Selection shapes diverse animal minds

03 - 04 June 2024 09:00 - 17:00 Apex City of Bath Hotel
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Two butterflies resting on a flower

Theo Murphy meeting organised by Professor Elli Leadbeater and Professor Alex Thornton.

What are the evolutionary processes that have produced extraordinary cognitive diversity across the animal kingdom? New approaches, informed by evolutionary biology, neuroscience and psychology, are allowing us to elucidate how different aspects of cognition enhance survival and reproduction for species that live very different lives. This meeting will explore how natural selection customizes animal minds to maximise evolutionary success.

The schedule of talks and speaker biographies is available below. Speaker abstracts will be available closer to the meeting date.

Poster session

There will be a poster session on Monday 3 June. If you would like to apply to present a poster please submit your proposed title, abstract (not more than 200 words and in third person), author list, name of the proposed presenter and institution to the Scientific Programmes no later than Friday 5 April. Please include the text ‘Poster abstract submission - Animal minds’ in the email subject line. Please note that places are limited and posters are selected at the scientific organisers’ discretion.

Attending this event

This event is intended for researchers in relevant fields, and is a residential meeting taking place at the Apex City of Bath Hotel, James Street West, Bath, BA1 2DA.

  • Free to attend
  • Advance registration essential
  • This is an in-person meeting
  • Catering options are available to purchase during registration. Participants are responsible for their own accommodation booking

Enquiries: contact the Scientific Programmes team

 

Organisers

  • Elli Leadbeater

    Professor Elli Leadbeater, Royal Holloway University of London, UK

    Elli's research centres around the ecology and evolution of social insects, and specifically the evolution of bee cognition. She is interested in how cognitive abilities have been shaped by natural selection to fit different ecological contexts, and also in how those same abilities function in the entirely novel environments presented by the Anthropocene. She is a Professor of Ecology and Evolution at Royal Holloway University of London, where she's been based for 10 years. Prior to that, she studied social wasp societies at the Institute of Zoology in London and the University of Sussex, having completed a PhD in bumblebee behaviour in 2008 at Queen Mary University of London. She is an ERC grantee and a former Leverhulme Early Career Fellowship holder, and was recently awarded the Scientific Medal of the Zoological Society of London.

  • Alex Thorton

    Professor Alex Thornton, University of Exeter, UK

    Alex Thornton is a Professor of Cognitive Evolution at the University of Exeter (Cornwall Campus), where he runs the Wild Cognition Research Group. His work seeks to understand how the challenges faced by animals in their natural environments shape their mental processes, how the ability to learn from others affects the behaviour of individuals and groups, and how culture itself evolves. His research incorporates approaches from evolutionary biology, psychology and anthropology using a range of different study systems. Current research focuses primarily on cognition and behaviour in wild jackdaws, the cognitive requirements of human culture and the application of cognitive research in conservation. 

Schedule

Chair

Elli Leadbeater

Professor Elli Leadbeater, Royal Holloway University of London, UK

09:00-09:10 Welcome by the Royal Society and lead organiser
09:10-09:35 A circuit view of evolving cognition

How animals perceive, process and respond to environmental cues is tightly tuned to the species-specific demands imposed by their ecology and life history. This specialisation is likely reflected in neural systems that support cognitive processes, as well as the behaviours expressed by those systems. In Heliconius butterflies the mushroom bodies - insect learning and memory centres - are significantly expanded relative to all other butterflies. Mushroom body expansion in Heliconius coincided with the evolution of a novel dietary shift towards active pollen feeding, and a spatial foraging behaviour, trap-lining, which is thought to require long-term spatial memory of visual scenes. I will discuss evidence that selection for trap-line foraging has reshaped Heliconius cognition along specific lines, reflected in both neuroanatomical specialisations and shifts in a restricted range of cognitive traits. By following the neural pathways that lead to and from the mushroom bodies, a mosaic pattern of neural adaptations is apparent, with shifts in cells and structures supporting visual and sparse coding within the mushroom body. Behavioural experiments closely mirror these changes, with improved performance in non-elemental learning and long-term memory in Heliconius, but specifically within a visual context. This provides a rare case where memory performance has been compared across species and sensory modalities, to identify a modality specific shift. These results are consistent with visual specialisation of the Heliconius mushroom body facilitating a specific enhancement of visual memory, likely due to the requirements of long-term foraging efficiency, and illustrate the precision with which selection can reshape animal cognition.

Dr Stephen Montgomery, University of Bristol, UK

Dr Stephen Montgomery, University of Bristol, UK

09:35-09:50 Discussion
09:50-10:15 Sequences and animal intelligence

The world is full of opportunities that organisms can potentially exploit through productive behaviour. However, there are different ideas about what mental capacities underlie productive behaviour, and how they are distributed across the animal kingdom. Here, focusing on sequential aspects of cognition and behaviour, we explore discrepancies between ideas about animal intelligence and recent research on how birds and non-human mammals recognize and remember sequential information. We note that our understanding of animal working memory is not well aligned with many ideas related to mental flexibility in non-human animals. We also look into whether processing stimulus sequences is required for performing behaviour sequences, and conclude that animals can execute such sequences without faithful sequence representations. Finally, we will discuss the evolutionary rationale behind these insights and their implications for the evolution of animal intelligence.

Senior Associate Professor Johan Lind, Linköping University, Sweden

Senior Associate Professor Johan Lind, Linköping University, Sweden

10:15-10:30 Discussion
10:30-10:50 Break
10:50-11:15 Lost in translation: are psychological concepts really species-neutral?

Work in comparative psychology and animal cognition assumes evolutionary—and hence psychological—continuity across the animal kingdom. The implicit assumption here is that it is possible to identify psychological phenomena in ways that are entirely species-neutral, and which allow us to map similarities and differences within and across different taxa. This assessment draws on psychological theories and capacities that have been, for the most part, derived from the study of our own species. If, however, human psychological capacities are “entangled”, in the philosopher, Alva Noë’s, sense, then we may be chasing a chimera. All is not lost, however, if we pare away the superficial and superfluous layers of human-flavoured intellectual coating that, ironically, are used to generate a sense of deep continuity. First and foremost, this entails recognising that evolution is not just about continuity but is also a diversity-generating process. Taking this on board allows us to generate a psychological landscape that can be explored very profitably by considering a more diverse range of theoretical frameworks in cognitive science. Using examples drawn from studies of memory and self-control, as well as recent work in neuroscience and brain evolution, I offer a view that may allow us to generate a better kind of continuity.

Professor Louise Barrett, University of Lethbridge, Canada

Professor Louise Barrett, University of Lethbridge, Canada

11:15-11:30 Discussion
11:30-11:55 Social drivers of cognitive evolution: the importance of strategic decisions

The challenges of social life have long been seen as key drivers of cognitive evolution. However, research has tended to focus on identifying human-like socio-cognitive traits in other animals while the fundamental question of whether and how animals benefit from making strategic social decisions has received relatively little attention. Here, we use automated field experiments to test whether wild jackdaws benefit from tracking information within dynamic social environments. For instance, while close proximity to other individuals can generate conflict, tolerating their presence may provide access to information or resources, so individuals may benefit from adjusting their tolerance in response to changing conditions. Accordingly, in an experiment where juveniles became valuable sources of information, we found that adults learned to increase their tolerance of juveniles and reduce aggressive displacements. This shows that jackdaws can adjust their information-use strategies to exploit new opportunities, in much the same way as the digital revolution has encouraged older people to learn from the youth. In a separate experiment, we find that jackdaws also modify their dyadic associations to interact preferentially with individuals that provide greater social foraging benefits. However, individuals in stable, long-term relationships maintained their associations regardless of the short-term benefits of strategic re-adjustment. This highlights a vital trade-off: investing in long-term bonds comes at the cost of missing out on benefits of wider social plasticity. We argue that understanding how animals manage trade-offs associated with different relationships is crucial to understand how sociality and cognition co-evolve.

Professor Alex Thornton, University of Exeter, UK

Professor Alex Thornton, University of Exeter, UK

11:55-12:10 Discussion
12:10-12:35 Spatial memory in the real world: its contribution to home ranges, predation and survival

A recent development in understanding the evolution of cognition has been to adopt a within-species Behavioural Ecology Approach (BEA) in which individual differences in specific or general cognitive abilities are assayed, their role in shaping particular behaviours is assumed or demonstrated, and the fitness consequences of these differences are tracked. Cognitive abilities that correlate with fitness benefits are considered to be selected for and thus their evolution explained. Whilst intuitive, this approach raises questions about how different cognitive abilities are related to one another; how a cognitive ability, or suite of cognitive abilities, is (or are) linked to a behaviour, or a set of behaviours; and how selection feeds back to the cognitive and neural mechanisms underlying the behaviours. We propose a series of cartoon models that may depict these links. We then consider the implications for each model for our understanding of how cognitive abilities might evolve. This also allows us to derive a series of predictions about what sorts of relationships we might expect to see between measures of cognition and fitness if a particular model operates. We review existing studies that use the BEA to understand the evolution of cognition and examine which, if any, of the predictions are supported and thus which model(s) might operate. We recommend that future research adopting a BEA clearly specify their assumed model of linkage between particular cognitive abilities, the behaviour of interest and the fitness consequence, and interpret their findings in light of this assumed model.

Dr Joah Madden, University of Exeter, UK

Dr Joah Madden, University of Exeter, UK

12:35-12:50 Discussion

Chair

Alex Thorton

Professor Alex Thornton, University of Exeter, UK

14:00-14:25 Ecology and the value of memory for foraging insects
Professor Elli Leadbeater, Royal Holloway University of London, UK

Professor Elli Leadbeater, Royal Holloway University of London, UK

14:25-14:40 Discussion
14:40-15:05 Spandrel brain? Human brain expansion as a means to another end

The human brain is thought to be exceptionally adaptive. It has enabled us to control our environments and to thrive across the planet and beyond, with little indication that the human brain has exhausted its reach. The human brain's perceived adaptive nature and immense complexity have long made natural selection the only credible explanation for why it evolved. Despite this, I describe modelling results that find that the human brain size may not have evolved due to direct selection for it, but due to changes in developmental constraints. I explain how human brain expansion arises in this model as a side-effect of selection for increased ovarian follicle numbers and their genetic correlation with brain size, a correlation generated by development under a challenging ecology and seemingly cumulative culture. These results raise the intriguing possibility that the large human brain size is a spandrel rather than an adaptation and warn against persistent practices of considering adaptiveness or directional evolution as always caused by direct selection. I discuss challenges of establishing selection pressures with model-less empirical data, particularly regarding hominin brain size evolution, and how a modelling approach integrated with empirical data offers a way forward. I further discuss how modelling approaches may be used in the future not just to determine why the human brain could have evolved but to address why it actually did.

Dr Mauricio González-Forero, University of St Andrews, UK

Dr Mauricio González-Forero, University of St Andrews, UK

15:05-15:20 Discussion
15:20-15:40 Break
15:40-16:05 Mutational origins and selection dynamics of cognitive traits in animals

Despite the many challenges in measuring and quantifying cognition, it is nevertheless clear that cognitive abilities evolve, often due to natural selection. How does this process unfold? Is cognitive evolution rapid or slow? How strong is selection on cognition? Does it mostly depend on standing genetic variation or require populations to wait for beneficial mutations to arise? Answering these questions will provide novel insights into the mode and tempo of cognitive evolution. At stake is understanding whether species’ cognitive abilities are limited by their mutational potential or simply by the selective benefits of cognitive traits. Here, I provide an overview of our empirical work investigating the evolution of individual facial recognition in the paper wasp Polistes fuscatus. Population genomic analyses of paper wasps show that much of the strongest and most recent selective sweeps in these wasps have been targeted toward loci involved in learning, memory, and vision, all traits related to individual recognition. Critically, selection in other species and populations of paper wasps that lack individual recognition do not show a similar pattern of recent selection. Additionally, genes that are differentially expressed during social interactions are over-represented among those under strong selection. Selective sweeps are derived from a combination of both standing variation and de novo mutations in P. fuscatus, suggesting that the evolution of novel cognitive traits, such as individual recognition in P. fuscatus, may be at least partially mutation limited. Approaches for examining the mode and temp of cognitive evolution across taxa are discussed.

Dr Michael Sheehan, Cornell University, USA

Dr Michael Sheehan, Cornell University, USA

16:05-16:20 Discussion
16:20-16:45 Demonstrating reproductive consequences of cognition

Reproductive success and its consequences for fitness are key to determining the role of natural selection in shaping cognitive abilities, and thus the all-important drivers for how and why cognition might change over evolutionary time. Demonstrating reproductive costs or benefits due to variation in cognitive ability, however, is hugely challenging. In some part this is because body size and body condition make the largest contribution to reproductive success, our ability to discriminate whether ‘being smart’ plays a role in fitness is already limited. Additionally, for many animals there is a multiplicity of ways to solve problems, only some of which will depend on their cognitive abilities. Escaping a predator, defending a food cache, or facing down a rival, for example, probably depend on energy levels, motivation, and morphological attributes. However, there may be specific instances in which key parts of animal’s life depend heavily, perhaps entirely on their cognitive abilities, and without them, the animal either won’t survive, or won’t get to reproduction.  Retrieving food caches seems to be one example, and evidence from nest building suggests that this might be another.  In the first, a specific cognitive ability (i.e. spatial memory) is key, while for nest building the pertinent ability is ‘experience’. Builders associate features of building, including material form and function, with consequent reproductive success. Until we can identify the specific cognitive abilities involved, perhaps ‘experience’ could also be used as a proxy in other contexts? If so, this might allow data collection in the field, and even in experiments that do not explicitly address cognition.  

Professor Sue Healy, University of St Andrews, UK

Professor Sue Healy, University of St Andrews, UK

16:45-17:00 Discussion
17:00-18:15 Poster session

Chair

Elli Leadbeater

Professor Elli Leadbeater, Royal Holloway University of London, UK

09:00-09:25 Cognitive evolution: the mechanisms may be simple but their fine-turning may not be

The evolution of cognition is frequently discussed as the evolution of cognitive abilities or the evolution of some neuronal structures in the brain. Yet, such cognitive traits or abilities can be quite complex and are usually not coded by single mutations. Therefore, to understand their evolution one should explain how they could have gradually evolved through selection on heritable variation in simpler cognitive mechanisms. With this in mind, and in light of a previously proposed theory and recent research in my group, I will use a few examples of well-studied cognitive abilities in animals to demonstrate how their evolution and diversification may be captured in terms of fine-tuning of learning mechanisms to different ecological conditions. Furthermore, I will claim that selection for achieving this adaptive fine-tuning may be stronger than selection for what is generally viewed as increasing cognitive abilities or general intelligence.

Professor Arnon Lotem, TAU

Professor Arnon Lotem, TAU

09:25-09:40 Discussion
09:40-10:05 Selection on cognition: the power of an integrative approach

Biological diversity arises from both historical and current processes. To understand how natural selection has shaped the extraordinary cognitive diversity seen across the animal kingdom, we need an integrative approach that combines contemporary (prospective) and historical (retrospective) perspectives. These complementary approaches can inform each other, and provide predictions that can be tested against one another. An evolutionary hypothesis gains credibility when both historical and contemporary evidence support it. When discrepancies arise, they can point toward additional factors or overlooked mechanisms that require further exploration. Although both prospective and retrospective approaches have their own limitations, and are currently insufficiently integrated in cognitive studies, combining them offers a more comprehensive view of the evolutionary diversification of the mind.

Professor Daniel Sol, IBE, Spain

Professor Daniel Sol, IBE, Spain

10:05-10:20 Discussion
10:20-10:40 Break
10:40-11:05 The primate origins of complex cognition

The origins of the human mind have long been a puzzle for biologists and psychologists, in part because human cognition is marked by a distinctive suite of multiple traits spanning flexible decision-making, high levels of cognitive control, and exacerbated social reasoning capacities. What are the evolutionary building blocks of these cognitive abilities in other animals, and why do such forms of complex cognition emerge in some species but not others? I will present research examining patterns of value-based decision making, executive functions, and components of theory of mind across several primate species that vary in their socioecology and life history characteristics. I will use this data to test hypotheses about the evolutionary processes shaping these skills, with a specific focus on the role of social complexity versus ecological complexity in explaining variation in these traits. While social complexity has predominated as an explanation for primate cognitive evolution, these findings suggest that ecological niche can also play an important role in shaping cognition. As such, cognition may evolve in a mosaic pattern, with different evolutionary processes shaping different domains of cognition. More generally, this comparative approach aims to understand why different facets of ‘intelligent’ behaviour emerge across species, including in our own evolutionary history.

Dr Alexandra Rosati, University of Michigan, USA

Dr Alexandra Rosati, University of Michigan, USA

11:05-11:20 Discussion
11:20-11:45 Simple minds yet profound insights: nematodes and fruitflies in the service of evolutionary ecology of cognition

Model organisms such as Caenorhabditis nematodes and Drosophila fruit flies provide powerful systems for studying the evolutionary processes that shape cognition. The advantages of these organisms stem from their well-characterised biology and their amenability to the experimental evolution approach and genetic manipulations. Through controlled manipulations across multiple generations, experimental evolution enables the direct observation of evolutionary changes in cognitive traits. Complementing this method, genetic manipulations facilitate the targeted dissection of specific genes and pathways that underpin cognitive function. In my presentation, I will outline the fundamental principles of experimental evolution, exploring its strengths, limitations, and relationship to other research approaches. Drawing on examples from my own research, I will demonstrate how experimental evolution and genetic manipulations, in conjunction with life-history and behavioural assays, advance our understanding of cognitive ecology. Specifically, I will focus on critical insights regarding 1) the genetic architecture of cognitive traits, including their heritability; 2) the selective costs and benefits of these traits; and 3) the specific selection pressures on these traits, with an emphasis on sex-specific selection—that is, selection that differs between males and females. I will conclude by highlighting future research opportunities that arise from integrating theoretical predictions about evolution under environmental change with time-series analyses of experimental evolution data, and advanced genomic techniques.

Dr Martyna Zwoinska, Uppsala University, Sweden

Dr Martyna Zwoinska, Uppsala University, Sweden

11:45-12:00 Discussion
12:00-12:25 The fish challenge to vertebrate cognitive evolution

There is tremendous variation in vertebrate brain size, shape, and structure across species and taxa. While many studies aim at identifying the ecological factors, both social and environmental, that may explain brain size variation within taxa, a more fundamental divide exists between endotherm and ectotherm vertebrates. Ectotherm vertebrates have brains that are, on average, ten times smaller than those of endotherms (mammals and birds). The existing hypotheses cannot explain this divide, as some endotherm species with relatively simpler social organization and diets than ectotherms still possess much larger brains. Furthermore, experiments and observations demonstrate that at least fishes possess a cognitive "tool kit" equivalent to that of many endotherms. We refer to this as the “fish challenge to vertebrate cognitive evolution”. We review hypothesised causes and consequences of brain size differences to propose two solutions to the “fish challenge”. First, the fish brain achieves modularity at a lower cost, but it is less efficient in problem-solving than an endothermic brain with domain-general organization. Second, the variation in brain size can be better explained by the variation in perception and motor skills rather than by variation in cognitive processes. In that case, the classical definition of cognition would need to be broadened. More specifically, it would be fitting to define animal cognition as how animals take in and process sensory information before deciding how to act on it with motor competencies.

Dr Zegni Triki, University of Bern, Switzerland

Dr Zegni Triki, University of Bern, Switzerland

12:25-12:40 Discussion

Chair

Alex Thorton

Professor Alex Thornton, University of Exeter, UK

13:40-14:05 Interactions of experimentally evolved bias and learning

Patterns of environmental change and of fixity influence when learning and when unlearned biases should evolve. A deep theoretical literature addresses these aspects of change in both the evolution and adaptive function of learning. Less attention is paid to the evolution of innate bias, which is assumed to evolve easily in fixed environment. However, this isn’t always the case. I describe the results from a large experimental evolution study in fruit flies where we test predictions from theory about when learning and when innate bias should evolve. We factorially manipulated levels of the reliability of the stimuli available for learning and the certainty with which a given behaviour predicts fitness. We find that innate bias evolves over larger areas of theoretical space than learning, and that innate bias interacts with learning. Using gene expression, we find that some of the mechanisms underlying the two types of evolved bias in this study vary, and that they differentially influence learning. Finally, I will describe results from a series of studies on how experimentally evolved bias interacts with learning and decision making across behavioural contexts. We find that innate bias influences aspects of patch use in foraging and the decisions females make about their evolved bias under the risk of predation. Finally, we directly address the potential interaction of bias and learning in an experiment testing how stimuli with an evolved bias might overshadow other potential stimuli in flies learning where to lay eggs.

Dr Aimee Dunlap, University of Missouri St Louis, USA

Dr Aimee Dunlap, University of Missouri St Louis, USA

14:05-14:20 Discussion
14:20-14:45 Levels of analysis? Sensorimotor competencies, life histories, conserved computational motifs and developmental linkages together generate brain organization

Research on the evolution of species differences in cognition and related brain organization generally compares the cognitive and neural correlates of specified sensorimotor capacities, environments and their interactions in extant species. Here we examine the neural outcomes of a large-scale environmental transition in evolution, the vertebrate emergence from water to land. Different information is highlighted by this approach. First, the biophysics of the energetic and sensorimotor affordances and constraints of the two realms must be described. Second, change in brain structures must be considered in light of how best to exploit new resources and conform to new constraints.  

Professor Barbara L Finlay, Cornell University, USA

Professor Barbara L Finlay, Cornell University, USA

14:45-15:00 Discussion
15:00-15:30 Break
15:30-15:55 Living on the edge – what food-caching chickadees can teach us about the evolution of cognition

In seasonally changing temperate environments, winters are characterized by harsh and unpredictable climatic conditions associated with limited food supply, low ambient temperature, snow cover and snowstorms which make foraging difficult. Food-caching appears to be at least one adaptation to harsh winters, and in scatter-hoarding species, such as chickadees, food-caching is associated with specialized spatial cognitive abilities needed to successfully recover cached food. I will present research from my lab based on investigating role of natural selection in shaping spatial cognitive abilities in wild food-caching chickadees ranging from comparing multiple populations from different environment to causes and consequences of individual variation in spatial learning and memory abilities including genetic basis of such variation. Our data show that (a) chickadees in harsher environment have better spatial cognitive abilities and larger hippocampus with larger number of hippocampal neurons, (b) differences between populations remain in common garden experiments, (c) chickadees show large individual variation in their learning and memory abilities in their natural environments, (d) such variation is highly heritable and has genetic basis and (e) such variation is associated with significant differences in survival and life span. Overall, our data provide strong evidence that spatial cognitive abilities in food-caching chickadees are shaped by natural selection, which generates differences among populations living in different environmental conditions. 

Professor Vladimir Pravosudov, University of Nevada, Reno, USA

Professor Vladimir Pravosudov, University of Nevada, Reno, USA

15:55-16:10 Proximate mechanisms underlying the coevolution of diet quality and relative brain size in primates

Many primates, including humans, have evolved brains that are surprisingly large relative to their body sizes. Studies of this variation have focused on either proximate (“how”) or ultimate (“why”) explanations by correlating species-average brain sizes with e.g., the rate of genetic changes or certain socioecological variables, respectively. Here, we combined proximate and ultimate perspectives to identify genes that modulated the co-evolutionary relationship between diet quality and relative brain size in primates. For N=52 species, we estimated root-to-tip dN/dS for ~8K genes and collected brain size, body size, and diet quality data. We then applied phylogenetic partial correlation analysis (to identify genes correlated with both brain size and diet quality) and phylogenetic path analysis (to compare different causal models). We identified N=14 genes that: i) show significant (p<0.05) and concordant (in the same direction) partial correlations with both brain size and diet quality; ii) are best fit to a causal model in which diet quality has direct and indirect (via body size and dN/dS) influences on brain size (for 8/14 [57%] genes, this model had the lowest CICc value); iii) are enriched for lipid metabolism (padj=0.02); and iv) are linked to human microcephaly (AARS1) and megalencephaly (AKT3). These findings are consistent with the fact that, after adipose tissue, brains exhibit the highest lipid content, and suggest that higher quality diets – which include more fats – facilitated the evolution of larger relative brain sizes in some primates lineages via alterations to fat metabolism.

Dr Alex DeCasien, National Institute of Mental Health, USA

Dr Alex DeCasien, National Institute of Mental Health, USA

16:10-17:00 Panel discussion