Transitive or Not: A Critical Appraisal of Transitive Inference in Animals

Transitive inference has been historically touted as a hallmark of human cognition. However, the ability of non‐human animals to perform this type of inference is being increasingly investigated. Experimentally, three main methods are commonly used to evaluate transitivity in animals: those that investigate social dominance relationships, the n‐term task series and the less well known associative transitivity task. Here, we revisit the question of what exactly constitutes transitive inference based upon a formal and habitual definition and propose two essential criteria for experimentally testing it in animals. We then apply these criteria to evaluate the existing body of work on this fundamental aspect of cognition using exemplars. Our evaluation reveals that some methods rely heavily on salient assumptions that are both questionable and almost impossible to verify in order to make a claim of transitive inference in animals. For example, we found shortcomings with most n‐term task designs in that they often do not provide an explicit transitive relationship and/or and ordered set on which transitive inference can be performed. Consequently, they rely on supplementary assumptions to make a claim of transitive inference. However, as these assumptions are either impossible or are extremely difficult to validate in non‐human animals, the results obtained using these specific n‐term tasks cannot be taken as unambiguous demonstrations (or the lack thereof) of transitive inference. This realisation is one that is generally overlooked in the literature. In contrast, the associative transitivity task and the dominance relationship test both meet the criteria for transitive inference. However, although the dominance relationship test can disambiguate between transitive inference accounts and associative ones, the associative transitivity test cannot. Our evaluation also highlights the limitations and future challenges of current associative models of transitive inference. We propose three new experimental methods that can be applied within any theoretical framework to ensure that the experimental behaviour observed is indeed the result of transitive inference whilst removing the need for supplementary assumptions: the test for the opposite transitive relation, the discrimination test between two separate and previously non‐reinforced items, and the control for absolute knowledge.     

Effect of stimulus orderability and reinforcement history on transitive responding in pigeons

Transitive responding in humans and non-human animals has attracted considerable attention because of its presumably inferential nature. In an attempt to replicate our earlier study with crows [Lazareva, O.F., Smirnova, A.A., Bagozkaja, M.S., Zorina, Z.A., Rayevsky, V.V., Wasserman, E.A., 2004. Transitive responding in hooded crows requires linearly ordered stimuli. J. Exp. Anal. Behav. 82, 1-19], we trained pigeons to discriminate overlapping pairs of colored squares (A+ B-, B+ C-, C+ D-, and D+ E-). For some birds, the colored squares, or primary stimuli, were followed by a circle of the same color (feedback stimuli) whose diameter decreased from A to E (Ordered Feedback group); these circles were made available to help order the stimuli along a physical dimension. For other birds, all of the feedback stimuli had the same diameter (Constant Feedback group). In later testing, novel choice pairs were presented, including the critical BD pair. The pigeons' reinforcement history with Stimuli B and D was controlled, so that the birds should not have chosen Stimulus B during the BD test. Unlike the crows, the pigeons selected Stimulus B over Stimulus D in both ordered and Constant Feedback groups, suggesting that the orderability of the post-choice feedback stimuli did not affect pigeons' transitive responding. Post hoc simulations showed that associative models [Wynne, C.D.L., 1995. Reinforcement accounts for transitive inference (TI) performance. Anim. Learn. Behav. 23, 207-217; Siemann, M., Delius, J.D., 1998. Algebraic learning and neural network models for transitive and non-transitive responding. Eur. J. Cogn. Psychol. 10, 307-334] failed to predict pigeons' responding in the BD test.     

Implicit Value Updating Explains Transitive Inference Performance: The Betasort Model

Transitive inference (the ability to infer that B > D given that B > C and C > D) is a widespread characteristic of serial learning, observed in dozens of species. Despite these robust behavioral effects, reinforcement learning models reliant on reward prediction error or associative strength routinely fail to perform these inferences. We propose an algorithm called betasort, inspired by cognitive processes, which performs transitive inference at low computational cost. This is accomplished by (1) representing stimulus positions along a unit span using beta distributions, (2) treating positive and negative feedback asymmetrically, and (3) updating the position of every stimulus during every trial, whether that stimulus was visible or not. Performance was compared for rhesus macaques, humans, and the betasort algorithm, as well as Q-learning, an established reward-prediction error (RPE) model. Of these, only Q-learning failed to respond above chance during critical test trials. Betasort’s success (when compared to RPE models) and its computational efficiency (when compared to full Markov decision process implementations) suggests that the study of reinforcement learning in organisms will be best served by a feature-driven approach to comparing formal models.     

Transitive inference in pigeons: measuring the associative values of Stimuli B and D

Several reinforcement-based models have been proposed to explain transitive-like behavior in nonverbal transitive inference tasks. These models assume that the initial training required for memorizing the premises produces an ordered series of associative values (A>B>C>D>E); these values can then be used to select the "transitively correct" stimulus in a novel pair (e.g., BD). Our study experimentally tested this assumption by using resistance-to-extinction and resistance-to-reinforcement techniques to obtain empirical measures of associative strength for Stimuli B and D. We first measured the associative strengths of these stimuli after completion of initial training with overlapping pairs of colored squares (A+B-, B+C-, C+D-, and D+E-) using resistance-to-extinction and resistance-to-reinforcement procedures. Next, we used massed presentations of Pair D+E- (termed bias reversal) that ought to increase the associative value of Stimulus D, and again measured the associative strengths of the stimuli. None of our experimental measures of associative strength correlated with pigeons' behavior in the BD test or with BD performance predicted by associative models either before or after bias reversal (Wynne, 1995; Siemann and Delius, 1998). These results question validity of reinforcement-based models for explaining animals' behavior in nonverbal TI tasks.     

Mechanistic constraints and the unlikely evolution of reciprocal cooperation

Social evolution theory faces a puzzle: a gap between theoretical and empirical results on reciprocity. On the one hand, models show that reciprocity should evolve easily in a wide range of circumstances. On the other hand, empirically, few clear instances of reciprocity (even in a broad sense) have been found in nonhuman animals. In this paper, I aim to suggest and evaluate a novel reason concurring to solve this puzzle. I propose that it is difficult for reciprocity to evolve because it raises an evolutionary problem of bootstrapping: it requires that two complementary functions: (i) the ability to cooperate and (ii) the ability to respond conditionally to the cooperation of others, arise together and reach a significant frequency, whereas neither of them can be favoured in the absence of the other. I develop analytical models and simulations showing that, for this reason, the evolutionary emergence of reciprocal cooperation is highly unlikely. I then discuss the consequences of this result for our understanding of cooperation.     

Nonverbal transitive inference: Effects of task and awareness on human performance

We studied human nonverbal transitive inference in two paradigms: with choice stimuli orderable along a physical dimension and with non-orderable choice stimuli. We taught 96 participants to discriminate four overlapping pairs of choice stimuli: A+ B−, B+ C−, C+ D−, and D+ E−. Half of the participants were provided with post-choice visual feedback stimuli which were orderable by size; the other half were not provided with orderable feedback stimuli. In later testing, we presented novel choice pairs: BD, AC, AD, AE, BE, and CE. We found that transitive responding depended on task awareness for all participants. Additionally, participants given ordered feedback showed clearer task awareness and stronger transitive responding than did participants not given ordered feedback. Associative models ( [Wynne, 1995] and [Siemann and Delius, 1998]) failed to predict the increase in transitive responding with increasing awareness. These results suggest that ordered and non-ordered transitive inference tasks support different patterns of performance.     

Transitive inference and awareness in humans

Thirty-nine participants performed a transitive inference task. During training, they were shown six pairs of imaginary sports teams and learnt which team was better in each pair. The pairs of teams were adjacent members of a seven-term series of team rankings (A-G). The participants were not explicitly informed of this underlying stimulus hierarchy. Once a participant reached the training criterion, they were tested on the six training pairs and three novel pairs (BD, CE, and DF) that required the participant to make a transitive inference. The participants completed a post-experimental questionnaire that measured their awareness of the stimulus hierarchy. A more-aware group and a less-aware group were created from answers to the questionnaire. The less-aware group were significantly less accurate than the more-aware group on some training pairs and all three novel pairs, and the less-aware group's pattern of performance bore similarities to non-human animal performance.     

Pigeon transitive inference: Tests of simple accounts of a complex performance

This study addressed pigeons' abilities to form transitive inferences and the mechanism by which they do so. Subjects were trained on four operant discriminations in a 5-term series-A + B − , B + C − , C + D − and D + E − (where [ + ] denotes reward, and [ −] non-reward in choice). In unreinforced tests, choice of B over D is evidence of transitive inference formation. Training proceeded without the subjects being presented the training pairs in blocks. Results show that randomized training degrades the performance of pigeons, just as it does human subjects, but that some subjects can still respond transitively under these conditions. In addition, the results support reinforcement models of transitive inference performance.     

Understanding movement data and movement processes: current and emerging directions

Animal movement has been the focus on much theoretical and empirical work in ecology over the last 25 years. By studying the causes and consequences of individual movement, ecologists have gained greater insight into the behavior of individuals and the spatial dynamics of populations at increasingly higher levels of organization. In particular, ecologists have focused on the interaction between individuals and their environment in an effort to understand future impacts from habitat loss and climate change. Tools to examine this interaction have included: fractal analysis, first passage time, Lévy flights, multi‐behavioral analysis, hidden markov models, and state‐space models. Concurrent with the development of movement models has been an increase in the sophistication and availability of hierarchical bayesian models. In this review we bring these two threads together by using hierarchical structures as a framework for reviewing individual models. We synthesize emerging themes in movement ecology, and propose a new hierarchical model for animal movement that builds on these emerging themes. This model moves away from traditional random walks, and instead focuses inference on how moving animals with complex behavior interact with their landscape and make choices about its suitability.     

Economic behaviours among non-human primates

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

The evolution of premating isolation: local adaptation and natural and sexual selection against hybrids

Although reinforcement is ostensibly driven by selection against hybrids, there are often other components in empirical cases and theoretical models of reinforcement that may contribute to premating isolation. One of these components is local adaptation of a trait used in mate choice. I use several different comparisons to assess the roles that local adaptation and selection against hybrids may play in reinforcement models. Both numerical simulations of exact recursion equations and analytical weak selection approximations are employed. I find that selection against hybrids may play a small role in driving preference evolution in a reinforcement model where the mating cue is separate from loci causing hybrid incompatibilities. When females have preferences directly for purebreds of their own population, however, selection against hybrids can play a large role in premating isolation evolution. I present some situations in which this type of selection is likely to exist. This work also illustrates shortfalls of using a weak selection approach to address questions about reinforcement.     

Animal morality: What is the debate about?

Empirical studies of the social lives of non-human primates, cetaceans, and other social animals have prompted scientists and philosophers to debate the question of whether morality and moral cognition exists in non-human animals. Some researchers have argued that morality does exist in several animal species, others that these species may possess various evolutionary building blocks or precursors to morality, but not quite the genuine article, while some have argued that nothing remotely resembling morality can be found in any non-human species. However, these different positions on animal morality generally appear to be motivated more by different conceptions of how the term “morality” is to be defined than by empirical disagreements about animal social behaviour and psychology. After delving deeper into the goals and methodologies of various of the protagonists, I argue that, despite appearances, there are actually two importantly distinct debates over animal morality going on, corresponding to two quite different ways of thinking about what it is to define “morality”, “moral cognition”, and associated notions. Several apparent skirmishes in the literature are thus cases of researchers simply talking past each other. I then focus on what I take to be the core debate over animal morality, which is concerned with understanding the nature and phylogenetic distribution of morality conceived as a psychological natural kind. I argue that this debate is in fact largely terminological and non-substantive. Finally, I reflect on how this core debate might best be re-framed.     

Receivers limit the prevalence of deception in humans: evidence from diving behaviour in soccer players

Deception remains a hotly debated topic in evolutionary and behavioural research. Our understanding of what impedes or facilitates the use and detection of deceptive signals in humans is still largely limited to studies of verbal deception under laboratory conditions. Recent theoretical models of non-human behaviour have suggested that the potential outcome for deceivers and the ability of receivers to discriminate signals can effectively maintain their honesty. In this paper, we empirically test these predictions in a real-world case of human deception, simulation in soccer. In support of theoretical predictions in signalling theory, we show that cost-free deceit by soccer players decreases as the potential outcome for the signaller becomes more costly. We further show that the ability of receivers (referees) to detect deceptive signals may limit the prevalence of deception by soccer players. Our study provides empirical support to recent theoretical models in signalling theory, and identifies conditions that may facilitate human deception and hinder its detection.     

Resource holding potential, subjective resource value, and game theoretical models of aggressiveness signalling

Empirical evidence suggests that aggressiveness (willingness to enter into, or escalate an aggressive interaction) may be more important than the ability to win fights in some species. Both empirical and theoretical traditions treat aggressiveness as a distinct property from the ability (RHP) or motivation (subjective resource value) to win a fight. I examine how these three traits are clearly distinct when modelled using a simple strategic model of escalation. I then examine game theoretical models of agonistic communication and demonstrate that models in which aggressiveness is signalled require: (1) a trait, aggressiveness, which is neither a correlate, nor consequence of RHP or motivation, (2) a handicap which negates any benefit to be gained through the use of a particular signal, and (3) the absence of any other asymmetry which could be used to assign roles to players. I conclude that it is unlikely that these assumptions are ever met, and that empirical examples of "aggressiveness" are far more likely to represent long-term differences in subjective resource value.     

Transfer of a Serial Representation between Two Distinct Tasks by Rhesus Macaques

Do animals form task-specific representations, or do those representations take a general form that can be applied to qualitatively different tasks? Rhesus monkeys (Macaca mulatta) learned the ordering of stimulus lists using two different serial tasks, in order to test whether prior experience in each task could be transfered to the other, enhancing performance. The simultaneous chaining paradigm delivered rewards only after subjects responded in the correct order to all stimuli displayed on a touch sensitive video monitor. The transitive inference paradigm presented pairs of items and delivered rewards when subjects selected the item with the lower ordinal rank. After learning a list in one paradigm, subjects’ knowledge of that list was tested using the other paradigm. Performance was enhanced from the very start of transfer training. Transitive inference performance was characterized by ‘symbolic distance effects,’ whereby the ordinal distance between stimuli in the implied list ordering was strongly predictive of the probability of a correct response. The patterns of error displayed by subjects in both tasks were best explained by a spatially coded representation of list items, regardless of which task was used to learn the list. Our analysis permits properties of this representation to be investigated without the confound of verbal reasoning.     

How general is cognitive ability in non-human animals? A meta-analytical and multi-level reanalysis approach

General intelligence has been a topic of high interest for over a century. Traditionally, research on general intelligence was based on principal component analyses and other dimensionality reduction approaches. The advent of high-speed computing has provided alternative statistical tools that have been used to test predictions of human general intelligence. In comparison, research on general intelligence in non-human animals is in its infancy and still relies mostly on factor-analytical procedures. Here, we argue that dimensionality reduction, when incorrectly applied, can lead to spurious results and limit our understanding of ecological and evolutionary causes of variation in animal cognition. Using a meta-analytical approach, we show, based on 555 bivariate correlations, that the average correlation among cognitive abilities is low (r = 0.185; 95% CI: 0.087–0.287), suggesting relatively weak support for general intelligence in animals. We then use a case study with relatedness (genetic) data to demonstrate how analysing traits using mixed models, without dimensionality reduction, provides new insights into the structure of phenotypic variance among cognitive traits, and uncovers genetic associations that would be hidden otherwise. We hope this article will stimulate the use of alternative tools in the study of cognition and its evolution in animals.     

Affective responses in tamarins elicited by species-specific music

Theories of music evolution agree that human music has an affective influence on listeners. Tests of non-humans provided little evidence of preferences for human music. However, prosodic features of speech (‘motherese’) influence affective behaviour of non-verbal infants as well as domestic animals, suggesting that features of music can influence the behaviour of non-human species. We incorporated acoustical characteristics of tamarin affiliation vocalizations and tamarin threat vocalizations into corresponding pieces of music. We compared music composed for tamarins with that composed for humans. Tamarins were generally indifferent to playbacks of human music, but responded with increased arousal to tamarin threat vocalization based music, and with decreased activity and increased calm behaviour to tamarin affective vocalization based music. Affective components in human music may have evolutionary origins in the structure of calls of non-human animals. In addition, animal signals may have evolved to manage the behaviour of listeners by influencing their affective state.     

Clarifying Baker's Law

Background

Baker''s Law states that colonization by self-compatible organisms is more likely to be successful than colonization by self-incompatible organisms because of the ability for self-compatible organisms to produce offspring without pollination agents. This simple model has proved very successful in plant ecology and has been applied to various contexts, including colonizing or ruderal species, islands colonizers, invasive species or mating system variation across distribution ranges. Moreover, it is one of the only models in population biology linking two traits of major importance in ecology, namely dispersal and mating system. Although Baker''s Law has stimulated a large number of empirical studies reporting the association of self-fertilization and colonizing ability in various contexts, the data have not established a general pattern for the association of traits.

Scope

In this paper, a critical position is adopted to discuss and clarify Baker''s Law. From the literature referring to Baker''s Law, an analysis made regarding how mating success is considered in such studies and discrepancies with population genetics theory of mating systems are highlighted. The data reporting the association of self-fertilization and colonizing ability are also briefly reviewed and the potential bias in interpretation is discussed. Lastly, a recent theoretical model analysing the link between colonizing ability and self-fertilization is considered.

Conclusions

Evolutionary predictions are actually more complex than Baker''s intuitive arguments. It appears that Baker''s Law encompasses a variety of ecological scenarios, which cannot be considered a priori as equivalent. Questioning what has been considered as self-evident for more than 50 years seems a reasonable objective to analyse in-depth dispersal and mating system traits.     

Context-Dependent Evolutionary Models for Non-Coding Sequences: An Overview of Several Decades of Research and an Analysis of Laurasiatheria and Primate Evolution

The past decade has seen a growing interest in evolutionary models that relax the assumption of site-independent evolution for non-coding sequences. While phylogenetic inference using such so-called context-dependent models is currently computationally prohibitive, these models have been shown to yield significant increases in model fit compared to site-independent evolutionary models, which remain the most widely used evolutionary models to study substitution patterns and perform phylogenetic inference. Context-dependent models have been shown to be suited to study the spontaneous deamination of cytosine in mammalian sequences. In this paper, I discuss various approaches presented in recent years to model context-dependent evolution. I start with discussing the empirical research and results that have led to the development of these models. To accurately estimate the context-dependent substitution patterns that arise from these models, accurate sampling of substitution histories under such models is required. Further, appropriate model selection techniques to assess model performance has become more important than ever, given the drastic increase in parameters of context-dependent models and the tendency of older model selection techniques to prefer parameter-rich models. I also present new results on two mammalian datasets (Primate and Laurasiatheria data) to shed a light on so-called lineage-dependent context-dependent evolution. I conclude this paper with a discussion on current challenges in the development of context-dependent modeling approaches.     

Experimental atherosclerosis: a historical overview

Almost one-hundred years ago the first evidence of experimental atherosclerosis was reported. Over the past century, significant advances have been made in the development of animal models of human coronary artery disease. In this minireview, induction of atherosclerotic lesions in several animal models including rodents (mice, rabbits, rats, hamsters, guinea pigs), avian (pigeons, chickens, quail), swine, carnivora (dogs, cats), and non-human primates is discussed. The limitations and advantages of the animal models of atherosclerosis have been summarized. The transgenic/knockout animal models have greatly enhanced our understanding of atherosclerosis. Compared to wild-type counterparts, the knockout/transgenic animals develop atherogenesis faster without a need for a highly atherogenic diet. Although almost all investigations support a causal role for increased plasma cholesterol levels in the development of atherosclerotic vascular disease, an increasing body of evidence indicates serious invqlvement of other factors including oxidative stress, inflammation, infection and other emerging risk factors.