Frozen Evolution. Or, that’s not the way it is, Mr. Darwin. A Farewell to Selfish Gene.

The biological fitness of an individual is frequently determined, not only by his phenotype, but also by the phenotypes of the other members of the population. For example, in any form of soft selection, the chances of survival of an individual depend not on the absolute value of his traits, but on the degree to which and the direction in which his traits differ from the traits of an average member of the given population.

However, more complicated cases also frequently occur, where the fitness of an individual changes stepwise in dependence on the frequency of his allele in the remaining population, even under the conditions of hard selection.  An example is the situation in which a population of prey, exposed to the activities of a certain predator, finds itself. It is known that a predator will frequently select the commonest type of prey as a target in a particular environment (Amalraj & Das 1996; Allen 1988; Gotmark & Olsson 1997). If the prey occurs in two different colour forms, determined, e.g., by a pair of alleles, then the predator will always concentrate on the bearer of the more common allele. Thus, the frequency of this allele will decrease in the population as a consequence of “apostatic selection” (Allen, Raison, & Weale 1998)until the bearers of the alternative allele predominate in the population. Then, the predator will concentrate on the bearers of the alternative allele, so that the fitness of the individuals with the originally frequent allele (now rare) will suddenly increase.

Frequency-dependent selectionoccurs, e.g., in some types of sexual selection. In some species of organisms, the rare-male advantage phenomenon  is active. Here females mate preferentially with the bearers of rare traits, i.e. the bearers of rare alleles (Dernoncourt-Sterpin, Leichien, & Elens 1991; Depiereux et al. 1990). Because of the preference for these males, the frequency of the rare alleles increases and thus other alleles become rare, i.e. advantageous. On the other hand, in some species, females can prefer the bearers of the most frequent alleles; in this case, we once again speak of frequency-dependent selection; however the less frequent alleles then rapidly disappear from the population.

Frequency-dependent selection acting in favour of less frequent alleles is probably one of the most important mechanisms for long-term maintenance of polymorphism in the population (Antonovics & Ellstrand 1984; Elena & Lenski 1997; Benkman 1996). As this type of selection can occur not only within populations and within species, but is also a matter of interspecies competition (a predator can select the members of the commonest species), frequency-dependent selection can create the preconditions for the long-term co-existence of two various species at a single location.

Frequency-dependent selection occurs if the selection coefficient for an allele is not constant, but changes in dependence on the frequency of this allele in the population. If this type of allele is to maintain polymorphism in the population, it is necessary that the selection value of this allele increase with decreasing frequency of this allele in the population. Then, if this allele is rare in the population, the fitness of its bearers is high; if it is frequent, the fitness of its bearers is low. A typical example is the situation occurring in a species that is capable of using two different resources in the environment. Only one of the two alleles of a certain gene is advantageous for using each of the two resources. If there is a greater frequency of one of the alleles in the population, most individuals will preferentially use the given resource, this will be rapidly exhausted, the bearers of the allele will begin to starve and will reproduce more slowly and their frequency, i.e. the frequency of the relevant allele in the population, will decrease.

For example, this phenomenon has been described for predaceous cichlids (Perissodus microlepis) (Hori 1993). Fish of this species feed on the scales off the bodies of other fish. They are adapted to this means of obtaining nutrition, amongst other things, in that their jaws are asymmetrical. Without regard to the external conditions in the individual water reservoirs, they all contain the same numbers of cichlids with left-handed and right-handed asymmetry. Research has shown that right-handed asymmetric cichlids can effectively bite off the scales on the left-hand side of fish and vice-versa. If right-handed asymmetric individuals multiply excessively in the reservoir, other fish will be wary of danger coming from the left, so left-handed asymmetric cichlids will be more successful and will, as a result, multiply more rapidly.

The right-handed and left-handed curvature of the bills of crossbills (Loxiacurvirostra) is a somewhat less exotic example. Once again, the ratio of the two forms in a flock is frequently just 1:1 and here it is also assumed that frequency-dependent selection is responsible for maintaining this ratio.In this case, the curvature of the bill is related to the effectiveness of removing seeds from tree cones; one curvature can utilize only half the seeds from poorly accessible cones, while the beak with the opposite curvature can reach the other seeds (Benkman 1996). The crossbills with the less common form of beak will thus be able to obtain more food than crossbills with the more common form and will thus multiply faster.As a consequence, the ratio of the two forms reaches an equilibrium value of 1:1 in every population.

Another, in principle, similar case occurs when the size of the population of a certain organism is limited by the activities of a predator that is capable of differentiating between the individuals of the two phenotypes.It has been repeatedly demonstrated in experiments with various model organisms that some kinds of predators regularly select the more common type as their prey (Brockmann 2001). If there are two very different forms in the population of prey, e.g. two coloured forms of grove snails (Cepaea nemoralis), these kinds of predators (in this case, thrushes (Turdus), concentrate on the type that is momentarily more common (Brockmann 2001). The less frequent type is attacked less and its frequency in the population can increase. As soon as it predominates in the population, it attracts the attention of thrushes and the size of its population again decreases.

Similar phenomena of preference for individuals with a less common phenotype is frequently important in sexual selection, where the females of some species of birds, mammals and even insects mate preferentially with males of the less common phenotype (Singh & Sisodia 2000). However, this rare-male phenomenon occurs only in some species; in others, to the contrary, males with the more common phenotype are preferred (see XV.4.3).