The Modern Evolutionary Synthesis MS forged in the mid-twentieth century was built on a notion of heredity that excluded soft inheritance, the inheritance of the effects of developmental modifications. However, the discovery of molecular mechanisms that generate random and developmentally induced epigenetic variations is leading to a broadening of the notion of biological heredity that has consequences for ideas about evolution. After presenting some old challenges to the MS that were raised, among others, by Karl Popper, I discuss recent research on epigenetic inheritance, which provides experimental and theoretical support for these challenges. There is now good evidence that epigenetic inheritance is ubiquitous and is involved in adaptive evolution and macroevolution. I argue that the many evolutionary consequences of epigenetic inheritance open up new research areas and require the extension of the evolutionary synthesis beyond the current neo-Darwinian model. This was not only because Popper suggested that the then-current version of Darwin's theory required serious revision, but also because he was deliberately provocative, adhering to his conviction that only sharp critique can awaken colleagues from their intellectual slumbers and stimulate discussions that lead to scientific progress.
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The Modern Evolutionary Synthesis MS forged in the mid-twentieth century was built on a notion of heredity that excluded soft inheritance, the inheritance of the effects of developmental modifications.
However, the discovery of molecular mechanisms that generate random and developmentally induced epigenetic variations is leading to a broadening of the notion of biological heredity that has consequences for ideas about evolution. After presenting some old challenges to the MS that were raised, among others, by Karl Popper, I discuss recent research on epigenetic inheritance, which provides experimental and theoretical support for these challenges.
There is now good evidence that epigenetic inheritance is ubiquitous and is involved in adaptive evolution and macroevolution. I argue that the many evolutionary consequences of epigenetic inheritance open up new research areas and require the extension of the evolutionary synthesis beyond the current neo-Darwinian model. This was not only because Popper suggested that the then-current version of Darwin's theory required serious revision, but also because he was deliberately provocative, adhering to his conviction that only sharp critique can awaken colleagues from their intellectual slumbers and stimulate discussions that lead to scientific progress.
There is an interesting link between Popper's lecture and the topic of this issue of Interface Focus : Popper raised some of the very same points that the advocates of an extended evolutionary synthesis are putting forward today, and suggested that the then-current version of Darwinism—what was and is still called the Modern Synthesis MS —needed to be revised.
Although Popper's call for a change was not very effective, his lecture shows that discontent with the MS version of evolution is not new. The MS was forged by the middle of the twentieth century: one of the historical landmarks was the post-war Princeton Conference on Genetics, Palaeontology and Evolution held in , which celebrated the successful unification of Darwinian ideas about natural selection with Mendelian genetics and palaeontology [ 2 , 3 ].
Of course, the MS has been updated and changed since then, but there are several aspects that right from the early days have been systematically downplayed or explicitly excluded [ 3 ]. One issue that was recognized but downplayed was the role of plasticity in evolution: Waddington's ideas did have some early impact, especially in Great Britain, but people lost interest very quickly [ 4 ]; similarly, there was little interest in the active role of the organism in the construction of its own selection regime and the evolutionary feedbacks that such niche construction generates, and little attention was given to the constraints and affordances imposed on phenotypic variations by the processes of development, or to the role of group selection reviewed in [ 5 ].
He firmly believed that developmental changes occurring at the individual level cannot be passed on to the next generation and lead to cumulative evolutionary change. For Mayr, as for most of the MS architects and their followers, this exclusion was one of the defining features of the synthesis. Before I discuss this excluded possibility, I want to briefly consider Popper's challenges of 30 years ago. His first challenge was the argument that evolutionary analysis should start by considering phenotypic variability and phenotypic adjustment, not random mutation.
He argued that living organisms are active agents ; they have goals the ultimate evolutionary goal being reproduction which they strive to fulfil through their activities. When the conditions of life change, organisms do not wait passively for a liberating mutation—they do what they can to cope, including changing where and how they live. This coping, this phenotypic adjustment, which can be the response to a new mutation as well as to a new change in external conditions, is far from random.
It is such goal-directed developmental responses, Popper suggested, not random mutations that should be the point of departure of an evolutionary explanation. That is to say, what comes before the mutation is a behavioural change, and the mutation comes afterwards' [ 10 , p.
The idea that changed behaviour may initiate evolutionary change was not original, of course. It goes back to Baldwin, Morgan and Osborn at the very end of the nineteenth century [ 11 ], and Popper was aware that Waddington had developed these ideas within the framework of Mendelian genetics [ 12 ].
However, the evolutionary significance of the Baldwin effect and of genetic assimilation was downplayed, for example, by Simpson [ 13 ], and this position has been uncritically parroted by biologists ever since for a notable exception, see [ 14 ].
The second of Popper's suggestions was that the non-random, goal-directed processes that lead to the organism's phenotypic adjustments involve developmental selection. Internal processes generate variation, which is followed by processes of selection or stabilization at the ontogenetic level. Popper's third suggestion was that developmental selection may lead to between-generation inheritance not only through genetic assimilation, but also through feedbacks between the soma and the germ line.
How this happened was not entirely clear to him, but he was very excited by Ted Steele's hypothesis that selected somatic mutations in the immune system can affect the germ line through the reverse transcription of RNAs that were abundantly expressed during the immune response [ 15 ]. Nevertheless, a strong element of stochasticity remains, and this allows the system to respond to the unexpected. For Popper, what was important in Steele's hypothesis was the combination of developmental, intra-organismal selection of stochastic variations and the intergenerational transmission of some selected variants, which resulted in a feedback between the effects of developmental selection in individuals and natural selection in populations.
Popper believed that incorporating developmental selection within evolutionary explanations reinforced Darwin's perception of the centrality of selective processes in evolution. Selection is not just natural selection in the classical sense, but any differential stabilization and amplification process occurring between and within organisms, with the different selection processes interacting.
There were many problems with the evolutionary ideas Popper advanced in his lecture, and I shall not dwell on them here for detailed discussion, see [ 1 , 12 , 16 ]. However, his insistence on the agency of organisms and his phenotype-first view of evolution, his focus on developmental selection and the possibility of interactions between within-individual developmental selection and between-individual selection resonate with the ideas developed by evolutionary biologists today [ 16 ].
Interestingly, Popper's view was almost identical to that expressed by Jean Piaget in the s and s, although the two men seem to have been unaware of their agreement and did not join forces to sophisticate and promote their point of view [ 17 ]. In the light of recent post-Popper and Piaget discoveries about epigenetic mechanisms and epigenetic inheritance, we can now take a fresh look at the challenges they and others posed to the MS in the twentieth century.
My focus here is on the effect of epigenetic, often partially biased, developmentally generated variations on evolutionary change, which, I argue, requires an extension of the MS.
There are several factors, in addition to similarities in DNA sequence, that contribute to the hereditary similarity between parents and offspring.
One is the inheritance of epigenetic variations originating in ancestors. Epigenetics has a wide sense, defined by Waddington, and a narrow sense which pertains mainly to cell memory and cell heredity.
In the narrower, modern sense, it is the study, in both prokaryotes and eukaryotes, of the developmental processes that lead to changes in an organism's state that persist in the absence of the original inducing input based on [ 18 , p. The epigenetic mechanisms that can lead to persistent developmental effects in both non-dividing e. These epigenetic control and cell memory mechanisms are commonly interconnected, sometimes forming persistent, self-maintaining, cellular networks, although they can, of course, lead to very transient changes.
They are also important in the recruitment and regulation of the natural cellular engineering processes that are involved in DNA repair and the control of transposition and recombination [ 20 ].
At a higher level of biological organization, these epigenetic mechanisms underlie self-sustaining interactions between groups of cells or between an organism and its environment, which are mediated by physiological e. Epigenetic inheritance is a component of epigenetics, not a synonym. It refers to the transmission to subsequent generations of cells or organisms of phenotypic variations that do not stem from variations in the DNA base sequence.
Transmission can occur during mitotic cell division, and also sometimes during the sexual processes of meiosis and gametogenesis. Mitotic and gametic epigenetic inheritance are mediated by essentially the same epigenetic mechanisms, although different factors and types of regulatory interactions are involved in different cell types.
Between-generation epigenetic inheritance need not, however, involve transmission through gametes. We are all conditioned by DNA replication as the mode of information transmission, so we tend to think that all transmission must involve replicative processes.
This preconception is wrong: in some types of both gametic and soma-to-soma transmission, inheritance takes place by a reconstruction rather than replication of parental states.
For example, a particular chromatin configuration, such as a particular methylation pattern, might initiate a self-sustaining loop that generates a protein or an RNA product that can take part in the establishment and perpetuation of that configuration.
This kind of mechanism may be involved in the transmission through the sperm of small RNAs that lead to hereditary similarity [ 25 ]. Alternatively, although most chromatin marks are erased, a fraction of them e. Epigenetic inheritance seems to involve both replicative and reconstructive processes. Epigenetic inheritance is ubiquitous. Today, no one doubts that this mode of inheritance occurs everywhere—it has been found wherever it was looked for, in all taxonomic groups for reviews, see [ 26 , 27 ] , and it includes various routes of transmission, including transmission of small regulatory RNAs from soma to germ line, a mode of transmission that seems to vindicate Darwin's pangenesis theory [ 28 ].
The fidelity with which epigenetic states are transmitted is condition- and taxon-dependent and is clearly variable. There have been in-depth analyses of particular types of epigenetic inheritance in some model organisms, such as the inheritance of methylation marks in Arabidopsis thaliana [ 29 — 31 ], which have shown that there are tens of thousands of differentially methylated CG sites in the genome, and thousands of differentially methylated regions DMRs.
The lower bound of the epimutation rate is 4. However, for most taxa, our knowledge about the rate and causes of epimutation is still rather poor, although the existing evidence suggests that heritable variations in epialleles cannot be ignored if we want to understand phenotypic variability in populations. For this reason, epigenetic inheritance is being taken very seriously in epidemiological studies and in medicine more generally.
But what does epigenetic inheritance mean for our conception of evolution? What new evolutionary questions does it raise? Do we need to change our models? If so, how? What is the conceptual significance of such changes? Answers to some of the evolutionary questions raised by epigenetic inheritance can be readily accommodated by the MS version of evolutionary theory, whereas others may require its extension and modification.
While the evolutionary origins and the genetic evolution of epigenetic inheritance strategies are non-problematic supplements to the MS, some of the effects of heritable epigenetic variations on evolutionary change challenge the view that non-guided DNA variations are the ultimate source of hereditary variations, and require the amendment of the MS.
It is not difficult to find the precursors of the various epigenetic mechanisms in multicellular eukaryotes, in unicellular eukaryotes, and in bacteria, where their roles are varied. In addition, RNA molecules may have had a role in defence against genomic parasites. Chromatin marking probably originated within the context of chromosome evolution, through selection to ensure the stability of chromosomes and the continuity of expression patterns following cell division; it also seems to have had an ancient defence function—silencing genomic parasites.
The self-reconstruction of three-dimensional structures ensures phenotypic stability and continuity of large protein complexes and complex membranes. Similarly, self-sustaining loops ensure phenotypic stability and continuity of gene expression following cell division, so these processes would have been selected for an overview, see [ 18 , pp. The origins of epigenetic mechanisms are therefore very ancient and related to basic biological maintenance and self-preservation functions.
Considering these requires no change in conventional MS ways of thinking about evolutionary dynamics. The genetic evolution of epigenetic strategies is related to the evolutionary origins question. Epigenetic inheritance can be seen as a strategy selected because it enables transgenerational plasticity through the selection of the reaction norm, with the family, groups or lineages being the unit of selection. Several models exploring the conditions in which epigenetic inheritance is beneficial have been constructed, and it has been shown that it is advantageous in randomly and regularly fluctuating conditions, when the cycle of changes is longer than the generation time of the individual [ 32 , 33 ].
Once epigenetic inheritance is in place, then provided its fidelity is not too low, evolution operating on this axis can be cumulative. A situation that has been given less attention than the evolutionary advantages of epigenetic inheritance when environmental conditions fluctuate is the possible benefit of epigenetic priming. If gene expression depends on the presence of an inducer, but expressivity is heritably altered by past inductions, epigenetic inheritance of primed states may often be beneficial because it does not lead to inappropriate responses.
Environmental induction is still necessary, but the threshold of response is lowered. In this case, the advantages of epigenetic priming are similar to those of neural learning, especially learning through sensitization [ 18 , pp. Both within-individual and between-individual epigenetic inheritance can have profound effects on adaptive evolution and on speciation. I start with the least controversial adaptive evolutionary effects of within-organism inheritance, and move to the more theoretically challenging consequences of between-generation epigenetic inheritance.
The most obvious role of epigenetic inheritance is in the evolution of multicellular organization: cell memory is a prerequisite for the evolution of complex multicellular organisms with lineages of different cell types [ 18 , 22 ]. There are, however, less obvious effects of somatic and germ-line epigenetic inheritance which can lead to evolutionary changes and, although these processes do not challenge the MS, it is curious that with a few exceptions e.
The potentially important evolutionary effects include:. This can be advantageous when conditions are rapidly and unpredictably fluctuating during ontogeny [ 35 ]. Provided there is sensitivity to gene dosage, stochastic silencing of extra copies can drive the evolution of new genetic functions by exposing duplicated alleles to selection [ 37 , 38 ]. For example, the transition rate of methylated CpG to TpG is 10—50 times higher than other transitional changes [ 38 ], and DNA methylation leads to a lower probability of recombination and recombination-based repair [ 41 ].
The existence of developmentally induced heritable and selectable epigenetic variations challenges the MS because it suggests that evolution can occur on an epigenetic axis, and that the rate at which variations are generated is sensitive to the environmental context. For there to be an epigenetic axis to evolutionary change, epigenetic variants must be independent of cis - or trans -acting DNA sequence changes, must be transmitted over generations and must be associated with heritable phenotypic variation.
Provided the fidelity of transmission of epigenetic variants is high enough, cumulative evolution on the epigenetic axis can occur. Moreover, Cortijo et al. These QTLepi are reproducible and can be subjected to artificial selection. Biologists are beginning to measure epigenetic variations in natural and experimental populations.
The best organisms to study would be clonal organisms, parthenogenetic ones or inbred lines, all of which would minimize genetic variation, but data are at present scarce.
Epigenetic inheritance and evolution : the Lamarckian dimension
Eva Jablonka , Marion J. Does the inheritance of acquired characteristics play a significant role in evolution? In this book, Eva Jablonka and Marion J. Lamb attempt to answer that question with an original, provocative exploration of the nature and origin of hereditary variations. Starting with a historical account of Lamarck's ideas and the reasons they have fallen in disrepute, the authors go on to challenge the prevailing assumption that all heritable variation is random and the result of variation in DNA base sequences. They also detail recent breakthroughs in our understanding of the molecular mechanisms underlying inheritance--including several pathways not envisioned by classical population genetics--and argue that these advances need to be more fully incorporated into mainstream evolutionary theory.
The evolutionary implications of epigenetic inheritance
Epigenetic Inheritance and Evolution discusses the evidence for and against the heritability of acquired characters. Since it presents original and controversial arguments about the importance of epigenetic inheritance, Epigenetic Inheritance and Evolution provides a basis for discussion, modelling, and experimental investigation of the role of environmentally induced variation in evolution. Of interest to a broad range of biologists and other scientists. With a new Preface describing the impact of the hardback edition on subsequent research and a new Appendix of selected publications influenced by Epigenetic Inheritance and Evolution. Even more refreshing is the absence of sloganeering, grandstanding, and "isms". Deutsch English.