Host–parasite coevolution

An allele is subject to negative frequency-dependent selection if a rare allelic variant has a selective advantage. For example, the parasite should adapt to the most common host genotype, because it can then infect a large number of hosts. In turn, a rare host genotype may then be favored by selection, its frequency will increase and eventually it becomes common. Subsequently, the parasite should adapt to the former infrequent genotype.[3][4]

Coevolution determined by negative frequency-dependent selection is rapid, potentially occurring across few generations.[3] It maintains high genetic diversity by favoring uncommon alleles. This selection mode is expected for multicellular hosts, because adaptations can occur without the need for novel advantageous mutations, which are less likely to be frequent in these hosts because of relatively small population sizes and relatively long generation times.[3]

Overdominance occurs if the heterozygote phenotype has a fitness advantage over both homozygotes (heterozygote advantage, causing heterosis).[5][6] One example is sickle cell anemia. It is due to a mutation in the hemoglobin gene leading to sickle shape formation of red blood cells, causing clotting in blood vessels, restricted blood flow, and reduced oxygen transport. At the same time, the mutation confers resistance to malaria, caused by Plasmodium parasites, which are passed off in red blood cells after transmission to humans by mosquitoes. Hence, homozygote and heterozygote genotypes for the sickle-cell disease allele show malaria resistance, while the homozygote suffers from severe disease phenotype. The alternative homozygote, which does not carry the sickle cell disease allele, is susceptible to infection by Plasmodium. As a consequence, the heterozygote genotype is selectively favored in areas with a high incidence of malaria.[7][8]

If an allele provides a fitness benefit, its frequency increases within a population – selection is directional or positive. A selective sweep is a form of directional selection where the increase in frequency eventually leads to the fixation of the advantageous allele and other alleles near it. The process is considered to be slower than negative frequency-dependent selection. It may produce an "arms race", consisting of the repeated origin and fixation of new virulence traits in the parasite and new defence traits in the host.[1]

This mode of selection is likely to occur in interactions between unicellular organisms and viruses due to large population sizes, short generation times, often haploid genomes and horizontal gene transfer, which increase the probability of beneficial mutations arising and spreading through populations.[3]

John N. Thompson's geographic mosaic theory of coevolution hypothesizes spatially divergent coevolutionary selection, producing genetic differentiation across populations.[9] The model assumes three elements that jointly fuel coevolution:[10][11][12]

Plantago lanceolata interacts with a powdery mildew (not shown) to create a geographic mosaic of genotypes of host and parasite.[13]

1) a selection mosaic among populations

Natural selection on interactions between species differs among populations. Thus genotype-by-genotype-by-environment (G x G x E) interactions affect fitness of the antagonists. In other words, the specific environmental conditions determine how any genotype of one species influences the fitness of another species.[10]

2) coevolutionary hotspots

Coevolutionary hotspots are communities in which selection on the interaction is truly reciprocal. These hotspots are intermixed with so-called coldspots in which only one or neither species adapts to the antagonist.[10]

3) geographic mixing of traits

Between the communities/regions there is a continuous "mixing" of traits by gene flow, random genetic drift, population extinction, or mutation. This remixing determines the exact dynamics of the geographic mosaic by shifting the spatial distributions of potentially coevolving alleles and traits.[10]

These processes have been intensively studied in a plant, Plantago lanceolata, and its parasite the powdery mildew Podosphaera plantaginis in Åland in south-western Finland.[13] The mildew obtains nutrients from its host, a perennial herb, by sending feeding roots into the plant. There are more than 3000 host populations in this region, where both populations can evolve freely, in the absence of human-imposed selection, in a heterogeneous landscape. Both partners can reproduce asexually and sexually. The mildew tends to become locally extinct in winter, and causes local epidemics in summer. The mildew's success at overwintering, and the intensity of host-pathogen encounters in summer, strongly vary geographically. The system has spatially divergent coevolutionary dynamics across two metapopulations as predicted by the mosaic theory.[14][9]

Potamopyrgus antipodarum tends to reproduce sexually when in the presence of trematode parasites.

The Red Queen hypothesis states that both host and parasite have to change continuously to keep up with each other's adaptations, like the description in Lewis Carroll's fiction.[2] The mathematical evolutionary biologist W. D. Hamilton further proposed that since sexual reproduction continually creates new combinations of genes, some of which may be advantageous, parasitism favours sexual reproduction in the host.[15][16]

The New Zealand freshwater snail Potamopyrgus antipodarum and its different trematode parasites represent a rather special model system. Populations of P. antipodarum consist of asexual clones and sexual individuals and therefore can be used to study the evolution and advantages of sexual reproduction. There is a high correlation between the presence of parasites and the frequency of sexual individuals within the different populations. This result is consistent with the favouring of sexual reproduction proposed in the Red Queen hypothesis.[17]

Tribolium castaneum

Tribolium castaneum, the red flour beetle, is a host for the microsporidian Nosema whitei. This parasitoid kills its host for transmission, so the host's lifespan is important for the parasite's success. In turn, parasite fitness most likely depends on a trade-off between transmission (spore load) and virulence.[18] A higher virulence would increase the potential for the production of more offspring, but a higher spore load would affect the host's lifespan and therefore the transmission rate. This trade-off is supported by coevolutionary experiments, which revealed the decrease of virulence, a constant transmission potential and an increase in the host's lifespan over a period of time.[18] Further experiments demonstrated a higher recombination rate in the host during coevolutionary interactions, which may be selectively advantageous because it should increase diversity of host genotypes.[19]

Resources are generally limited. Therefore, favouring one trait, like virulence or immunity, limits other life-history traits, such as reproductive rate. Moreover, genes are often pleiotropic, having multiple effects. Thus, a change in a pleiotropic immunity or virulence gene can automatically affect other traits. There is thus a trade-off between benefits and costs of the adaptive changes that may prevent the host population from becoming fully resistant or the parasite population from being highly pathogenic. The costs of gene pleiotropy have been investigated in coevolving Escherichia coli and bacteriophages. To inject their genetic material, phages need to bind to a specific bacterial cell surface receptor. The bacterium may prevent injection by altering the relevant binding site, e.g. in response to point mutations or deletion of the receptor. However, these receptors have important functions in bacterial metabolism. Their loss would thus decrease fitness (i.e. population growth rate). As a consequence, there is a trade-off between the advantages and disadvantages of a mutated receptor, leading to polymorphism at this locus.[20]