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Strong selection on complex traits can lead to skewed trait means and reduced trait variability in populations. An example of this phenomenon can be evidenced in allele frequency changes and skewed trait distributions driven by persistent human-directed selective pressures in domesticated species. Dog domestication is linked to several genomic variants; however, the functional impacts of these variants may not always be straightforward when found in non-coding regions of the genome. Four polymorphic transposable elements (TE) found within non-coding sites along a 5 Mb region on canine CFA6 have evolved due to directional selection associated with heightened human-directed hyper-sociability in domesticated dogs. We found that the polymorphic TE in intron 17 of the canine GTF2I gene, which was previously reported to be negatively correlated with canid human-directed hyper-sociability, is associated with altered chromatin looping and hence distinct cis-regulatory landscapes. We reported supporting evidence of an E2F1-DNA binding peak concordant with the altered loop and higher expression of GTF2I exon 18, indicative of alternative splicing. Globally, we discovered differences in pathways regulating the extra-cellular matrix with respect to TE copy number. Overall, we reported evidence suggesting an intriguing molecular convergence between the emergence of hypersocial behaviors in dogs and the same genes that, when hemizygous, produce human Williams Beuren Syndrome characterized by cranio-facial defects and heightened social behaviors. Our results additionally emphasize the often-overlooked potential role of chromatin architecture in social evolution.
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Cromatina , Elementos de DNA Transponíveis , Cães , Animais , Cromatina/genética , Humanos , Comportamento Animal , Comportamento SocialRESUMO
Emotionally expressive vocalizations can elicit approach-avoidance responses in humans and non-human animals. We investigated whether artificially generated sounds have similar effects on humans. We assessed whether subjects' reactions were linked to acoustic properties, and associated valence and intensity. We generated 343 artificial sounds with differing call lengths, fundamental frequencies and added acoustic features across 7 categories and 3 levels of biological complexity. We assessed the hypothetical behavioural response using an online questionnaire with a manikin task, in which 172 participants indicated whether they would approach or withdraw from an object emitting the sound. (1) Quieter sounds elicited approach, while loud sounds were associated with avoidance. (2) The effect of pitch was modulated by category, call length and loudness. (2a) Low-pitched sounds in complex sound categories prompted avoidance, while in other categories they elicited approach. (2b) Higher pitch in loud sounds had a distancing effect, while higher pitch in quieter sounds prompted approach. (2c) Longer sounds promoted avoidance, especially at high frequencies. (3) Sounds with higher intensity and negative valence elicited avoidance. We conclude that biologically based acoustic signals can be used to regulate the distance between social robots and humans, which can provide an advantage in interactive scenarios.
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Estimulação Acústica , Motivação , Som , Humanos , Masculino , Feminino , Adulto , Motivação/fisiologia , Adulto Jovem , Inquéritos e Questionários , Emoções/fisiologiaRESUMO
Research into dogs' olfactory ability is growing rapidly. However, generalising based on scientific results is challenging, because research has been typically conducted on a few specially trained subjects of a few breeds tested in different environmental conditions. We investigated the effects of temperature and humidity (outdoors), age, test location, sex, neutering status, and repeated testing (outdoors and indoors) on the olfactory performance of untrained family dogs (N = 411) of various breeds. We employed the Natural Detection Task with three difficulty levels, from which we derived two performance metrics: Top Level and Success Score. Temperature (0-25 °C) and humidity (18-90%) did not affect olfactory performance. Young adult dogs surpassed other age groups in reaching the Top Level. Sex and neutering status showed no discernible influence on Top Level and Success Score. Dogs performed better in both metrics when tested indoors compared to outdoors. In the test-retest procedure no significant learning effect was observed. We confirmed on untrained companion dogs that olfactory performance declines with age and rejected some factors that have been previously hypothesised to significantly affect dogs' olfactory success. The influence of the testing environment was notable, emphasising the need to consider various factors in understanding dogs' olfactory capabilities.
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Olfato , Animais , Cães , Masculino , Olfato/fisiologia , Feminino , Comportamento Animal/fisiologia , Temperatura , Umidade , Fatores Etários , Percepção Olfatória/fisiologiaRESUMO
Amongst fishes, zebrafish (Danio rerio) has gained popularity as a model system over most other species and while their value as a model is well documented, their usefulness is limited in certain fields of research such as behavior. By embracing other, less conventional experimental organisms, opportunities arise to gain broader insights into evolution and development, as well as studying behavioral aspects not available in current popular model systems. The anabantoid paradise fish (Macropodus opercularis), an "air-breather" species has a highly complex behavioral repertoire and has been the subject of many ethological investigations but lacks genomic resources. Here we report the reference genome assembly of M. opercularis using long-read sequences at 150-fold coverage. The final assembly consisted of 483,077,705 base pairs (~483 Mb) on 152 contigs. Within the assembled genome we identified and annotated 20,157 protein coding genes and assigned ~90% of them to orthogroups.
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Peixes , Genoma , Animais , Peixes/genéticaRESUMO
Dogs that have a vocabulary of object labels (Gifted Word Learner dogs-GWL dogs) have great potential as a comparative model for studying a variety of cognitive mechanisms. However, only a handful of studies, with a small sample size of 1 or 2 dogs, have examined this phenomenon. GWL dogs appear to share many of the same distinctive characteristics, but due to their rarity, it is not clear if these similarities are only anecdotal or indeed reflect characteristics that are similar in these rare individuals. Here we present the first study conducted on a relatively large sample of 41 GWL dogs that were recruited and tested using a citizen science model. After testing the dogs' receptive vocabulary of toy names, we asked the owners to complete a questionnaire about their and their dog's life experiences. Our findings highlight several characteristics that are shared among most GWL dogs, such as their learning speed, their large vocabulary, and that they learned the names of the toys spontaneously, without the explicit intent of their owners. Our findings validate previous anecdotal evidence on common characteristics of GWL dogs and supply additional support to the hypothesis that these dogs represent a unique group of dogs.
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Ciência do Cidadão , Vínculo Humano-Animal , Cães , Animais , Aprendizagem , Cognição , VocabulárioRESUMO
The dog is a so far unique species to study interspecific communication and a promising evolutionary model for preverbal human communication. Recently cats were reported to show some similar skills to dogs. Here we directly compared both the testability and the success of companion dogs and cats in relying on human distal pointing gestures. Due to differences in their domestication, social and ecological background, and developmental processes, we expected better performance from dogs compared to cats. Using an object-choice task, cats made considerably fewer choices than dogs in the laboratory environment, and their tendency to make a choice declined during trials. They were slightly more testable at home, where their willingness to choose did not decrease over time. Dogs made more successful choices than cats, both at the group and individual level, irrespective of the type of the pointing gesture. Older cats were more successful. Despite the two species' rather similar role nowadays as human companions, our results support previous findings suggesting that, compared to the dog, the cat is a less ideal model to study some human communicative abilities in a laboratory environment.
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Doenças do Gato , Doenças do Cão , Humanos , Cães , Animais , Gatos , Gestos , DomesticaçãoRESUMO
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.
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Despite serious health and longevity problems, small brachycephalic breeds are becoming increasingly popular among pet owners. Motivations for choosing short-nosed breeds have been extensively investigated in recent years; however, this issue has been addressed mainly by relying on owner reports, resulting in explanations of "cute looks", referring to the baby-schema phenomenon and "behaviour well suited for companionship". We aimed to compare the behaviour of two brachycephalic (English and French bulldogs) and one mesocephalic (Mudi) breed in a problem-solving context. The dogs were given the task of opening boxes containing food rewards. We investigated human-directed behaviour elements over success and latency (indicators of motivation and ability). We found that both English and French bulldogs were significantly less successful in solving the problem than mudis. Both brachycephalic breeds had longer opening latencies than the mesocephalic breed. Brachycephalic breeds oriented less at the problem box and more at humans present. In summary, the short-headed breeds were less successful but oriented much more toward humans than mesocephalic dogs. Owners might interpret these behaviours as "helplessness" and dependence. The results support the hypothesis that infant-like traits may be present not only in appearance but also in behaviour in brachycephalic breeds, eliciting caring behaviour in owners.
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Relações Interpessoais , Motivação , Lactente , Humanos , Cães , Animais , Cruzamento , Emoções , AlimentosRESUMO
In their recent paper, Hansen Wheat et al. (Ecology and Evolution, 2022, 12, e9299) claimed that hand raised 23-week-old wolves showed the same attachment behaviour towards their handler in the Strange Situation Test (SST) (Determinants of infant behavior, 1969, 4, 111) as dogs. At first glance, their results seem to contradict previous findings that domestication caused a unique change in social-affiliative behaviours in dogs (Animal Behaviour, 2005, 70, 1367). We argue that no persuading evidence was presented to claim that "wolves can show attachment behaviours towards humans comparable to those of dogs". When dealing with a behaviour system (Child Development, 1977, 48, 1184), the subjects' behaviour must meet consistent criteria (Behavioural and Brain Science, 1978, 3, 417), and a few behavioural preferences should not be used to claim the presence of an attachment system, especially, if the experiment violates basic assumptions of the original test. We believe the intriguing scientific question is whether the dog-owner relationship is qualitatively different from what could be observed in the wolf-hand raiser relation. Assessing all available data, our answer is still yes; dogs are unique in this respect.
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We have investigated dogs' (Canis familiaris) abilities in associating different sounds with appetitive stimuli of different incentive values. The association's establishment was first tested on family dogs (n = 20) in a problem-solving behavioural paradigm (experiment 1), then in a problem-solving behavioural paradigm as well as an fMRI study on specially trained family dogs (n = 20) (experiment 2). The aim was to show behavioural and parallel neural effects of the association formed between the two sounds and two different associated appetitive stimuli. The latency of solving the problem was considered an indicator of the motivational state. In our first experiment, where only behaviour was studied, we found that dogs were quicker in solving a problem upon hearing the sound associated with food higher in reward value, suggesting that they have successfully associated the sounds with the corresponding food value. In our second experiment, this behaviour difference was not significant. In the fMRI study, the cerebral response to the two sounds was compared both before and after the associative training. Two bilateral regions of interest were explored: the caudate nucleus and the amygdala. After the associative training, the response in the caudate nucleus was higher to the sound related to a higher reward value food than to the sound related to a lower reward value food, which difference was not present before the associative training. We found an increase in the amygdala response to both sounds after the training. In a whole-brain representational similarity analysis, we found that cerebral patterns in the caudate nucleus to the two sounds were different only after the training. Moreover, we found a positive correlation between the dissimilarity index in the caudate nucleus for activation responses to the two sounds and the difference in latencies (i.e. high reward value associated sound condition latency-low reward value associated sound condition latency) to solve the behavioural task: the bigger the difference between the conditions in latency to solve the task, the greater the difference in the neural representation of the two sounds was. In summary, family dogs' brain activation patterns reflected their expectations based on what they learned about the relationship between two sounds and their associated appetitive stimuli.
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Núcleo Caudado , Resolução de Problemas , Cães , Animais , Núcleo Caudado/diagnóstico por imagem , Encéfalo , Aprendizagem , RecompensaRESUMO
Over the decades, a small number of model species, each representative of a larger taxa, have dominated the field of biological research. Amongst fishes, zebrafish (Danio rerio) has gained popularity over most other species and while their value as a model is well documented, their usefulness is limited in certain fields of research such as behavior. By embracing other, less conventional experimental organisms, opportunities arise to gain broader insights into evolution and development, as well as studying behavioral aspects not available in current popular model systems. The anabantoid paradise fish (Macropodus opercularis), an "air-breather" species from Southeast Asia, has a highly complex behavioral repertoire and has been the subject of many ethological investigations, but lacks genomic resources. Here we report the reference genome assembly of Macropodus opercularis using long-read sequences at 150-fold coverage. The final assembly consisted of ≈483 Mb on 152 contigs. Within the assembled genome we identified and annotated 20,157 protein coding genes and assigned ≈90% of them to orthogroups. Completeness analysis showed that 98.5% of the Actinopterygii core gene set (ODB10) was present as a complete ortholog in our reference genome with a further 1.2 % being present in a fragmented form. Additionally, we cloned multiple genes important during early development and using newly developed in situ hybridization protocols, we showed that they have conserved expression patterns.
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Innovation is a critical component of human society, setting us apart from other animals. We possess a unique capacity to design and produce new things through cultivating a culture that values and encourages innovation. One remarkable instance of innovation in the field of biology and medicine is the mRNA vaccine platform developed by Katalin Karikó and her colleagues. In this article, we delve into the evolution of mRNA-based therapy, beginning with animal models and concluding with the first clinical trials. The history of mRNA research began with the identification of its role in protein synthesis, leading to the development of mRNA vaccine technology. Karikó's pivotal innovation was discovering the need to integrate modified nucleosides into the mRNA, decreasing its recognition by the immune system. Her story offers valuable lessons, including the importance of market demand as a booster effect, the role of emerging technologies, the significance of universities and academic institutions in fostering innovation, the role of perseverance and faith, and the role of chance.
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RNA Mensageiro , Vacinas de mRNA , HumanosRESUMO
Since the dawn of comparative cognitive research, dogs were suspected to possess some capacity for responding to human spoken language. Neuroimaging studies have supported the existence of relevant mechanisms, but convincing behavioral performance is rare, with only few exceptional dogs worldwide demonstrating a lexicon of object-labels they respond to. In the present study we aimed to investigate if and how a capacity for processing verbal stimuli is expressed in dogs (N = 20), whose alleged knowledge of verbal labels is only backed-up by owner reports taken at face value, and concerning only a few words (on average 5). Dogs were tested in a two-choice paradigm with familiar objects. The experiment was divided into a cue-control condition (objects visible to the owner vs. shielded by a panel, thereby controlling the owner's ability to emit cues to the dog) and a response type condition (fetching vs. looking). Above chance performance in fetching and looking at the named object emerged on the level of the sample as a whole. Only one individual performed reliably above chance, but the group-level effect did not depend on this data point. The presence of the panel also had no influence, which supports that performance was not driven by non-verbal cues from the owners. The group-level effect suggests that in typical dogs object-label learning is an instable process, either due to the animals primarily engaging in contextual learning or possibly analogous to the early stages of implicit, statistical learning of words in humans and opposed to the rapid mapping reported in exceptional dogs with larger passive vocabulary.
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Sinais (Psicologia) , Aprendizagem , Humanos , Cães , AnimaisRESUMO
Animal-robot interaction studies provide outstanding opportunities to understand the principles of social interactions. Here we investigated whether dogs' behaviour toward a cooperative artificial agent (Unidentified Moving Object (UMO)) is influenced by receiving a reward directly from the agent, and by variability in the UMO's location. In a problem-solving task, the UMO either helped dogs to obtain food (Direct Reward Group, DRG) or to fetch an object followed by an indirect reward from the owner/experimenter (Indirect Reward Group, IRG). During the Familiarization, the UMO either started from the same location or changed its starting location in all trials. In the Test phase, dogs faced the same task, but additionally a second, unfamiliar UMO was present. We found that both reward groups gazed at the UMO with decreasing latency during the Familiarization, with the IRG showing more gaze alternations between UMO and hiding location. Dogs showed no preference for either UMO in the Test phase but looked at the familiar UMO sooner if it had changed its location during the Familiarization. Thus, direct reward is not necessary to elicit elements of socially competent behavior in dogs, but variability in its motion may be important to improve the UMO's animacy and promote flexible learning.
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Comportamento Animal , Comportamento Social , Animais , Cães , Resolução de Problemas , Aprendizagem , RecompensaRESUMO
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.
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Etologia , Psicologia Comparada , Animais , Cognição , Resolução de ProblemasRESUMO
Research on the socio-cognitive skills of different species often benefit from comparative experiments, however, the ecology of the species and development of the individuals may differently determine how they react to the same test situation. In this study, our aims were twofold: to observe and compare the spontaneous behaviour of companion cats and dogs in the same novel environment, and to habituate them (if needed) to the novel environment in the presence of their owners and an unfamiliar experimenter. The behaviour of 62 family cats, 31 experienced (which had the opportunity to meet strangers and explore unfamiliar places) and 31 inexperienced cats, and 27 family dogs was compared in an unfamiliar room. The subjects' behaviour was coded during the first five minutes in the presence of two passive persons, their owners, and an unfamiliar experimenter. Then, based on a set of rules, first the owner, and then the experimenter tried to initiate interactions with the subjects and the subjects' willingness to interact was evaluated. To pass the habituation test, subjects were expected to play with the experimenter or accept food from them. All dogs passed the test on the first occasion, while almost 60% of the cats failed. The cats' experience did not play a significant role, in fact, younger cats passed more easily. We found marked differences between dogs and cats in all behavioural variables; compared to dogs, cats spent more time crouching and close to their box, while less time exploring or close to the owner. We did not find a difference in the cats' behaviour based on their experience. Our results support the hypothesis that unlike dogs, cats need extensive habituation in a novel environment. This could partially be explained by the difference in the ecology and/or domestication process of the species, although developmental effects cannot be excluded. Our findings have fundamental consequences not only for the considerations of the testability of cats and on the interpretation of their data collected in the laboratory, but in a more general sense on developing comparative experiments.
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Self-propelled motion cues elicit the perception of inanimate objects as animate. Studies usually rely on the looking behaviour of subjects towards stimuli displayed on a screen, but utilizing artificial unidentified moving objects (UMOs) provides a more natural, interactive context. Here, we investigated whether cats and dogs discriminate between UMOs showing animate vs inanimate motion, and how they react to the UMOs' interactive behaviour. Subjects first observed, in turn, the motion of an animate and an inanimate UMO, and then they could move freely for 2 min while both UMOs were present (two-way choice phase). In the following specific motion phase, the animate UMO showed one of three interactive behaviours: pushing a ball, a luring motion, or moving towards the subject (between-subject design). Then, subjects could move freely for 2 min again while the UMO was motionless. At the end, subjects were free to move in the room while the UMO was moving semi-randomly in the room. We found that dogs approached and touched the UMO(s) sooner and more frequently than cats, regardless of the context. In the two-way choice phase, dogs looked at the animate UMO more often, and both species touched the animate UMO more frequently. However, whether the UMO showed playing, luring or assertive behaviour did not influence subjects' behaviour. In summary, both species displayed distinctive behaviour towards the animate UMO, but in dogs, in addition to the physical contact this was also reflected by the looking behaviour. Overall, dogs were more keen to explore and interact with the UMO than cats, which might be due to the general increased stress of cats in novel environments. The findings indicate the importance of measuring multiple behaviours when assessing responses to animacy. The live demonstration using artificial agents provides a unique opportunity to study social perception in nonhuman species.
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Percepção de Movimento , Cães , Gatos , Animais , Percepção de Movimento/fisiologia , Sinais (Psicologia) , Movimento (Física)RESUMO
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.
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Gatos , Cães , Percepção de Movimento , Animais , Humanos , Sinais (Psicologia) , Atenção , Comportamento AnimalRESUMO
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.