Host-parasite coevolution
Encyclopedia
Host–parasite coevolution is a special case of coevolution, which is defined as the reciprocal adaptive genetic
change of two antagonists (e.g. different species or genes) through reciprocal selective pressures. In the particular case of host–parasite coevolution the antagonists are different species of host
and parasite.
and parasites
exert reciprocal selective pressures on each other, which may lead to rapid reciprocal adaptation. For organisms with short generation times host–parasite coevolution can be observed in comparatively small time periods, making it possible to study evolutionary change in real-time under both field and laboratory conditions. These interactions may thus serve as a counter-example to the common notion that evolution can only be detected across extended time scales.
The high dynamics associated with these interactions are summarized in the Red Queen hypothesis. It states that "it takes all the running you can do to keep in the same place", i.e. both host and parasite have to change continuously to keep up with each other's adaptations.
-parasite coevolution is a ubiquitous phenomenon of potential importance to all living organisms, including humans. Many medically relevant diseases (e.g. malaria
, AIDS
and influenza
) are caused by coevolving parasites. Therefore detailed understanding of the coevolutionary adaptations between parasite ‘attack strategy’ and host immune system
may result in the development of novel medications and vaccines and thus help save human life.
Furthermore these interactions are of major concern in agriculture. Coevolving parasites are responsible for crop failure and especially in industrial agriculture
, pesticides are indispensable. Livestock is similarly affected by numerous coevolving parasites. Therefore a clearer understanding of host–parasite coevolution will point to new possibilities for organic farming
and reduce the application of ecologically harmful chemicals.
frequencies within populations. These changes may be determined by three main types of selection dynamics.
, 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.
Coevolution determined by negative frequency dependent selection is rapid, potentially occurring across few generations. 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.
has a fitness advantage over both homozygotes ("heterozygote advantage
" or "heterosis
"). 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 of 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 Plasmodium. As a consequence, the heterozygote genotype is selectively favored in areas with a high incidence of malaria.
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.
In addition the modes of selection can differ between the various loci
involved in host–parasite interactions. Therefore the various loci may be subject to different selection dynamics.
The model assumes that there are three crucial elements that jointly fuel ongoing coevolutionary change:
1) There is a selection mosaic among populations.
Natural selection on interspecific interactions 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 (biotic and abiotic components).
2) There are 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.
3) There is a geographic mixing of traits.
Between the communities/regions there is a continuous "mixing" of traits by gene flow
, random genetic drift, population extinction
, or mutations. This remixing determines the exact dynamics of the Geographic Mosaic by shifting the spatial distributions of potentially coevolving alleles and traits.
In summary, the theory claims that species interactions commonly coevolve as complex geographic mosaics of populations, formed by differences in local selection and gene flow.
It ties together the processes operating over space and time to determine the outcome of coevolutionary interactions and furthermore provides a reference framework for future (especially field) research on this topic.
or immunity
) limits investment in other life-history traits (e.g. reproductive rate). Moreoever, genes often have pleiotropic effects. Thus, a change in a pleiotropic immunity or virulence gene may automatically affect other traits. There is thus a trade-off between benefits and costs of the adaptive changes that then may prevent the host population to become fully resistant or the parasite population to express very high pathogenicity.
One example for costs related to gene pleiotropy was found for 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. growth rate). As a consequence, there is a trade-off between the advantages and disadvantages of a mutated receptor, leading to polymorphisms at this locus within bacterial populations coevolving with phages.
systems with long generation times, for which temporal changes cannot be easily assessed within the often restricted timeline of research projects. Such spatial studies rely on the concept of local adaptation: Due to chance effects and varying environmental conditions host
and parasite are likely to coevolve along different trajectories in different locations. The comparison of locations may reveal various stages of the coevolutionary cycle. A major challenge is to distinguish patterns of local adaptation caused by reciprocal coevolutionary change versus directional selection
to any other environmental factor.
Long term field studies of populations from one or more sites represent the ideal approach to analyse the dynamics and consequences of coevolution, because they allow the direct detection of reciprocal genetic change. A particular challenge is to relate the temporal dynamics to variation in environmental factors (i.e. G x G x E effects). Long term studies including several locations may also help to understand the dynamics of the geographic mosaic of coevolution.
or invertebrates. A particular challenge is to relate the results from the artificial laboratory environment to the complexity encountered in nature.
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
.
Long term laboratory experiments and field studies revealed that 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 Red Queen hypothesis that sexual reproduction is favoured during host–parasite coevolution. At the same time, the persistance of sex may also rely on other factors, for example Muller's ratchet
and/or the avoidance of the accummulation of deleterious mutations (deterministic mutation model).
The nematode Caenorhabditis elegans
and the bacterium Bacillus thuringiensis
were only recently established as a model system for studying host–parasite coevolution. Laboratory evolution experiments provided evidence for many of the basic predictions of these coevolutionary interactions, including reciprocal genetic change, and increases in the rate of evolution and genetic diversity.
The widespread use of C. elegans in different branches of biology makes it a good choice for evolutionary research. On the one hand evolutionary studies may help to close the gaps in knowledge still persistent for C. elegans biology. On the other hand the information already available on this species may help to work out the molecular mechanisms underlying evolutionary change.
and its numerous parasites have become one of the main model systems for studying coevolution.
One valuable characteristic of this system is that the reproduction of the host can be asexual as well as sexual (inducing by changes in the external environment), so that conditions for sexual reproduction can be stimulated in the laboratory.
Coevolution was especially studied between Daphnia magna
and the bacterium Pasteuria ramosa. For example, Decaestecker et al. reconstructed the evolution of the populations across decades, by reanimating resting stages of both species from laminated pond sediments and exposed hosts from each layer to parasites from the past, the same and the future layers. The study demonstrated that parasites were on average most infective on their contemporary hosts. in consistency with negative frequency dependent selection
As many other arthropods Tribolium castaneum, the red flour beetle
, is a host for the microsporidia
Nosema whitei.
Nosema whitei kills its host for transmission, thus 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
: 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.
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.
and its parasite Podosphaera plantaginis, which has been intensively studied on the Aland islands
in south-western Finland. P. plantaginis is a powdery mildew
obtaining nutrients from its host, a perennial herb, by sending feeding roots into the plant.
There are more than 3000 host populations known in this region, where both populations can evolve freely, in absence of human-imposed selection, in a very heterogeneous landscape. Both antagonists can reproduce asexually or sexually. This system was used to demonstrate spatially divergent coevolutionary dynamics across two metapopulations and it provided support for the predictions of the Mosaic Theory of Coevolution.
or Pseudomonas fluorescens
and their bacteriophages.
E. coli, a Gram-negative
proteobacterium, is a common model in biological research, for which comprehensive data on various aspects of its life-history is available. It has been used extensively for evolution
experiments, including those related to coevolution with phages. These studies revealed - among others - that coevolutionary adaptation
may be influenced by pleiotropic effects of the involved genes
. In particular, binding of the bacteriophage
to E. coli surface receptor
is the crucial step in the virus
infection
cycle. A mutation
in the receptor's binding site may cause resistance
. Such mutations often show pleiotropic effects and may cause a cost of resistance. In the presence of phages, such pleiotropy may lead to polymorphisms
in the bacterial population and thus enhance biodiversity
in the community.
Another model system consists of the plant- and animal-colonizing bacterium Pseudomonas
and its bacteriophages. This system provided new insights into the dynamics of coevolutionary change. It demonstrated that coevolution may proceed via recurrent selective sweeps, favouring generalists for both antagonists. Furthermore, coevolution with phages may promote allopatric diversity, potentially enhancing biodiversity and possibly speciation
. Host
-parasite coevolution may also affect the underlying genetics
, for example by favouring increased mutation rates in the host.
Laine AL (2006): Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proceedings of the Royal Society of London: Biological Sciences 273: 267-273
Rudgers JA, Strauss SY (2004): A selection mosaic in the facultative mutualism between ants and wild cotton. Proceedings of the Royal Society of London: Biological Sciences271: 2481-2488
Thompson JN, Cunningham BM (2002): Geographic structure and dynamics of coevolutionary selection. Nature 417:735-738
Thompson JN (1994): The Coevolutionary process.The University of Chicago Press, Chicago
Potamopyrgus antipodarum and its trematodes
Koskella B, Lively CM (2007): Advice of the rose:experimental coevolution of a trematode parasite and its snail host. Evolution61:152-159
EAWAG Department of Aquatic Ecology| EAWAG Department of Aquatic Ecology
Caenorhabditis elegans and Bacillus thuringiensis
Department of Evolutionary Ecology and Genetics, CAU Kiel
Institute for Evolution and Biodiversity, University of Münster
Daphnia and its parasites
TJ Little Lab Homepage
E Decaestecker Lab Homepage
D Ebert Lab Homepage
Duncan AB, Little TJ (2007): Parasite driven genetic change in a natural population of Daphnia. Evolution 61:796-803
Decaestecker E, Vergote A, Ebert D, De Meester L (2003): Evidence for strong host-clone parasite species interactions in the Daphnia-parasite system. Evolution 57:784-792
Ebert D (2005). Ecology, Epidemiology, and Evolution of Parasitism in Daphnia.
http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books.
Altermatt F, Ebert D (2008): Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology letters 11: 918–928
Tribolium castaneum and Nosema whitei
Experimental Ecology, University of Zürich
Animal Evolutionary Ecology, University Münster
Plantago and its parasites
J Burdon Lab Homepage
I Hanski Lab Homepage
AL Laine Lab Homepage
Burdon J, Thrall P (2009):Coevolution of plants and their pathogens in natural habitats. Science 324,5928:755 - 756
Laine A-L, Hanski I (2006): Large-scale spatial dynamics of specialist plant pathogen. Journal of Ecology 92: 990-1000.
Bacteria and their bacteriophages
JN Thompson Lab Homepage
Center of Ecology and Evolutionary Biology, University of Oregon
BJM Bohannan Lab Homepage
Pseudomonas Genome Database
Genetics
Genetics , a discipline of biology, is the science of genes, heredity, and variation in living organisms....
change of two antagonists (e.g. different species or genes) through reciprocal selective pressures. In the particular case of host–parasite coevolution the antagonists are different species of host
Host (biology)
In biology, a host is an organism that harbors a parasite, or a mutual or commensal symbiont, typically providing nourishment and shelter. In botany, a host plant is one that supplies food resources and substrate for certain insects or other fauna...
and parasite.
Introduction
HostsHost (biology)
In biology, a host is an organism that harbors a parasite, or a mutual or commensal symbiont, typically providing nourishment and shelter. In botany, a host plant is one that supplies food resources and substrate for certain insects or other fauna...
and parasites
Parasitism
Parasitism is a type of symbiotic relationship between organisms of different species where one organism, the parasite, benefits at the expense of the other, the host. Traditionally parasite referred to organisms with lifestages that needed more than one host . These are now called macroparasites...
exert reciprocal selective pressures on each other, which may lead to rapid reciprocal adaptation. For organisms with short generation times host–parasite coevolution can be observed in comparatively small time periods, making it possible to study evolutionary change in real-time under both field and laboratory conditions. These interactions may thus serve as a counter-example to the common notion that evolution can only be detected across extended time scales.
The high dynamics associated with these interactions are summarized in the Red Queen hypothesis. It states that "it takes all the running you can do to keep in the same place", i.e. both host and parasite have to change continuously to keep up with each other's adaptations.
Relevance
HostHost (biology)
In biology, a host is an organism that harbors a parasite, or a mutual or commensal symbiont, typically providing nourishment and shelter. In botany, a host plant is one that supplies food resources and substrate for certain insects or other fauna...
-parasite coevolution is a ubiquitous phenomenon of potential importance to all living organisms, including humans. Many medically relevant diseases (e.g. malaria
Malaria
Malaria is a mosquito-borne infectious disease of humans and other animals caused by eukaryotic protists of the genus Plasmodium. The disease results from the multiplication of Plasmodium parasites within red blood cells, causing symptoms that typically include fever and headache, in severe cases...
, AIDS
AIDS
Acquired immune deficiency syndrome or acquired immunodeficiency syndrome is a disease of the human immune system caused by the human immunodeficiency virus...
and influenza
Influenza
Influenza, commonly referred to as the flu, is an infectious disease caused by RNA viruses of the family Orthomyxoviridae , that affects birds and mammals...
) are caused by coevolving parasites. Therefore detailed understanding of the coevolutionary adaptations between parasite ‘attack strategy’ and host immune system
Immune system
An immune system is a system of biological structures and processes within an organism that protects against disease by identifying and killing pathogens and tumor cells. It detects a wide variety of agents, from viruses to parasitic worms, and needs to distinguish them from the organism's own...
may result in the development of novel medications and vaccines and thus help save human life.
Furthermore these interactions are of major concern in agriculture. Coevolving parasites are responsible for crop failure and especially in industrial agriculture
Industrial agriculture
Industrial farming is a form of modern farming that refers to the industrialized production of livestock, poultry, fish, and crops. The methods of industrial agriculture are technoscientific, economic, and political...
, pesticides are indispensable. Livestock is similarly affected by numerous coevolving parasites. Therefore a clearer understanding of host–parasite coevolution will point to new possibilities for organic farming
Organic farming
Organic farming is the form of agriculture that relies on techniques such as crop rotation, green manure, compost and biological pest control to maintain soil productivity and control pests on a farm...
and reduce the application of ecologically harmful chemicals.
Selection Dynamics
Host-parasite coevolution is characterized by reciprocal genetic change and thus changes in alleleAllele
An allele is one of two or more forms of a gene or a genetic locus . "Allel" is an abbreviation of allelomorph. Sometimes, different alleles can result in different observable phenotypic traits, such as different pigmentation...
frequencies within populations. These changes may be determined by three main types of selection dynamics.
Negative frequency dependent selection
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 genotypeGenotype
The genotype is the genetic makeup of a cell, an organism, or an individual usually with reference to a specific character under consideration...
, 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.
Coevolution determined by negative frequency dependent selection is rapid, potentially occurring across few generations. 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.
Overdominant selection
Overdominance occurs if the heterozygote phenotypePhenotype
A phenotype is an organism's observable characteristics or traits: such as its morphology, development, biochemical or physiological properties, behavior, and products of behavior...
has a fitness advantage over both homozygotes ("heterozygote advantage
Heterozygote advantage
A heterozygote advantage describes the case in which the heterozygote genotype has a higher relative fitness than either the homozygote dominant or homozygote recessive genotype. The specific case of heterozygote advantage is due to a single locus known as overdominance...
" or "heterosis
Heterosis
Heterosis, or hybrid vigor, or outbreeding enhancement, is the improved or increased function of any biological quality in a hybrid offspring. The adjective derived from heterosis is heterotic....
"). One example is sickle cell anemia. It is due to a mutation
Mutation
In molecular biology and genetics, mutations are changes in a genomic sequence: the DNA sequence of a cell's genome or the DNA or RNA sequence of a virus. They can be defined as sudden and spontaneous changes in the cell. Mutations are caused by radiation, viruses, transposons and mutagenic...
in the hemoglobin
Hemoglobin
Hemoglobin is the iron-containing oxygen-transport metalloprotein in the red blood cells of all vertebrates, with the exception of the fish family Channichthyidae, as well as the tissues of some invertebrates...
gene leading to sickle shape formation of red blood cells, causing clotting of blood vessels, restricted blood flow and reduced oxygen transport. At the same time, the mutation confers resistance to malaria
Malaria
Malaria is a mosquito-borne infectious disease of humans and other animals caused by eukaryotic protists of the genus Plasmodium. The disease results from the multiplication of Plasmodium parasites within red blood cells, causing symptoms that typically include fever and headache, in severe cases...
, caused by Plasmodium
Plasmodium
Plasmodium is a genus of parasitic protists. Infection by these organisms is known as malaria. The genus Plasmodium was described in 1885 by Ettore Marchiafava and Angelo Celli. Currently over 200 species of this genus are recognized and new species continue to be described.Of the over 200 known...
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 Plasmodium. As a consequence, the heterozygote genotype is selectively favored in areas with a high incidence of malaria.
Directional selection
If an allele provides a fitness benefit, its frequency will increase within a population - selection is directional or positive. Selective sweeps are one form of directional selection, where the increase in frequency will eventually lead to the fixation of the advantageous allele. The process is considered to be slower in comparison to negative frequency dependent selection. It may produce an "arms race", consisting of the repeated origin and fixation of new parasite virulence and host defence traits.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.
Current challenges
The relative importance of these different selective dynamics for host–parasite coevolution is still under debate. One problem is that the unambiguous identification of the underlying dynamics is not straightforward. For example, if the plot of allele frequency changes indicates a selective sweep, then it is possible that the curve represents a small part of the fluctuating cycles expected for negative frequency dependent selection and that the time scale of the analysis is too short to allow clear discrimination of the alternatives.In addition the modes of selection can differ between the various loci
Locus (genetics)
In the fields of genetics and genetic computation, a locus is the specific location of a gene or DNA sequence on a chromosome. A variant of the DNA sequence at a given locus is called an allele. The ordered list of loci known for a particular genome is called a genetic map...
involved in host–parasite interactions. Therefore the various loci may be subject to different selection dynamics.
Geographic Mosaic Theory of Coevolution
The Geographic Mosaic Theory of Coevolution by John N. Thompson hypothesizes that there is spatially divergent coevolutionary selection, producing genetic differentiation across populations.The model assumes that there are three crucial elements that jointly fuel ongoing coevolutionary change:
1) There is a selection mosaic among populations.
Natural selection on interspecific interactions 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 (biotic and abiotic components).
2) There are 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.
3) There is a geographic mixing of traits.
Between the communities/regions there is a continuous "mixing" of traits by gene flow
Gene flow
In population genetics, gene flow is the transfer of alleles of genes from one population to another.Migration into or out of a population may be responsible for a marked change in allele frequencies...
, random genetic drift, population extinction
Extinction
In biology and ecology, extinction is the end of an organism or of a group of organisms , normally a species. The moment of extinction is generally considered to be the death of the last individual of the species, although the capacity to breed and recover may have been lost before this point...
, or mutations. This remixing determines the exact dynamics of the Geographic Mosaic by shifting the spatial distributions of potentially coevolving alleles and traits.
In summary, the theory claims that species interactions commonly coevolve as complex geographic mosaics of populations, formed by differences in local selection and gene flow.
It ties together the processes operating over space and time to determine the outcome of coevolutionary interactions and furthermore provides a reference framework for future (especially field) research on this topic.
Costs of adaptation
Resources are generally limited. Therefore, investment in one trait (e.g. virulenceVirulence
Virulence is by MeSH definition the degree of pathogenicity within a group or species of parasites as indicated by case fatality rates and/or the ability of the organism to invade the tissues of the host. The pathogenicity of an organism - its ability to cause disease - is determined by its...
or immunity
Immunity (medical)
Immunity is a biological term that describes a state of having sufficient biological defenses to avoid infection, disease, or other unwanted biological invasion. Immunity involves both specific and non-specific components. The non-specific components act either as barriers or as eliminators of wide...
) limits investment in other life-history traits (e.g. reproductive rate). Moreoever, genes often have pleiotropic effects. Thus, a change in a pleiotropic immunity or virulence gene may automatically affect other traits. There is thus a trade-off between benefits and costs of the adaptive changes that then may prevent the host population to become fully resistant or the parasite population to express very high pathogenicity.
One example for costs related to gene pleiotropy was found for coevolving Escherichia coli
Escherichia coli
Escherichia coli is a Gram-negative, rod-shaped bacterium that is commonly found in the lower intestine of warm-blooded organisms . Most E. coli strains are harmless, but some serotypes can cause serious food poisoning in humans, and are occasionally responsible for product recalls...
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. growth rate). As a consequence, there is a trade-off between the advantages and disadvantages of a mutated receptor, leading to polymorphisms at this locus within bacterial populations coevolving with phages.
Field studies across space and/or time
Field studies across space at a single time point may be useful to study coevolution for hostHost (biology)
In biology, a host is an organism that harbors a parasite, or a mutual or commensal symbiont, typically providing nourishment and shelter. In botany, a host plant is one that supplies food resources and substrate for certain insects or other fauna...
systems with long generation times, for which temporal changes cannot be easily assessed within the often restricted timeline of research projects. Such spatial studies rely on the concept of local adaptation: Due to chance effects and varying environmental conditions host
Host (biology)
In biology, a host is an organism that harbors a parasite, or a mutual or commensal symbiont, typically providing nourishment and shelter. In botany, a host plant is one that supplies food resources and substrate for certain insects or other fauna...
and parasite are likely to coevolve along different trajectories in different locations. The comparison of locations may reveal various stages of the coevolutionary cycle. A major challenge is to distinguish patterns of local adaptation caused by reciprocal coevolutionary change versus directional selection
Directional selection
In population genetics, directional selection is a mode of natural selection in which a single phenotype is favored, causing the allele frequency to continuously shift in one direction...
to any other environmental factor.
Long term field studies of populations from one or more sites represent the ideal approach to analyse the dynamics and consequences of coevolution, because they allow the direct detection of reciprocal genetic change. A particular challenge is to relate the temporal dynamics to variation in environmental factors (i.e. G x G x E effects). Long term studies including several locations may also help to understand the dynamics of the geographic mosaic of coevolution.
Experiments under controlled lab conditions
Laboratory-based evolution experiments may represent a highly efficient approach to dissect the importance of particular selective factors and to characterize in detail the dynamics and consequences of coevolution. Most importantly, they allow to minimize confounding environmental influences and to test single factors, which can be varied between treatments. Therefore, this approach may allow distinction of cause and effect. Such evolution experiments require host systems with short generation times like bacteriaBacteria
Bacteria are a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...
or invertebrates. A particular challenge is to relate the results from the artificial laboratory environment to the complexity encountered in nature.
Potamopyrgus antipodarum and its trematode
Sexual reproduction
Sexual reproduction is the creation of a new organism by combining the genetic material of two organisms. There are two main processes during sexual reproduction; they are: meiosis, involving the halving of the number of chromosomes; and fertilization, involving the fusion of two gametes and the...
.
Long term laboratory experiments and field studies revealed that 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 Red Queen hypothesis that sexual reproduction is favoured during host–parasite coevolution. At the same time, the persistance of sex may also rely on other factors, for example Muller's ratchet
Muller's ratchet
In evolutionary genetics, Muller's ratchet is the process by which the genomes of an asexual population accumulate deleterious mutations in an irreversible manner....
and/or the avoidance of the accummulation of deleterious mutations (deterministic mutation model).
Caenorhabditis elegans and Bacillus thuringiensis
Caenorhabditis elegans
Caenorhabditis elegans is a free-living, transparent nematode , about 1 mm in length, which lives in temperate soil environments. Research into the molecular and developmental biology of C. elegans was begun in 1974 by Sydney Brenner and it has since been used extensively as a model...
and the bacterium Bacillus thuringiensis
Bacillus thuringiensis
Bacillus thuringiensis is a Gram-positive, soil-dwelling bacterium, commonly used as a biological pesticide; alternatively, the Cry toxin may be extracted and used as a pesticide. B...
were only recently established as a model system for studying host–parasite coevolution. Laboratory evolution experiments provided evidence for many of the basic predictions of these coevolutionary interactions, including reciprocal genetic change, and increases in the rate of evolution and genetic diversity.
The widespread use of C. elegans in different branches of biology makes it a good choice for evolutionary research. On the one hand evolutionary studies may help to close the gaps in knowledge still persistent for C. elegans biology. On the other hand the information already available on this species may help to work out the molecular mechanisms underlying evolutionary change.
Daphnia and its parasites
The crustacean DaphniaDaphnia
Daphnia are small, planktonic crustaceans, between 0.2 and 5 mm in length. Daphnia are members of the order Cladocera, and are one of the several small aquatic crustaceans commonly called water fleas because of their saltatory swimming style...
and its numerous parasites have become one of the main model systems for studying coevolution.
One valuable characteristic of this system is that the reproduction of the host can be asexual as well as sexual (inducing by changes in the external environment), so that conditions for sexual reproduction can be stimulated in the laboratory.
Coevolution was especially studied between Daphnia magna
Daphnia magna
Daphnia magna is a species of Daphnia which is native to northern and western North America. It is also widely distributed in Eurasia and in some regions of Africa.- Laboratory animal :...
and the bacterium Pasteuria ramosa. For example, Decaestecker et al. reconstructed the evolution of the populations across decades, by reanimating resting stages of both species from laminated pond sediments and exposed hosts from each layer to parasites from the past, the same and the future layers. The study demonstrated that parasites were on average most infective on their contemporary hosts. in consistency with negative frequency dependent selection
Tribolium castaneum and Nosema whitei
Red flour beetle
The red flour beetle is a tenebrionid beetle. It is a worldwide stored product pest.Red flour beetles attack stored grain products causing loss and damage...
, is a host for the microsporidia
Microsporidia
The microsporidia constitute a phylum of spore-forming unicellular parasites. They were once thought to be protists but are now known to be fungi. Loosely 1500 of the probably more than one million species are named now. Microsporidia are restricted to animal hosts, and all major groups of animals...
Nosema whitei.
Nosema whitei kills its host for transmission, thus 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
Virulence
Virulence is by MeSH definition the degree of pathogenicity within a group or species of parasites as indicated by case fatality rates and/or the ability of the organism to invade the tissues of the host. The pathogenicity of an organism - its ability to cause disease - is determined by its...
: 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.
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.
Plantago and its parasites
Host-parasite coevolution is studied in a diversity of plant systems. One example is Plantago lanceolataPlantago lanceolata
Plantago lanceolata is a species of genus Plantago known by the common names ribwort plantain, English plantain, and narrowleaf plantain. It is a common weed of cultivated land....
and its parasite Podosphaera plantaginis, which has been intensively studied on the Aland islands
Åland Islands
The Åland Islands form an archipelago in the Baltic Sea. They are situated at the entrance to the Gulf of Bothnia and form an autonomous, demilitarised, monolingually Swedish-speaking region of Finland...
in south-western Finland. P. plantaginis is a powdery mildew
Powdery mildew
Powdery mildew is a fungal disease that affects a wide range of plants. Powdery mildew diseases are caused by many different species of fungi in the order Erysiphales. It is one of the easier diseases to spot, as its symptoms are quite distinctive. Infected plants display white powdery spots on the...
obtaining nutrients from its host, a perennial herb, by sending feeding roots into the plant.
There are more than 3000 host populations known in this region, where both populations can evolve freely, in absence of human-imposed selection, in a very heterogeneous landscape. Both antagonists can reproduce asexually or sexually. This system was used to demonstrate spatially divergent coevolutionary dynamics across two metapopulations and it provided support for the predictions of the Mosaic Theory of Coevolution.
Bacteria and their parasites
Biological communities are often complex, they are influenced by diverse factors, and therefore, they are very difficult to study. A possible solution is to focus on simple community systems under controlled laboratory conditions, for example microbial communities consisting of Escherichia coliEscherichia coli
Escherichia coli is a Gram-negative, rod-shaped bacterium that is commonly found in the lower intestine of warm-blooded organisms . Most E. coli strains are harmless, but some serotypes can cause serious food poisoning in humans, and are occasionally responsible for product recalls...
or Pseudomonas fluorescens
Pseudomonas fluorescens
Pseudomonas fluorescens is a common Gram-negative, rod-shaped bacterium. It belongs to the Pseudomonas genus; 16S rRNA analysis has placed P. fluorescens in the P. fluorescens group within the genus, to which it lends its name....
and their bacteriophages.
Gram-negative
Gram-negative bacteria are bacteria that do not retain crystal violet dye in the Gram staining protocol. In a Gram stain test, a counterstain is added after the crystal violet, coloring all Gram-negative bacteria with a red or pink color...
proteobacterium, is a common model in biological research, for which comprehensive data on various aspects of its life-history is available. It has been used extensively for evolution
Evolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
experiments, including those related to coevolution with phages. These studies revealed - among others - that coevolutionary adaptation
Adaptation
An adaptation in biology is a trait with a current functional role in the life history of an organism that is maintained and evolved by means of natural selection. An adaptation refers to both the current state of being adapted and to the dynamic evolutionary process that leads to the adaptation....
may be influenced by pleiotropic effects of the involved genes
Gênes
Gênes is the name of a département of the First French Empire in present Italy, named after the city of Genoa. It was formed in 1805, when Napoleon Bonaparte occupied the Republic of Genoa. Its capital was Genoa, and it was divided in the arrondissements of Genoa, Bobbio, Novi Ligure, Tortona and...
. In particular, binding of the bacteriophage
Bacteriophage
A bacteriophage is any one of a number of viruses that infect bacteria. They do this by injecting genetic material, which they carry enclosed in an outer protein capsid...
to E. coli surface receptor
Receptor (biochemistry)
In biochemistry, a receptor is a molecule found on the surface of a cell, which receives specific chemical signals from neighbouring cells or the wider environment within an organism...
is the crucial step in the virus
Virus
A virus is a small infectious agent that can replicate only inside the living cells of organisms. Viruses infect all types of organisms, from animals and plants to bacteria and archaea...
infection
Infection
An infection is the colonization of a host organism by parasite species. Infecting parasites seek to use the host's resources to reproduce, often resulting in disease...
cycle. A mutation
Mutation
In molecular biology and genetics, mutations are changes in a genomic sequence: the DNA sequence of a cell's genome or the DNA or RNA sequence of a virus. They can be defined as sudden and spontaneous changes in the cell. Mutations are caused by radiation, viruses, transposons and mutagenic...
in the receptor's binding site may cause resistance
Antibiotic resistance
Antibiotic resistance is a type of drug resistance where a microorganism is able to survive exposure to an antibiotic. While a spontaneous or induced genetic mutation in bacteria may confer resistance to antimicrobial drugs, genes that confer resistance can be transferred between bacteria in a...
. Such mutations often show pleiotropic effects and may cause a cost of resistance. In the presence of phages, such pleiotropy may lead to polymorphisms
Polymorphism (biology)
Polymorphism in biology occurs when two or more clearly different phenotypes exist in the same population of a species — in other words, the occurrence of more than one form or morph...
in the bacterial population and thus enhance biodiversity
Biodiversity
Biodiversity is the degree of variation of life forms within a given ecosystem, biome, or an entire planet. Biodiversity is a measure of the health of ecosystems. Biodiversity is in part a function of climate. In terrestrial habitats, tropical regions are typically rich whereas polar regions...
in the community.
Another model system consists of the plant- and animal-colonizing bacterium Pseudomonas
Pseudomonas
Pseudomonas is a genus of gammaproteobacteria, belonging to the family Pseudomonadaceae containing 191 validly described species.Recently, 16S rRNA sequence analysis has redefined the taxonomy of many bacterial species. As a result, the genus Pseudomonas includes strains formerly classified in the...
and its bacteriophages. This system provided new insights into the dynamics of coevolutionary change. It demonstrated that coevolution may proceed via recurrent selective sweeps, favouring generalists for both antagonists. Furthermore, coevolution with phages may promote allopatric diversity, potentially enhancing biodiversity and possibly speciation
Speciation
Speciation is the evolutionary process by which new biological species arise. The biologist Orator F. Cook seems to have been the first to coin the term 'speciation' for the splitting of lineages or 'cladogenesis,' as opposed to 'anagenesis' or 'phyletic evolution' occurring within lineages...
. Host
Host (biology)
In biology, a host is an organism that harbors a parasite, or a mutual or commensal symbiont, typically providing nourishment and shelter. In botany, a host plant is one that supplies food resources and substrate for certain insects or other fauna...
-parasite coevolution may also affect the underlying genetics
Genetics
Genetics , a discipline of biology, is the science of genes, heredity, and variation in living organisms....
, for example by favouring increased mutation rates in the host.
Links/Further reading
Mosaic ModelLaine AL (2006): Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proceedings of the Royal Society of London: Biological Sciences 273: 267-273
Rudgers JA, Strauss SY (2004): A selection mosaic in the facultative mutualism between ants and wild cotton. Proceedings of the Royal Society of London: Biological Sciences271: 2481-2488
Thompson JN, Cunningham BM (2002): Geographic structure and dynamics of coevolutionary selection. Nature 417:735-738
Thompson JN (1994): The Coevolutionary process.The University of Chicago Press, Chicago
Potamopyrgus antipodarum and its trematodes
Koskella B, Lively CM (2007): Advice of the rose:experimental coevolution of a trematode parasite and its snail host. Evolution61:152-159
EAWAG Department of Aquatic Ecology| EAWAG Department of Aquatic Ecology
Caenorhabditis elegans and Bacillus thuringiensis
Department of Evolutionary Ecology and Genetics, CAU Kiel
Institute for Evolution and Biodiversity, University of Münster
Daphnia and its parasites
TJ Little Lab Homepage
E Decaestecker Lab Homepage
D Ebert Lab Homepage
Duncan AB, Little TJ (2007): Parasite driven genetic change in a natural population of Daphnia. Evolution 61:796-803
Decaestecker E, Vergote A, Ebert D, De Meester L (2003): Evidence for strong host-clone parasite species interactions in the Daphnia-parasite system. Evolution 57:784-792
Ebert D (2005). Ecology, Epidemiology, and Evolution of Parasitism in Daphnia.
http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books.
Altermatt F, Ebert D (2008): Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology letters 11: 918–928
Tribolium castaneum and Nosema whitei
Experimental Ecology, University of Zürich
Animal Evolutionary Ecology, University Münster
Plantago and its parasites
J Burdon Lab Homepage
I Hanski Lab Homepage
AL Laine Lab Homepage
Burdon J, Thrall P (2009):Coevolution of plants and their pathogens in natural habitats. Science 324,5928:755 - 756
Laine A-L, Hanski I (2006): Large-scale spatial dynamics of specialist plant pathogen. Journal of Ecology 92: 990-1000.
Bacteria and their bacteriophages
JN Thompson Lab Homepage
Center of Ecology and Evolutionary Biology, University of Oregon
BJM Bohannan Lab Homepage
Pseudomonas Genome Database