In some interactions between parasites and hosts, coevolution can take a specific form called gene-for-gene coevolution or matching-gene coevolution. It is a form of reciprocal evolutionary change based on the idea that, if one member of a coevolving relationship has a gene that affects the relationship, the other member has a gene to counter this effect. These genes evolve reciprocally and provide the genetic basis for certain types of coevolution. This relationship has been demonstrated between plants and a number of their parasites, including rust fungi, nematodes, bacteria, viruses, and one insect species. Its principles also form the basis of many plant breeding programs designed to increase resistance against pathogens.

The process of gene-for-gene coevolution begins when a parasite population encounters a new plant host. Most host individuals will not be able to detect the presence of the parasite. Certain host individuals, however, may have a mutated gene, dubbed the resistance gene in this scenario, that allows them to detect a substance the parasite emits, encoded by a so-called avirulence gene. After being alerted to the threat of the parasite, the host responds to prevent the parasite from invading. The resistance gene will confer an advantage to plants that carry it, allowing individuals to survive and pass on their genotype to future generations. Individuals that do not possess this gene will not be able to resist invasion by the parasite and will die, unable to pass on their genotype. Thus, the new resistance gene will spread through the plant population. At this point the parasite might seem to be outwitted, but actually it may be able to circumvent this genetic evasion by the host with a genetic trick of its own. If a mutation arises in the gene that codes for the product that the host recognizes, the gene product will be altered and the host will no longer be able to resist the parasite. The spread of this mutant gene in the parasite population will be favoured by natural selection. A genetic Ping-Pong match between the two species can then ensue, as the host develops another mutation in any gene that allows it to detect the parasite, and the parasite responds to this defensive maneuver with a genetic alteration to avoid detection. The host and parasite populations therefore coevolve by the accumulation of these matching genes.

In agriculture, gene-for-gene relationships are maintained by introducing new resistance genes into all plants that cover a large area. In natural populations, each new resistance gene appears as a mutant in a single individual and then spreads by natural selection throughout the population in subsequent generations. Demonstrating a gene-for-gene relationship in natural populations is a difficult and time-consuming process because it demands detailed genetic and ecological studies of the plants and their pathogens that take many years.

The best-studied example is that of wild flax (Linum marginale) and flax rust (Melampsora lini) in Australia. Local populations of flax plants and flax rust harbour multiple matching genes for resistance and avirulence. The number of genes and their frequency within local populations fluctuate greatly over time as coevolution continues. In small populations, the resistance genes can be lost by chance alone through the process of genetic drift (see biosphere: The diversity of life). New genes in the host and parasite populations can appear through either mutation or the influx of genes from other populations. Consequently, the long-term dynamics of the gene-for-gene coevolution between flax and flax rust depend on the rate at which new genes appear within local populations of the parasite and host, the intensity with which natural selection acts on these genes (which, in turn, depends on the virulence of the particular parasite genotype), the population sizes of both host and parasite, and the rate that genes are transferred among populations.

Not all interactions between plants and parasites coevolve in a gene-for-gene manner. Resistance in a plant host is often determined by many genes rather than by a single gene. Examples of gene-for-gene coevolution, however, are slowly accumulating, and these are providing a powerful tool in breeding crop plants that are resistant to pathogens and parasites. As other forms of coevolution are studied in natural populations, the results will help determine still other ways of selecting for more durable resistance in crop plants. Such studies, however, require that intact biological communities are preserved as precious natural laboratories for understanding the coevolutionary process.

The geographic mosaic theory of coevolution

The study of evolving interactions in natural biological communities has indicated that the long-term dynamics of coevolution may occur over large geographic ranges rather than within local populations. This view is called the geographic mosaic theory of coevolution. It is based on the observation that a species may adapt and become specialized to another species differently in separate regions. A species that is involved in an interspecific interaction in one geographic area may not even be present in another geographic area. This geographic mosaic in evolving interactions provides the raw material for the overall direction of coevolution, which proceeds as genes that are favoured in local interactions spread out into other populations.

Some local populations may contribute little to the overall direction of coevolution between two or more species, whereas other populations may be crucial to the process. A highly virulent form of a parasite that recently has been introduced into a local population may cause the extinction of its host population, thereby causing its own extinction. In another population the evolution of a powerful host resistance gene may cause the local extinction of the parasite population. In still other populations the two species may continue to coexist but coevolve in different ways. Over a long period some adaptations in these populations will spread to other populations and influence the overall direction of coevolution between the parasite and host species. Similar geographic differences in interactions are known to occur between predators and prey and between competitors and mutualists.

For some forms of coevolution to occur at a geographic level, many populations of the interacting species must be maintained on a local scale (metapopulations) as well as across broader geographic ranges. Should a species be reduced to a few populations, the geographic mosaic of diverse adaptations that fuels the coevolutionary process is diminished.

Coevolution of one species with several species

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In the process called coevolutionary alternation, one species coevolves with several other species by shifting among the species with which it interacts over many generations. European cuckoos (Cuculus canorus) provide an example of this type of coevolution. The cuckoos behave as brood parasites, laying their eggs in the nests of other avian species and depending on these hosts to raise their young. The four major host species for cuckoos in Britain are meadow pipits (Anthus pratensis), reed warblers (Acrocephalus scirpaceus), pied wagtails (Motacilla alba yarrellii), and dunnocks (Prunella modularis).

Cuckoo populations have evolved many adaptations that enable them to trick their hosts into rearing their young, the most impressive of which is the production of eggs that resemble those of their host. Cuckoos can produce eggs that are very similar in colour to the eggs of meadow pipits, reed warblers, or pied wagtails. Three different cuckoo genotypes are responsible for the production of these three different egg colours, and thus cuckoos are said to be polymorphic with respect to egg colour. These genotypes are maintained in cuckoo populations because natural selection is continually changing which genotype is favoured. This occurs because after many generations the host species can develop defenses against the cuckoo, such as the ability to discriminate between eggs and eject those that have only minute differences from their own. (That this ability to reject eggs is evolved is evidenced by the fact that in Iceland, where cuckoos are not indigenous, pied wagtails and meadow pipits will accept cuckoo eggs placed in their nests by researchers.) As the gene for this defensive maneuver spreads throughout the host population, cuckoos with genotypes that allow them to produce eggs mimicking the egg colour of a new host are favoured.

By alternating among hosts, cuckoos are coevolving with a number of bird species in Britain. Some of their current hosts, including dunnocks, have few defenses against cuckoos and do not reject cuckoo eggs, which may indicate that these hosts have been targeted by cuckoos relatively recently. Some other potential hosts that cuckoos do not currently colonize will strongly reject any eggs that are not exactly like their own, suggesting that these bird species may have been hosts in the recent past but were abandoned by cuckoos after defenses against them evolved. Over many generations, these former hosts will probably lose their defenses because the evolutionary pressure to retain them has been relaxed—they are no longer being attacked by cuckoos. In Britain the loss of these kinds of defenses makes the birds once again targets for attack by cuckoos, thereby continuing the process of coevolutionary alternation among hosts.