2.1  Negative SelectionCitation

Selection is a powerful force in evolution, and it works in many ways. In the end, however, selection constantly sorts through the variation that is produced by mutations to select the fit and remove the unfit, while ignoring neutral changes. A few distinct types of selection are illustrated in Figure 1.

• Stabilizing selection keeps the population at one stable optimal value
• Directional selection transforms the value of a trait by increasing the frequency of individuals closer to a distant optimum
• Disruptive selection increases the frequency of large and small values of a trait at the expense of intermediate values
• Balancing selection selects the optimal compromise among several constraints

At their core, all forms of selection involve individuals with inherited differences in fitness competing within the same population. This competition is about fitness as measured by survival rates, fecundity, or some other trait that correlates with fitness. The "winner" of the competition is positively selected, and its genotype increases in frequency; on the other hand, the "loser" is negatively selected, and the frequency of its genotype decreases. Thus, negative selection and positive selection cannot be separated. To make communication easier, however, scientists talk about positive selection when the focus of a particular study is on an increase in rare variants that improve optimal fitness, and they speak of negative selection when the focus is on the removal of harmful variants.

Because more DNA changes are harmful than are beneficial, negative selection plays an important role in maintaining the long-term stability of biological structures by removing deleterious mutations. Thus, negative selection is sometimes also called purifying selection or background selection. One key reason why this form of selection is so prevalent is the success of evolution in optimizing biological structures: As soon as a system has been improved, there is the danger of losing that improvement by a deleterious mutation. Purifying selection makes sure that deleterious mutations cannot take over a population and that any improved structures—once fixed in a population—are maintained as long as they are needed. A dramatic example of such maintenance can be found in so-called "living fossils": If a species' ecological niche happens not to change for millions of years, fossil forms of the species can be almost indistinguishable from their present-day descendants (Figure 2).

More short-term negative selection is also widespread, especially due to ecological reasons. Many structures in biology are only conditionally optimal, because they depend upon the details of other structures or circumstances to perform their function. If such other structures are within the same organism, this relationship is termed epistasis. For example, two proteins could interact epistatically in such a way that a deleterious mutation in one protein could be either compensated for or aggravated by a mutation in the other protein (Burch & Chao, 1999). Frequently, ecological circumstances also play a role in determining mutational effects. For instance, if the niche of a species stays the same, some mutations that would be beneficial in other niches will be under negative selection. If the niche changes, however, some traits that were previously under negative selection may suddenly be beneficial and have a greater fitness than the majority of the previously favored genotypes.

If environmental interactions include other rapidly evolving species, then the pressure to change may never stop, and the evolutionary optimum will always remain some steps ahead. Host-parasite interactions are a famous example of this sort of situation. Here, the host immune system evolves to recognize a special structure on the parasite and allow its removal. This in turn induces negative selection on the current form of the parasite while leading to positive selection of variants that cannot be recognized by the host. Furthermore, if such variant parasites exist, they will increase in frequency and in turn induce negative selection of the current variant of the host, which will lead to the positive selection of hosts that can again recognize the parasite, and so on. Negative (and positive) selection in such a system never rests, which is why one hypothesis describing these systems was named after the Red Queen in the book Alice in Wonderland, who famously stated that it takes a great amount of running to stay in the same place.