On the surface, the logic underlying the theory of natural selection is pretty simple. Individuals exist in an environment, each carrying different genetic variants; one (or more) of these variants are better suited to that environment; and hence this variant is more likely to be passed on to offspring, and spread through the entire population over time. In reality, the means by which adaptations appear and evolve can be wildly complex and counterintuitive. In particular there is a large element of chance that is often overlooked; many adaptive types can easily be lost by bad luck. Far from being of minor evolutionary importance, this effect of chance is fundamental with regards to not only how we think about evolution, but also related issues such as conservation and infectious disease emergence. Furthermore, clarifying the likelihood that new adaptations emerge proved imperative in understanding how powerful natural selection is at driving evolution.
The certainty of chance
Let’s illustrate this point with a hypothetical example. Imagine a dainty field of flowers in tightly packed rows, which you might see if you took a cycling tour of Holland. Now, one of these flowers developed a mutated gene, allowing it to grow taller than the others. This alteration would be beneficial for the flower; it would have premium access to sunlight, water, and pollen with are needed for reproduction. If this flower were particularly lucky, it would be able to leave offspring, each of which would be equally tall. This process repeats over time, until all flowers in the field carry this adaptation and are larger as a result.
For this adaptation to spread though, the first flower has to survive. If you trod on it as you marched your way across this field to visit a historic Dutch windmill, then the adaptation dies with the flower itself. Tough luck, evolution.
In this toy example, the adaptation causing increased height would be likely to spread as it offers a large advantage to reproduction. Yet most beneficial mutations are not so prominent. They’re usually tweaks to the existing body, such as creating refined teeth for eating, or generating muscle protein more efficiently. These types of mutations are much more vulnerable to being killed off by chance. Let’s say that such a mutation appears, which causes the individual carrying it to have a 2% higher chance of leaving offspring, and therefore to pass on this new adaptation, over its lifespan. A classic evolutionary genetics result shows that the probability that it will spread through the population at large is only 4%. (Generally, if the advantage is denoted s, the fixation probability is 2s.)
Why is that? In the example above involving tall flowers, the danger for the new mutant is its rarity. If it is only present in one individual, then the death of its sole carrier will also prevent the adaptation from spreading. When the advantage of the mutant is low, then for the most part the carrier will produce as many offspring as non-mutated individuals. Hence this mutant will be present in only a few individuals for long durations of time; its advantage will only become apparent later. It only takes one population shock during this period to eliminate the adaptive form.
A role for natural selection
Exploring the role of chance in adaptation was an important question for the first wave of evolutionary genetic theorists, most notably Ronald Fisher and John Haldane. They wanted to resolve whether natural selection could indeed cause the appearance of adaptive forms in nature, and what other forces affected it. At the turn of the twentieth century, Darwin’s idea of evolution was widely accepted, but his explanation for it – natural selection – was hotly debated. The old criticism was that chance selection events could not form the complex biology surrounding us. Some variants of this argument are still used by creationists to argue against the theory of evolution.
Fisher and Haldane’s work on this subject made it clear that while natural selection is not guaranteed, it is still a potent force in driving adaptation. While the chance of any individual adaptation arising is small, it is still much more probable than having these mutations spread without the driving force of natural selection. In the non-selected, or neutral case, the fixation probability is instead one over the population size. Given potentially hundreds of thousands of individuals, this value is much smaller than that expected with selection. Furthermore, mechanisms exists that can increase the emergence probability, such as repeated mutation reintroducing the adaptive type, or evolution proceeding via incremental changes. Indeed, one of Fisher’s favourite quotes was: “Natural selection is a mechanism for generating an exceedingly high degree of improbability”.
A role in infectious disease spread
Considering this chance effect still plays a role in modern studies of adaptation and evolution, and the same logic can be applied to other types of biological phenomena. In 2013, I wrote a paper with Sam Alizon explaining how similar thinking can be used to quantify the danger from emerging infectious diseases. In 1978 a strain of smallpox escaped from a university laboratory, leading to a tragic single fatal case. This lone patient was quickly isolated, preventing a full-scale outbreak in a similar way that removing a rare adaptation above halted its evolution. However, since infectious diseases can rapidly spread from person to person, the role of chance is massively reduced.