipulation used in Experiment 2, making it unlikely that a failure to perceive the color manipulation accounted for our findings. Our results show that NHPs do not always expect that knowledgeable agents will act on their knowledge to obtain their goals, consistent with heuristic-based accounts of how NHPs represent others' mental states. These findings also suggest that geometric changes that occur outside the agent's perceptual access may disrupt attribution of awareness more so than non-geometric changes.
• MacLean, E. L., Fine, A., Herzog, H., Strauss, E., & Cobb, M. L. (2021). The New Era of Canine Science: Reshaping Our Relationships With Dogs. Frontiers in veterinary science, 8, 675782.
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  Canine science is rapidly maturing into an interdisciplinary and highly impactful field with great potential for both basic and translational research. The articles in this Research Topic, , arise from two meetings sponsored by the Wallis Annenberg PetSpace Leadership Institute, which convened experts from diverse areas of canine science to assess the state of the field and challenges and opportunities for its future. In this final paper, we identify a set of overarching themes that will be critical for a productive and sustainable future in canine science. We explore the roles of dog welfare, science communication, and research funding, with an emphasis on developing approaches that benefit people and dogs, alike.
• Salomons, H., Smith, K. C., Callahan-Beckel, M., Callahan, M., Levy, K., Kennedy, B. S., Bray, E. E., Gnanadesikan, G. E., Horschler, D. J., Gruen, M., Tan, J., White, P., vonHoldt, B. M., MacLean, E. L., & Hare, B. (2021). Cooperative Communication with Humans Evolved to Emerge Early in Domestic Dogs. Current biology : CB, 31(14), 3137-3144.e11.
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  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. 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. 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.
• Strauss, E. G., McCune, S., MacLean, E., & Fine, A. (2021). Editorial: Our Canine Connection: The History, Benefits and Future of Human-Dog Interactions. Frontiers in veterinary science, 8, 784491.
• Bray, E. E., Gruen, M. E., Gnanadesikan, G. E., Horschler, D. J., Levy, K. M., Kennedy, B. S., Hare, B. A., & MacLean, E. L. (2020). Cognitive characteristics of 8- to 10-week-old assistance dog puppies. Animal behaviour, 166, 193-206.
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  To characterize the early ontogeny of dog cognition, we tested 168 domestic dog, , 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.
• Carter, C. S., Kenkel, W. M., MacLean, E. L., Wilson, S. R., Perkeybile, A. M., Yee, J. R., Ferris, C. F., Nazarloo, H. P., Porges, S. W., Davis, J. M., Connelly, J. J., & Kingsbury, M. A. (2020). Is Oxytocin "Nature's Medicine"?. Pharmacological reviews, 72(4), 829-861.
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  Oxytocin is a pleiotropic, peptide hormone with broad implications for general health, adaptation, development, reproduction, and social behavior. Endogenous oxytocin and stimulation of the oxytocin receptor support patterns of growth, resilience, and healing. Oxytocin can function as a stress-coping molecule, an anti-inflammatory, and an antioxidant, with protective effects especially in the face of adversity or trauma. Oxytocin influences the autonomic nervous system and the immune system. These properties of oxytocin may help explain the benefits of positive social experiences and have drawn attention to this molecule as a possible therapeutic in a host of disorders. However, as detailed here, the unique chemical properties of oxytocin, including active disulfide bonds, and its capacity to shift chemical forms and bind to other molecules make this molecule difficult to work with and to measure. The effects of oxytocin also are context-dependent, sexually dimorphic, and altered by experience. In part, this is because many of the actions of oxytocin rely on its capacity to interact with the more ancient peptide molecule, vasopressin, and the vasopressin receptors. In addition, oxytocin receptor(s) are epigenetically tuned by experience, especially in early life. Stimulation of G-protein-coupled receptors triggers subcellular cascades allowing these neuropeptides to have multiple functions. The adaptive properties of oxytocin make this ancient molecule of special importance to human evolution as well as modern medicine and health; these same characteristics also present challenges to the use of oxytocin-like molecules as drugs that are only now being recognized. SIGNIFICANCE STATEMENT: Oxytocin is an ancient molecule with a major role in mammalian behavior and health. Although oxytocin has the capacity to act as a "natural medicine" protecting against stress and illness, the unique characteristics of the oxytocin molecule and its receptors and its relationship to a related hormone, vasopressin, have created challenges for its use as a therapeutic drug.
• Gnanadesikan, G. E., Hare, B., Snyder-Mackler, N., & MacLean, E. L. (2020). Estimating the heritability of cognitive traits across dog breeds reveals highly heritable inhibitory control and communication factors. Animal cognition, 23(5), 953-964.
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  Trait heritability is necessary for evolution by both natural and artificial selection, yet we know little about the heritability of cognitive traits. Domestic dogs are a valuable study system for questions regarding the evolution of phenotypic diversity due to their extraordinary intraspecific variation. While previous studies have investigated morphological and behavioral variation across dog breeds, few studies have systematically assessed breed differences in cognition. We integrated data from Dognition.com-a citizen science project on dog cognition-with breed-averaged genetic data from published sources to estimate the among-breed heritability of cognitive traits using mixed models. The resulting dataset included 11 cognitive measures for 1508 adult dogs across 36 breeds. A factor analysis yielded four factors interpreted as reflecting inhibitory control, communication, memory, and physical reasoning. Narrow-sense among-breed heritability estimates-reflecting the proportion of cognitive variance attributable to additive genetic variation-revealed that scores on the inhibitory control and communication factors were highly heritable (inhibitory control: h = 0.70; communication: h = 0.39), while memory and physical reasoning were less heritable (memory: h = 0.17; physical reasoning: h = 0.21). Although the heritability of inhibitory control is partially explained by body weight, controlling for breed-average weight still yields a high heritability estimate (h = 0.50), while other factors are minimally affected. Our results indicate that cognitive phenotypes in dogs covary with breed relatedness and suggest that cognitive traits have strong potential to undergo selection. The highest heritabilities were observed for inhibitory control and communication, both of which are hypothesized to have been altered by domestication.
• Gnanadesikan, G. E., Hare, B., Snyder-Mackler, N., Call, J., Kaminski, J., Miklósi, ., & MacLean, E. L. (2020). Breed Differences in Dog Cognition Associated with Brain-Expressed Genes and Neurological Functions. Integrative and comparative biology, 60(4), 976-990.
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  Given their remarkable phenotypic diversity, dogs present a unique opportunity for investigating the genetic bases of cognitive and behavioral traits. Our previous work demonstrated that genetic relatedness among breeds accounts for a substantial portion of variation in dog cognition. Here, we investigated the genetic architecture of breed differences in cognition, seeking to identify genes that contribute to variation in cognitive phenotypes. To do so, we combined cognitive data from the citizen science project Dognition.com with published breed-average genetic polymorphism data, resulting in a dataset of 1654 individuals with cognitive phenotypes representing 49 breeds. We conducted a breed-average genome-wide association study to identify specific polymorphisms associated with breed differences in inhibitory control, communication, memory, and physical reasoning. We found five single nucleotide polymorphisms (SNPs) that reached genome-wide significance after Bonferroni correction, located in EML1, OR52E2, HS3ST5, a U6 spliceosomal RNA, and a long noncoding RNA. When we combined results across multiple SNPs within the same gene, we identified 188 genes implicated in breed differences in cognition. This gene set included more genes than expected by chance that were (1) differentially expressed in brain tissue and (2) involved in nervous system functions including peripheral nervous system development, Wnt signaling, presynapse assembly, and synaptic vesicle exocytosis. These results advance our understanding of the genetic underpinnings of complex cognitive phenotypes and identify specific genetic variants for further research.
• Horschler, D. J., MacLean, E. L., & Santos, L. R. (2020). Advancing Gaze-Based Research on Primate Theory of Mind. Trends in cognitive sciences, 24(10), 778-779.
• Horschler, D. J., MacLean, E. L., & Santos, L. R. (2020). Do Non-Human Primates Really Represent Others' Beliefs?. Trends in cognitive sciences, 24(8), 594-605.
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  Over two decades of research have produced compelling evidence that non-human primates understand some psychological states in other individuals but are unable to represent others' beliefs. Recently, three studies employing anticipatory looking (AL) paradigms reported that non-human primates do show hints of implicitly understanding the beliefs of others. However, measures of AL have been increasingly scrutinized in the human literature owing to extensive replication problems. We argue that new reports of belief representation in non-human primates using AL should be interpreted cautiously because of methodological and theoretical challenges paralleling trends in the human literature. We explore how future work can address these challenges, and conclude by identifying new evolutionary questions raised by the prospect that non-human primates implicitly represent others' beliefs without an explicit belief representation system that guides fitness-relevant behavior.
• Watowich, M. M., MacLean, E. L., Hare, B., Call, J., Kaminski, J., Miklósi, ., & Snyder-Mackler, N. (2020). Age influences domestic dog cognitive performance independent of average breed lifespan. Animal cognition, 23(4), 795-805.
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  Across mammals, increased body size is positively associated with lifespan. However, within species, this relationship is inverted. This is well illustrated in dogs (Canis familiaris), where larger dogs exhibit accelerated life trajectories: growing faster and dying younger than smaller dogs. Similarly, some age-associated traits (e.g., growth rate and physiological pace of aging) exhibit accelerated trajectories in larger breeds. Yet, it is unknown whether cognitive performance also demonstrates an accelerated life course trajectory in larger dogs. Here, we measured cognitive development and aging in a cross-sectional study of over 4000 dogs from 66 breeds using nine memory and decision-making tasks performed by citizen scientists as part of the Dognition project. Specifically, we tested whether cognitive traits follow a compressed (accelerated) trajectory in larger dogs, or the same trajectory for all breeds, which would result in limited cognitive decline in larger breeds. We found that all breeds, regardless of size or lifespan, tended to follow the same quadratic trajectory of cognitive aging-with a period of cognitive development in early life and decline in later life. Taken together, our results suggest that cognitive performance follows similar age-related trajectories across dog breeds, despite remarkable variation in developmental rates and lifespan.
• Bray, E. E., Levy, K. M., Kennedy, B. S., Duffy, D. L., Serpell, J. A., & MacLean, E. L. (2019). Predictive Models of Assistance Dog Training Outcomes Using the Canine Behavioral Assessment and Research Questionnaire and a Standardized Temperament Evaluation. Frontiers in veterinary science, 6, 49.
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  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 ( = 3,569), IFT scores ( = 5,967), and a combination of scores from both instruments ( = 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.
• Horschler, D. J., & MacLean, E. L. (2019). Leveraging brain-body scaling relationships for comparative studies. Animal cognition, 22(6), 1197-1202.
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  In Horschler et al. (Anim Cognit 22(2):187-198, 2019), we found that two components of executive function (short-term memory and self-control) were strongly associated with estimated absolute brain weight across dog breeds, and argued that dogs present a powerful model for studying evolutionary links between cognition and neuroanatomy due to their extraordinary degree of intraspecific morphological variation. In a commentary on this work, Montgomery (Anim Cognit, 2019) raises concerns about the practice of estimating brain weights from brain-body scaling relationships. Montgomery explores the practical significance of this approach, ultimately concluding that such estimations should be avoided. In this response, we point out some limitations of the analyses presented by Montgomery and consider his conclusions in light of these issues. We then explore the extent to which body weight serves as a valid proxy for brain weight under varying conditions. Through simulations, we show that the consequences of using body weight as a proxy for brain weight depend on parameters including effect size, the correlation between brain and body weight, and the variance in brain and body weight within a sample. Under conditions approximating those in Horschler et al. (Anim Cognit 22(2):187-198, 2019), we find that body weight is a reliable proxy for brain weight, and that statistical results from models using either brain weight or body weight as predictor variables are highly convergent. Nonetheless, we wholeheartedly agree with Montgomery that empirical data on brain weight, structure, and cellular composition will be critical for creating new opportunities to investigate the relationships between neuroanatomy and cognition in dogs.
• Horschler, D. J., Hare, B., Call, J., Kaminski, J., Miklósi, ., & MacLean, E. L. (2019). Absolute brain size predicts dog breed differences in executive function. Animal cognition, 22(2), 187-198.
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  Large-scale phylogenetic studies of animal cognition have revealed robust links between absolute brain volume and species differences in executive function. However, past comparative samples have been composed largely of primates, which are characterized by evolutionarily derived neural scaling rules. Therefore, it is currently unknown whether positive associations between brain volume and executive function reflect a broad-scale evolutionary phenomenon, or alternatively, a unique consequence of primate brain evolution. Domestic dogs provide a powerful opportunity for investigating this question due to their close genetic relatedness, but vast intraspecific variation. Using citizen science data on more than 7000 purebred dogs from 74 breeds, and controlling for genetic relatedness between breeds, we identify strong relationships between estimated absolute brain weight and breed differences in cognition. Specifically, larger-brained breeds performed significantly better on measures of short-term memory and self-control. However, the relationships between estimated brain weight and other cognitive measures varied widely, supporting domain-specific accounts of cognitive evolution. Our results suggest that evolutionary increases in brain size are positively associated with taxonomic differences in executive function, even in the absence of primate-like neuroanatomy. These findings also suggest that variation between dog breeds may present a powerful model for investigating correlated changes in neuroanatomy and cognition among closely related taxa.
• Horschler, D. J., Santos, L. R., & MacLean, E. L. (2019). Do non-human primates really represent others' ignorance? A test of the awareness relations hypothesis. Cognition, 190, 72-80.
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  Non-human primates can often predict how another agent will behave based on that agent's knowledge about the world. But how do non-human primates represent others' knowledge states? Researchers have recently proposed that non-human primates form "awareness relations" to attribute objectively true information to other minds, as opposed to human-like representations that track others' ignorance or false belief states. We present the first explicit test of the awareness relations hypothesis by examining when rhesus macaques' understanding of other agents' knowledge falters. In Experiment 1, monkeys watched an agent observe a piece of fruit (the target object) being hidden in one of two boxes. While the agent's view was occluded, either the fruit moved out of its box and directly back into it, or the box containing the fruit opened and immediately closed. We found that monkeys looked significantly longer when the agent reached incorrectly rather than correctly after the box's movement, but not after the fruit's movement. This result suggests that monkeys did not expect the agent to know the fruit's location when it briefly and arbitrarily moved while the agent could not see it, but did expect the agent to know the fruit's location when only the box moved while the agent could not see it. In Experiment 2, we replicated and extended both findings with a larger sample, a different target object, and opposite directions of motion in the test trials. These findings suggest that monkeys reason about others' knowledge of objects by forming awareness relations which are disrupted by arbitrary spatial manipulation of the target object while an agent has no perceptual access to it.
• MacLean, E. L., Snyder-Mackler, N., vonHoldt, B. M., & Serpell, J. A. (2019). Highly heritable and functionally relevant breed differences in dog behaviour. Proceedings. Biological sciences, 286(1912), 20190716.
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  Variation across dog breeds presents a unique opportunity to investigate the evolution and biological basis of complex behavioural traits. We integrated behavioural data from more than 14 000 dogs from 101 breeds with breed-averaged genotypic data ( = 5697 dogs) from over 100 000 loci in the dog genome. We found high levels of among-breed heritability for 14 behavioural traits (the proportion of trait variance attributable to genetic similarity among breeds). We next identified 131 single nucleotide polymorphisms associated with breed differences in behaviour, which were found in genes that are highly expressed in the brain and enriched for neurobiological functions and developmental processes, suggesting that they may be functionally associated with behavioural differences. Our results shed light on the heritability and genetic architecture of complex behavioural traits and identify dogs as a powerful model in which to address these questions.
• MacLean, E. L., Wilson, S. R., Martin, W. L., Davis, J. M., Nazarloo, H. P., & Carter, C. S. (2019). Challenges for measuring oxytocin: The blind men and the elephant?. Psychoneuroendocrinology, 107, 225-231.
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  Since its discovery more than a century ago, oxytocin has become one of the most intensively studied molecules in behavioral biology. In the last five years, Psychoneuroendocrinology has published more than 500 articles with oxytocin in the title, with many of these articles including measures of endogenous oxytocin concentrations. Despite longstanding interest, methods of measuring endogenous oxytocin are still in active development. The widely varying oxytocin concentrations detected by different approaches to measurement - and lack of correlation among these techniques - has led to controversy and confusion. We identify features of oxytocin that may help to explain why various approaches may be differentially sensitive to diverse conformational states of the oxytocin molecule. We propose that discrepancies in data generated by different methods of measurement are not necessarily an indicator that some methods are valid whereas others are not. Rather, we propose that current challenges in the measurement of oxytocin may be analogous to the parable of the blind men and the elephant, with different methods of sample preparation and measurement being sensitive to different states in which the oxytocin molecule can exist.
• Lucca, K., MacLean, E. L., & Hare, B. (2018). The development and flexibility of gaze alternations in bonobos and chimpanzees. Developmental science, 21(4), e12598.
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  Infants' early gaze alternations are one of their first steps towards a sophisticated understanding of the social world. This ability, to gaze alternate between an object of interest and another individual also attending to that object, has been considered foundational to the development of many complex social-cognitive abilities, such as theory of mind and language. However, to understand the evolution of these abilities, it is important to identify whether and how gaze alternations are used and develop in our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Here, we evaluated the development of gaze alternations in a large, developmental sample of bonobos (N = 17) and chimpanzees (N = 35). To assess the flexibility of ape gaze alternations, we tested whether they produced gaze alternations when requesting food from a human who was either visually attentive or visually inattentive. Similarly to human infants, both bonobos and chimpanzees produced gaze alternations, and did so more frequently when a human communicative partner was visually attentive. However, unlike humans, who gaze alternate frequently from early in development, chimpanzees did not begin to gaze alternate frequently until adulthood. Bonobos produced very few gaze alternations, regardless of age. Thus, it may be the early emergence of gaze alternations, as opposed gaze alternations themselves, that is derived in the human lineage. The distinctively early emergence of gaze alternations in humans may be a critical underpinning for the development of complex human social-cognitive abilities.
• MacLean, E. L., & Hare, B. (2018). Enhanced Selection of Assistance and Explosive Detection Dogs Using Cognitive Measures. Frontiers in veterinary science, 5, 236.
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  Working dogs play a variety of important roles, ranging from assisting individuals with disabilities, to explosive and medical detection work. Despite widespread demand, only a subset of dogs bred and trained for these roles ultimately succeed, creating a need for objective measures that can predict working dog aptitude. Most previous research has focused on temperamental characteristics of successful dogs. However, working dogs also face diverse cognitive challenges both in training, and throughout their working lives. We conducted a series of studies investigating the relationships between individual differences in dog cognition, and success as an assistance or detection dog. Assistance dogs ( = 164) and detection dogs ( = 222) were tested in the Dog Cognition Test Battery, a 25-item instrument probing diverse aspects of dog cognition. Through exploratory analyses we identified a subset of tasks associated with success in each training program, and developed shorter test batteries including only these measures. We then used predictive modeling in a prospective study with an independent sample of assistance dogs ( = 180), and conducted a replication study with an independent sample of detection dogs ( = 90). In assistance dogs, models using data on individual differences in cognition predicted higher probabilities of success for dogs that ultimately succeeded in the program, than for those who did not. For the subset of dogs with predicted probabilities of success in the 4th quartile (highest predicted probability of success), model predictions were 86% accurate, on average. In both the exploratory and prospective studies, successful dogs were more likely to engage in eye contact with a human experimenter when faced with an unsolvable task, or when a joint social activity was disrupted. In detection dogs, we replicated our exploratory findings that the most successful dogs scored higher on measures of sensitivity to human communicative intentions, and two measures of short term memory. These findings suggest that that (1) individual differences in cognition contribute to variance in working dog success, and (2) that objective measures of dog cognition can be used to improve the processes through which working dogs are evaluated and selected.
• MacLean, E. L., Gesquiere, L. R., Gee, N., Levy, K., Martin, W. L., & Carter, C. S. (2018). Validation of salivary oxytocin and vasopressin as biomarkers in domestic dogs. Journal of neuroscience methods, 293, 67-76.
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  Oxytocin (OT) and Vasopressin (AVP) are phylogenetically conserved neuropeptides with effects on social behavior, cognition and stress responses. Although OT and AVP are most commonly measured in blood, urine and cerebrospinal fluid (CSF), these approaches present an array of challenges including concerns related to the invasiveness of sample collection, the potential for matrix interference in immunoassays, and whether samples can be collected at precise time points to assess event-linked endocrine responses.
• MacLean, E. L., Gesquiere, L. R., Gee, N. R., Levy, K., Martin, W. L., & Carter, C. S. (2017). Effects of Affiliative Human-Animal Interaction on Dog Salivary and Plasma Oxytocin and Vasopressin. Frontiers in psychology, 8, 1606.
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  Oxytocin (OT) and vasopressin (AVP) are neuropeptides with diverse effects on social behavior, cognition and stress responses. Recent studies suggest that OT facilitates and responds to affiliative forms of human-animal interaction (HAI). However, previous studies measuring OT and AVP in dogs have been limited to measures from blood or urine, which present concerns related to the invasiveness of sample collection, the potential for matrix interference in immunoassays, and whether samples can be collected at precise time points to assess event-linked endocrine responses. Previous studies from our laboratory validated salivary measures of OT and AVP in dogs, however, it is currently unknown whether these measures respond dynamically to aspects of HAI. Here, we investigated the effects of affiliative forms of HAI on both plasma and salivary OT and AVP in dogs. We employed a within- and between-subjects design with a group of Labrador retrievers and Labrador retriever × golden retriever crosses (23 females, 15 males). Half of the dogs engaged in 10 min of free-form friendly interaction with a human experimenter (HAI condition), and the other half rested quietly in the same environment, without human interaction (control condition). We collected blood and saliva samples before, and immediately following both experimental conditions, and all samples were analyzed using enzyme-linked immunosorbent assays (ELISAs) following previously validated protocols. Dogs participating in HAI exhibited a significant increase in both salivary OT (+39%) and plasma OT (+5.7%) whereas dogs in the control group did not. Salivary AVP showed no change in the HAI group but increased significantly (+33%) in the control group. Plasma AVP decreased significantly following HAI (-13%) but did not change across time in the control condition. Within the dogs exposed to HAI, increases in salivary OT, and decreases in plasma AVP, were predicted by the extent of affiliative behavior between the dog and human (indexed by scores from a principal components analysis of social behaviors between the dog and human). Collectively our results suggest that measures of salivary OT and AVP provide useful biomarkers in studies of HAI, and afford a flexible and non-invasive toolkit than can be employed in diverse research contexts.
• MacLean, E. L., Gesquiere, L. R., Gruen, M. E., Sherman, B. L., Martin, W. L., & Carter, C. S. (2017). Endogenous Oxytocin, Vasopressin, and Aggression in Domestic Dogs. Frontiers in psychology, 8, 1613.
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  Aggressive behavior in dogs poses public health and animal welfare concerns, however the biological mechanisms regulating dog aggression are not well understood. We investigated the relationships between endogenous plasma oxytocin (OT) and vasopressin (AVP)-neuropeptides that have been linked to affiliative and aggressive behavior in other mammalian species-and aggression in domestic dogs. We first validated enzyme-linked immunosorbent assays (ELISAs) for the measurement of free (unbound) and total (free + bound) OT and AVP in dog plasma. In Experiment 1 we evaluated behavioral and neuroendocrine differences between a population of pet dogs with a history of chronic aggression toward conspecifics and a matched control group. Dogs with a history of aggression exhibited more aggressive behavior during simulated encounters with conspecifics, and had lower free, but higher total plasma AVP than matched controls, but there were no group differences for OT. In Experiment 2 we compared OT and AVP concentrations between pet dogs and a population of assistance dogs that have been bred for affiliative and non-aggressive temperaments, and investigated neuroendocrine predictors of individual differences in social behavior within the assistance dog population. Compared to pet dogs, assistance dogs had higher free and total OT, but there were no differences in either measure for AVP. Within the assistance dog population, dogs who behaved more aggressively toward a threatening stranger had higher total AVP than dogs who did not. Collectively these data suggest that endogenous OT and AVP may play critical roles in shaping dog social behavior, including aspects of both affiliation and aggression.
• Brandtzaeg, O. K., Johnsen, E., Roberg-Larsen, H., Seip, K. F., MacLean, E. L., Gesquiere, L. R., Leknes, S., Lundanes, E., & Wilson, S. R. (2016). Proteomics tools reveal startlingly high amounts of oxytocin in plasma and serum. Scientific reports, 6, 31693.
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  The neuropeptide oxytocin (OT) is associated with a plethora of social behaviors, and is a key topic at the intersection of psychology and biology. However, tools for measuring OT are still not fully developed. We describe a robust nano liquid chromatography-mass spectrometry (nanoLC-MS) platform for measuring the total amount of OT in human plasma/serum. OT binds strongly to plasma proteins, but a reduction/alkylation (R/A) procedure breaks this bond, enabling ample detection of total OT. The method (R/A + robust nanoLC-MS) was used to determine total OT plasma/serum levels to startlingly high concentrations (high pg/mL-ng/mL). Similar results were obtained when combining R/A and ELISA. Compared to measuring free OT, measuring total OT can have advantages in e.g. biomarker studies.
• MacLean, E. L. (2016). Unraveling the evolution of uniquely human cognition. Proceedings of the National Academy of Sciences of the United States of America, 113(23), 6348-54.
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  A satisfactory account of human cognitive evolution will explain not only the psychological mechanisms that make our species unique, but also how, when, and why these traits evolved. To date, researchers have made substantial progress toward defining uniquely human aspects of cognition, but considerably less effort has been devoted to questions about the evolutionary processes through which these traits have arisen. In this article, I aim to link these complementary aims by synthesizing recent advances in our understanding of what makes human cognition unique, with theory and data regarding the processes of cognitive evolution. I review evidence that uniquely human cognition depends on synergism between both representational and motivational factors and is unlikely to be accounted for by changes to any singular cognitive system. I argue that, whereas no nonhuman animal possesses the full constellation of traits that define the human mind, homologies and analogies of critical aspects of human psychology can be found in diverse nonhuman taxa. I suggest that phylogenetic approaches to the study of animal cognition-which can address questions about the selective pressures and proximate mechanisms driving cognitive change-have the potential to yield important insights regarding the processes through which the human cognitive phenotype evolved.
• Reddy, R. B., Krupenye, C., MacLean, E. L., & Hare, B. (2016). No evidence for contagious yawning in lemurs. Animal cognition, 19(5), 889-98.
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  Among some haplorhine primates, including humans, relaxed yawns spread contagiously. Such contagious yawning has been linked to social bonds and empathy in some species. However, no studies have investigated contagious yawning in strepsirhines. We conducted an experimental study of contagious yawning in strepsirhines, testing ring-tailed and ruffed lemurs (n = 24) in a paradigm similar to one that has induced contagious yawning in haplorhines. First, in a control experiment, we investigated whether lemurs responded to projected video content in general (experiment 1). We showed them two videos to which we expected differential responses: one featured a terrestrial predator and the other a caretaker holding food. Next, to test for yawn contagion, we showed individual lemurs life-size video projections of groupmates and conspecific strangers yawning, and control footage of the same individuals at rest (experiment 2). Then, to examine whether a group context might enhance or allow for contagion, we exposed subjects to the same videos in a group setting (experiment 3). Lemurs produced alarm vocalizations and moved upward while viewing the predator, but not the caretaker, demonstrating that they do perceive video content meaningfully. However, lemurs did not yawn in response to yawning stimuli when tested alone, or with their groupmates. This study provides preliminary evidence that lemurs do not respond to yawning stimuli similarly to haplorhines, and suggests that this behavior may have evolved or become more exaggerated in haplorhines after the two major primate lineages split.
• Bray, E. E., MacLean, E. L., & Hare, B. A. (2015). Increasing arousal enhances inhibitory control in calm but not excitable dogs. Animal cognition, 18(6), 1317-29.
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  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.
• MacLean, E. L., & Hare, B. (2015). Evolution. Dogs hijack the human bonding pathway. Science (New York, N.Y.), 348(6232), 280-1.
• Reddy, R. B., MacLean, E. L., Sandel, A. A., & Hare, B. (2015). Social inhibitory control in five lemur species. Primates; journal of primatology, 56(3), 241-52.
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  We tested five lemur species-ring-tailed lemurs, ruffed lemurs, mongoose lemurs, black lemurs, and Coquerel's sifakas-(N = 52) in an experiment that evaluated skills for inhibitory control in a social context. First, two human experimenters presented identical food rewards; the "generous" experimenter allowed the subject to eat from her hand, whereas the "competitive" experimenter always withheld the reward. Lemurs quickly learned to approach the generous experimenter and avoid the competitive one. In the inhibition test phase, we endowed the competitive experimenter with a more valuable food reward but the competitive experimenter continued to withhold food from the subject. Thus, lemurs were required to inhibit approaching the more desirable reward in favor of the lesser but obtainable reward presented by the generous experimenter. In test trials, lemurs' tendency to approach the competitive experimenter increased from the reputation phase, demonstrating sensitivity to the experimental manipulation. However, subjects approached the larger reward less frequently in test trials compared with pretest food-preference trials, evidencing some capacity for inhibitory control in this context. Despite differences in sociality and ecology, the five lemur species did not differ in this ability. Although the study did not uncover species differences, this experimental task may provide a useful measure of social inhibition in broader comparative studies.
• Stewart, L., MacLean, E. L., Ivy, D., Woods, V., Cohen, E., Rodriguez, K., McIntyre, M., Mukherjee, S., Call, J., Kaminski, J., Miklósi, ., Wrangham, R. W., & Hare, B. (2015). Citizen Science as a New Tool in Dog Cognition Research. PloS one, 10(9), e0135176.
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  Family dogs and dog owners offer a potentially powerful way to conduct citizen science to answer questions about animal behavior that are difficult to answer with more conventional approaches. Here we evaluate the quality of the first data on dog cognition collected by citizen scientists using the Dognition.com website. We conducted analyses to understand if data generated by over 500 citizen scientists replicates internally and in comparison to previously published findings. Half of participants participated for free while the other half paid for access. The website provided each participant a temperament questionnaire and instructions on how to conduct a series of ten cognitive tests. Participation required internet access, a dog and some common household items. Participants could record their responses on any PC, tablet or smartphone from anywhere in the world and data were retained on servers. Results from citizen scientists and their dogs replicated a number of previously described phenomena from conventional lab-based research. There was little evidence that citizen scientists manipulated their results. To illustrate the potential uses of relatively large samples of citizen science data, we then used factor analysis to examine individual differences across the cognitive tasks. The data were best explained by multiple factors in support of the hypothesis that nonhumans, including dogs, can evolve multiple cognitive domains that vary independently. This analysis suggests that in the future, citizen scientists will generate useful datasets that test hypotheses and answer questions as a complement to conventional laboratory techniques used to study dog psychology.
• Bray, E. E., MacLean, E. L., & Hare, B. A. (2014). Context specificity of inhibitory control in dogs. Animal cognition, 17(1), 15-31.
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  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.
• MacLean, E. L., Hare, B., Nunn, C. L., Addessi, E., Amici, F., Anderson, R. C., Aureli, F., Baker, J. M., Bania, A. E., Barnard, A. M., Boogert, N. J., Brannon, E. M., Bray, E. E., Bray, J., Brent, L. J., Burkart, J. M., Call, J., Cantlon, J. F., Cheke, L. G., , Clayton, N. S., et al. (2014). The evolution of self-control. Proceedings of the National Academy of Sciences of the United States of America, 111(20), E2140-8.
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  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.
• MacLean, E. L., Krupenye, C., & Hare, B. (2014). Dogs (Canis familiaris) account for body orientation but not visual barriers when responding to pointing gestures. Journal of comparative psychology (Washington, D.C. : 1983), 128(3), 285-97.
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  In a series of four experiments we investigated whether dogs use information about a human's visual perspective when responding to pointing gestures. While there is evidence that dogs may know what humans can and cannot see, and that they flexibly use human communicative gestures, it is unknown if they can integrate these two skills. In Experiment 1 we first determined that dogs were capable of using basic information about a human's body orientation (indicative of her visual perspective) in a point following context. Subjects were familiarized with experimenters who either faced the dog and accurately indicated the location of hidden food, or faced away from the dog and (falsely) indicated the unbaited container. In test trials these cues were pitted against one another and dogs tended to follow the gesture from the individual who faced them while pointing. In Experiments 2-4 the experimenter pointed ambiguously toward two possible locations where food could be hidden. On test trials a visual barrier occluded the pointer's view of one container, while dogs could always see both containers. We predicted that if dogs could take the pointer's visual perspective they should search in the only container visible to the pointer. This hypothesis was supported only in Experiment 2. We conclude that while dogs are skilled both at following human gestures, and exploiting information about others' visual perspectives, they may not integrate these skills in the manner characteristic of human children.
• MacLean, E., & Hare, B. (2013). Spontaneous triadic engagement in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Journal of comparative psychology (Washington, D.C. : 1983), 127(3), 245-255.
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  Humans are believed to have evolved a unique motivation to participate in joint activities that first develops during infancy and supports the development of shared intentionality. We conducted five experiments with bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) (Total n = 119) to assess their motivation to spontaneously participate in joint activities with a conspecific or a human. We found that even the youngest subjects preferred to interact together with a human and a toy rather than engaging in an identical game alone. In addition, we found that subjects could spontaneously interact with a human in a turn-taking game involving passing a ball back and forth and used behaviors to elicit additional interaction when the game was disrupted. However, when paired with a conspecific, subjects preferred to interact with an object individually rather than together. Our results indicate that nonhuman apes are motivated to engage in triadic activities if they occur spontaneously with humans and require a minimum amount of coordination. These findings leave open the question of whether these activities are coordinated through shared intentions.
• Maclean, E. L., Sandel, A. A., Bray, J., Oldenkamp, R. E., Reddy, R. B., & Hare, B. A. (2013). Group Size Predicts Social but Not Nonsocial Cognition in Lemurs. PloS one, 8(6), e66359.
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  The social intelligence hypothesis suggests that living in large social networks was the primary selective pressure for the evolution of complex cognition in primates. This hypothesis is supported by comparative studies demonstrating a positive relationship between social group size and relative brain size across primates. However, the relationship between brain size and cognition remains equivocal. Moreover, there have been no experimental studies directly testing the association between group size and cognition across primates. We tested the social intelligence hypothesis by comparing 6 primate species (total N = 96) characterized by different group sizes on two cognitive tasks. Here, we show that a species' typical social group size predicts performance on cognitive measures of social cognition, but not a nonsocial measure of inhibitory control. We also show that a species' mean brain size (in absolute or relative terms) does not predict performance on either task in these species. These data provide evidence for a relationship between group size and social cognition in primates, and reveal the potential for cognitive evolution without concomitant changes in brain size. Furthermore our results underscore the need for more empirical studies of animal cognition, which have the power to reveal species differences in cognition not detectable by proxy variables, such as brain size.
• MacLean, E. L., Mandalaywala, T. M., & Brannon, E. M. (2012). Variance-sensitive choice in lemurs: constancy trumps quantity. Animal cognition, 15(1), 15-25.
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  Numerous studies have demonstrated that animals' tolerance for risk when foraging can be affected by changes in metabolic state. Specifically, animals on a negative energy budget increase their preferences for risk, while animals on a positive energy budget are typically risk-averse. The malleability of these preferences may be evolutionarily advantageous, and important for maximizing chances of survival during brief periods of energetic stress. However, animals adapted to living in unpredictable conditions are unlikely to benefit from risk-seeking strategies, and instead are expected to reduce energetic demands while maintaining risk-aversion. We measured risk preferences in lemurs, a group of primates restricted to the island of Madagascar. Lemurs have evolved diverse anatomical and behavioral traits for survival in a harsh and unpredictable ecology, and these traits have been explained as forms of anatomical and behavioral risk reduction. We therefore predicted that lemurs would also be risk-averse in a behavioral task that offered subjects a choice between a small certain reward, and an uncertain but potentially large reward. In Experiment 1, the average rewards associated with the constant and variable options were equal and lemurs exhibited high levels of risk-aversion, replicating a phenomenon that has been demonstrated in dozens of taxa. In Experiment 2, we gradually increased the average value of the variable option relative to the constant option. Lemurs' preferences tracked these changes and subjects became more risk-seeking as the risk premium increased. However, many subjects maintained high levels of risk-aversion even when the average payout of the variable option yielded double that of the constant option. These results are consistent with the notion that lemur cognition has evolved to minimize risk in an unpredictable island environment.
• MacLean, E. L., Matthews, L. J., Hare, B. A., Nunn, C. L., Anderson, R. C., Aureli, F., Brannon, E. M., Call, J., Drea, C. M., Emery, N. J., Haun, D. B., Herrmann, E., Jacobs, L. F., Platt, M. L., Rosati, A. G., Sandel, A. A., Schroepfer, K. K., Seed, A. M., Tan, J., , van Schaik, C. P., et al. (2012). How does cognition evolve? Phylogenetic comparative psychology. Animal cognition, 15(2), 223-38.
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  Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.
• Merritt, D. J., Maclean, E. L., Crawford, J. C., & Brannon, E. M. (2011). Numerical rule-learning in ring-tailed lemurs (lemur catta). Frontiers in psychology, 2, 23.
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  We investigated numerical discrimination and numerical rule-learning in ring-tailed lemurs (Lemur catta). Two ring-tailed lemurs were trained to respond to two visual arrays, each of which contained between one and four elements, in numerically ascending order. In Experiment 1, lemurs were trained with 36 exemplars of each of the numerosities 1-4 and then showed positive transfer to trial-unique novel exemplars of the values 1-4. In Experiments 2A and 2B, lemurs were tested on their ability to transfer an ascending numerical rule from the values 1-4 to novel values 5-9. Both lemurs successfully ordered the novel values with above chance accuracy. Accuracy was modulated by the ratio between the two numerical values suggesting that lemurs accessed the approximate number system when performing the task.
• MacLean, E. L., Barrickman, N. L., Johnson, E. M., & Wall, C. E. (2009). Sociality, ecology, and relative brain size in lemurs. Journal of human evolution, 56(5), 471-8.
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  The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.
• MacLean, E. L., Prior, S. R., Platt, M. L., & Brannon, E. M. (2009). Primate location preference in a double-tier cage: the effects of illumination and cage height. Journal of applied animal welfare science : JAAWS, 12(1), 73-81.
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  Nonhuman primates are frequently housed in double-tier arrangements with significant differences between the environments of the upper and lower-row cages. Although several studies have investigated whether this arrangement alters monkeys' behavior, no studies have addressed the two most notable differences, light and height, individually to determine their relative importance. This experiment examined how rhesus and long-tailed macaques allocated their time between the upper and lower-row cages of a 1-over-1 apartment module under different lighting conditions. In Condition A, monkeys' baseline degree of preference for the upper- and lower-row was tested. In Condition B, the lighting environment was reversed by limiting illumination in the upper-row cage and increasing illumination in the lower-row cage. In both conditions, monkeys spent more time in the upper-row cage, thus indicating a strong preference for elevation regardless of illumination. The amount of time that monkeys spent in the lower-row cage increased by 7% under reversed lighting, but this trend was not significant. These results corroborate the importance of providing captive primates with access to elevated areas.
• Jordan, K. E., Maclean, E. L., & Brannon, E. M. (2008). Monkeys match and tally quantities across senses. Cognition, 108(3), 617-25.
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  We report here that monkeys can actively match the number of sounds they hear to the number of shapes they see and present the first evidence that monkeys sum over sounds and sights. In Experiment 1, two monkeys were trained to choose a simultaneous array of 1-9 squares that numerically matched a sample sequence of shapes or sounds. Monkeys numerically matched across (audio-visual) and within (visual-visual) modalities with equal accuracy and transferred to novel numerical values. In Experiment 2, monkeys presented with sample sequences of randomly ordered shapes or tones were able to choose an array of 2-9 squares that was the numerical sum of the shapes and sounds in the sample sequence. In both experiments, accuracy and reaction time depended on the ratio between the correct numerical match and incorrect choice. These findings suggest monkeys and humans share an abstract numerical code that can be divorced from the modality in which stimuli are first experienced.
• Maclean, E. L., Merritt, D. J., & Brannon, E. M. (2008). Social Complexity Predicts Transitive Reasoning in Prosimian Primates. Animal behaviour, 76(2), 479-486.
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  Transitive Inference is a form of deductive reasoning that has been suggested as one cognitive mechanism by which animals could learn the many relationships within their group's dominance hierarchy. This process thus bears relevance to the social intelligence hypothesis which posits evolutionary links between various forms of social and nonsocial cognition. Recent evidence corroborates the link between social complexity and transitive inference and indicates that highly social animals may show superior transitive reasoning even in nonsocial contexts. We examined the relationship between social complexity and transitive inference in two species of prosimians, a group of primates that diverged from the common ancestor of monkeys, apes, and humans over 50 million years ago. In Experiment 1, highly social ring-tailed lemurs, Lemur catta, outperformed the less social mongoose lemurs, Eulemur mongoz, in tests of transitive inference and showed more robust representations of the underlying ordinal relationships between the stimuli. In Experiment 2, after training under a correction procedure that emphasized the underlying linear dimension of the series, both species showed similar transitive inference. This finding suggests that the two lemur species differ not in their fundamental ability to make transitive inferences, but rather in their predisposition to mentally organize information along a common underlying dimension. Together, these results support the hypothesis that social complexity is an important selective pressure for the evolution of cognitive abilities relevant to transitive reasoning.
• Merritt, D., Maclean, E. L., Jaffe, S., & Brannon, E. M. (2007). A comparative analysis of serial ordering in ring-tailed lemurs (Lemur catta). Journal of comparative psychology (Washington, D.C. : 1983), 121(4), 363-71.
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  Research over the last 25 years has demonstrated that animals are able to organize sequences in memory and retrieve ordered sequences without language. Qualitative differences have been found between the serial organization of behavior in pigeons and monkeys. Here the authors test serial ordering abilities in ring-tailed lemurs, a strepsirrhine primate whose ancestral lineage diverged from that of monkeys, apes, and humans approximately 63 million years ago. Lemurs' accuracy and response times were similar to monkeys, thus suggesting that they may share mechanisms for serial organization that dates to a common primate ancestor.