The paradise fish, an advanced animal model for behavioral genetics and evolutionary developmental biology.

Paradise fish (Macropodus opercularis) is an air-breathing freshwater fish species with a signature labyrinth organ capable of extracting oxygen from the air that helps these fish to survive in hypoxic environments. The appearance of this evolutionary innovation in anabantoids resulted in a rewired circulatory system, but also in the emergence of species-specific behaviors, such as territorial display, courtship and parental care in the case of the paradise fish. Early zoologists were intrigued by the structure and function of the labyrinth apparatus and a series of detailed descriptive histological studies at the beginning of the 20th century revealed the ontogenesis and function of this specialized system. A few decades later, these fish became the subject of numerous ethological studies, and detailed ethograms of their behavior were constructed. These latter studies also demonstrated a strong genetic component underlying their behavior, but due to lack of adequate molecular tools, the fine genetic dissection of the behavior was not possible at the time. The technological breakthroughs that transformed developmental biology and behavioral genetics in the past decades, however, give us now a unique opportunity to revisit these old questions. Building on the classic descriptive studies, the new methodologies will allow us to follow the development of the labyrinth apparatus at a cellular resolution, reveal the genes involved in this process and also the genetic architecture behind the complex behaviors that we can observe in this species.

After 150 years of watching: is there a need for synthetic ethology?

The Darwinian idea of mental continuity is about 150 years old. Although nobody has strongly denied this evolutionary link, both conceptually and practically, relative slow advance has been made by ethology and comparative psychology to quantify mental evolution. Debates on the mechanistic interpretation of cognition often struggle with the same old issues (e.g., associationism vs cognitivism), and in general, experimental methods have made also relative slow progress since the introduction of the puzzle box. In this paper, we illustrate the prevailing issues using examples on 'mental state attribution' and 'perspective taking" and argue that the situation could be improved by the introduction of novel methodological inventions and insights. We suggest that focusing on problem-solving skills and constructing artificial agents that aim to correspond and interact with biological ones, may help to understand the functioning of the mind. We urge the establishment of a novel approach, synthetic ethology, in which researchers take on a practical stance and construct artificial embodied minds relying of specific computational architectures the performance of which can be compared directly to biological agents.

Chasing perception in domestic cats and dogs.

Chasing motion is often used to study the perception of inanimate objects as animate. When chasing interaction and independent motions between two agents are displayed simultaneously on a screen, we expect observers to quickly perceive and recognise the chasing pattern (because of its familiarity) and turn their attention to the independent motion (novelty effect). In case of isosceles triangles as moving figures, dogs and humans both display this behaviour, but dogs initially preferred to look at the chasing pattern whereas humans started to increase their gaze towards the independent motion earlier. Here, we compared whether family cats perceive moving inanimate objects as animate and whether their looking behaviour is similar to that of small family dogs. We displayed a chasing and independent motion side by side on a screen in two consecutive trials and assessed subjects' looking behaviour towards the motions. Similarly to previous studies, we found that dogs eventually looked longer at the independent motion, but cats preferred to look at the independent motion at the beginning of the video display and only later shifted their attention to the chasing motion. No difference was found in the frequency of gaze alternation of the two species. Thus, although cats discriminate between the chasing and independent motions, it is not clear whether this discrimination is controlled by animate motion cues. The difference may originate from their ecological situation and/or may be explained by specific perceptual mechanisms.

Multisensory mental representation of objects in typical and Gifted Word Learner dogs.

Little research has been conducted on dogs' (Canis familiaris) ability to integrate information obtained through different sensory modalities during object discrimination and recognition tasks. Such a process would indicate the formation of multisensory mental representations. In Experiment 1, we tested the ability of 3 Gifted Word Learner (GWL) dogs that can rapidly learn the verbal labels of toys, and 10 Typical (T) dogs to discriminate an object recently associated with a reward, from distractor objects, under light and dark conditions. While the success rate did not differ between the two groups and conditions, a detailed behavioral analysis showed that all dogs searched for longer and sniffed more in the dark. This suggests that, when possible, dogs relied mostly on vision, and switched to using only other sensory modalities, including olfaction, when searching in the dark. In Experiment 2, we investigated whether, for the GWL dogs (N = 4), hearing the object verbal labels activates a memory of a multisensory mental representation. We did so by testing their ability to recognize objects based on their names under dark and light conditions. Their success rate did not differ between the two conditions, whereas the dogs' search behavior did, indicating a flexible use of different sensory modalities. Little is known about the cognitive mechanisms involved in the ability of GWL dogs to recognize labeled objects. These findings supply the first evidence that for GWL dogs, verbal labels evoke a multisensory mental representation of the objects.

Individual recognition and long-term memory of inanimate interactive agents and humans in dogs.

Investigation of individual recognition (IR) is difficult due to the lack of proper control of cues and previous experiences of subjects. Utilization of artificial agents (Unidentified Moving Objects: UMOs) may offer a better approach than using conspecifics or humans as partners. In Experiment 1, we investigated whether dogs are able to develop IR of UMOs (that is stable for at least 24 h) or that they only retain a more generalised memory about them. The UMO helped dogs to obtain an unreachable ball and played with them. One day, one week or one month later, we tested whether dogs display specific behaviour toward the familiar UMO over unfamiliar ones (four-way choice test). Dogs were also re-tested in the same helping context and playing interaction. Subjects did not approach the familiar UMO sooner than the others; however, they gazed at the familiar UMO earlier during re-testing of the problem solving task, irrespectively of the delay. In Experiment 2, we repeated the same procedure with human partners, applying a two-way choice test after a week delay, to study whether lack of IR was specific to the UMO. Dogs did not approach the familiar human sooner than the unfamiliar, but they gazed at the familiar partner earlier during re-testing. Thus, dogs do not seem to recognise an individual UMO or human after a short experience, but they remember the interaction with the novel partner in general, even after a long delay. We suggest that dogs need more experience with a specific social partner for the development of long-term memory.

An exploratory analysis of head-tilting in dogs.

Little is known about head-tilts in dogs. Based on previous investigations on the head turning and the lateralised brain pattern of human speech processing in dogs, we hypothesised that head-tilts may be related to increased attention and could be explained by lateralised mental functions. We observed 40 dogs during object-label knowledge tests and analysed head-tilts occurring while listening to humans requesting verbally to fetch a familiar toy. Our results indicate that only dogs that had learned the name of the objects tilted their heads frequently. Besides, the side of the tilt was stable across several months and tests. Thus, we suggest a relationship between head-tilting and processing relevant, meaningful stimuli.

Comparative Brain Imaging Reveals Analogous and Divergent Patterns of Species and Face Sensitivity in Humans and Dogs.

Conspecific-preference in social perception is evident for multiple sensory modalities and in many species. There is also a dedicated neural network for face processing in primates. However, the evolutionary origin and the relative role of neural species sensitivity and face sensitivity in visuo-social processing are largely unknown. In this comparative study, species sensitivity and face sensitivity to identical visual stimuli (videos of human and dog faces and occiputs) were examined using functional magnetic resonance imaging in dogs (n = 20; 45% female) and humans (n = 30; 50% female). In dogs, the bilateral mid suprasylvian gyrus showed conspecific-preference, no regions exhibited face-preference, and the majority of the visually-responsive cortex showed greater conspecific-preference than face-preference. In humans, conspecific-preferring regions (the right amygdala/hippocampus and the posterior superior temporal sulcus) also showed face-preference, and much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Multivariate pattern analyses (MVPAs) identified species-sensitive regions in both species, but face-sensitive regions only in humans. Across-species representational similarity analyses (RSAs) revealed stronger correspondence between dog and human response patterns for distinguishing conspecific from heterospecific faces than other contrasts. Results unveil functional analogies in dog and human visuo-social processing of conspecificity but suggest that cortical specialization for face perception may not be ubiquitous across mammals.SIGNIFICANCE STATEMENT To explore the evolutionary origins of human face-preference and its relationship to conspecific-preference, we conducted the first comparative and noninvasive visual neuroimaging study of a non-primate and a primate species, dogs and humans. Conspecific-preferring brain regions were observed in both species, but face-preferring brain regions were observed only in humans. In dogs, an overwhelming majority of visually-responsive cortex exhibited greater conspecific-preference than face-preference, whereas in humans, much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Together, these findings unveil functional analogies and differences in the organizing principles of visuo-social processing across two phylogenetically distant mammal species.

Social relationship-dependent neural response to speech in dogs.

In humans, social relationship with the speaker affects neural processing of speech, as exemplified by children's auditory and reward responses to their mother's utterances. Family dogs show human analogue attachment behavior towards the owner, and neuroimaging revealed auditory cortex and reward center sensitivity to verbal praises in dog brains. Combining behavioral and non-invasive fMRI data, we investigated the effect of dogs' social relationship with the speaker on speech processing. Dogs listened to praising and neutral speech from their owners and a control person. We found positive correlation between dogs' behaviorally measured attachment scores towards their owners and neural activity increase for the owner's voice in the caudate nucleus; and activity increase in the secondary auditory caudal ectosylvian gyrus and the caudate nucleus for the owner's praise. Through identifying social relationship-dependent neural reward responses, our study reveals similarities in neural mechanisms modulated by infant-mother and dog-owner attachment.

Searching where the treasure is: on the emergence of human companion animal partnership (HCAP).

In our view, the discipline, often referred to as human-animal interaction (HAI), lacks a well-defined conceptual framework. It is too narrow both with respect to the animal species investigated and the nature of human-animal interactions studied. So instead, we introduce the term human-companion animal partnership (HCAP) that is not only a better descriptor for most research efforts within HAI but also helps to direct research efforts on an ethological basis. In our approach, 'companion' is a function and not a feature of some species. This means that many species had and could have a potential to form mixed social groups with humans if they evolve some capacity of social competence. This view may initiate new comparative research involving a range of species to find out how complex social engagement could be maintained in such hetero-specific social groups based on evolutionary heritage, recent selection and individual experience (socialisation). Our approach emphasises the role of human caring behaviour and social competence in the emergence of a partnership with several species, and thus could also help in setting expectations for welfare and aid in designing artificial companions for specific purposes.

Did we find a copycat? Do as I Do in a domestic cat (Felis catus).

This study shows evidence of a domestic cat (Felis catus) being able to successfully learn to reproduce human-demonstrated actions based on the Do as I Do paradigm. The subject was trained to reproduce a small set of familiar actions on command "Do it!" before the study began. To test feature-contingent behavioural similarity and control for stimulus enhancement, our test consisted of a modified version of the two-action procedure, combined with the Do as I Do paradigm. Instead of showing two different actions on an object to different subjects, we applied a within-subject design and showed the two actions to the same subject in separate trials. We show evidence that a well-socialized companion cat was able to reproduce actions demonstrated by a human model by reproducing two different actions that were demonstrated on the same object. Our experiment provides the first evidence that the Do as I Do paradigm can be applied to cats, suggesting that the ability to recognize behavioural similarity may fall within the range of the socio-cognitive skills of this species. The ability of reproducing the actions of a heterospecific human model in well-socialized cats may pave the way for future studies addressing cats' imitative skills.

The lack of validity hinders research in animal cognition.

Comparability of specific behavioral skills in diverse animal species is of central importance in animal cognition. Yet, as the present analysis of "rescuing behavior" shows, the lack of validity analysis may lead to contradictory results.

Non-adherence to preventive behaviours during the COVID-19 epidemic: findings from a community study.

BACKGROUNDS: Preventive behaviours are an essential way to slow down and eliminate the transmission of SARS-CoV-2. The aim of this study was to estimate adherence to preventive behaviors and to identify whether any subgroups were not adopting these behaviours and for whom greater engagement in these approaches was indicated. METHODS: In this cross-sectional study, we obtained data from a random sample of a panel representing men and women of adult age residing in Hungary (N = 5254). The survey included questions about the frequencies of preventive behaviours, perceived susceptibility and severity of COVID-19. RESULTS: We found four factors of preventive behaviours: using physical barriers (mask and gloves), avoidance of close contacts, personal hygiene, and preparation. We identified two broadly adherent groups (36.8 and 45.3%) and two non-adherent groups (13.1 and 4.8%). Being male and being aged between 18 and 29 years were the strongest predictors of non-adherence. Concern about the severity of COVID-19 was a predictor of adherence. CONCLUSIONS: To ensure maximal adherence to preventive behaviours for COVID-19, additional strategies should focus on their adoption by men and young adults.

The role of common ancestry and gene flow in the evolution of human-directed play behaviour in dogs.

Among-population variance of phenotypic traits is of high relevance for understanding evolutionary mechanisms that operate in relatively short timescales, but various sources of nonindependence, such as common ancestry and gene flow, can hamper the interpretations. In this comparative analysis of 138 dog breeds, we demonstrate how such confounders can independently shape the evolution of a behavioural trait (human-directed play behaviour from the Dog Mentality Assessment project). We combined information on genetic relatedness and haplotype sharing to reflect common ancestry and gene flow, respectively, and entered these into a phylogenetic mixed model to partition the among-breed variance of human-directed play behaviour while also accounting for within-breed variance. We found that 75% of the among-breed variance was explained by overall genetic relatedness among breeds, whereas 15% could be attributed to haplotype sharing that arises from gene flow. Therefore, most of the differences in human-directed play behaviour among breeds have likely been caused by constraints of common ancestry as a likely consequence of past selection regimes. On the other hand, gene flow caused by crosses among breeds has played a minor, but not negligible role. Our study serves as an example of an analytical approach that can be applied to comparative situations where the effects of shared origin and gene flow require quantification and appropriate statistical control in a within-species/among-population framework. Altogether, our results suggest that the evolutionary history of dog breeds has left remarkable signatures on the among-breed variation of a behavioural phenotype.

The molecular effect of a polymorphic microRNA binding site of Wolfram syndrome 1 gene in dogs.

BACKGROUND: Although the molecular function of wolframin remains unclear, the lack of this protein is known to cause stress in the endoplasmic reticulum. Some variants in the Wolfram Syndrome 1 gene (WFS1) were associated with various neuropsychiatric disorders in humans, such as aggressiveness, impulsivity and anxiety. RESULTS: Here we present an in silico study predicting a single nucleotide polymorphism (rs852850348) in the canine WFS1 gene which was verified by direct sequencing and was genotyped by a PCR-based technique. We found that the rs852850348 polymorphism is located in a putative microRNA (cfa-miR-8834a and cfa-miR-1838) binding site. Therefore, the molecular effect of allelic variants was studied in a luciferase reporter system that allowed assessing gene expression. We demonstrated that the variant reduced the activity of the reporter protein expression in an allele-specific manner. Additionally, we performed a behavioral experiment and investigated the association with this locus to different performance in this test. Association was found between food possessivity and the studied WFS1 gene polymorphism in the Border collie breed. CONCLUSIONS: Based on our findings, the rs852850348 locus might contribute to the genetic risk of possessivity behavior of dogs in at least one breed and might influence the regulation of wolframin expression.

Age influences domestic dog cognitive performance independent of average breed lifespan.

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.

The link between selection for function and human-directed play behaviour in dogs.

Human-directed play behaviour is a distinct behavioural feature of domestic dogs. But the role that artificial selection for contemporary dog breeds has played for human-directed play behaviour remains elusive. Here, we investigate how human-directed play behaviour has evolved in relation to the selection for different functions, considering processes of shared ancestry and gene flow among the different breeds. We use the American Kennel Club (AKC) breed group categorization to reflect the major functional differences and combine this with observational data on human-directed play behaviour for over 132 breeds across 89 352 individuals from the Swedish Dog Mentality Assessment project. Our analyses demonstrate that ancestor dogs already showed intermediate levels of human-directed play behaviour, levels that are shared with several modern breed types. Herding and Sporting breeds display higher levels of human-directed play behaviour, statistically distinguishable from Non-sporting and Toy breeds. Our results suggest that human-directed play behaviour played a role in the early domestication of dogs and that subsequent artificial selection for function has been important for contemporary variation in a behavioural phenotype mediating the social bond with humans.

Absolute brain size predicts dog breed differences in executive function.

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.

Is a local sample internationally representative? Reproducibility of four cognitive tests in family dogs across testing sites and breeds.

A fundamental precept of the scientific method is reproducibility of methods and results, and there is growing concern over the failure to reproduce significant results. Family dogs have become a favoured species in comparative cognition research, but they may be subject to cognitive differences arising from genetic (breeding lines) or cultural differences (e.g. preferred training methods). Such variation is of concern as it affects the validity and generalisability of experimental results. Despite its importance, this problem has not been specifically addressed to date. Therefore, we aimed to test the influence of three factors on reproducibility: testing site (proximal environment), breed and sex (phenotype). The same experimenter tested cognitive performance by more than 200 dogs in four experiments. Additionally, dogs' performance was tested in an obedience task administered by the owner. Breed of dog and testing site were found to influence the level of performance only mildly, and only in a means-end experiment and the obedience task. Our findings demonstrate that by applying the same test protocols on sufficiently large samples, the reported phenomena in these cognitive tests can be reproduced, but slight differences in performance levels can occur between different samples. Accordingly, we recommend the utilisation of well-described protocols supported by video examples of the whole experimental procedure. Findings should focus on the main outcome variables of the experiments, rather than speculating about the general importance of small or secondary performance outcomes which are more susceptible to random or local noise.

Perception of animacy in dogs and humans.

Humans have a tendency to perceive inanimate objects as animate based on simple motion cues. Although animacy is considered as a complex cognitive property, this recognition seems to be spontaneous. Researchers have found that young human infants discriminate between dependent and independent movement patterns. However, quick visual perception of animate entities may be crucial to non-human species as well. Based on general mammalian homology, dogs may possess similar skills to humans. Here, we investigated whether dogs and humans discriminate similarly between dependent and independent motion patterns performed by geometric shapes. We projected a side-by-side video display of the two patterns and measured looking times towards each side, in two trials. We found that in Trial 1, both dogs and humans were equally interested in the two patterns, but in Trial 2 of both species, looking times towards the dependent pattern decreased, whereas they increased towards the independent pattern. We argue that dogs and humans spontaneously recognized the specific pattern and habituated to it rapidly, but continued to show interest in the 'puzzling' pattern. This suggests that both species tend to recognize inanimate agents as animate relying solely on their motions.

Interacting effect of two social factors on 18-month-old infants' imitative behavior: Communicative cues and demonstrator presence.

Certain aspects of a demonstration have been shown to influence infants' interpretation of an observational situation and result in selective imitation. Studying social factors that trigger selective imitation may improve our understanding of how infants encode certain situations. However, only a few studies have investigated the possible interactions among these factors. In our study, 18-month-old infants (N=54) observed an adult demonstrator retrieve a toy from under an opaque ("baited") container by manipulating another transparent empty one. Infants were assigned to one of four conditions representing all combinations of two social factors: ostensive communication during demonstration (Communicative vs. Non-communicative) and presence of the demonstrator during reenactment (D-present vs. D-not present). Results suggest that infants' choice behavior was formed in two steps: during the demonstration and during the test phase. Furthermore, an interaction between the effects of the two levels was observed. Communication during the demonstration triggered imitative learning. Infants tended to copy the observed manipulation to learn the communicatively assigned way to reach the goal. This choice behavior was not influenced later by the presence or absence of the demonstrator. The non-communicative demonstration, however, did not elicit a particular learning mechanism. Therefore, in this situation, infants' choice behavior was affected by the demonstrator's presence or absence. Infants developed an individual solution and chose the baited container in the D-not present condition, indicative of emulation. In the D-present situation, they were more likely to reproduce the observed manipulation, which can be interpreted as a tendency to communicate with or conform to the demonstrator.