As a student of evolutionary biology, one of the first things I learnt is that there are no strict laws in biology. Consider the Weismannian concept that there exists a segregation between germ and somatic cells, a notion often thought to be true of all multicellular organisms. As Leo Buss () pointed out, this is, in fact, only true for a fraction of all multicellular-organism taxa. Furthermore, this distinction does not make sense in the context of unicellular organisms.
Over the last three decades, Eva Jablonka and Marion Lamb have led the charge against another commonly held view in evolutionary biology—one not unrelated to germ–soma segregation—namely, that biological, or more accurately organismic, characters are transmitted from one generation to the next almost exclusively by genetic means.
Directly challenging this aspect of the received view of evolution—which crystallized in the middle of the twentieth century into what is now known as the Modern Synthesis—Jablonka and Lamb argue that inheritance can and does occur by means other than purely genetic transmission. Broadly put, these other modes of transmission are known as ‘epigenetic inheritance’. In the context of the growing acceptance and prevalence of epigenetic inheritance, Jablonka and Lamb propose an ‘extended evolutionary synthesis’. Their intention here is to dethrone the Modern Synthesis and challenge its status as the received view of evolution.
In this concise and easily readable book, Jablonka and Lamb present an up-to-date version of their argument. The book is composed of four chapters, the first of which provides a brief history of the rise of the Modern Synthesis and its core tenets. Drawing from some of their previous work (Jablonka and Lamb ), the authors distinguish ten of these tenets, the most important being the idea that DNA transmission is the sole means by which organismic inheritance occurs. They helpfully document how some ideas that did not accord with the tenets—in particular, those of Waddington—along with a body of empirical data were marginalized within mainstream evolutionary biology (that is, the Modern Synthesis).
The second chapter is dedicated to the classification of different inheritance systems along several dimensions, representing (a) the mode by which information is transmitted, and (b) the means by which heritable variation from a system is generated over both the ontogenetic and evolutionary timescales. The range of different inheritance systems examined by the authors includes the genetic system, ‘molecular’ epigenetic systems—such as chromatin marking and inheritance mediated by small RNAs—broader mechanisms such as social learning, and finally symbolic inheritance, which mostly occurs in humans. For each system, the authors consider, amongst other things, whether inheritance has an unlimited range of variation, the fidelity of transmission, whether the variation produced is blind or targeted, and whether the inheritance system enables open-ended evolution.
The third chapter details the evolutionary implications of the existence of these epigenetic inheritance systems, beginning with a review of four arguments for the case that epigenetic inheritance is negligible from an evolutionary perspective. I have reformulated them as follows: (i) the Modern Synthesis can readily encompass other sources of heritable variation; (ii) most epigenetic transmission occurs between somatic cells with almost no intergenerational epigenetic effects; (iii) intergenerational epigenetic inheritance is marked by low fidelity; and (iv) evidence for the evolutionary significance of epigenetic inheritance is scant.
Jablonka and Lamb respond as follows: To (i), they counter that the existence of epigenetic inheritance of developmentally acquired variation (that sometimes involves the cognition of the organisms transmitting the information) cannot be easily accommodated by population genetics models that form the heart of the Modern Synthesis. In response to (ii), they argue that the segregation between germ and soma, which, as noted earlier, only exists in a minority of taxa, is not required. In reply to (iii), the authors argue that there is a wide range of variability in epigenetic transmission and that in many cases variation can be stably transmitted across multiple generations. A substantial component of this chapter is dedicated towards challenging (iv). Here, Jablonka and Lamb review the mounting body of evidence that epigenetic inheritance occurs in nature. The rest of the chapter explores the evolutionary effects of social learning and cultural (symbol-based) learning, in addition to the potential integration of all of these modes under a single framework, namely, the Price equation (Price ; for an introduction, see Okasha , Chapter 1).
The fourth and final chapter of the book is devoted to the philosophical implications of the existence and significance of epigenetic inheritance systems. First, the authors argue that Darwinian evolution, encapsulated by the motto ‘heritable variation and fitness difference’, is permissive with regard to the mechanisms of inheritance, whether the production of new variation is blind or partly directed, and the level of organization at which Darwinian evolution can occur. This, they argue, vindicates their perspective. Second, they propose that the existence of epigenetic inheritance systems challenges the distinction between ‘proximal’ mechanisms that produce variation during development, and ‘ultimate’ mechanisms that filter (by natural selection or drift) this variation between generations. Because, the authors note, the acquisition mechanisms of epigenetic variation are not necessarily blind or random—as they are supposed to be, following the Modern Synthesis—to fully understand evolution, one must also investigate development, that is, the period during which new epigenetic variation is acquired. Third, they ponder the implications of various inheritance systems for the notion of homology. Following Powell and Shea (), they argue that a trait can be regarded as homologous in distinct taxa even if the inheritance mechanisms involved differ between those taxa. Fourth, they contend that the concepts of an evolutionary individual and of transitions in individuality cannot be thoroughly understood without proper consideration of inheritance systems. Finally, they link inheritance to Shannon information theory (see Shannon ) and offer an interesting suggestion: that an extension of the Price equation using information theory would be a worthwhile step towards enabling a comparison of different inheritance systems at varying scales.
The authors conclude the book by asking whether the extended evolutionary synthesis represents a different ‘thought style’ from that of the Modern Synthesis, an idea they derive from sociologist of science Ludwig Fleck. Their answer, although not conclusive, is that it probably does.
Jablonka and Lamb have, in this concise and engaging book, communicated their ideas clearly and largely convincingly. It is an excellent resource for anyone seeking an accessible introduction to the debate surrounding epigenetic inheritance in evolutionary biology and philosophy of biology. Something to keep in mind is that Jablonka and Lamb lean heavily towards one side of the debate over the significance of epigenetic inheritance. The book is a valuable addition to the debate largely because their case is presented honestly and compellingly.
I will now provide some thoughts as to why one might resist the move towards the extended evolutionary synthesis proposed by Jablonka and Lamb (and others), despite objecting neither to their evidence nor arguments. I, for instance, readily accept most of what Lamb and Jablonka present, but I do not find their call for an extended evolutionary synthesis compelling.
There are several reasons to consider here. The first is simple and may be obvious: A generational difference between scholars has emerged over the last thirty years in terms of how narrowly the Modern Synthesis is defined. Jablonka and Lamb were pioneers of a movement that required forceful distancing from the Modern Synthesis and its powerful defenders. When they first presented their work to other biologists, they would have been expecting challenges from leading figures on the opposing side. However, I am not sure that the tenets of the Modern Synthesis as described by Jablonka and Lamb are enforced to the extent or the degree they argue they are nowadays, at least not when it comes to the younger generation of scholars. Certainly, I have not experienced the kind of resistance that the authors did (and apparently still do). This change is no different than the current meaning of ‘Darwinian’ differing from its meaning during Darwin’s lifetime, or the period shortly after his death. In short, the cultural offspring of the Modern Synthesis have a less than perfect resemblance to their parent in terms of what they understand themselves to oppose.
This last remark is one version of criticism (i), which leads me to a second point. I find the claim that population genetics cannot accommodate epigenetic inheritance the least convincing argument put forward by the authors. Surely, biased mutations can easily be incorporated into population genetic models, as can a lag of one or two generations between the occurrence of a mutation and its phenotypic effects. Furthermore, Jablonka and Lamb are favourably disposed towards the Price equation, which is one of the main contemporary tools used in conventional evolutionary biology (for a review, see Luque ). The Price equation can be straightforwardly linked to quantitative genetics (see Walsh and Lynch , Chapter 6), which has been just as foundational as population genetics when it comes to the Modern Synthesis. This suggests that many contemporary evolutionary biologists (or at least those acquainted with quantitative genetics or the Price equation) are potentially open to the idea of extending evolution beyond genetic transmission.
A third concern is that while Jablonka and Lamb provide in Chapter 2 an abstract definition of an inheritance system, they do not provide any criteria or conditions to limit what can count as an inheritance system or mechanism, nor the sort of entities to which they apply. The worry here is one of overbreadth. For instance, it would seem that the traditional organism is their main focus, but they discuss, perhaps too uncritically, the notion of inheritance in the case of the holobiont—a host and its microbes. However, while one can decide to see a holobiont as a unit with different inheritance systems, one can also decide not to (Moran and Sloan ; Bourrat and Griffiths ). Why not go beyond and count a whole ecosystem as having distinct inheritance systems? It would have been useful to state boundary conditions for what can count as an inheritance system and to which sort of entities this concept can be applied. In their push for us to take into consideration robust evidence for epigenetic inheritance, Jablonka and Lamb ask us to embrace an all-encompassing version of evolution that I think goes too far.
There is another point I felt was missing in their discussion. Jablonka and Lamb use the concept of the ‘gene’ in its molecular sense. While this notion is commonly and widely used, it is not representative of how it tends to be employed by evolutionary biologists (Griffiths and Stotz ; Lu and Bourrat ), and in particular by those versed in the theoretical side of evolution (for example, quantitative geneticists). A discussion of what different actors mean by ‘genes’ and why Jablonka and Lamb consider the molecular notion to be the most relevant would have been welcome here. It would have strengthened their case for the importance, and wide-ranging implications, of thinking about inheritance systems beyond the DNA-based (genetic) inheritance system.
But while I would have liked to see discussed a few more, mostly theoretical, questions, I don’t think it’s contentious to say that the target audience for this book are readers who are unaware of, or at least not fully informed about, the empirical facts surrounding epigenetic inheritance, rather than those versed in theoretical considerations about evolution. There is no denying the authors hit their mark.
I thank Eva Jablonka, Marion Lamb, Paul Griffiths, Carl Brusse, Marianne McAllister, editors for the BJPS, and the Theory and Method in Biosciences at the University of Sydney for comments and suggestions on previous versions of the manuscript.
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