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Modern Genetic Analysis Chapter 17. Population and Evolutionary Genetics
Selection

So far in this chapter, we have considered changes in a population arising from forces of mutation, migration, recombination, and breeding structure. But these changes are random with respect to the way in which organisms make a living in the environments in which they live. Changes in a species in response to a changing environment occur because the different genotypes produced by mutation and recombination have different abilities to survive and reproduce. The differential rates of survival and reproduction are what is meant by selection, and the process of selection results in changes in the frequencies of the various genotypes in the population.

Fitness and the Struggle for Existence

Darwin recognized that evolution consists of two processes, both of which must be explained. One is the origin of the diversity of organisms, and the second is the origin of the adaptation of these same organisms. Evolution is not simply the origin and extinction of different organic forms; rather, it is also a process that creates some kind of match between the phenotypes of species and the environments in which they live. Darwin's explanation of that match was that there is a constant struggle for existence. Organisms with phenotypes that are better suited to the environment have a greater probability of surviving the struggle and will leave more offspring. Presumably, the better an organism can see, the better chance it has of locating food, defending itself, finding mates, and so forth, and the greater will be its chance of survival and reproduction. Darwin called the process of differential survival and reproduction of different types natural selection by analogy with the artificial selection carried out by animal and plant breeders when they deliberately select some individuals of a preferred type.

The relative probability of survival and rate of reproduction of a phenotype or genotype is now called its Darwinian fitness. Although geneticists sometimes speak loosely of the fitness of an individual, the concept of fitness really applies to the average survival and reproduction of individuals in a phenotypic or genotypic class. Because of chance events in the life histories of individuals, even two organisms with identical genotypes and identical environments will differ in their survival and reproduction rates. It is the fitness of a genotype on average over all its possessors that matters.

Fitness is a consequence of the relation between the phenotype of the organism and the environment in which the organism lives, so the same genotype will have different fitnesses in different environments. In part, this difference is because exposure to different environments during development will result in different phenotypes for the same genotypes. But, even if the phenotype is the same, the success of the organism depends on the environment. Having webbed feet is fine for paddling in water but a positive disadvantage for walking on land, as a few moments spent observing a duck walk will reveal. No genotype is unconditionally superior in fitness to all others in all environments.

Furthermore, the environment is not a fixed situation that is experienced passively by an organism. The environment of an organism is defined by the activities of the organism itself. Dry grass is part of the environment of a junco, so juncos that are most efficient at gathering it may waste less energy in nest building and thus have a higher reproductive fitness. But dry grass is part of a junco's environment because juncos gather it to make nests. The rocks among which the grass grows are not part of the junco's environment, although the rocks are physically present there. But the rocks are part of the environment of thrushes; these birds use the rocks to break open snails. Moreover, the environment that is defined by the life activities of an organism evolves as a result of those activities. The structure of the soil that is in part determinative of the kinds of plants that will grow is altered by the growth of those very plants. Environment is both the cause and the result of the evolution of organisms. As primitive plants evolved photosynthesis, they changed Earth's atmosphere from one that had had essentially no free oxygen and a high concentration of carbon dioxide to the atmosphere that we know today, which contains 21 percent oxygen and only 0.03 percent carbon dioxide. Plants that evolve today must do so in an environment created by the evolution of their own ancestors.

Darwinian or reproductive fitness is not to be confused with "physical fitness" in the everyday sense of the term, although they may be related. No matter how strong, healthy, and mentally alert the possessor of a genotype may be, that genotype has a fitness of zero if for some reason its possessors leave no offspring. Thus such statements as the "unfit are outreproducing the fit, so the species may become extinct" are meaningless. The fitness of a genotype is a consequence of all the phenotypic effects of the genes involved. Thus, an allele that doubles the fecundity of its carriers but at the same time reduces the average lifetime of its possessors by 10 percent will be more fit than its alternatives, despite its life-shortening property. The most common example is parental care. An adult bird that expends a great deal of its energy gathering food for its young will have a lower probability of survival than one that keeps all the food for itself. But a totally selfish bird will leave no offspring, because its young cannot fend for themselves. As a consequence, parental care is favored by natural selection.

Two Forms of the Struggle for Existence

Darwin saw the "struggle for existence" as having two quite different forms, with different consequences for fitness. In one form, the organism "struggles" with the environment directly. Darwin's example was the plant that is struggling for water at the edge of a desert. The fitness of a genotype in such a case does not depend on whether it is frequent or rare in the population, because fitness is not mediated through the interactions of individuals but is a direct consequence of the individual's physical relation to the external environment. Fitness is then frequency independent.

The other form of struggle is between organisms competing for a resource in short supply or otherwise interacting so that their relative abundances do determine fitness. An example is Mullerian mimicry in butterflies. Some species of brightly colored butterflies (such as monarchs and viceroys) are distasteful to birds, which learn, after a few trials, to avoid attacking butterflies with that pattern (Figure 17-7). If two species differ in their pattern, there will be selection to make them more similar because both will be protected and they share the burden of the birds' initial learning period. The less frequent pattern will be at a disadvantage with respect to the more frequent one, because birds will less often learn to avoid them. Within a species, rarer patterns will be selected against for the same reason. The rarer the pattern, the greater is the selective disadvantage, because birds will be unlikely to have had a prior experience of a lowfrequency pattern and therefore will not avoid it. This selection to blend in with the crowd is an example of frequency-dependent fitness.

For reasons of mathematical convenience, most models of natural selection are based on frequencyindependent fitness. In fact, however, a very large number of selective processes (perhaps most) are frequency dependent. The kinetics of the evolutionary process depend on the exact form of frequency dependence, and, for that reason alone, it is difficult to make any generalizations. The result of positive frequency dependence (such as competing predators, where fitness increases with increasing frequency) is quite different from that of negative frequency dependence (where fitness of a genotype declines with increasing frequency). For the sake of simplicity and as an illustration of the main qualitative features of selection, we deal only with models of frequency-independent selection in this chapter, but convenience should not be confused with reality.

Measuring Fitness Differences

For the most part, the differential fitness of different genotypes can be most easily measured when the genotypes differ at many loci. In very few cases (except for laboratory mutants, horticultural varieties, and major metabolic disorders) does the effect of an allelic substitution at a single locus make enough difference to the phenotype to be reflected in measurable fitness differences. Figure 17-8 shows the probability of survival from egg to adultthat is, the viabilityof a number of second-chromosome homozygotes of D. pseudoobscura at three different temperatures. As is generally the case, the fitness (in this case, a component of the total fitness, viability) is different in different environments. A few homozygotes are lethal or nearly so at all three temperatures, whereas a few have consistently high viability. Most genotypes, however, are not consistent in viability between temperatures, and no genotype is unconditionally the most fit at all temperatures. The fitness of these chromosomal homozygotes was not measured in competition with each other; all are measured against a common standard, so we do not know whether they are frequency dependent.

Examples of clear-cut fitness differences associated with single-gene substitutions are the many "inborn errors of metabolism," where a recessive allele interferes with a metabolic pathway and causes lethality of the homozygotes. An example in humans is phenylketonuria, where tissue degeneration is the result of the accumulation of a toxic intermediate in the pathway of tyrosine metabolism. A case that illustrates the relation of fitness to environment is sickle-cell anemia. An allelic substitution at the structural-gene locus for the b chain of hemoglobin results in substitution of valine for the normal glutamic acid at chain position 6. The abnormal hemoglobin crystallizes at low oxygen pressure, and the red cells deform and hemolyze. Homozygotes HbS / HbS have a severe anemia, and survivorship is low. Heterozygotes have a mild anemia and under ordinary circumstances exhibit the same or only slightly lower fitness than normal homozygotes HbA / HbA. However, in regions of Africa with a high incidence of falciparum malaria, heterozygotes (HbA / HbS) have a higher fitness than normal homozygotes because the presence of some sickling hemoglobin apparently protects them from the malaria. Where malaria is absent, as in North America, the fitness advantage of heterozygosity is lost.

It has not been possible to measure fitness differences for most single-locus polymorphisms. The evidence for differential net fitness for different ABO or MN blood types is shaky at best. The extensive enzyme polymorphism present in all sexually reproducing species has for the most part not been connected with measurable fitness differences, although, in Drosophila, clear-cut differences in the fitness of different genotypes have been demonstrated in the laboratory for a few loci such as those encoding a -amylase and alcohol dehydrogenase.

How Selection Works

The simplest way to see the effect of selection is to consider an allele, a, that is completely lethal before reproductive age in homozygous condition, such as the allele that leads to Tay-Sachs disease. Suppose that, in some generation, the allele frequency of this gene is 0.10. Then, in a random mating population, the proportions of the three genotypes after fertilization are

At reproductive age, however, the homozygotes a / a will have already died, leaving the genotypes at this stage as

But these proportions add up to only 0.99 because only 99% of the population is still surviving. Among the actual surviving reproducing population, the proportions must be recalculated by dividing by 0.99 so that the total proportions add up to 1.00. After this readjustment, we have

The frequency of the lethal a allele among the gametes produced by these survivors is then

and the change in allelic frequency in one generation, expressed as the new value minus the old one, has been 0.091 0.100 = 0.019. We can repeat this calculation in each successive generation to obtain the predicted frequencies of the lethal and normal alleles in a succession of future generations.

The same kind of calculation can be carried out if genotypes are not simply lethal or normal, but if each genotype has some relative probability of survival. This general calculation is shown in Genetics in Process 17-6: after one generation of selection, the new value of the frequency of A is equal to the old value (p) multiplied by the ratio of the average fitness of A alleles to the fitness of the whole population. If the fitness of A alleles is greater than the average fitness of all alleles, then

© 1999 by W. H. Freeman and Company. All rights reserved.