Evolutionary Processes
Michael C. Whitlock
As the great population geneticist (and statistician) Sir Ronald Fisher said in the first sentence of his foundational Genetical Theory of Evolution, “Natural selection is not evolution.” A population evolves when the frequencies of its genotypes change over time. The most important of these changes are typically caused by natural selection, but selection is not the only mechanism by which evolution occurs. When alleles are passed from one generation to the next, the next generation may by chance not exactly match the generation of its parents, especially if the population size is small. Alleles can mutate to new alleles, and alleles can arrive by migration from genetically diverged populations. DNA sequences may recombine with genetically distinct sequences. The details of mating can matter, because genotype frequencies can change as a result of mating between relatives, mating between similar individuals, or mating with nearby individuals. All these factors—random genetic drift, mutation, migration, recombination, and nonrandom mating—can change the genotype frequencies in a population from one generation to the next; in other words, they can cause evolution.
This section discusses these nonselective evolutionary processes and some of their important consequences. We start with a discussion of random genetic drift (see chapter IV.1). In a finite population, chance in part dictates which individuals happen to succeed and leave offspring; therefore, chance can cause the allele frequency to change from one generation to the next. This random process, called genetic drift, changes the allele frequency from one generation to the next. Such drift has greatest effect for alleles that have very small effects on fitness. However, most of the genetic variation in a typical genome may be close to selectively neutral, making drift an important part of the evolutionary process for a large fraction of the genome.
New alleles appear in populations as a consequence of mutation (see chapter IV.2). Ultimately, without mutation the evolutionary process would cease, because all genetic variation has its origin in a mutation and all evolution depends on genetic variation. Mutation brings in new variants that may be selectively beneficial, but it also introduces alleles that are deleterious for their carriers. Some mutations may even have little selective effect at all. The net effect on evolution of mutation rests in the balance of these classes of mutants and in the ways mutation interacts with other evolutionary processes.
Dispersal and migration are also sources of new alleles to a population; moreover, gene flow from other places tends to make a population more similar to other populations in the species (see chapter IV.3). Gene flow is the glue holding species together; without dispersal, populations would grow more and more different from each other until they were unrecognizable as the same species. Movement between populations can bring in valuable new alleles that have proven successful elsewhere; on the other hand, an influx of alleles from elsewhere can interfere with adaptation to local conditions.
Migration, mutation, and drift change allele frequencies and genotype frequencies. Other evolutionary processes change the frequencies of combinations of alleles without directly affecting the frequencies of those alleles; for example, recombination mixes alleles into new chromosome combinations, changing the patterns of association of alleles at different loci (see chapter IV.4). If new beneficial alleles appear on different genetic backgrounds, only recombination can bring them together so that all individuals might benefit from both. Most of the other evolutionary processes—including selection, mutation, migration, and drift—can generate associations between alleles at different loci, and recombination whittles those associations away. The benefits of recombination are largely responsible for the evolution of sex, a characteristic feature of many organisms.
Deleterious alleles repeatedly appear in every population by mutation. They are ultimately removed mainly by selection, but this is not instantaneous. As a result, populations usually have extremely large numbers of deleterious alleles, mostly at low frequency, and for some species each individual may carry hundreds or even thousands of alleles that reduce fitness (see chapter IV.5). This causes a reduction in the mean fitness of the population called mutation load. Other factors can reduce fitness of a population as well; for example, genetic drift can cause mildly deleterious alleles to reach high frequencies and recombination can break up favorable combinations of alleles that work well together.
Inbreeding and other forms of nonrandom mating affect the combinations of alleles at the same locus in diploid individuals; more inbred individuals are more likely to have two copies of the same allele at a locus than expected in a randomly mated population (see chapter IV.6). As a result, inbred individuals are more likely to be homozygous with increased expression of the effects of recessive alleles. Many of these recessive alleles are deleterious, meaning that inbred individuals can have reduced fitness relative to what is possible for outbred individuals (inbreeding depression).
Inbreeding is not a fixed property of a species, however, and the tendency of an organism to inbreed can respond to selection and evolve over time. Many plants (and some animals) are capable of an extreme form of inbreeding called selfing, in which a hermaphrodite individual fertilizes its own ovules with its own sperm or pollen. All else being equal, this gives the selfing individual a genetic advantage, because it can transfer two copies of its genes into each offspring. Many factors promote an increase in the rate of selfing; many, including inbreeding depression select against self-mating. Mating system evolution is a fascinating, active area of investigation (see chapter IV.8).
The mechanisms of evolution discussed in this section usually take as a starting place the rules of genetic inheritance as described by Mendel; however, in many cases, evolution can occur because of biases in transmission of genetic elements. “Selfish genetic elements” can transfer from one generation to the next in excess of the proportions expected under Mendelian inheritance (see chapter IV.7). Differences between one allele and another can cause one allele to be passed into offspring differentially; in other words, there can be selection within an individual for which genetic material is transmitted to offspring. This can take the form of genetic parasites like transposable elements or reproductive parasites like Wolbachia infections that can sometimes change sex ratios of their hosts’ offspring to their own advantage. Moreover, some alleles can differentially be passed to offspring at the expense of the other copy of a gene in the parent. These processes can have dramatic effects, ranging from skewed sex ratios to potential speciation. Evolution can occur even in the seemingly simple process of transmission of genetic material to offspring.
Both selective and nonselective processes can generate evolution. The demographic and genetic processes discussed in this section can have strong influences on each other, and on the mechanisms by which selection operates. The amount of genetic variation in a species is the raw material of evolution, and this variation is determined by a balance between different kinds of selection, genetic drift, mutation, migration, recombination, and patterns of mating. Each of these processes interacts in myriad ways, giving rise to many important features of biological evolution. None of these factors alone—even selection—is sufficient to understand evolution.
In the evolutionary theater, natural selection without doubt is the star of the show, but important roles are played by mutation, migration, recombination, drift, and details of the transmission of genetic material. These other players change the pace and direction of evolution, and without them the outcome of natural selection would be completely different.