The Selfish Gene Is Actually A Crippling, Zero-Sum Theory Of Evolution

aeon  |  In late summer of 1976, two colleagues at Oxford University Press, Michael Rodgers and Richard Charkin, were discussing a book on evolution soon to be published. It was by a first-time author, a junior zoology don in town, and had been given an initial print run of 5,000 copies. As the two publishers debated the book’s fate, Charkin confided that he doubted it would sell more than 2,000 copies. In response, Rodgers, who was the editor who had acquired the manuscript, suggested a bet whereby he would pay Charkin £1 for every 1,000 copies under 5,000, and Charkin was to buy Rodgers a pint of beer for every 1,000 copies over 5,000. By now, the book is one of OUP’s most successful titles, and it has sold more than a million copies in dozens of languages, spread across four editions. That book was Richard Dawkins’s The Selfish Gene, and Charkin is ‘holding back payment in the interests of [Rodgers’s] health and wellbeing’.

In the decades following that bet, The Selfish Gene has come to play a unique role in evolutionary biology, simultaneously influential and contentious. At the heart of the disagreements lay the book’s advocacy of what has become known as the gene’s-eye view of evolution. To its supporters, the gene’s-eye view presents an unrivalled introduction to the logic of natural selection. To its critics, ‘selfish genes’ is a dated metaphor that paints a simplistic picture of evolution while failing to incorporate recent empirical findings. To me, it is one of biology’s most powerful thinking tools. However, as with all tools, in order to make the most of it, you must understand what it was designed to do.

When Charles Darwin first introduced his theory of evolution by natural selection in 1859, he had in mind a theory about individual organisms. In Darwin’s telling, individuals differ in how long they live and how good they are at attracting mates; if the traits that enhance these strengths are heritable, they will become more abundant over time. The gene’s-eye view discussed by Dawkins introduces a shift in perspective that might seem subtle at first, but which comes with rather radical implications.

The idea emerged from the tenets of population genetics in the 1920s and ’30s. Here, scientists said that you could mathematically describe evolution through changes in the frequency of certain genetic variants, known as alleles, over time. Population genetics was an integral part of the modern synthesis of evolution and married Darwin’s idea of gradual evolutionary change with a functioning theory of inheritance, based on Gregor Mendel’s discovery that genes were transmitted as discrete entities. Under the framework of population genetics, evolution is captured by mathematically describing the increase and decrease of alleles in a population over time.

The gene’s-eye view took this a step further, to argue that biologists are always better off thinking about evolution and natural selection in terms of genes rather than organisms. This is because organisms lack the evolutionary longevity required to be the central unit in evolutionary explanations. They are too temporary on an evolutionary timescale, a unique combination of genes and environment – here in this generation but gone in the next. Genes, in contrast, pass on their structure intact from one generation to the next, ignoring mutation and recombination. Therefore, only they possess the required evolutionary longevity. Traits that you can see, the argument goes, such as the particular fur of a polar bear or the flower of an orchid (known as a phenotype), are not for the good of the organism, but of the genes. The genes, and not the organism, are the ultimate beneficiaries of natural selection.

This approach has also been called selfish-gene thinking, because natural selection is conceptualised as a struggle between genes, typically through how they affect the fitness of the organism in which they reside, for transmission to the next generation. At an after-dinner speech at a conference banquet, Dawkins once summarised the key argument in limerick form:

An itinerant selfish gene
Said: ‘Bodies a-plenty I’ve seen.
You think you’re so clever,
But I’ll live for ever.
You’re just a survival machine.’

In this telling, evolution is the process by which immortal selfish genes housed in transient organisms struggle for representation in future generations. Moving beyond the poetry and making the point more formally, Dawkins argued that evolution involves two entities: replicators and vehicles, playing complementary roles. Replicators are those entities that copies are made of and that are transmitted faithfully from one generation to the next; in practice, this usually means genes. The second entity, vehicles, are where replicators are bundled together: this is the entity that actually comes into contact with the external environment and interacts with it. The most common kind of vehicle is the organism, such as an animal or a plant, though it can also be a cell, as in the case of cancer.