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Overview

Scientific discussion meeting organised in partnership with the British Academy by Professor Denis Noble CBE FMedSci FRS, Professor Nancy Cartwright FBA, Professor Sir Patrick Bateson FRS, Professor John Dupré and Professor Kevin Laland.

Developments in evolutionary biology and adjacent fields have produced calls for revision of the standard theory of evolution, although the issues involved remain hotly contested. This meeting presented these developments and arguments and encouraged cross-disciplinary discussion, which involved the humanities and social sciences in order to provide further analytical perspectives and explore the social and philosophical implications.

The schedule of talks, biographies and abstracts are available below. 

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Recorded audio of the presentations are available below. Meeting papers will be published in a future issue of Interface Focus.

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Organisers

Schedule

09:15-09:45
The extended evolutionary synthesis

Abstract

Since the last major conceptual integration in evolutionary biology – the Modern Synthesis of the 1940s – the biosciences have made significant advances. The rise of molecular biology and evolutionary developmental biology, the recognition of ecological development, niche construction and of multiple inheritance systems, the -omics revolution and the science of systems biology, among other developments, have provided a wealth of new knowledge regarding the mechanisms of evolutionary change. Some of these results are in agreement with the classical Synthetic Theory and others reveal different properties of evolutionary change. A renewed and extended evolutionary synthesis unites pertinent concepts emerging from these novel fields with elements from the standard theory, but it differs from the latter in its core logic and predictive capacities. Whereas the classical theory had concentrated on genes and adaptive variation in populations, the extended framework emphasises the role of constructive processes, environmental induction, and systems dynamics in the evolution of organismal complexity. Single level and unilinear causation is replaced by multilevel and reciprocal causation. Among other consequences, this entails a revised understanding of the role of natural selection in the evolutionary process. The extended evolutionary synthesis complements the traditional gene centric perspective and stimulates research into new areas of evolutionary biology.

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09:55-10:25
The evolutionary synthesis today: extend or amend?

Abstract

Evolutionary theory has been extended almost continually since the Evolutionary Synthesis, but the principal tenets of the Synthesis have been strongly supported, the single most important exception being the greater importance accorded genetic drift, especially in molecular evolution. The calls for an extended synthesis today are largely a continuation of this process. Some elements of the EES movement, such as the role of niche construction, are welcome emphases on long recognised but perhaps under-studied processes. The union of population genetic theory with mechanistic understanding of molecular and developmental processes is a potentially productive conjunction of ultimate and proximal causation; but the latter does not replace or invalidate the former. Newly discovered molecular genetic phenomena have been easily accommodated by orthodox evolutionary theory in the past, and this appears to hold also for phenomena such as epigenetic inheritance today. In several of these areas, empirical evidence is needed to evaluate enthusiastic speculation. Evolutionary theory today will continue to be extended, but there is no sign that it requires emendation.

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11:05-11:35
Developmental plasticity: re-conceiving the genotype

Abstract

For several decades, the phenotype of an organism (i.e, its traits and behaviour) has been studied as the outcome of developmental ‘instructions’ coded in its DNA. According to this model, each genotype is expressed as a specific phenotype; individual differences in fitness-related traits are seen to arise from this stably inherited internal information. This simplified view of development provides the foundation for a Modern Synthesis approach to adaptive evolution as a sorting process among genetic variants. As developmental biologists are aware, however, an organism’s phenotype is not strictly pre-determined by its genotype, but rather takes shape through the interplay of genetic factors with the organism’s environmental conditions. By means of this developmental plasticity, a given genotype may express different phenotypes under different environmental conditions. Accordingly, the genotype can be understood as a repertoire of potential developmental outcomes or norm of reaction.  

Re-conceiving the genotype as an environmental response repertoire rather than a fixed developmental programme leads to three critical insights, as illustrated by norm of reaction data from Polygonum plants. Plastic responses to specific conditions often comprise functionally appropriate trait adjustments, resulting in an individual-level, developmental mode of adaptive variation. Environmental responses can extend across generations via effects on progeny growth and fitness, a form of inherited yet non-genetic adaptation. Finally, because genotypes are differently expressed depending on the environment, the genetic diversity available to natural selection is itself environmentally contingent.

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11:45-12:15
Evolution of phenotypic plasticity

Abstract

The scope and relative rates of adaptive phenotypic change from plasticity versus standard Darwinian evolution adaptive genetic changes depend on the time scale and the range of phenotypic alteration being considered. This distinction becomes blurred when plasticity itself evolves. Using standard methods from neo-Darwinian population genetic theory, I review recent models on the evolution of phenotypic plasticity in changing environments, emphasising the roles of environmental predictability and costs of plasticity in constant and labile characters. Adaptation to a novel environment may often occur by rapid evolution of increased plasticity followed by slow genetic assimilation of the new phenotype. I elucidate the connection between environmental tolerance and plasticity. The theory of evolution of phenotypic plasticity is an important extension to neo-Darwinism, but does not necessitate a major revision of its foundations. The same conclusion applies to epigenetic mechanisms including interactions between genes or tissues in development, and to transgenerational phenotypic effects such as somatic inheritance, maternal effects and DNA methylation.

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13:50-14:20
Heredity and evolutionary theory

Abstract

Heredity is a central concept in biology and one of the core principles needed for evolution by natural selection. For most of the past century inheritance has been conceptualised and defined in terms of transmission of genes. Emerging developmental perspectives on evolution appear to challenge this perspective in several ways. Here I will explain how evolutionary biologists treat heredity conceptually and mathematically. These perspectives are heuristically useful but they impose a certain structure on evolutionary theory and leave out aspects of heredity that may be important to understand evolution. An alternative representation understands heredity as an outcome of developmental processes. I will suggest that this perspective helps to clarify how different mechanisms of inheritance contributes to evolution.

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14:30-15:00
The ontology of evolutionary process

Abstract

Ontology is the branch of philosophy that considers in the most general way the nature of reality. An ancient and fundamental ontological question is whether reality is ultimately composed of stable things or is everywhere processual, in flux. A number of distinguished 20th century biologists, including, for instance Conrad Waddington, Joseph Needham, and Ludwig von Bertalanffy, thought it important to stress the fundamentally dynamic, processual character of living systems. While evolution is of course a process, it is often implicitly supposed that the entities that evolve or that constitute the evolutionary process, whether genes, organisms, populations, or whatever, are kinds of things. Following the authors mentioned above, I argue that these too are better seen as processes, albeit highly stabilised processes.

In this talk I shall argue that a process ontology is correct and that it has important implications for how we should think about evolution. First, with regard to the constituents of the evolutionary process, process ontology highlights the limitations of atemporal descriptions of organisms, for example in terms of gene sequence, and of populations as atemporal abstractions from evolving lineages. Second, whereas in an ontology of things the primary explanatory task is that of understanding change, in a world of process it is of equal or even greater importance to explain stability. The first step in articulating a fully processual view of evolution is to describe the processes that sustain persisting lineages. Doing so should provide fresh perspectives on the processes that can produce changes in lineages. 

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15:40-16:10
Does the way in which development works bias the paths taken by evolution?

Abstract

Developmental bias was defined in a seminal review some thirty years ago that resulted from an early ‘meeting of minds’ of developmental and evolutionary biologists driven by John Maynard Smith and Lewis Wolpert. Although there has been dramatic progress since then in revealing in exquisite detail how morphologies develop, there are few well-worked case studies of potential developmental bias, as well as little understanding of how important the process has been in shaping the evolution of animal form. Therefore, it is timely to think about what is needed to facilitate the analysis of the extent to which patterns of evolutionary diversification are biased by how development works, and indeed whether it is useful to distinguish this process from that of genetic channeling.

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16:20-16:50
The middle ground between artificial and natural selection: niche construction as developmental bias

Abstract

Organisms modify and choose components of their local environments. This ‘niche construction’ is subject to extensive research across several academic fields. It is well appreciated that niche construction can alter ecological processes, modify natural selection, and contribute to inheritance through ecological legacies. However, niche construction is not usually regarded as an evolutionary process, probably because traditional evolutionary accounts restrict evolutionary processes to phenomena that directly change gene frequencies (e.g. selection, mutation, drift). 

Alternative perspectives can be of value if they generate novel predictions, open up new lines of enquiry, or generate new insights. The niche-construction perspective within evolutionary biology provides an alternative account of the causal relations underlying adaptation, a stance that has already led to a number of valuable insights. Here I suggest that there is heuristic value in regarding niche construction as an evolutionary process, on the grounds that it initiates and modifies the selection acting back on the constructor (and other species) in an orderly and directional manner. As a consequence, niche construction co-directs adaptive evolution by imposing a statistical bias on selection (an externally expressed form of developmental bias). 

I illustrate how niche construction can generate developmental bias by comparing it with artificial selection, where I suggest it occupies the middle ground between artificial and natural selection. This perspective has heuristic value for the evolutionary biologist, leading to testable predictions related to: (i) trait evolution, including the evolution of sequences of traits and parallel evolution; (ii) responses to natural selection in the wild; and (iii) biodiversity. 

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09:05-09:35
Biological action in Read-Write genome evolution

Abstract

Many of the most important evolutionary variations that generated phenotypic adaptations and originated novel taxa resulted from complex cellular activities affecting genome content and expression. These activities included: (i) the symbiogenetic cell merger that produced the mitochondrion-bearing ancestor of all extant eukaryotes; (ii) symbiogenetic cell mergers that produced chloroplast-bearing ancestors of photosynthetic eukaryotes; and (iii) interspecific hybridisations and genome doublings that have generated adaptive radiations and new species of higher plants and animals. Adaptive variations have also arisen by horizontal DNA transfers (frequently involving infectious agents), by natural genetic engineering of coding sequence DNA in protein evolution (e.g. exon shuffling), and by mobile DNA rewiring of transcriptional regulatory networks, such as those essential to viviparous reproduction in mammals. In the most highly evolved multicellular organisms, we now know that biological complexity scales with ‘non-coding’ DNA content rather than with protein-coding capacity in the genome. Coincidentally, we have come to recognise that ‘non-coding’ RNAs rich in repetitive mobile DNA sequences function as key regulators of complex adaptive phenotypes, such as stem cell pluripotency. The intersections of cell activities and Read-Write genome modifications provide a rich molecular and biological foundation for understanding how ecological disruptions can stimulate productive, often abrupt, evolutionary transformations.

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09:45-10:15
Genetic, epigenetic and exogenetic information in development and evolution

Abstract

I outline an approach to measuring biological information where ‘information’ is understood in the sense found in Francis Crick’s foundational contributions to molecular biology. Genes contain information in this sense, but so do epigenetic factors, as many biologists have recognised. The term ‘epigenetic’ is ambiguous, and I introduce a distinction between epigenetic and exogenetic inheritance to clarify one aspect of this ambiguity. These three heredity systems play complementary roles in development and evolution.

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10:55-11:25
The role of epigenetic inheritance in evolution

Abstract

The construction of the ‘Modern Evolutionary Synthesis’ in the mid-twentieth century involved the exclusion of soft inheritance – the inheritance of the effects of developmental modifications – and, by implication, the possibility of any form of ‘Lamarckian’ evolution. However, in later decades, discoveries of molecular mechanisms that can support such inheritance led to a broadening of the notion of biological heredity. After discussing the historical context in which this change occurred, I present an extended notion of inheritance, focusing on epigenetic inheritance and its underlying mechanisms. I examine the evidence for the ubiquity of epigenetic inheritance, present models of population epigenetics, and discuss the involvement of epigenetic inheritance in adaptive evolutionary change and macro-evolution. I argue that considering the many evolutionary consequences of epigenetic inheritance requires an extension of the evolutionary synthesis beyond the current neo-Darwinian model.

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11:35-12:05
Extended genomes: symbiosis and evolution

Abstract

Multicellular organisms do not live in an axenic world, but in one populated by microbes. Indeed, it can be argued that what we see as an individual animal or plant is in fact biologically a composite of the animal/plant and associated microbes. The individual generated is not simply a passive result of associations, but commonly an integrated one. Animal/plant development occurs in concert with microbes, and microbiome constitution is determined in part by the animal/plant, which may select particular microbes. In my talk I will focus on the most integrated symbioses, where microbes pass from a mother to offspring and thus represent part of host heredity. I will discuss why hereditary symbiosis evolves, how it widens our view of evolutionary processes, and how it affects what we mean by an ‘individual’.

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13:50-14:20
Evolution viewed from medicine and physiology

Abstract

Medicine and physiology are multi-level disciplines. So is physics. From physics we learn that ordered properties at high levels co-exist with randomness at lower levels. Molecules in organisms must obey the same principles. Stochasticity at low levels does not therefore exclude order at higher levels. Organisms enlist stochasticity in their development of functional behaviour, through restraints exerted by higher over lower levels. The physics of organisms must therefore interact with their genomes to produce the phenotype1,2. Reverse engineering from physiological models is then required to understand genotype-phenotype relations3. There is no privileged level of causality4, nor privileged level of selection5. Evolution involves interaction between several processes at multiple levels, as Charles Darwin also believed5,6. Without understanding these interactions, gene-centred approaches will continue to produce disappointing results in healthcare7,8, including trans-generational disease risks.  

1. Alvarez-Buylla ER et al. 2016. Bioscience 66, 371-383.
2. Edelman DB et al. 2016. Progress in Biophysics and Molecular Biology (doi:10.1016/j.pbiomolbio.2016.06.007) 
3. Noble D. 2011. Interface Focus 1, 7-15.
4. Noble D. 2012. Interface Focus 2, 55-64. 
5. Noble D. 2016 Dance to the Tune of Life. Biological Relativity. CUP.
6. Noble D. 2015. Journal of Experimental Biology 218, 7-13. 
7. Editorial, 2010 Nature 464, 649-650.
8. Joyner MJ, Prendergast FG. 2014. Journal of Physiology 592, 2381-2388.

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14:30-15:00
Anthropomorphism in evolutionary biology

Abstract

A longstanding tension exists in evolutionary biology between behavioural ecology – in which organisms are treated as having adaptive, fitness-maximising agendas; and population genetics – in which such notions are decried as naïve ‘anthropomorphism’ and are widely rejected. I explore the formal and scientific justification for evolutionary anthropomorphism and consider its application to the understanding of adaptive design at the level of genes, individuals and societies.

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15:40-16:10
Adaptability and evolution

Abstract

The capacity of organisms to respond in their own lifetimes to new challenges in their environments probably appeared early in biological evolution. At present few studies have shown how such adaptability could influence the inherited characteristics of an organism’s descendants. Nevertheless such effects on biological evolution are likely to have been important and when they occurred accelerated the pace of evolution. Ways in which this might have happened have been suggested many times since the 1870s. I shall review these proposals and discuss their relevance to modern thought.

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16:20-17:00
Round table discussion

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09:05-09:35
Evolution and the metaphor of agency

Abstract

It is striking that evolutionary biology often uses the language of intentional psychology to describe the behaviour of evolved organisms, their genes, and the process of natural selection that led to their evolution. Thus a cuckoo chick ‘deceives’ its host; a worker ant ‘prefers’ to tend the queen's eggs to those of other workers; a swallow ‘realises’ that winter is approaching and ‘wants’ to escape it; an imprinted gene ‘knows’ whether it was inherited paternally or maternally; and natural selection ‘chooses’ some phenotypes over others. 

This intentional idiom is a symptom of a broader way of thinking about and modelling evolution, which I call ‘agential’. This involves treating evolved entities, paradigmatically individual organisms, as if they were agents trying to achieve a goal, namely maximisation of reproductive fitness (or some proxy). The use of rational choice models, originally intended to apply to deliberate human action, in an evolutionary context, is one symptom of agential thinking. 

I offer a cautious defence of agential thinking in evolutionary biology. I argue that this mode of thinking does genuine intellectual work, and is not ‘idle metaphor’. The key point is that attributions of agency presuppose a ‘unity of purpose’. Therefore an evolved organism can only be treated as agent-like to the extent that its phenotypic traits have complementary rather than antagonistic functions, i.e. contribute to a single overall goal. Where this is not the case, e.g. because of unresolved intra-genomic conflict, the metaphor of agency ceases to be applicable.

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09:45-10:15
Developmental niche construction

Abstract

In the last decade niche construction has been heralded as the neglected process in evolution. But niche construction is just one way in which the organism’s interaction with, and construction of the environment, can have potential evolutionary significance. This constructed environment not just selects for, it also produces new variation. Nearly three decades ago, and in parallel with Odling-Smee’s book chapter ‘Niche-constructing phenotypes’, West and King introduced the ‘Ontogenetic Niche’ to give the phenomena of exogenetic inheritance a formal name. Since then a range of fields in the life sciences and medicine has amassed evidence that parents influence their offspring by means other than DNA (parental effects). Diverse scientists use different theoretical constructs for overlapping sets of processes, all of which show one way or another how heritable variation can be environmentally induced and developmentally regulated. Here I propose the concept of ‘developmental niche construction’ as a framework to integrate findings from fields ranging from molecular biology to developmental psychology. It elucidates how a diverse range of mechanisms contributes to the transgenerational transfer of developmental resources. This talk will explore the overall significance of these developments in the life sciences, and particularly how they advance the ongoing integration of development, heredity, ecology, and evolution.

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10:55-11:25
Human nature, human culture: the case of cultural evolution

Abstract

In recent years, far from arguing that evolutionary approaches to our own species permit us to describe the fundamental character of human nature, a prominent group of cultural evolutionary theorists has instead argued that the very idea of 'human nature' is one we should reject. It makes no sense, they argue, to speak of human nature in opposition to human culture. But the very same sceptical arguments have also led some thinkers – usually from social anthropology – to dismiss the related idea that we can talk of human culture in opposition to human nature. 

How, then, are we supposed to understand the cultural evolutionary project itself, which seems to rely on a closely allied distinction between 'organic' and 'cultural' evolution? This talk defends the cultural evolutionary project against the charge that, in refusing to endorse the concept of human nature, it has inadvertently sabotaged itself.

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11:35-12:05
Human niche, human behaviour, human nature

Abstract

Scholars from a diverse range of disciplines disagree on what human nature is, what it could be, or even if there is one. There is no single ‘best’ discourse on, or mode of approach to, human nature. However, in the context of what we know about the evolutionary history, anthropology, and biology of Homo sapiens sapiens it is clear that an evolutionary approach should be among the principal modes of inquiry. At present we are faced with a few different narratives as to exactly what such an evolutionary approach entails. However, one point is clear: we need a robust and dynamic theoretical toolkit in order to develop a richer, and more nuanced, understanding of the cognitively sophisticated genus Homo and the diverse sorts of niches humans constructed and occupied across the Pleistocene, Holocene, and into the Anthropocene. In this talk I review current evolutionary approaches to ‘human nature’ and argue that we benefit from re-framing our investigations via the concept of the human niche and in the context of the Extended Evolutionary Synthesis (EES). In providing an overview of human evolution and the human niche I illustrate the benefits of moving the discourse on human nature(s) to an integrated evolutionary approach incorporating processes of the Extended Evolutionary Synthesis. This is not a replacement of earlier evolutionary approaches but rather an expansion and enhancement, a broadening of our toolkit and the landscape of inquiry. I offer brief examples from human evolutionary histories in support of these assertions.

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13:50-14:20
A second inheritance system: the extension of biology through culture

Abstract

By the mid-twentieth century the behavioural sciences could offer only the sketchy beginnings of a scientific literature documenting evidence for cultural inheritance in animals – the transmission of traditional behaviours via imitation and other processes of learning from others (social learning). By contrast, recent decades have seen a massive growth in the documentation of such cultural phenomena, driven by long-term field studies and complementary laboratory experiments. Here I first offer an overview of the major discoveries in this field, which increasingly suggest that this ‘second inheritance system’, built on the shoulders of the primary genetic inheritance system, occurs widely amongst vertebrates and possibly in insects and other invertebrates too. Its novel characteristics suggest it should have major implications for our understanding of evolutionary biology. Two major questions arising are accordingly addressed. One concerns the extent to which this second system echoes or differs from the principal properties of the primary evolutionary system described in the neo-Darwinian synthesis of the twentieth century and its extensions under discussion at this meeting. A subsidiary issue here is how the answers may differ much according to whether the focus is on the massively cumulative cultural evolution distinctive of our own species, or on the forms of cultural transmission documented for other species. The second major, and related, question concerns the extent to which the new discoveries about animal cultural transmission extend evolutionary theory, either in addition to or through interaction with the primary, genetically based inheritance systems.

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14:30-15:00
Human evolution, niche construction and plasticity

Abstract

Recent humans are biocultural organisms. Our worldwide distribution and status as the lone surviving species of our genus signal a level of evolutionary success often explained by both biological and cultural mechanisms. A bio-behavioural package of traits that co-exist in Homo sapiens, including large brains and bodies, small teeth and jaws, extensive cooperative care, a great deal of developmental plasticity, and an extensive amount of niche construction, are variously implicated in our success or seen as its result.

It is broadly accepted that recent humans are ‘different’, particularly in the extent of our cultural interventions, than our earlier hominin forebears. But whether this is a difference in kind or degree, how far back that difference stretches, and whether those outcomes modifiable over an individual’s lifetime are important to human evolution is open to debate. Regardless of whether we accept exogenetic changes – including developmental niche construction – as consistent with an extension of, or break with the evolutionary synthesis, Homo erectus has often been proposed as the locus at which more ‘human like’ modes of behaviour (and presumably more biocultural evolution) is seated.  But the paucity of the fossil record and the tenuously established links between bones and behaviours of interest limit our ability to test these assertions. I review the evolution of Homo and recent attempts to locate the transition to a biocultural organism with new data and by both working back from recent humans through archaeological time and working forward from ancestral genera. 

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15:40-16:10
Domestication: a model system for evolutionary biology

Abstract

In his book The Variation of Animals and Plants under Domestication Darwin used domestication as a model system to explore his theories about the role of natural selection in evolution. Gregor Mendel used peas to trace the rules of heredity that formed the basis of the science of genetics, and that, when combined with Darwinian evolution, formed the basis of the Modern Synthesis. It seems only appropriate for domestication to serve once again as a model system for assessing how recent insights into the role of multiple shaping processes and forms of inheritance can be incorporated into an extended understanding of evolution. This presentation explores the value of domestication in evaluating core assumptions that differentiate the classical Modern Synthesis and the Extended Evolutionary Synthesis including: 1. reciprocal causation, 2. developmental processes as drivers of evolutionary change, 3. inclusive inheritance, and 4. the tempo and rate of evolutionary change.

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16:20-17:00
Round table discussion

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