Selfish Genery: J. Arvid Ågren’s “The Gene’s-Eye View of Evolution”

An Oxford undergraduate once wrote a brilliant answer to an exam question about the logic of natural selection, ending with the statement: “And here I rely heavily on the words of Richard Dawkins.” When the exam marker, one Marian Stamp Dawkins, noticed this, she wrote in the margin of the paper: “Yes. Don’t we all?”

J. Arvid Ågren relates this anecdote (originally told by Stamp Dawkins herself) in his recent book, The Gene’s-Eye View of Evolution—and he notes how apt it is: Richard Dawkins has had an enormous influence on evolutionary biology since the 1976 publication of his first book, The Selfish Gene (critics and supporters both agree with this—they just differ over whether it is a good thing). The Selfish Gene explains and argues for the gene’s-eye view: the idea that natural selection can best be understood as taking place at the level of the gene, rather than at the level of the individual organism, group or species.

And yet, there has been no recent comprehensive overview until now of the gene’s-eye view that Dawkins did so much to extend and popularise. Thank goodness for Ågren, then: as he notes, evolution is our modern creation story and the gene’s-eye view “strikes right at the heart of the question of what evolution is, and how we go about studying it.”

Ågren’s overview is objective, broad, comprehensive and (mostly) accessible to lay audiences as well as useful to scientists. In less than 200 pages, he describes the intellectual history of the gene’s eye view, the arguments it has engendered, the questions it has raised, its strengths and weaknesses and how it stands today. He also looks briefly at how the idea has been received in various parts of the world, so it is fitting that Ågren dedicates his book not only to his father, a biologist, but also to his mother, a cultural historian.

Ågren discusses not only Dawkins’ ideas, but the ideas of the many other researchers on whose work Dawkins explicitly drew in writing The Selfish Gene, including Charles Darwin, R. A. Fisher, W. D. Hamilton, Robert Trivers, George C. Williams and John Maynard Smith. R. A. Fisher was one of the architects of the modern synthesis (the reconciliation of Darwinian natural selection with Mendelian genetics that is the foundation of mainstream evolutionary biology today). Ågren suggests, following A. W. F. Edwards, that Fisher’s 1918 paper, “The Correlation between Relatives on the Supposition of Mendelian Inheritance,” was the first articulation of the gene’s-eye-view as we now understand it. And he gives pride of place to the work of George C. Williams, whose 1966 Adaptation and Natural Selection was perhaps the most important influence on Dawkins’ thinking after Darwin himself—Williams might be called the grandfather of the gene’s-eye view.

It might seem surprising that, as Dawkins has noted, another of the figures who most influenced him (and the gene’s-eye view more broadly) was William Paley, whose 1803 Natural Theology or Evidences of the Existence and Attributes of the Deity, Collected from the Appearances of Nature is still the most famous elucidation of the argument from design. Like Paley, Darwin saw the complexity of nature as a special question in need of a special answer. Darwin, of course, provided the true, mechanistic answer to this question, but, as Ågren notes, Paley’s legacy, as is apparent from the work of Dawkins and in British evolutionary biology in general, is adaptationism. Whereas Americans and continental Europeans are more concerned with “the origin and constraint on diversity,” Brits have seen adaptation—the illusion of design—as the main problem to be solved by evolutionary theory (these are broad generalisations, of course, as Ågren himself notes—Williams was an American.)

So, while the most vociferous critic of the gene’s-eye view, Stephen Jay Gould, cared more about fossils and organisms, the gene-centrists were more interested in the logic of evolution and natural selection. This suggests another cause of arguments over the gene’s-eye view: whereas Williams and Dawkins saw the gene in a philosophical and logical light, others, particularly molecular biologists, were more interested in the material details of DNA (note that Fisher’s gene-centrism predated the great discoveries of Crick and Watson). Gene-centrists saw the gene as a replicator of information and were less concerned about the molecular details; this difference of perspective accounts for much of the controversy around the gene’s-eye view.

Ågren argues that this pushback helped inspire the development of the now-flourishing but previously barely-existent field of the philosophy of biology. In support of this proposition, Ågren quotes from an afterword that Daniel Dennett—one of the most prominent scholars in that field—wrote for the 1999 edition of Dawkins’ second book:

Is The Extended Phenotype science or philosophy? It is both; it is science, certainly, but it is also what philosophy should be, and only intermittently is: a scrupulously reasoned argument that opens our eyes to a new perspective, clarifying what had been murky and ill-understood, and giving us a new way of thinking about topics we thought we already understood … [Dawkins] shows how our traditional way of thinking about organisms should be replaced by a richer version in which the boundary between organism and environment first dissolves and then gets partially rebuilt on a deeper foundation. [Emphasis in Dennett’s original.]

Dennett goes on to say, “For the professional philosopher … there is a feast: [this book contains] some of the most masterful, sustained chains of rigorous argument I have ever encountered … There are even some sidelong but substantial contributions to philosophical controversies undreamt of by Dawkins.” Dennett’s assessment should give pause to those, like John Gray, who have claimed that Dawkins lacks philosophical sophistication—as Dawkins points out in the second volume of his memoirs.

Like the gene-centrists, Ågren is interested in the logical, philosophical and theoretical implications of the gene’s eye view. He laments that he is “a poor naturalist,” which calls to mind Dawkins’ similar acknowledgment: “My interest in biology has been largely driven by questions about origins and the nature of life, rather than—as is the case for most young biologists I have taught—by a love of natural history.”

But while Ågren rebuts the most common critiques of the gene’s eye view, such as the accusation that Dawkins anthropomorphizes genes, he also argues that it has some shortcomings. For example, Ågren points out Dawkins’ occasional failure to emphasise that the gene’s-eye view is only one of several lenses through which evolutionary biology can legitimately be examined. One of the book’s great strengths is that Ågren acknowledges the merit in some of those other ways of looking at evolution, such as the Extended Evolutionary Synthesis—he is a sympathiser with the gene’s-eye view, but not a blind partisan. This enables him to provide a probing and objective overview of this most contentious and influential piece of evolutionary theory.

My favourite part of the book was the chapter examining some of the empirical consequences of the gene’s-eye view, including increased attention to extended phenotypes and the emergence of Ågren’s own research speciality, which he describes as the study of selfish genetic elements. These are “stretches of DNA that can promote their own transmission at the expense of other genes in the genome while having either no effect or a negative effect on organismal fitness.” The Selfish Gene mentions such genes only briefly, but it “brought them to the forefront of evolutionary biology [and] reciprocally, selfish genetic elements have often been considered the best evidence for the power of the gene’s-eye view.” Ågren’s book points out, for example, that the study of selfish genetic elements helped lead to the development of CRISPR-Cas9 technology.

As an admirer of the works of Salman Rushdie, that bard of cosmopolitism and fragmentation, I can’t help but see a similarity between his literary orientation and the gene’s-eye view. Discussing the evolutionary “coming-together of entities that were previously surviving and reproducing on their own [e.g. unicellular life into multicellular life],” Ågren refers to “the suppression of conflict at the lower levels,” a process that “is never complete, and the unity of the individual is therefore constantly threatened from within.” He quotes the great Darwinian W. D. Hamilton:

Seemingly inescapable conflict within diploid organisms came to me as both a new agonizing challenge and at the same time as a release from a personal problem I had had all my life … Given my realization of an eternal disquiet within, couldn’t I feel better about my own inability to be consistent in what I was doing, about indecision in matters ranging from daily trivialities up to the very nature of right and wrong? … As I write these words, even as to be able to write them, I am pretending to a unity that, deep inside myself, I now know does not exist. I am fundamentally mixed, male with female, parent with offspring, warring segments of chromosomes.

Evolutionary biology raises the fundamental question: what are we? Are we hybrid conglomerations of once-independent lifeforms, forced into cooperation and semi-cohesiveness by the imperatives of evolution, our constituent parts fated to remain forever in tension—mitochondrial DNA against nuclear DNA, for example? And is human consciousness, including our sense of self and capacity for abstract thought—the source of all our anxieties, ambivalences, conflicts and contradictions—merely a pale and ephemeral reflection of these ongoing evolutionary struggles? As Ågren notes, it is because evolutionary biology raises such questions that it can feel far more personal than any other branch of the so-called hard sciences. And Ågren’s adeptness at communicating its often-difficult concepts almost makes up for the nigh-incomprehensible mathematical equations he foists upon poor, innumerate readers like me.

Ågren’s book may be less accessible to readers who are unfamiliar with evolutionary theory and with the gene’s-eye-view in particular. But, for those with at least some prior knowledge, his ability to communicate difficult concepts to the layman is a real achievement.

Towards the end of the book, Ågren falters slightly: he brings up the political controversies in which Dawkins has been involved on Twitter, which are irrelevant to his writings on the gene’s-eye view. But that is a hiccup in an otherwise excellent book. And one of Ågren’s parting reflections, on the role of metaphor in science, is especially pertinent given Dawkins’ reputation as a prose stylist and logician. Ågren notes that metaphorical thinking in science can sometimes lead one astray, but that it is also sometimes enormously fruitful: “Verbal conceptual models often lead the way to new areas that can then be captured in a more formal way.”

In his concluding section, Ågren speculates about the role of rhetoric in science, and specifically about why Williams and Dawkins were so successful in propagating their perspective on evolution. Why was the “gene meme” (to adopt David Haig’s phrase) so successful? Perhaps it was partly because—while Stephen Jay Gould, for example, presented his ideas about spandrels and punctuated equilibrium as if they completely revolutionised evolutionary theory—Williams and Dawkins presented the gene’s-eye view as a refinement of what was already known, even though it was actually quite a radical departure from much of what had come before. Ågren recommends further sociological study of how the gene’s-eye view has been received by scientists from various cultures around the world and notes that he has studied this topic in depth but that he did not have room to address it in his book. I hope he returns to it in future.

In sum, Ågren has provided both an overview of an important scientific idea and a deeply philosophical examination of evolution and of the nature of life. He shows that both scientists and interested laypeople do indeed rely heavily on the words of Richard Dawkins—and those of Charles Darwin, George C. Williams, W. D. Hamilton, and the many other thinkers whose work he discusses. We may now add to that list of thinkers the name of J. Arvid Ågren. I hope that his fascinating book is read widely; it is unmissable for anyone interested in evolution—and in life itself.