Commemorating Darwin: human nature revisited

Séminaire du 27 avril au 2 mai 2009 organisé par Halldor Stefansson et Denis Duboule


Marion Blute, Ghislaine Dehaene, Stanislas Dehaene, Denis Duboule (organisateur), Brigitte Galliot, Jean Gayon, Jean-Pierre Gibrat, Scott Gilbert, Ritta Hari, Philippe Janvier, Johannes Krause, Nicole Le Douarin, Daniel E. Lieberman, Pierre Magistretti, Axel Meyer, Alain Prochiantz, Benjamin Prud’homme, Hilary Rose, Steven P.R. Rose, Dan Sperber, Halldor Stefansson (organisateur), Alexandre Bon, Etienne Carton de Grammont, Henri Maïkoff (de l’Association Science Télévision).

Compte rendu

The idea of this interdisciplinary workshop was to focus on how, in our times, biology and genetics have up-rooted conventional understanding of what constitutes ‘human nature’, as well as age-old categories of humans, in the context of Darwinian evolution. These sciences have radically undermined the concept of race and introduced a new view of genetic diversity. This transformation in common self-conception further invites reassessment of the foundations of mega-paradigms such as ‘evolution’, subjecting them to a range of epistemological lenses that are at once scientific, technological, but also, importantly, social and historical. We have gone a long way from the ethos echoed in the subtitle Darwin chose for his Origin of Species: ‘Preservation of Favoured Races in the Struggle for Life’.

Re-ordering of humans and animals also lends itself well to addressing the most current topics of chimera research from all disciplinary perspectives. In what way did Darwin’s ideas challenge social boundaries of human versus animal? And what has happened in the molecular age? Has the fragmentation of life into cells and genes blurred or reinforced the human/animal boundary?

Can human nature be ultimately deconstructed and disposed of through the atomizing approaches of modern life science, or is there an intangible residue, internal or external, that makes us qualitatively different from all other life forms on earth? How would that exceptionalism have emerged through natural selection?

Clearly, evolutionary theory is the right framework to adopt when we seek to account for the sources and constraints of variation in mutable lineages within large populations. Thus, Darwinism is particularly suitable for elucidating a stunning range of phenomena, from the dynamics and variability of genomes, to the origin and progression of disease, the processes of speciation, and the origins and use of language. Ultimately, not only language, but all our beloved human faculties, were forged through selective processes in interactions between genes and environment. But the really tricky question still remains: to what extent and in what sense, as builders of our own environment, have we transcended nature?

The first day of the meeting was devoted to the history of the theory of evolution, some recent advances and a review of the fruitful interactions between evolutionary biology and the field of development and genetics (evo-devo).
Jean Gayon (Paris) talked about “Darwin and Wallace: a Constitutive Debate for the Theory of Natural Selection ». The essential questions of a discipline are usually specified by the first competent thinkers to enter it » (Gould 1977). This sentence applies well to the multifacetted debate that Alfred Russel Wallace and Charles Darwin had on many subjects about evolution. Gayon first raised the question whether the theories conjointly proposed by Darwin and Wallace in 1858 were basically identical or not. He insisted upon two major differences: (1) whereas Darwin defended an individualistic theory of competition and natural selection, Wallace emphasized the role of groups and species; (2) heredity was crucial to Darwin’s notion of selection, but it played almost no role in Wallace’s paper, whose approach was more « ecological ». Gayon then examined the various disensions that Darwin and Wallace had after the publication of On the Origin of Species. These disagreements can be classified into three categories. (1) Theory of selection. The two authors had two controversies, over group and species selection, and over sexual selection (which Wallace fiercely criticized). (2) Role of natural selection in the explanation of particular phenomena, with three major disagreements: over the origin of hybrid sterility, over the origin of sexual dimorphism, and over the origin of Man and human races. (3) Scope of the principle of natural selection in evolutionary theory. Whereas Darwin had a relatively nuanced perspective on the limits of natural selection, Wallace held a panadaptationist and panselectionist view of evolution as a whole. After this review, Jean Gayon emphasized the fundamental importance of all these debates all along the history of evolutionary biology up to now. He also commented on the ambiguity of the term « Darwinism ».
Steven Rose discussed: From Dobzhansky’s dictum to developmental systems theory. Dobzhansky, famously, said ‘nothing in biology makes sense except in the light of evolution.’ But, as Darwin himself said, natural selection is the major but not the only driver of evolutionary change. Furthermore, what evolves becomes a crucial question, asked for all living organisms by developmental systems theory (amongst others). What does the 98.4% similarity between chimpanzee and human genome tell us about the limits of biological evolutionary theory in its attempts to explain ‘the human condition’? S. Rose finished his presentation arguing that: nothing in evolution makes sense except in the light of development. For humans, he added, neither makes sense except in the light of culture, technology and human history. Denis Duboule echoed on Rose’s talk and discussed the question of Natural selection versus constrained variation ? He talked about the impact of the past 25 years of molecular developmental genetics upon our way to think macroevolution, in particular regarding the balance between the ‘why’ approach (natural selection) and the ‘how’ approach (variation). While the weight of the theory has been traditionally put on the former, it is perhaps time to see if our progresses in the understanding of molecular mechanisms can give some support to more internalist views of evolution, whereby significant variations may be highly constrained by the generative rules of the systems. He illustrated this with a few issues dealing with the genetic control of development and what this can teach us about evolution and constraints. Finally, he briefly discussed the rise and fall of Evo-Devo, a discipline whose transitory and instable status reflects the great difficulties to associate scientific fields, which, despite their tight relationships, have fundamentally different rules.
The emerging field of Evolutionary Developmental Biology (Evolution by Epigenesis) was discussed by Scott Gilbert. In 1893, Thomas Huxley, wrote, « Evolution is not a speculation but a fact; and it takes place by epigenesis. » Note that evolution’s chief British defender did not complete his sentence with the phrase « natural selection’, for Huxley was interested in the generation of the diversity needed for natural selection. That phase of evolution was regulated by development. Recent work has established several mechanisms for the generation of anatomical diversity through changes in development, and Gilbert’s talk reviewed  them and provided examples from the recent literature. The genetic mechanisms include: heterochrony (change in timing of gene expression), heterotopy (change in the type of cell expressing the gene), heterometry (change in the amount of gene expression), and heterotypy (change in the identity of the gene being expressed. The epigenetic mechanisms for variation include epialleles (chromatin modification that can be inherited from generation to generation), phenotypic plasticity (and its fixation by assimilation), and developmental symbiosis (wherein co-development occurs with other species).   S. Gilbert further argued that these developmental phenomena allow for more types of variation and for the relatively rapid evolution of new anatomical structures.
S. Gilbert’s talk was followed by  a presentation by Axel Meyer, who discussed about Adaptive radiations of cichlid fishes: endless forms most beautiful? Cichlid fishes are a well-known model system for extreme forms diversification.  In Lake Victoria more than 500 species of endemic fish originated in less than 100 000 years. In crater lakes in Nicaragua examples were found of new species that are probably only a few hundred years old.  Many species are not only extremely young, but also extremely specialized and occupy entirely surprising ecological niches. Yet, although cichlid fish hold the world record for rates of speciation and phenotypic diversification and have been argued to be a prime textbook example for the « phantasy of evolution », they also provide stunning examples for parallelisms and convergent evolution. The species flocks in East Africa show that similar ecological types, that sometimes even have similar coloration, have evolved in parallel in Lakes Victoria, Malawi and Tanganyika.  Why and how does evolution repeat itself? What – if any – are the (internal and external) rules that shape these adaptive radiations? These are amongst those questions that Meyer addressed in his presentation. Keeping with the problem of speciation and evolution of body forms, Benjamin Prud’homme discussed From developmental genes to body forms and from neurons to behaviors: towards an integrated understanding of animal evolution. The comparative analyses of genes and developmental mechanisms have revealed general principles underlying how animal forms are built and evolve. In particular, the emergence of morphological novelty, diversity and complexity can be appreciated as the result of the co-option and recombination of existing genetic features, rather than the creation of new components. Prud’homme discussed the extent to which the concepts derived from developmental genetics can be generalized and used as working hypotheses to study how neural circuits underlying divergent behavior can evolve. He illustrated these ideas using the drosophila wing pigmentation patterns that have evolved in concert with innate courtship behaviors.

The second day was orientated towards the evolution of vertebrates, or of features found in this group of animals. Philippe Janvier gave his views as a paleontologist: The Deep Time of vertebrate history: Gaps and inferences in vertebrate phylogeny. He mentioned that the vertebrate tree has been pruned by a number of major extinctions, notably in Paleozoic times, which leaves us with large gaps and important disparity on the extant diversity of the group. Fossils, however poorly preserved, may help in filling these gaps with a limited number of reliable characters and taxa, and have received a reciprocal illumination from current advances in developmental genetics, as in the case of the origin of jaws or of paired limbs. In a world without fossils, our morphology- or molecule- based vertebrate trees would probably be much the same as the current ones, yet fossils provide hints at the competitions and contingencies which have shaped it. Nicole Le Douarin discussed the critical importance of neural crest cells in vertebrate evolution (The Neural Crest, an important asset in the evolution of Vertebrates). She argued that the major evolutionary success of vertebrates and the extreme degree of complexity reached by their brain, which culminates in humans, is among the most spectacular features of the history of life. During the last decades, significant progress has been made in our understanding of the changes in the Chordate phylum that are likely to be responsible for the emergence of Vertebrate novelties. Chordates include, together with vertebrates, cephalocordates and tunicates. Among these novelties are the emergence of the Neural Crest and related structures the ectodermal cranial Placodes. The latter are at the origin of the sense organ associated with the brain. The cells which compose the Neural Crest are highly pluripotent, undergo an epithelio-mesenchymal transition, migrate within the developing embryo and differentiate into a large variety of cell types. They are namely at the origin of the Peripheral Nervous System and of most of the head mesenchyme, of the facial skeleton including the jaw and most of the cranial vault. Our recent results indicate that the NC plays also a key role in the development of the most recent part of the brain. In this so far unsuspected function, the NC acts as a signaling center regulating the production of major growth and survival factors which control the conspicuous development of the fore- and mid-brain in higher Vertebrates. The NC can thus be considered as being at the origin of a New Head, which characterizes the Vertebrates among the other Chordates.

Brigitte Galliot discussed the distribution and evolution of the regenerative potential in animals (Towards a parsimonious analysis of regeneration and self-repair in animal evolution). All metazoan phyla contain species that undergo regeneration after amputation. Simple organisms as hydra or planarians regenerate their main body axes, while salamanders and fish regenerate complex structures such as limbs, fins, tails but also heart, retina, lens. Hence, in these species the developmental programs remain accessible to reactivation throughout life, whereas in frogs they become locked after metamorphosis and in most mammals, adult regeneration is restricted to tissues as bone, liver. The consensus view is that regeneration is an ancestral character, randomly maintained or lost along evolution. If true, this means that core regenerative processes could be characterized by comparing the regenerative processes across evolution, and possibly reactivated when necessary. B. Galliot discussed the criteria that should be considered to identify or rule out the putative homologies among the various regenerative processes. Once caracterized, these features can be assembled to form a « regenerative code » that defines each regenerative context and these regenerative codes can be submitted to parsimonious analysis to define groups of processes sharing common features. Finally, she discussed the validity of this approach that combines both developmental, cellular and molecular parameters.
A particular view at The evolution of signal transduction was presented by Alain Prochiantz. Homeoprotein intercellular transfer, he argued, is a very simple and probably extremely ancient mode of signal transduction shared by plants and animals. In his presentation, he developed the hypothesis that this loose mode of signaling may have come first, followed by the recruitment of other signaling mechanisms selected on the basis of their ability to enhance developmental robustness. This hypothesis was discussed in the context of the evolution of the nervous system, from the positioning of boundaries between compartment in the developing neuro-epithelium, to the establishment and physiology of functional circuits.

The second half of the meeting was more specifically devoted to various aspects of human evolution. Johannes Krause discussed: ‘What makes us human: Insights from sequencing the Neandertal genome’. Neandertals, a hominid group that appeared in the European fossil record around 400, 000 years ago and disappeared around 30.000 years ago, are believed to be our closest extinct relatives. Although Neandertals and modern humans overlapped in certain regions in time and space, the relationship between us and them is unclear and contentious. A genetic comparison between modern humans and Neandertals could both address the relationship between us and them and offer the possibility to identify genetic changes that happened specifically on the human lineage. Furthermore it may allow identifying and understanding the evolutionary history of genes and positions in the modern human genome that experienced recent positive selection after Neandertals and humans separated and that might play an important role in human evolution, such as the FOXP2 gene. Krause described a combination of high-throughput DNA sequencing technologies and multiple improvements in ancient DNA retrieval and library construction, which help to determine the sequences of over one billion DNA fragments from Neandertal bones from Vindija Cave, Croatia. From these DNA sequences, about 4, 5 Gb of Neandertal DNA has been identified. Estimates of modern human contamination range from 0.3% for mtDNA and 0.5% for Y chromosomal DNA. The average divergence of Neandertal and modern human DNA sequences is over 800, 000 years. To learn more about the size and potential structure of the Neandertal population, Krause explained how various targeted methods were implemented to sequence specific parts of the Neandertal genome, such as complete mitochondrial genome sequences, in Neandertals from various sites in Europe suggesting a small effective population size in Neandertals similar to modern Europeans.

Daniel Lieberman discussed the role of energy in evolution (Energy and human evolution), with a particular focus on the role and importance of locomotion in human evolution.  Natural selection is an emergent process that results from the combination of heritable variation, competition (often brought about by environmental change), and differential reproductive success.  Natural selection is therefore expected to drive animals towards energetic optima because individuals who extract and use energy better than their competitors will tend to have higher fitness.  But what energetic parameters does natural selection optimize?  Many biologists have traditionally focused on efficiency, under the reasonable assumption that acquiring more per unit time and/or using less energy per unit of work will improve an organism’s energetic balance, allowing it to devote more energy towards tasks that increase fitness.  But this assumption obviously oversimplifies many cases, particularly in locomotion where selection for speed and power drive predator/prey co-evolution (faster predators and faster prey). Lieberman used this framework to examine Darwin’s prescient suggestion (made in 1871 without any fossil evidence) that the adoption of bipedalism was a key event that started the human lineage on its separate trajectory from the African apes. His presentation focused on two major events and their energetic consequences.  The first was the origins of bipedalism, which was probably selected to increase locomotor economy at the expense of power in the context of habitat change at the end of the Miocene.  Early bipedal hominins, however, faced serious constraints on speed and power, which created the conditions for a second major selective force at the end of the Pliocene, the evolution of endurance.  There are multiple lines of evidence that adaptations for endurance (and for thermoregulation) enabled the genus Homo to occupy a new and very successful niche:  a diurnal, social carnivore and forager, able to extract much more energy and devote it towards larger brains, larger bodies, and shorter inter-birth intervals.  The positive feedback cycle unleashed by this unusual combination has been a major factor driving change in the genus Homo and continues until this very day.

Ritta Hari took ‘a neuroscientist’s view on brain, mind, and environment. She explained that neuroscientists often look at brain function in rather artificial situations, focusing on stimulus–response connections, motor actions, and brain states. However, to understand the dynamical shaping of the human brain and mind—both during evolution and ontogeny—it appears essential to consider the brain as a part of an action–perception loop that tightly, and bi-directionally, binds the individual to his/her environment that includes other people, tools, and cultural artifacts and practices. She argued that an enormous future challenge will be to incorporate the direct and technology-mediated social interaction into human neuroscience, both conceptually and methodologically. This view was echoed by Pierre Magistretti (Plasticity and discontinuity in the emergence of individuality), who discussedthree issues. The first one related to neuronal plasticity and its central role in mediating the emergence of individuality. Magistretti discussed some paradoxes of neuronal plasticity as it can be viewed both as a deterministic process and, at the same time, as a process, which,  through the re-association of traces left by experience,  introduces a discontinuity freeing the individual from other determinants. This lead him to address a second issue, as a brief discussion of the distinctions that can be made between the terms of instinct in animals and drive in humans. As a third issue,  he discussed the energetic constraints of information processing by the brain: indeed the energetic demands associated to brain function are very high, corresponding to at least 15% of the overall energy consumption of the organism. Why is it so? Does energy availability represent a theoretical limit to brain function? Was it optimized or can it be better optimized?        

Speech processing in adults relies on precise and specialized networks, located primarily in the left hemisphere. Ghislaine Dehaene-Lambertz (How does early brain organization promote language acquisition in humans?) discussed behavioral studies in infants, which indicate that a considerable amount of language learning already takes place in the first year of life in the domains of phonology, prosody, and word segmentation. Thanks to the progress of neuro-imaging, she showed how one can now move beyond behavioral methods and examine how the infant’s brain processes verbal stimuli before learning. These studies reveal a structural and functional organization close to what is described in adults, especially strong and early asymmetries in the posterior temporal region. This suggests an important bias for speech processing in these regions that might guide infants in the discovery of the properties of their native language.

‘Reconciling brain evolution and human culture: The concept of neuronal recycling’ was the title of the presentation by Stanislas Dehaene. Human brain imaging has revealed that there are fixed cortical regions in the adult brain, which are reproducibly allocated to cultural activities such as recognition of written words or mental calculation. Yet how is it possible for brain areas to specialize in domains that are obviously recent cultural inventions? There has not been enough time or pressure for evolution to assemble specific circuits for word recognition or symbolic arithmetic. In his presentation, Dehaene argued that these domains provide evidence for a ‘cultural neuronal recycling’ – the pre-emption of some pre-existing brain circuits for another, more or less distant, cultural activity. According to this idea, cultural inventions such as reading are possible only inasmuch as they find a cerebral “niche”, a set of appropriately organized cerebral circuits, that can be minimally changed to implement the requested function. This was illustrated throughout the presentation using a detailed analysis of the brain mechanisms that allow us to acquire reading. Learning to read entails the specialization of a left occipito-temporal region, the visual word form area, which becomes attuned to orthographic regularities in the reader’s language. This specialization reflects the “recycling” of a visual area, which is present in all primates and evolved a number of desirable features for invariant object recognition. Brain imaging of illiterates suggests that face perception may be one of the competitors of reading in occipito-temporal cortex. The peculiar phenomenon of mirror reading can be explained by the prior propensity of this region for mirror-image generalization, which needs to be unlearned during reading acquisition. According to Dehaene, the brain did not evolve for writing – rather, cultural evolution adapted our writing systems so that they could be efficiently acquired given the structure of our visual brain.This analysis suggests a new vision of the relations between culture and brain evolution. At expense with the dominant view in social sciences, this hypothesis implies that human cultural traits are tightly constrained by our biological heritage and are therefore not infinitely variable and malleable.

The meeting terminated with three presentations from social scientists. Marion Blute, discussed the:Darwinian Sociocultural Evolution: Evolutionary Solutions to Theoretical Dilemmas in Cultural and Social Theory’. She argued that Darwinism in the social sciences comes in three broad forms – the gene-based biological, the social learning or meme-based sociocultural, and gene-culture co-evolution. The subject of her talk was the second, Darwinian sociocultural evolution. She sketched six theoretical dilemmas in cultural and social theory on which Darwinian sociocultural evolutionary theory can shed some light and then discussed into more depth on two of them. These are whether something, everything, or nothing is “socially constructed” and the role of history or the idiographic versus science or the nomothetic in understanding human affairs. Hilary Rose presentation was entitled: Evolution, Natural and  Assisted Selection. She explained that Darwin’s theory of natural and sexual selection has long had multiple readings. Natural scientists, particularly life scientists, consider Social Darwinism as a misreading of Darwin; others from the social studies of science, conscious of Darwin’s debt to Malthus, are less convinced. But it was Galton’s thesis of inherited genius and his science of eugenics, both endorsed by Darwin, which introduced the idea that artificial selection could be deployed to improve the human population. Regardless of political stance this was supported (bar Catholics) by the cultural and social elite, and most industrialized countries began to practice the science of eugenics. This state eugenics did not end with the defeat of the Nazis, but continued, though rarely acknowledged as eugenics, to the mid 1970s. Defeated by the new social justice movements, eugenics lay dormant until the rise and rise of molecular genetics within an increasingly neo-liberal economy. Eugenics was reborn, this time as consumer eugenics. While as a social scientist H. Rose holds her own primarily social concerns, what she asked to the life scientists attending the meeting was: what are the techniques of IVF, PGD, sex selection, saviour siblings, ‘designer babies’ and cloning doing to human evolution? And should we care? Finally, Dan Sperber talked about Evolutionary approaches to culture: Challenges and solutions.Current evolutionary approaches to culture borrow their explanatory framework from population genetics and their ontology form the standard social sciences. They aim for instance at explaining ‘religion’, ‘norm’, or ‘institutions’ when there is no naturalistic understanding of these notions. Attributing natural biological causes to non-natural cultural effects falls short of providing a naturalistic account of culture. A first challenge then is to naturalize the ontology of culture.

Cultural things (representations, practices and artifacts) are relatively stable at the scale of population and in historical time (or else, there would be no culture to speak of). This is taken to imply that the micro-episodes of cultural transmission must have a degree of fidelity that wholly or largely explains this macro-stability. However empirical studies of cultural transmission show a much lower degree of fidelity than would be needed to explain macro-stability. A second challenge then is to provide an explanation of cultural stability that is both formally and empirically plausible. Sperber presentation aimed at providing a unified solution to both challenges.

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