Ideas about heredity and evolution are undergoing a revolutionary change. New findings in molecular biology challenge the gene-centered version of Darwinian theory according to which adaptation occurs only through natural selection of chance DNA variations. In Evolution in Four Dimensions, Eva Jablonka and Marion Lamb argue that there is more to heredity than genes. They trace four "dimensions" in evolution -- four inheritance systems that play a role in evolution: genetic, epigenetic, behavioral, and symbolic. These systems, they argue, can all (...) provide variations on which natural selection can act. Evolution in Four Dimensions offers a richer, more complex view of evolution than the gene-based, one-dimensional view held by many today. The new synthesis advanced by Jablonka and Lamb makes clear that induced and acquired changes also play a role in evolution.After discussing each of the four inheritance systems in detail, Jablonka and Lamb "put Humpty Dumpty together again" by showing how all of these systems interact. They consider how each may have originated and guided evolutionary history and they discuss the social and philosophical implications of the four-dimensional view of evolution. Each chapter ends with a dialogue in which the authors engage the contrarieties of the fictional "I.M.," or Ifcha Mistabra -- Aramaic for "the opposite conjecture" -- refining their arguments against I.M.'s vigorous counterarguments. The lucid and accessible text is accompanied by artist-physician Anna Zeligowski's lively drawings, which humorously and effectively illustrate the authors' points. (shrink)

In his target article, Koonin discusses the insights into the evolution of bacterial genomes provided by the CRISPR-Cas system. This evolved defense system is based on intrinsic processes of genome engineering which, as he argues, enable Lamarckian inheritance. In this commentary I discuss some historical and conceptual issues that pertain to Koonin’s analysis of this aspect of the CRISPR-Cas system, extending and qualifying his discussion.

'...a challenging and useful book, both because it provokes a careful scrutiny of one's own basic ideas regarding evolutionary theory, and because it cuts across so many biological disciplines.' -The Quarterly Review of Biology 'In my view, this work exemplifies Theoretical Biology at its best...here is rampant speculation that is consistently based on cautious reasoning from the available data. Even more refreshing is the absence of sloganeering, grandstanding, and 'isms'.' -Biology and Philosophy 'Epigenetics is fundamental to understanding both development and (...) gene expression, and not surprisingly, evolutionary biologists have long been fascinated with its proper place in evolutionary theory...Enter Jablonka and Lamb, who provide a thoughtful review of the recent molecular literature and suggest a number of potential consequences.' -EvolutionSince first publication of this controversial book, much of the initial opposition to the ideas it contained has been replaced by a general, although often grudging, acceptance of them. Advances in knowledge, especially at the molecular level, have enhanced general awareness and interest in epigenetics and the evolution of systems that store and transmit information and put any of the authors' speculations on a more solid basis. This paperback edition contains a new Preface that sets out the major changes in the scientific world and in the authors' own thinking that have occurred since the book was published. A new Appendix provides a selected bibliography of the many books and articles about epigenetic inheritance and its role in evolution that have appeared since first publication. (shrink)

The semantic concept of information is one of the most important, and one of the most problematical concepts in biology. I suggest a broad definition of biological information: a source becomes an informational input when an interpreting receiver can react to the form of the source (and variations in this form) in a functional manner. The definition accommodates information stemming from environmental cues as well as from evolved signals, and calls for a comparison between information‐transmission in different types of inheritance (...) systems—the genetic, the epigenetic, the behavioral, and the cultural‐symbolic. This comparative perspective highlights the different ways in which information is acquired and transmitted, and the role that such information plays in heredity and evolution. Focusing on the special properties of the transfer of information, which are very different from those associated with the transfer of materials or energy, also helps to uncover interesting evolutionary effects and suggests better explanations for some aspects of the evolution of communication. (shrink)

What role does non-genetic inheritance play in evolution? In recent work we have independently and collectively argued that the existence and scope of non-genetic inheritance systems, including epigenetic inheritance, niche construction/ecological inheritance, and cultural inheritance—alongside certain other theory revisions—necessitates an extension to the neo-Darwinian Modern Synthesis (MS) in the form of an Extended Evolutionary Synthesis (EES). However, this argument has been challenged on the grounds that non-genetic inheritance systems are exclusively proximate mechanisms that serve the ultimate function of calibrating organisms (...) to stochastic environments. In this paper we defend our claims, pointing out that critics of the EES (1) conflate non-genetic inheritance with early 20th-century notions of soft inheritance; (2) misunderstand the nature of the EES in relation to the MS; (3) confuse individual phenotypic plasticity with trans-generational non-genetic inheritance; (4) fail to address the extensive theoretical and empirical literature which shows that non-genetic inheritance can generate novel targets for selection, create new genetic equilibria that would not exist in the absence of non-genetic inheritance, and generate phenotypic variation that is independent of genetic variation; (5) artificially limit ultimate explanations for traits to gene-based selection, which is unsatisfactory for phenotypic traits that originate and spread via non-genetic inheritance systems; and (6) fail to provide an explanation for biological organization. We conclude by noting ways in which we feel that an overly gene-centric theory of evolution is hindering progress in biology and other sciences. (shrink)

There are many different notions of information in logic, epistemology, psychology, biology and cognitive science, which are employed differently in each discipline, often with little overlap. Since our interest here is in biological processes and organisms, we develop a taxonomy of functional information that extends the standard cue/signal distinction. Three general, main claims are advanced here. This new taxonomy can be useful in describing learning and communication. It avoids some problems that the natural/non-natural information distinction faces. Functional information is​ ​produced (...) through exploration and stabilisation processes. (shrink)

In his theory of evolution, Darwin recognized that the conditions of life play a role in the generation of hereditary variations, as well as in their selection. However, as evolutionary theory was developed further, heredity became identified with genetics, and variation was seen in terms of combinations of randomly generated gene mutations. We argue that this view is now changing, because it is clear that a notion of hereditary variation that is based solely on randomly varying genes that are unaffected (...) by developmental conditions is an inadequate basis for evolutionary theories. Such a view not only fails to provide satisfying explanations of many evolutionary phenomena, it also makes assumptions that are not consistent with the data that are emerging from disciplines ranging from molecular biology to cultural studies. These data show that the genome is far more responsive to the environment than previously thought, and that not all transmissible variation is underlain by genetic differences. In Evolution in Four Dimensions (2005) we identify four types of inheritance (genetic, epigenetic, behavioral, and symbol-based), each of which can provide variations on which natural selection will act. Some of these variations arise in response to developmental conditions, so there are Lamarckian aspects to evolution. We argue that a better insight into evolutionary processes will result from recognizing that transmitted variations that are not based on DNA differences have played a role. This is particularly true for understanding the evolution of human behavior, where all four dimensions of heredity have been important. (shrink)

The dichotomy between Nature and Nurture, which has been dismantled within the framework of development, remains embodied in the notions of plasticity and evolvability. We argue that plasticity and evolvability, like development and heredity, are neither dichotomous nor distinct: the very same mechanisms may be involved in both, and the research perspective chosen depends to a large extent on the type of problem being explored and the kinds of questions being asked. Epigenetic inheritance leads to transgenerationally extended plasticity, and developmentally-induced (...) heritable epigenetic variations provide additional foci for selection that can lead to evolutionary change. Moreover, hereditary innovations may result from developmentally induced large-scale genomic repatterning events, which are akin to Goldschmidtian “systemic mutations”. The epigenetic mechanisms involved in repatterning can be activated by both environmental and genomic stress, and lead to phylogenetic as well as ontogenetic changes. Hence, the effects and the mechanisms of plasticity directly contribute to evolvability. (shrink)

This is the first of two papers in which we propose an evolutionary route for the transition from sensory processing to unlimited experiencing, or basic consciousness. We argue that although an evolutionary analysis does not provide a formal definition and set of sufficient conditions for consciousness, it can identify crucial factors and suggest what evolutionary changes enabled the transition. We believe that the raw material from which feelings were molded by natural selection was a global sensory state that we call (...) overall sensation, which is a by-product of the incessant activity of the highly interconnected nervous systems that characterize all neural animals. We argue that global sensory states generated limited experiencing once they became coupled to the simplest kinds of nervous-system-mediated learning, a coupling that occurred in the most ancient taxa of neural animals, which were similar to present-day cnidarians and ctenophores. In such animals, limited experiencing involves a small number of persistent global sensory states. These sensory states, however, do not have a function and do not act as motivational states. As we argue in the next paper, with the evolution of associative learning they evolved into systems that gave animals basic consciousness. (shrink)

We discuss the evolutionary transition from animals with limited experiencing to animals with unlimited experiencing and basic consciousness. This transition was, we suggest, intimately linked with the evolution of associative learning and with flexible reward systems based on, and modifiable by, learning. During associative learning, new pathways relating stimuli and effects are formed within a highly integrated and continuously active nervous system. We argue that the memory traces left by such new stimulus-effect relations form dynamic, flexible, and varied global sensory (...) states, which we call categorizing sensory states . These CSSs acquired a function: they came to act as internal “evaluators” and led to positive and negative reinforcement of new behavior. They are therefore the simplest, distinct, first-person motivational states that an animal can have. They constitute what we call basic consciousness, and are the hallmark of animals that can experience. Since associative learning has been found in many invertebrate taxa that first appeared during the Cambrian era, we propose that the processes underlying basic consciousness are phylogenetically ancient, and that their emergence may have fueled the Cambrian explosion. (shrink)

In responding to three reviews of Evolution in Four Dimensions (Jablonka and Lamb, 2005, MIT Press), we briefly consider the historical background to the present genecentred view of evolution, especially the way in which Weismann’s theories have influenced it, and discuss the origins of the notion of epigenetic inheritance. We reaffirm our belief that all types of hereditary information—genetic, epigenetic, behavioural and cultural—have contributed to evolutionary change, and outline recent evidence, mainly from epigenetic studies, that suggests that non-DNA heritable variations (...) are not rare and can be quite stable. We describe ways in which such variations may have influenced evolution. The approach we take leads to broader definitions of terms such as ‘units of heredity’, ‘units of evolution’, and ‘units of selection’, and we maintain that ‘information’ can be a useful concept if it is defined in terms of its effects on the receiver. Although we agree that evolutionary theory is not undergoing a Kuhnian revolution, the incorporation of new data and ideas about hereditary variation, and about the role of development in generating it, is leading to a version of Darwinism that is very different from the gene-centred one that dominated evolutionary thinking in the second half of the twentieth century. (shrink)

Building on Dor’s theory of language as a social technology for the instruction of imagination, I suggest that autobiographical memory evolved culturally as a response to the problems of false memory and deliberate deceit that were introduced by that technology. I propose that sapiens’ linguistic communication about past and future events initially occurred in small groups, and this helped to correct individual memory defects. However, when human groups grew in size and became more socially differentiated, and movement between groups prevented (...) story-verification, misattributions of events became more common. In such conditions individuals with better autobiographical memory had an advantage because they could evaluate their own contents and sources of information, as well as that of others, more accurately; this not only benefitted them directly, but also improved their reliability as social partners. Autobiographical memory thus evolved in the context of human linguistic communication through selection for communicative reliability. However, the advantages of imagination, which enables forward-planning and decision-Making, meant that memory distortions, although controlled and moderated by autobiographical memory, could not be totally eradicated. This may have driven the evolution of additional forms of memory control involving social and linguistic norms. I interpret the language and the social norms of the Pirahã as the outcome of the cultural-evolutionary control of memory distortions. Some ways of testing aspects of this proposal are outlined. (shrink)

This volume joins a growing list of books, monographs, and proceedings from scientific meetings that attempt to consolidate the wide spectrum of approaches emphasizing the role of development in evolution into a coherent and productive synthesis, often called evo-devo. Evo-devo is seen as a replacement or amendment of the modern synthesis that has dominated the field of evolution since the 1940s and which, as even its architects confessed, was fundamentally incomplete because development remained outside its theoretical framework (Mayr and Provine (...) 1980).As the volume attests, there is now a strong feeling that the time is ripe for the onsolidation of evo-devo, and that the field is mature enough so that mapping the theoretical terrain and experimental approaches is both feasible and scientifically productive. Now is an appropriate time to try to weave the strands of reasoning leading to the developmental perspective and offer a synthesis. (shrink)

Adaptive evolution is usually assumed to be directed by selective processes, development by instructive processes; evolution involves random genetic changes, development involves induced epigenetic changes. However, these distinctions are no longer unequivocal. Selection of genetic changes is a normal part of development in some organisms, and through the epigenetic system external factors can induce selectable heritable variations. Incorporating the effects of instructive processes into evolutionary thinking alters ideas about the way environmental changes lead to evolutionary change, and about the interplay (...) between genetic and epigenetic systems. (shrink)

We claim that much of the confusion associated with the "tautology problem" about survival of the fittest is due to the mistake of attributing fitness to individuals instead of to types. We argue further that the problem itself cannot be solved merely by taking fitness as the aggregate cause of reproductive success. We suggest that a satisfying explanation must center not on logical analysis of the concept of general adaptedness but on the empirical analysis of single adapted traits and their (...) causal relationship to changes in allele frequencies. (shrink)

We suggest that, in animals, the core-affect system is linked to partially assimilated behavioral dispositions that act as developmental scaffolds for the ontogenetic construction of emotions. We also propose that in humans the evolution of language altered the control of emotions, leading to categories that can be adequately captured only by emotion-words.

The commentaries on Evolution in Four Dimensions reflect views ranging from total adherence to gene-centered neo-Darwinism, to the acceptance of non-genetic and Lamarckian processes in evolution. We maintain that genetic, epigenetic, behavioral, and cultural variations have all been significant, and that the developmental aspects of heredity and evolution are an important bridge that can unite seemingly conflicting research programs and different disciplines.

In his thought-provoking book, Alex Mesoudi argues for an evolutionary, unifying framework for the social sciences, which is based on the principles of Darwinian theory. Mesoudi maintains that cultural change can be illuminated by using the genotype-phenotype distinction, and that it is sufficiently similar to biological change to warrant a theory of culture-change based on evolutionary models. He describes examples of cultural microevolution, within-population changes, and the biologically inspired population genetics models used to study them. He also shows that some (...) aspects of large-scale cultural transformation can be studied by using ecological models and phylogenetic comparative techniques. We argue that although Mesoudi's evolution-based perspective offers many useful insights, his ambition—the unification of the social sciences within a Darwinian framework through the use of the methods and models he describes—suffers from a major theoretical limitation. His reductive approach leads to overlooking culture as a system with emergent processes and features. Mesoudi therefore does not engage with any of the central past and present theories in sociology and anthropology for which the systems view of culture is central, and he does not analyze the emergent, high-level properties of human cultural-social systems. We suggest that a systems perspective, using some analogies and metaphors from developmental biology, can complement the evolutionary approach and is more in tune with a systems view of society. Such an approach, which stresses feedback and self-sustaining interactions within social networks, and engages with the insights of sociological and anthropological theories, can contribute to the understanding of cultural systems by highlighting the evolution of processes of social cohesion, and by making use of the mathematical approaches of complexity theory. (shrink)

predators stalk their chosen prey, and so forth. The genius of “instinct†comes in abundant variety, and breeds true. “It must be in the genesâ€â€“that’s what we tend to conclude. But when we do, we may be jumping to conclusions, because there are other possibilities: the clever behavior we observe could be the do-it-yourself invention or discovery of the individual behaver or it could be a clever trick copied from an elder member of its species, most likely one of its (...) parents. This last possibility is an ancient doctrine, enshrined in folklore about animal parents sternly but lovingly training their young, and in countless anecdotes, but this appealing idea of animals benefitting from hand-me-down wisdom from earlier generations much the way we do has recently languished in the shadow of the genes, an oversight this book seeks to correct. The folklore is not all fanciful; some of it can be supported by good science, which moreover will open up surprising vistas on the role of individual behavior in evolution. The book is fascinating on at least three levels: first, it provides a vivid and insightful survey.. (shrink)