Host–parasite coevolution favours parasite genetic diversity and horizontal gene transfer

Host–parasite coevolution is predicted to favour genetic diversity and the underlying mechanisms (e.g. sexual reproduction and, more generally, genetic exchange), because diversity enhances the antagonists' potential for rapid adaptation. To date, this prediction has mainly been tested and confirmed for the host. It should similarly apply to the parasite. Indeed, our previous work demonstrated that experimental coevolution between the nematode Caenorhabditis elegans and its microparasite Bacillus thuringiensis selects for genetic diversity in both antagonists. For the parasite, the previous analysis was based on plasmid‐encoded toxin gene markers. Thus, it was restricted to a very small part of the bacterial genome and did not cover the main chromosome, which harbours a large variety of virulence factors. Here, we present new data for chromosomal gene markers of B. thuringiensis and combine this information with the previous results on plasmid‐encoded toxins. Our new results demonstrate that, in comparison with the control treatment, coevolution with a host similarly leads to higher levels of genetic diversity in the bacterial chromosome, thus indicating the relevance of chromosomal genes for coevolution. Furthermore, the frequency of toxin gene gain is significantly elevated during coevolution, highlighting the importance of horizontal gene transfer as a diversity‐generating mechanism. In conclusion, our study emphasizes the strong influence of antagonistic coevolution on parasite genetic diversity and gene exchange.     

Spatial population genetic structure of a bacterial parasite in close coevolution with its host

Knowledge of a species’ population genetic structure can provide insight into fundamental ecological and evolutionary processes including gene flow, genetic drift and adaptive evolution. Such inference is of particular importance for parasites, as an understanding of their population structure can illuminate epidemiological and coevolutionary dynamics. Here, we describe the population genetic structure of the bacterium Pasteuria ramosa, a parasite that infects planktonic crustaceans of the genus Daphnia. This system has become a model for investigations of host–parasite interactions and represents an example of coevolution via negative frequency‐dependent selection (aka “Red Queen” dynamics). To sample P. ramosa, we experimentally infected a panel of Daphnia hosts with natural spore banks from the sediments of 25 ponds throughout much of the species range in Europe and western Asia. Using 12 polymorphic variable number tandem repeat loci (VNTR loci), we identified substantial genetic diversity, both within and among localities, that was structured geographically among ponds. Genetic diversity was also structured among host genotypes within ponds, although this pattern varied by locality, with P. ramosa at some localities partitioned into distinct host‐specific lineages, and other localities where recombination had shuffled genetic variation among different infection phenotypes. Across the sample range, there was a pattern of isolation by distance, and principal components analysis coupled with Procrustes rotation identified congruence between patterns of genetic variation and geography. Our findings support the hypothesis that Pasteuria is an endemic parasite coevolving closely with its host. These results provide important context for previous studies of this model system and inform hypotheses for future research.     

Antagonistic coevolution with parasites maintains host genetic diversity: an experimental test

Genetic variation in natural populations is a prime prerequisite allowing populations to respond to selection, but is under constant threat from forces that tend to reduce it, such as genetic drift and many types of selection. Haldane emphasized the potential importance of parasites as a driving force of genetic diversity. His theory has been taken for granted ever since, but despite numerous studies showing correlations between genetic diversity and parasitism, Haldane''s hypothesis has rarely been tested experimentally for unambiguous support. We experimentally staged antagonistic coevolution between the host Tribolium castaneum and its natural microsporidian parasite, Nosema whitei, to test for the relative importance of two separate evolutionary forces (drift and parasite-induced selection) on the maintenance of genetic variation. Our results demonstrate that coevolution with parasites indeed counteracts drift as coevolving populations had significantly higher levels of heterozygosity and allelic diversity. Genetic drift remained a strong force, strongly reducing genetic variation and increasing genetic differentiation in small populations. To our surprise, differentiation between the evolving populations was smaller when they coevolved with parasites, suggesting parallel balancing selection. Hence, our results experimentally vindicate Haldane''s original hypothesis 60 years after its conception.     

An epidemiological model of host–parasite coevolution and sex

The Red Queen hypothesis posits a promising way to explain the widespread existence of sexual reproduction despite the cost of producing males. The essence of the hypothesis is that coevolutionary interactions between hosts and parasites select for the genetic diversification of offspring via cross‐fertilization. Here, I relax a common assumption of many Red Queen models that each host is exposed to one parasite. Instead, I assume that the number of propagules encountered by each host depends on the number of infected hosts in the previous generation, which leads to additional complexities. The results suggest that epidemiological feedbacks, combined with frequency‐dependent selection, could lead to the long‐term persistence of sex under biologically reasonable conditions.     

The maintenance of sex: host–parasite coevolution with density‐dependent virulence

Why don’t asexual females replace sexual females in most natural populations of eukaryotes? One promising explanation is that parasites could counter the reproductive advantages of asexual reproduction by exerting frequency‐dependent selection against common clones (the Red Queen hypothesis). One apparent limitation of the Red Queen theory, however, is that parasites would seem to be required by theory to be highly virulent. In the present study, I present a population‐dynamic view of competition between sexual females and asexual females that interact with co‐evolving parasites. The results show that asexual populations have higher carrying capacities, and more unstable population dynamics, than sexual populations. The results also suggest that the spread of a clone into a sexual population could increase the effective parasite virulence as population density increases. This combination of parasite‐mediated frequency‐dependent selection, and density‐dependent virulence, could lead to the coexistence of sexual and asexual reproductive strategies and the long‐term persistence of sex.     

Host‐parasite coevolution can promote the evolution of seed banking as a bet‐hedging strategy

Seed (egg) banking is a common bet‐hedging strategy maximizing the fitness of organisms facing environmental unpredictability by the delayed emergence of offspring. Yet, this condition often requires fast and drastic stochastic shifts between good and bad years. We hypothesize that the host seed banking strategy can evolve in response to coevolution with parasites because the coevolutionary cycles promote a gradually changing environment over longer times than seed persistence. We study the evolution of host germination fraction as a quantitative trait using both pairwise competition and multiple mutant competition methods, while the germination locus can be genetically linked or unlinked with the host locus under coevolution. In a gene‐for‐gene model of coevolution, hosts evolve a seed bank strategy under unstable coevolutionary cycles promoted by moderate to high costs of resistance or strong disease severity. Moreover, when assuming genetic linkage between coevolving and germination loci, the resistant genotype always evolves seed banking in contrast to susceptible hosts. Under a matching‐allele interaction, both hosts’ genotypes exhibit the same seed banking strategy irrespective of the genetic linkage between loci. We suggest host–parasite coevolution as an additional hypothesis for the evolution of seed banking as a temporal bet‐hedging strategy.     

Host–parasite coevolution: Partitioning the effects of natural selection and environmental change using coupled Price equations

George Price showed how the effects of natural selection and environmental change could be mathematically partitioned. This partitioning may be especially useful for understanding host–parasite coevolution, where each species represents the environment for the other species. Here, we use coupled Price equations to study this kind of antagonistic coevolution. We made the common assumption that parasites must genetically match their host''s genotype to avoid detection by the host''s self/nonself recognition system, but we allowed for the possibility that non‐matching parasites have some fitness. Our results show how natural selection on one species results in environmental change for the other species. Numerical iterations of the model show that these environmental changes can periodically exceed the changes in mean fitness due to natural selection, as suggested by R.A. Fisher. Taken together, the results give an algebraic dissection of the eco‐evolutionary feedbacks created during host–parasite coevolution.     

Sex differences in host defence interfere with parasite‐mediated selection for outcrossing during host–parasite coevolution

The Red Queen hypothesis proposes that coevolving parasites select for outcrossing in the host. Outcrossing relies on males, which often show lower immune investment due to, for example, sexual selection. Here, we demonstrate that such sex differences in immunity interfere with parasite‐mediated selection for outcrossing. Two independent coevolution experiments with Caenorhabditis elegans and its microparasite Bacillus thuringiensis produced decreased yet stable frequencies of outcrossing male hosts. A subsequent systematic analysis verified that male C. elegans suffered from a direct selective disadvantage under parasite pressure (i.e. lower resistance, decreased sexual activity, increased escape behaviour), which can reduce outcrossing and thus male frequencies. At the same time, males offered an indirect selective benefit, because male‐mediated outcrossing increased offspring resistance, thus favouring male persistence in the evolving populations. As sex differences in immunity are widespread, such interference of opposing selective constraints is likely of central importance during host adaptation to a coevolving parasite.     

Specific interactions between host and parasite genotypes do not act as a constraint on the evolution of antiviral resistance in Drosophila

Genetic correlations between parasite resistance and other traits can act as an evolutionary constraint and prevent a population from evolving increased resistance. For example, previous studies have found negative genetic correlations between host resistance and life-history traits. In invertebrates, the level of resistance often depends on the combination of the host and parasite genotypes, and in this study, we have investigated whether such specific resistance also acts as an evolutionary constraint. We measured the resistance of different genotypes of the fruit fly Drosophila melanogaster to different genotypes of a naturally occurring pathogen, the sigma virus. Using a multitrait analysis, we examine whether genetic covariances alter the potential to select for general resistance against all of the different viral genotypes. We found large amounts of heritable variation in resistance, and evidence for specific interactions between host and parasite, but these interactions resulted in little constraint on Drosophila evolving greater resistance.     

Crowding and disease: effects of host density on response to infection in a butterfly–parasite interaction

Abstract. 1. Hosts experiencing frequent variation in density are thought to benefit from allocating more resources to parasite defence when density is high (‘density‐dependent prophylaxis’). However, high density conditions can increase intra‐specific competition and induce physiological stress, hence increasing host susceptibility to infection (‘crowding‐stress hypothesis’). 2. We studied monarch butterflies (Danaus plexippus) and quantified the effects of larval rearing density on susceptibility to the protozoan parasite Ophryocystis elektroscirrha. Larvae were inoculated with parasite spores and reared at three density treatments: low, moderate, and high. We examined the effects of larval density on parasite loads, host survival, development rates, body size, and wing melanism. 3. Results showed an increase in infection probability with greater larval density. Monarchs in the moderate and high density treatments also suffered the greatest negative effects of parasite infection on body size, development rate, and adult longevity. 4. We observed greater body sizes and shorter development times for monarchs reared at moderate densities, and this was true for both unparasitised and parasite‐treated monarchs. We hypothesise that this effect could result from greater larval feeding rates at moderate densities, combined with greater physiological stress at the highest densities. 5. Although monarch larvae are assumed to occur at very low densities in the wild, an analysis of continent‐wide monarch larval abundance data showed that larval densities can reach high levels in year‐round resident populations and during the late phase of the breeding season. Treatment levels used in our experiment captured ecologically‐relevant variation in larval density observed in the wild.     

Plant and insect genetic variation mediate the impact of arbuscular mycorrhizal fungi on a natural plant–herbivore interaction

1. While both arbuscular mycorrhizal (AM) fungi and plant and insect genotype are well known to influence plant and herbivore growth and performance, information is lacking on how these factors jointly influence the relationship between plants and their natural herbivores. 2. The aim of the present study was to investigate how a natural community of arbuscular mycorrhizal fungi affects the growth of the perennial herb Plantago lanceolata L. (Plantaginaceae), as well as its interaction with the Glanville fritillary butterfly [Melitaea cinxia L. (Nymphalidae)]. For this, a multifactorial experiment was conducted using plant lines originating from multiple plant populations in the Åland Islands, Finland, grown either with or without mycorrhizal fungi. For a subset of plant lines, the impact of mycorrhizal inoculation, plant line, and larval family on the performance of M. cinxia larvae were tested. 3. Arbuscular mycorrhizal inoculation did not have a consistently positive or negative impact on plant growth or herbivore performance. Instead, plant genetic variation mediated the impact of arbuscular mycorrhizal fungi on plant growth, and both plant genetic variation and herbivore genetic variation mediated the response of the herbivore. For both the plant and insect, the impact of the arbuscular mycorrhizal community ranged from mutualistic to antagonistic. Overall, the present findings illustrate that genetic variation in response to mycorrhizal fungi may play a key role in the ecology and evolution of plant–insect interactions.     

Virulence and age at reproduction: new insights into host–parasite coevolution

We consider an explicit mutation–selection process to investigate the dynamics underlying the coevolution of parasite’s virulence and host’s prereproductive life span in a system with discrete generations. Conforming with earlier models, our model predicts that virulence generally increases with natural mortality of the host, and that a moderate increase in virulence selects for lower ages at reproduction. However, the epidemiological feedback in our model also gives rise to unusual and unexpected patterns. In particular, if virulence is sufficiently high the model can lead to a bifurcation pattern, where two strategies coexist in the host population. The first is to develop rapidly to reproduce before being infected. Individuals following this strategy suffer, however, from reduced fecundity. The second strategy is to develop much more slowly. Because of the high virulence, the effective period of transmission is short, so that a few slowly developing individuals escape infection. These individuals, although choosing a risky strategy, benefit from high fecundity.     

Mistletoes Play Different Roles in a Modular Host–Parasite Network

Antagonistic interactions between host plants and mistletoes often form complex networks of interacting species. Adequate characterization of network organization requires a combination of qualitative and quantitative data. Therefore, we assessed the distribution of interactions between mistletoes and hosts in the Brazilian Pantanal and characterized the network structure in relation to nestedness and modularity. Interactions were highly asymmetric, with mistletoes presenting low host specificity (i.e., weak dependence) and with hosts being highly susceptible to mistletoe‐specific infections. We found a non‐nested and modular pattern of interactions, wherein each mistletoe species interacted with a particular set of host species. Psittacanthus spp. infected more species and individuals and also caused a high number of infections per individual, whereas the other mistletoes showed a more specialized pattern of infection. For this reason, Psittacanthus spp. were regarded as module hubs while the other mistletoe species showed a peripheral role. We hypothesize that this pattern is primarily the result of different seed dispersal systems. Although all mistletoe species in our study are bird dispersed, the frugivorous assemblage of Psittacanthus spp. is composed of a larger suite of birds, whereas Phoradendron are mainly dispersed by Euphonia species. The larger assemblage of bird species dispersing Psittacanthus seeds may also increase the number of hosts colonized and, consequently, its dominance in the study area. Nevertheless, other restrictions on the interactions among species, such as the differential capacity of mistletoe infections, defense strategies of hosts and habitat types, can also generate or enhance the observed pattern. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

Food stoichiometry affects the outcome of Daphnia–parasite interaction

Phosphorus (P) is an essential nutrient for growth in consumers. P‐limitation and parasite infection comprise one of the most common stressor pairs consumers confront in nature. We conducted a life‐table study using a Daphnia–microsporidian parasite model, feeding uninfected or infected Daphnia with either P‐sufficient or P‐limited algae, and assessed the impact of the two stressors on life‐history traits of the host. Both infection and P‐limitation negatively affected some life‐history traits tested. However, under P‐limitation, infected animals had higher juvenile growth rate as compared with uninfected animals. All P‐limited individuals died before maturation, regardless of infection. The numbers of spore clusters of the microsporidian parasite did not differ in P‐limited or P‐sufficient hosts. P‐limitation, but not infection, decreased body phosphorus content and ingestion rates of Daphnia tested in separate experiments. As parasite spore production did not suffer even under extreme P‐limitation, our results suggest that parasite was less limited by P than the host. We discuss possible interpretations concerning the stoichiometrical demands of parasite and suggest that our results are explained by parasite‐driven changes in carbon (C) allocation of the hosts. We conclude that the impact of nutrient starvation and parasite infection on consumers depends not only on the stoichiometric demands of host but also those of the parasite.     

Experimental parasite infection reveals costs and benefits of paternal effects

Forces shaping an individual's phenotype are complex and include transgenerational effects. Despite low investment into reproduction, a father's environment and phenotype can shape its offspring's phenotype. Whether and when such paternal effects are adaptive, however, remains elusive. Using three‐spined sticklebacks in controlled infection experiments, we show that sperm deficiencies in exposed males compared to their unexposed brothers functionally translated into reduced reproductive success in sperm competition trials. In non‐competitive fertilisations, offspring of exposed males suffered significant costs of reduced hatching success and survival but they reached a higher body condition than their counterparts from unexposed fathers after experimental infection. Interestingly, those benefits of paternal infection did not result from increased resistance but from increased tolerance to the parasite. Altogether, these results demonstrate that parasite resistance and tolerance are shaped by processes involving both genetic and non‐genetic inheritance and suggest a context‐dependent adaptive value of paternal effects.     

Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs

Host organisms are believed to evolve defense mechanisms (i.e., resistance and/or tolerance) under selective pressures exerted by natural enemies. A prerequisite for the evolution of resistance and tolerance is the existence of genetic variation in these traits for natural selection to act. However, selection for resistance and/or tolerance may be constrained by negative genetic correlations with other traits that affect host fitness. We studied genetic variation in resistance and tolerance against parasitic infection and the potential fitness costs associated with these traits using a novel study system, namely the interaction between a flowering plant and a parasitic plant. In this system, parasitic infection has significant negative effects on host growth and reproduction and may thus act as a selective agent. We conducted a greenhouse experiment in which we grew host plants, Urtica dioica, that originated from a single natural population and represented 20 maternal families either uninfected or infected with the holoparasitic dodder, Cuscuta europaea. that originated from the same site. We calculated correlations among resistance, tolerance, and host performance to test for costs of resistance and tolerance. We measured resistance as parasite performance (quantitative resistance) and tolerance as the slopes of regressions relating the vegetative and reproductive biomass of host plants to damage level (measured as parasite biomass). We observed significant differences among host families in parasite resistance and in parasite tolerance in terms of reproductive biomass, a result that suggests genetic variation in these traits. Furthermore, we found differences in resistance and tolerance between female and male host plants. In addition, the correlations indicate costs of resistance in terms of host growth and reproduction and costs of tolerance in terms of host reproduction. Our results thus indicate that host tolerance and resistance can evolve as a response to infection by a parasitic plant and that costs of resistance and tolerance may be one factor maintaining genetic variation in these traits.     

Geographic variation in the evolution and coevolution of a tritrophic interaction

The geographic mosaic theory of coevolution predicts that geographic variation in species interactions will lead to differing selective pressures on interacting species, producing geographic variation in the traits of interacting species (Thompson 2005). We supported this hypothesis in a study of the geographic variation in the interactions among Eurosta solidaginis and its natural enemies. Eurosta solidaginis is a fly (Diptera: Tephritidae) that induces galls on subspecies of tall goldenrod, Solidago altissima altissima and S. a. gilvocanescens. We measured selection on E. solidaginis gall size and shape in the prairie and forest biomes in Minnesota and North Dakota over an 11-year period. Galls were larger and more spherical in the prairie than in the forest. We supported the hypothesis that the divergence in gall morphology in the two biomes is due to different selection regimes exerted by natural enemies of E. solidaginis. Each natural enemy exerted similar selection on gall diameter in both biomes, but differences in the frequency of natural enemy attack created strong differences in overall selection between the prairie and forest. Bird predation increased with gall diameter, creating selection for smaller-diameter galls. A parasitic wasp, Eurytoma gigantea, and Mordellistena convicta, an inquiline beetle, both caused higher E. solidaginis mortality in smaller galls, exerting selection for increased gall diameter. In the forest there was stabilizing selection on gall diameter due to a combination of bird predation on larvae in large galls, and M. convicta- and E. gigantea-induced mortality on larvae in small galls. In the prairie there was directional selection for larger galls due to M. convicta and E. gigantea mortality on larvae in small galls. Mordellistena convicta-induced mortality was consistently higher in the prairie than in the forest, whereas there was no significant difference in E. gigantea-induced mortality between biomes. Bird predation was nonexistent in the prairie so the selection against large galls found in the forest was absent. We supported the hypothesis that natural enemies of E. solidaginis exerted selection for spherical galls in both biomes. In the prairie M. convicta exerts stabilizing selection to maintain spherical galls. In the forest there was directional selection for more spherical galls. Eurytoma gigantea exerted selection on gall shape in the forest in a complex manner that varied among years. We also supported the hypothesis that E. gigantea is coevolving with E. solidaginis. The parasitoid had significantly longer ovipositors in the prairie than in the forest, indicating the possibility that it has evolved in response to selection to reach larvae in the larger-diameter prairie galls.     

Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae

Due to the close association between parasites and their hosts, many ‘generalist’ parasites have a high potential to become specialized on different host species. We investigated this hypothesis for a common ectoparasite of seabirds, the tick Ixodes uriae that is often found in mixed host sites. We examined patterns of neutral genetic variation between ticks collected from Black‐legged kittiwakes (Rissa tridactyla) and Atlantic puffins (Fratercula arctica) in sympatry. To control for a potential distance effect, values were compared to differences among ticks from the same host in nearby monospecific sites. As predicted, there was higher genetic differentiation between ticks from different sympatric host species than between ticks from nearby allopatric populations of the same host species. Patterns suggesting isolation by distance were found among tick populations of each host group, but no such patterns existed between tick populations of different hosts. Overall, results suggest that host‐related selection pressures have led to the specialization of I. uriae and that host race formation may be an important diversifying mechanism in parasites.     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Red Queen dancing in the lek: effects of mating skew on host–parasite interactions

The RQH (Red Queen hypothesis), which argues that hosts need to be continuously finding new ways to avoid parasites that are able to infect common host genotypes, has been at the center of discussions on the maintenance of sex. This is because diversity is favored under the host–parasite coevolution based on negative frequency‐dependent selection, and sexual reproduction is a mechanism that generates genetic diversity in the host population. Together with parasite infections, sexual organisms are usually under sexual selection, which leads to mating skew or mating success biased toward males with a particular phenotype. Thus, strong mating skew would affect genetic variance in a population and should affect the benefit of the RQH. However, most models have investigated the RQH under a random mating system and not under mating skew. In this study, I show that sexual selection and the resultant mating skew may increase parasite load in the hosts. An IBM (individual‐based model), which included host–parasite interactions and sexual selection among hosts, demonstrates that mating skew influenced parasite infection in the hosts under various conditions. Moreover, the IBM showed that the mating skew evolves easily in cases of male–male competition and female mate choice, even though it imposes an increased risk of parasite infection on the hosts. These findings indicated that whether the RQH favored sexual reproduction depended on the condition of mating skew. That is, consideration of the host mating system would provide further understanding of conditions in which the RQH favors sexual reproduction in real organisms.