Insights into adaptive behavioural plasticity from the guppy model system.

Behavioural plasticity allows organisms to respond to environmental challenges on short time scales. But what are the ecological and evolutionary processes that underlie behavioural plasticity? The answer to this question is complex and requires experimental dissection of the physiological, neural and molecular mechanisms contributing to behavioural plasticity as well as an understanding of the ecological and evolutionary contexts under which behavioural plasticity is adaptive. Here, we discuss key insights that research with Trinidadian guppies has provided on the underpinnings of adaptive behavioural plasticity. First, we present evidence that guppies exhibit contextual, developmental and transgenerational behavioural plasticity. Next, we review work on behavioural plasticity in guppies spanning three ecological contexts (predation, parasitism and turbidity) and three underlying mechanisms (endocrinological, neurobiological and genetic). Finally, we provide three outstanding questions that could leverage guppies further as a study system and give suggestions for how this research could be done. Research on behavioural plasticity in guppies has provided, and will continue to provide, a valuable opportunity to improve understanding of the ecological and evolutionary causes and consequences of behavioural plasticity.

Alarm cues and alarmed conspecifics: neural activity during social learning from different cues in Trinidadian guppies.

Learning to respond appropriately to novel dangers is often essential to survival and success, but carries risks. Learning about novel threats from others (social learning) can reduce these risks. Many species, including the Trinidadian guppy (Poecilia reticulata), respond defensively to both conspecific chemical alarm cues and conspecific anti-predator behaviours, and in other fish such social information can lead to a learned aversion to novel threats. However, relatively little is known about the neural substrates underlying social learning and the degree to which different forms of learning share similar neural mechanisms. Here, we explored the neural substrates mediating social learning of novel threats from two different conspecific cues (i.e. social cue-based threat learning). We first demonstrated that guppies rapidly learn about threats paired with either alarm cues or with conspecific threat responses (demonstration). Then, focusing on acquisition rather than recall, we discovered that phospho-S6 expression, a marker of neural activity, was elevated in guppies during learning from alarm cues in the putative homologue of the mammalian lateral septum and the preoptic area. Surprisingly, these changes in neural activity were not observed in fish learning from conspecific demonstration. Together, these results implicate forebrain areas in social learning about threat but raise the possibility that circuits contribute to such learning in a stimulus-specific manner.

An investigation of population variation in maze exploration and its predictors in wild Trinidadian guppies (Poecilia reticulata).

Individuals often face unpredictable and harsh environments, presenting them with novel ecological problems. Behaviour can provide an adaptive response in such conditions and where these conditions vary between populations, we may predict development and evolution to shape differences in behaviour such as exploration, innovation, and learning, as well as other traits. Here, we compared in the wild the maze swimming performance of groups of female guppies from two Trinidadian populations that differ in numerous ecological characteristics, the Upper and Lower Aripo river. Compared to Upper Aripo fish, Lower Aripo fish were slower to complete the maze, our measure of propensity to innovate, and scored lower on a combined measure of activity and exploration. More active-exploratory groups were faster to complete the maze, but only in the Lower Aripo. We found no evidence for learning the maze. Our results suggest that activity-exploratory and innovative propensities can vary between populations, as can predictors of innovation. These findings are consistent with high predation risk shaping decreased activity-exploratory propensities, but further population comparisons are required to reliably determine the drivers of the observed population difference. Our results emphasize that individual and population differences in activity-exploration and innovation can be shaped by numerous factors.

An Open Resource for Non-human Primate Imaging.

Non-human primate neuroimaging is a rapidly growing area of research that promises to transform and scale translational and cross-species comparative neuroscience. Unfortunately, the technological and methodological advances of the past two decades have outpaced the accrual of data, which is particularly challenging given the relatively few centers that have the necessary facilities and capabilities. The PRIMatE Data Exchange (PRIME-DE) addresses this challenge by aggregating independently acquired non-human primate magnetic resonance imaging (MRI) datasets and openly sharing them via the International Neuroimaging Data-sharing Initiative (INDI). Here, we present the rationale, design, and procedures for the PRIME-DE consortium, as well as the initial release, consisting of 25 independent data collections aggregated across 22 sites (total = 217 non-human primates). We also outline the unique pitfalls and challenges that should be considered in the analysis of non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets.

Primate Brain Anatomy: New Volumetric MRI Measurements for Neuroanatomical Studies.

Since the publication of the primate brain volumetric dataset of Stephan and colleagues in the early 1980s, no major new comparative datasets covering multiple brain regions and a large number of primate species have become available. However, technological and other advances in the last two decades, particularly magnetic resonance imaging (MRI) and the creation of institutions devoted to the collection and preservation of rare brain specimens, provide opportunities to rectify this situation. Here, we present a new dataset including brain region volumetric measurements of 39 species, including 20 species not previously available in the literature, with measurements of 16 brain areas. These volumes were extracted from MRI of 46 brains of 38 species from the Netherlands Institute of Neuroscience Primate Brain Bank, scanned at high resolution with a 9.4-T scanner, plus a further 7 donated MRI of 4 primate species. Partial measurements were made on an additional 8 brains of 5 species. We make the dataset and MRI scans available online in the hope that they will be of value to researchers conducting comparative studies of primate evolution.

Forebrain activation during social exposure in wild-type guppies.

The neural mechanisms regulating social behaviour have received extensive attention in recent years, with much focus on 'complex' forms of sociality. Comparatively little research has addressed fundamental social behaviour, such as grouping, which impacts multiple determinants of fitness, such as foraging and avoiding predation. We are interested in the degree to which brain areas that regulate other forms of sociality are also involved in grouping behaviour, and so we investigated shoal-elicited activation of the brain in the guppy (Poecilia reticulata). Guppies are small, social fish that live in the rivers of Trinidad and, like many social fish, exhibit preferences for larger shoals. We first confirmed that our study population of wild-type guppies preferred to join a larger shoal, and then investigated the activation of four brain regions proposed to be involved in social behaviour and reward (the preoptic area, the dorsal part of the ventral telencephalon, the ventral part of the ventral telencephalon, and the supracommissural part of the ventral pallium). Subjects were exposed to a large shoal, a small shoal, or to a tank empty of conspecifics, and we used immediate early gene expression (egr-1) to assess neuronal activation. We found increased activation in the preoptic area when fish were exposed to a large shoal compared to controls that had no social exposure. There were no significant differences in activation within the other brain areas examined, possibly because these brain areas are not key regulators of grouping behaviour or have only a secondary role. The higher activation of the preoptic area during social exposure suggests functional homology in this highly-conserved region across all vertebrates.

Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates.

Explanations for primate brain expansion and the evolution of human cognition and culture remain contentious despite extensive research. While multiple comparative analyses have investigated variation in brain size across primate species, very few have addressed why primates vary in how much they use social learning. Here, we evaluate the hypothesis that the enhanced reliance on socially transmitted behavior observed in some primates has coevolved with enlarged brains, complex sociality, and extended lifespans. Using recently developed phylogenetic comparative methods we show that, across primate species, a measure of social learning proclivity increases with absolute and relative brain volume, longevity (specifically reproductive lifespan), and social group size, correcting for research effort. We also confirm relationships of absolute and relative brain volume with longevity (both juvenile period and reproductive lifespan) and social group size, although longevity is generally the stronger predictor. Relationships between social learning, brain volume, and longevity remain when controlling for maternal investment and are therefore not simply explained as a by-product of the generally slower life history expected for larger brained species. Our findings suggest that both brain expansion and high reliance on culturally transmitted behavior coevolved with sociality and extended lifespan in primates. This coevolution is consistent with the hypothesis that the evolution of large brains, sociality, and long lifespans has promoted reliance on culture, with reliance on culture in turn driving further increases in brain volume, cognitive abilities, and lifespans in some primate lineages.

Technical and conceptual considerations for using animated stimuli in studies of animal behavior.

Rapid technical advances in the field of computer animation (CA) and virtual reality (VR) have opened new avenues in animal behavior research. Animated stimuli are powerful tools as they offer standardization, repeatability, and complete control over the stimulus presented, thereby "reducing" and "replacing" the animals used, and "refining" the experimental design in line with the 3Rs. However, appropriate use of these technologies raises conceptual and technical questions. In this review, we offer guidelines for common technical and conceptual considerations related to the use of animated stimuli in animal behavior research. Following the steps required to create an animated stimulus, we discuss (I) the creation, (II) the presentation, and (III) the validation of CAs and VRs. Although our review is geared toward computer-graphically designed stimuli, considerations on presentation and validation also apply to video playbacks. CA and VR allow both new behavioral questions to be addressed and existing questions to be addressed in new ways, thus we expect a rich future for these methods in both ultimate and proximate studies of animal behavior.

Animal social learning: associations and adaptations.

Social learning, learning from others, is a powerful process known to impact the success and survival of humans and non-human animals alike. Yet we understand little about the neurocognitive and other processes that underpin social learning. Social learning has often been assumed to involve specialized, derived cognitive processes that evolve and develop independently from other processes. However, this assumption is increasingly questioned, and evidence from a variety of organisms demonstrates that current, recent, and early life experience all predict the reliance on social information and thus can potentially explain variation in social learning as a result of experiential effects rather than evolved differences. General associative learning processes, rather than adaptive specializations, may underpin much social learning, as well as social learning strategies. Uncovering these distinctions is important to a variety of fields, for example by widening current views of the possible breadth and adaptive flexibility of social learning. Nonetheless, just like adaptationist evolutionary explanations, associationist explanations for social learning cannot be assumed, and empirical work is required to uncover the mechanisms involved and their impact on the efficacy of social learning. This work is being done, but more is needed. Current evidence suggests that much social learning may be based on 'ordinary' processes but with extraordinary consequences.

Animal and human innovation: novel problems and novel solutions.

This theme issue explores how and why behavioural innovation occurs, and the consequences of innovation for individuals, groups and populations. A vast literature on human innovation exists, from the development of problem-solving in children, to the evolution of technology, to the cultural systems supporting innovation. A more recent development is a growing literature on animal innovation, which has demonstrated links between innovation and personality traits, cognitive traits, neural measures, changing conditions, and the current state of the social and physical environment. Here, we introduce these fields, define key terms and discuss the potential for fruitful exchange between the diverse fields researching innovation. Comparisons of innovation between human and non-human animals provide opportunities, but also pitfalls. We also summarize some key findings specifying the circumstances in which innovation occurs, discussing factors such as the intrinsic nature of innovative individuals and the environmental and socio-ecological conditions that promote innovation, such as necessity, opportunity and free resources. We also highlight key controversies, including the relationship between innovation and intelligence, and the notion of innovativeness as an individual-level trait. Finally, we discuss current research methods and suggest some novel approaches that could fruitfully be deployed.

The coevolution of innovation and technical intelligence in primates.

In birds and primates, the frequency of behavioural innovation has been shown to covary with absolute and relative brain size, leading to the suggestion that large brains allow animals to innovate, and/or that selection for innovativeness, together with social learning, may have driven brain enlargement. We examined the relationship between primate brain size and both technical (i.e. tool using) and non-technical innovation, deploying a combination of phylogenetically informed regression and exploratory causal graph analyses. Regression analyses revealed that absolute and relative brain size correlated positively with technical innovation, and exhibited consistently weaker, but still positive, relationships with non-technical innovation. These findings mirror similar results in birds. Our exploratory causal graph analyses suggested that technical innovation shares strong direct relationships with brain size, body size, social learning rate and social group size, whereas non-technical innovation did not exhibit a direct relationship with brain size. Nonetheless, non-technical innovation was linked to brain size indirectly via diet and life-history variables. Our findings support 'technical intelligence' hypotheses in linking technical innovation to encephalization in the restricted set of primate lineages where technical innovation has been reported. Our findings also provide support for a broad co-evolving complex of brain, behaviour, life-history, social and dietary variables, providing secondary support for social and ecological intelligence hypotheses. The ability to gain access to difficult-to-extract, but potentially nutrient-rich, resources through tool use may have conferred on some primates adaptive advantages, leading to selection for brain circuitry that underlies technical proficiency.

Demasculinization of male guppies increases resistance to a common and harmful ectoparasite.

Parasites are detrimental to host fitness and therefore should strongly select for host defence mechanisms. Yet, hosts vary considerably in their observed parasite loads. One notable source of inter-individual variation in parasitism is host sex. Such variation could be caused by the immunomodulatory effects of gonadal steroids. Here we assess the influence of gonadal steroids on the ability of guppies (Poecilia reticulata) to defend themselves against a common and deleterious parasite (Gyrodactylus turnbulli). Adult male guppies underwent 31 days of artificial demasculinization with the androgen receptor-antagonist flutamide, or feminization with a combination of flutamide and the synthetic oestrogen 17 ß-estradiol, and their parasite loads were compared over time to untreated males and females. Both demasculinized and feminized male guppies had lower G. turnbulli loads than the untreated males and females, but this effect appeared to be mainly the result of demasculinization, with feminization having no additional measurable effect. Furthermore, demasculinized males, feminized males and untreated females all suffered lower Gyrodactylus-induced mortality than untreated males. Together, these results suggest that androgens reduce the ability of guppies to control parasite loads, and modulate resistance to and survival from infection. We discuss the relevance of these findings for understanding constraints on the evolution of resistance in guppies and other vertebrates.

Causes of Individual Differences in Animal Exploration and Search.

Numerous studies have documented individual differences in exploratory tendencies and other phenomena related to search, and these differences have been linked to fitness. Here, I discuss the origins of these differences, focusing on how experience shapes animal search and exploration. The origin of individual differences will also depend upon the alternatives to exploration that are available. Given that search and exploration frequently carry significant costs, we might expect individuals to utilize cues indicating the potential net payoffs of exploration versus the exploitation of known acts. Informative cues could arise from both recent and early-life experiences, from both the social and physical environment. Open questions are the extent to which an individual's exploratory tendencies are fixed throughout life versus being flexibly adjusted according to prevailing conditions and the actions of other individuals, and the extent to which individual differences in exploration extend across domains and are independent of other processes.

Behavioural responses of feral and domestic guppies (Poecilia reticulata) to predators and their cues.

Predation is an important factor during adaptation to novel environments, and the feralisation of introduced domestic species often involves responding appropriately to allopatric predators despite a background of domestication and inbreeding. Twenty years ago, domestic guppies were introduced to a semi-natural environment at Burgers' Zoo in the Netherlands, where they have since been exposed to avian predation. We compared predation-linked behaviours in this feral population and in domestic guppies akin to the original founders. We found that both populations responded to a novel predator and to conspecific alarm cues. However, shoaling, an important anti-predator behaviour, was higher among feral guppies both at baseline and when exposed to the novel predator. We did not observe a linked suite of anti-predator behaviours across shoaling, predator inspection, alarm substance sensitivity and boldness, suggesting that these responses may be decoupled from one another depending on local predation regimes. As we compared two populations, we cannot identify the causal factors determining population differences, however, our results do suggest that shoaling is either a particularly consequential anti-predator adaptation or the most labile of the behaviours we tested. Finally, the behavioural adaptability of domestic guppies may help to explain their success as an invasive species.

Infectious disease, behavioural flexibility and the evolution of culture in primates.

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans.

Does all teaching rest on evolved traits?

Classification schemes are useful when they elucidate common underlying mechanisms, bring together diverse examples, or illustrate gaps in knowledge for empirical investigation. Kline's scheme merges different approaches, but is orthogonal to existing schemes and overemphasizes evolved specializations, potentially at the detriment of clarifying teaching processes. Focus on underlying mechanisms, what is learned, and consequences for information transfer may provide additional utility.

The evolution of self-control.

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

Experiential effects on mirror systems and social learning: implications for social intelligence.

Investigations of biases and experiential effects on social learning, social information use, and mirror systems can usefully inform one another. Unconstrained learning is predicted to shape mirror systems when the optimal response to an observed act varies, but constraints may emerge when immediate error-free responses are required and evolutionary or developmental history reliably predicts the optimal response. Given the power of associative learning, such constraints may be rare.

What shapes social decision making?

Outcome transparency and the weight given to social information both play important roles in decision making, but we argue that an overarching influence is the degree to which individuals can and do gather information. Evolution, experience, and development may shape individual specializations in social decision making that carry over across contexts, and these individual differences may influence collective behavior and cultural evolution.

Individual consistency and flexibility in human social information use.

Copying others appears to be a cost-effective way of obtaining adaptive information, particularly when flexibly employed. However, adult humans differ considerably in their propensity to use information from others, even when this 'social information' is beneficial, raising the possibility that stable individual differences constrain flexibility in social information use. We used two dissimilar decision-making computer games to investigate whether individuals flexibly adjusted their use of social information to current conditions or whether they valued social information similarly in both games. Participants also completed established personality questionnaires. We found that participants demonstrated considerable flexibility, adjusting social information use to current conditions. In particular, individuals employed a 'copy-when-uncertain' social learning strategy, supporting a core, but untested, assumption of influential theoretical models of cultural transmission. Moreover, participants adjusted the amount invested in their decision based on the perceived reliability of personally gathered information combined with the available social information. However, despite this strategic flexibility, participants also exhibited consistent individual differences in their propensities to use and value social information. Moreover, individuals who favoured social information self-reported as more collectivist than others. We discuss the implications of our results for social information use and cultural transmission.