Collective animal behaviour through time

Collective cognition – where interactions between individuals allow groups to function as integrated sensory, information-processing and decision-making units with superior powers compared to individuals – is one of the key advantages of sociality. However, to what extent collectives as a whole are able to exhibit a ubiquitous individual cognitive capacity – learning – is still relatively poorly understood. Nonetheless, burgeoning evidence from several species now suggests that groups are indeed capable of learning from collective experiences and thus of enhancing their performance beyond the bounds of individual maxima. This process can even give rise to the cultural accumulation of increasingly better solutions to problems repeatedly encountered by a given group, even in the face of turnovers in membership. In this talk, the researchers develop a framework for exploring the mechanisms underlying such collective learning, arguing that while it incorporates elements of both individual and social learning, its drivers extend beyond these. They propose three non-mutually-exclusive mechanisms (individual, empathetic, and organisational learning), the latter two of which represent emergent properties of groups. They look for empirical evidence for each type of learning in their model system (the development of travel routes in homing pigeon flocks), and discuss how the ecology, social organisation and life-history of different species might shape which type of collective learning and cultural accumulation they may expect to find manifested during collective problem-solving specific to their needs.

Professor Dora Biro, University of Oxford, UK and University of Rochester, USA

Professor Dora Biro, University of Oxford, UK and University of Rochester, USA

Dora Biro received her PhD in Zoology from the University of Oxford. She subsequently held a JSPS postdoctoral research fellowship and a visiting professorship at the Primate Research Institute of Kyoto University, Japan, before returning to Oxford as a Royal Society University Research Fellow in 2007. She was appointed Associate Professor at the Department of Zoology and Tutorial Fellow of St Hugh’s College, University of Oxford in 2013, and Professor of Animal Behaviour in 2019. She is currently Professor of Brain and Cognitive Sciences at the University of Rochester, USA. Her research interests are centred on animal cognition, particularly in the contexts of navigation, tool use, culture and collective decision-making

Collective behaviour is a subfield of behavioural ecology, making extensive use of its tools of observation, experimental manipulation, and model building. However a fundamental behavioural ecology approach, the application of optimality theory, has been comparatively neglected in collective behaviour. This talk seeks to address this imbalance, by outlining an evolutionary theory framework for the discipline. The application of optimality theory to collective behaviour requires a number of questions to be addressed: First, what is the correct quantity to optimise? This is achieved via a combination of considering the organisms' life history, alongside tools such as statistical decision theory and stochastic dynamic programming. Second, what mechanism is appropriate for optimal behaviour? This involves ensuring that models are self-consistent rather than containing arbitrary assumptions. Third, at what level of selection does optimisation act? Selection acts at the level of individuals except in very particular circumstances, yet collective behaviour phenomena are group-level, thus introducing a risk of confusing at what level adaptive properties emerge. This talk presents examples under each of the three questions, as well as discussing mismatches between theory and observation. In doing so, it is hoped that collective behaviour fully inherits the tools and philosophy of its parent discipline of behavioural ecology.

Professor James Marshall, Opteran Technologies and The University of Sheffield, UK

Professor James Marshall, Opteran Technologies and The University of Sheffield, UK

James Marshall is Professor of Theoretical and Computational Biology at the University of Sheffield, and Chief Science Officer at Opteran Technologies. His interests span collective behaviour, evolutionary theory, and decision theory. Recently he has moved towards using robots as a testbed for the models he works on, and in 2020 co-founded Opteran as a spinout from the University of Sheffield, to develop a new approach for robot autonomy based on reverse-engineering insect brains.

Lekking is a spectacular mating system in which males maintain tightly organised clustering of tiny territories during the mating season, and females visit these leks for mating. This mating strategy is likely a costly behaviour that requires males engage in exaggerated displays and compete vigorously to maintain their territories as well as to gain matings. Various hypotheses – ranging from predation dilution to mating benefit – offer potential explanations for the evolution of this peculiar mating strategy. However, many of these classic hypotheses rarely consider the spatial dynamics that produce and maintain the lek. In this manuscript, the researchers propose to view lekking through the perspective of spatial ecology and collective behaviour, in which simple local interactions between organisms as well as habitat likely produce and maintain leks. Such local interactions are likely shaped by the interplay of selection pressures, such as predation, mate-competition and mate choice, on both males and females. To test these ideas at both proximate and ultimate levels, the researchers argue that the concepts and tools from the literature of collective animal behaviour, such as high-resolution video tracking that enables capturing fine-scale spatiotemporal interactions, could be useful. They illustrate the promise of this approach using blackbuck (Antilope cervicapra) leks as a case study. Broadly, they argue that a lens of spatial ecology and collective behaviour can provide novel insights into understanding both the proximate and ultimate factors that shape leks. 

Dr Vishwesha Guttal, Indian Institute of Science, India

Dr Vishwesha Guttal, Indian Institute of Science, India

Vishwesha (Vishu) Guttal is fascinated by the patterns and functions of self-organisation in the biological world. He did his PhD in Physics with Jayaprakash (at The Ohio State University, USA), working on applying tools of physics to ecosystem self-organisation. He did his postdoc with Iain Couzin at Princeton University, working on the evolution of collective motion in animal groups. Vishu is currently an Associate Professor at the Centre for Ecological Sciences at the Indian Institute of Science where he and his lab members use theory, computation, experiments and field work to understand patterns and functions of collective motion and more broadly self-organising ecosystems. 

The collective behaviour of animals has attracted considerable attention in recent years, with many studies exploring how local interactions between individuals can give rise to global group properties. The functional aspects of collective behaviour are less well studied, especially in the field and relatively few studies have investigated the adaptive benefits of collective behaviour in situations where prey are attacked by predators. This paucity of studies is unsurprising because predator-prey interactions in the field are difficult to observe. Furthermore, the focus in recent studies on predator-prey interactions has been on the collective behaviour of the prey rather than on the behaviour of the predator. Here the researchers present a field study that investigated the anti-predator benefits of waves produced by fish at the water surface when diving down collectively in response to attacks of avian predators. Fish engaged in surface waves that were highly conspicuous, repetitive, and rhythmic involving many thousands of individuals for up to 2 min. Experimentally induced fish waves doubled the time birds waited until their next attack, therefore substantially reducing attack frequency. In one avian predator, capture probability, too, decreased with wave number and birds switched perches in response to wave displays more often than in control treatments, suggesting that they directed their attacks elsewhere. Taken together, these results support an antipredator function of fish waves. The attack delay could be a result of a confusion effect or a consequence of waves acting as a perception advertisement, which requires further exploration.

Professor Jens Krause, Leibniz Institute of Freshwater Ecology and Inland Fisheries, Germany

Professor Jens Krause, Leibniz Institute of Freshwater Ecology and Inland Fisheries, Germany

Jens Krause is a behavioural ecologist with a strong interest in collective behaviour and social networks. He has published a number of books (Living in Groups, OUP; Fish Cognition and Behavior, Wiley/Blackwells; Exploring Animal Social Networks, PUP; Animal Social Networks, OUP) and articles on the mechanisms and functions of living in groups. He is currently Professor for Fish Biology and Ecology in the Faculty of Life Science at the Humboldt University Berlin, Head of Department at the Leibniz-Institute of Freshwater Ecology and Inland Fisheries and on the executive board of the excellence cluster 'Science of intelligence'. He started his university education at the Free University Berlin and obtained his PhD from St John’s College Cambridge, UK, followed by postdocs at Mount Allison University, Canada, and Princeton University, USA, and held a Professorship for behavioural ecology at Leeds University, UK, for several years before moving back to Berlin in 2009. 

Collective behaviour forms the basis for many diverse and complex anti-predator strategies. To evolve, and remain adaptive, these behaviours must depend on their positive impact on individual fitness in the ecological and social context of an individual’s environment, as well at their internal motivational state. Like any behaviour, collective movement or decision making depends on the integration of multiple sensory inputs, and the neural pathways that link the internal and external environment and produce the coordinated response. A coherent understanding of how these processes are coordinated therefore requires and integrative approach that spans traditional disciplines in behavioural biology. Here, the researchers argue that Lepidopteran larvae are well placed to serve as model systems for understanding the integrative biology of collective behaviour.  Lepidopteran larvae display striking diversity in social behaviour, the repeated convergent evolution of collective behaviour, and illustrate critical interactions between ecological, morphological and behavioural traits. While previous, sometimes classic, work has provided an understanding of how and why social behaviours have evolved in Lepidoptera, little is known about the developmental and mechanistic basis of these traits. Recent advances in the quantification of behaviour, and the availability of genomic resources and manipulative tools, allied with the exploitation of the behavioural diversity of tractable Lepidopteran clades, will change this. In doing so, the researchers will be able to address previously unapproachable questions such as: How is age dependent plasticity in collective behaviour facilitated by developing neural systems, and why does it evolve? Are similar neural pathways implicated in the convergent evolution of collective behaviour? To what extent is this convergence shaped by the wider sensory and host plant ecology and evolutionary history of a lineage? And how easy is it for selection to modify neural pathways to switch behavioural strategies from individualist to collectivist?

Dr Stephen Montgomery, University of Bristol, UK

Dr Stephen Montgomery, University of Bristol, UK

Dr Montgomery's primary interests are focused around how brains and behaviour evolve. He did his PhD on primate brain evolution with Dr Nick Mundy, at the University of Cambridge, and then held a series of fellowships at Oxford and UCL, with Professor Judith Mank, before returning to Cambridge to establish his own group. He is currently a Senior Research Fellow, funded by a NERC Fellowship and an ERC Starter Grant, and Proleptic Senior Lecturer at the School of Biological Sciences, University of Bristol. His group is interested in how brains adapt to different environments, how changes in brain structure produce behavioural differences, and how selection navigates developmental and functional constraints that may limit or channel the adaptive response. They take a comparative approach to tackling these questions, comparing molecular and phenotypic data across species.