THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE POPULATION STRUCTURES FOR A SNAIL AND ITS TREMATODE PARASITE

Gene flow and the genetic structure of host and parasite populations are critical to the coevolutionary process, including the conditions under which antagonistic coevolution favors sexual reproduction. Here we compare the genetic structures of different populations of a freshwater New Zealand snail (Potamopyrgus antipodarum) with its trematode parasite (Microphallus sp.) using allozyme frequency data. Allozyme variation among snail populations was found to be highly structured among lakes; but for the parasite there was little allozyme structure among lake populations, suggesting much higher levels of parasite gene flow. The overall pattern of variation was confirmed with principal component analysis, which also showed that the organization of genetic differentiation for the snail (but not the parasite) was strongly related to the geographic arrangement of lakes. Some snail populations from different sides of the Alps near mountain passes were more similar to each other than to other snail populations on the same side of the Alps. Furthermore, genetic distances among parasite populations were correlated with the genetic distances among host populations, and genetic distances among both host and parasite populations were correlated with “stepping-stone” distances among lakes. Hence, the host snail and its trematode parasite seem to be dispersing to adjacent lakes in a stepping-stone fashion, although parasite dispersal among lakes is clearly greater. High parasite gene flow should help to continuously reintroduce genetic diversity within local populations where strong selection might otherwise isolate “host races.” Parasite gene flow can thereby facilitate the coevolutionary (Red Queen) dynamics that confer an advantage to sexual reproduction by restoring lost genetic variation.     

Clonal diversity driven by parasitism in a freshwater snail

One explanation for the widespread abundance of sexual reproduction is the advantage that genetically diverse sexual lineages have under strong pressure from virulent coevolving parasites. Such parasites are believed to track common asexual host genotypes, resulting in negative frequency‐dependent selection that counterbalances the population growth‐rate advantage of asexuals in comparison with sexuals. In the face of genetically diverse asexual lineages, this advantage of sexual reproduction might be eroded, and instead sexual populations would be replaced by diverse assemblages of clonal lineages. We investigated whether parasite‐mediated selection promotes clonal diversity in 22 natural populations of the freshwater snail Melanoides tuberculata. We found that infection prevalence explains the observed variation in the clonal diversity of M. tuberculata populations, whereas no such relationship was found between infection prevalence and male frequency. Clonal diversity and male frequency were independent of snail population density. Incorporating ecological factors such as presence/absence of fish, habitat geography and habitat type did not improve the predictive power of regression models. Approximately 11% of the clonal snail genotypes were shared among 2–4 populations, creating a web of 17 interconnected populations. Taken together, our study suggests that parasite‐mediated selection coupled with host dispersal ecology promotes clonal diversity. This, in return, may erode the advantage of sexual reproduction in M. tuberculata populations.     

Parasite-induced parthenogenesis in a freshwater snail: stable,persistent patterns of parasitism

Summary The role of parasites in the evolution of host reproductive modes has gained renewed interest in evolutionary ecology. It was previously argued that obligate parthenogenesis (all-female reproduction) arose in a freshwater snail, Campeloma decisum, as a consequence of severe sperm limitation caused by an unencysted trematode, Leucochloridiomorpha constantiae. In the present study, certain conditions are examined for parasitic castration to account for the maintenance of parthenogenesis: the spatial patterns of the prevalence and intensity of infection on a broad geographical scale and its relationship to host genotype; the recovery from infection after isolation from sources of infection; age-related patterns of infections; and the effects of L. constantiae on snail fecundity.In contrast to the common pattern of the aggregated distribution of parasites within host populations, many snail populations with high prevalence and intensity of infection have non-aggregated parasite distributions. Clonal genotype of the host explained little of the variation in intensity and prevalence of infection by the parasite. Female snails maintained similar prevalence and intensity of infection after isolation, and individuals accumulated parasites throughout their lifespan, both of which suggest there is no effective immune response to infection by L. constantiae. Snail fecundity is not significantly influenced by the intensity of infection. These results suggest that L. constantiae may have represented a strong selective force against males during the initial introduction of this parasite into sexual snail populations because of the persistent nature of infection.     

Density-dependent effects in a parasitic nematode,Elaphostrongylus rangiferi,in the snnail intermediate host

Summary Density-dependent effects in Elaphostrongylus rangiferi, a parasitic nematode in the CNS and muscular system of reindeer, were studied in a laboratory population of the snail intermediate host, Arianta arbustorum. The rates in parasite growth, development and mortality were all affected by parasite density. The effects on growth and development were, however, much more marked, than the effect on mortality.All density-dependent rates were intensified by decreasing snail size, and by snail starvation. The snail host showed marked tissue reactions against infection, and the intensity of these reactions increased with increasing parasite density. The mechanism behind the observed density-dependent rates is discussed, and is tentatively concluded to be competition for nutritive substances in the host tissue.The importance of a density-dependent developmental rate in natural populations of this parasite is discussed, and it is hypothesized that this effect may counteract the strong temperature-dependent developmental rate of E. rangiferi In a more general context it is pointed out that density-dependent developmental rates, although common amongst animal populations, has been neglected in models of population dynamics. Developmental rates are usually represented by a constant time lag in such models, but should be treated as a density-dependent variable.     

Genetic variation in sexual and clonal lineages of a freshwater snail

Sexual reproduction within natural populations of most plants and animals continues to remain an enigma in evolutionary biology. That the enigma persists is not for lack of testable hypotheses but rather because of the lack of suitable study systems in which sexual and asexual females coexist. Here we review our studies on one such organism, the freshwater snail Potamopyrgus antipodarum (Gray). We also present new data that bear on hypotheses for the maintenance of sex and its relationship to clonal diversity. We have found that sexual populations of the snail are composed of diploid females and males, while clonal populations are composed of a high diversity of triploid apomictic females. Sexual and asexual individuals coexist in stable frequencies in many ‘mixed’ populations; genetic data indicate that clones from these mixed populations originated from the local population of sexual individuals without interspecific hybridization. Field data show that clonal and sexual snails have completely overlapping life histories, but individual clonal genotypes are less variable than individuals from the sympatric sexual population. Field data also show segregation of clones among depth‐specific habitat zones within a lake, but clonal diversity remains high even within habitats. A new laboratory experiment revealed extensive clonal variation in reproductive rate, a result which suggests that clonal diversity would be low in nature without some form of frequency‐dependent selection. New results from a long‐term field study of a natural, asexual population reveal that clonal diversity remained nearly constant over a 10‐year period. Nonetheless, clonal turnover occurs, and it occurs in a manner that is consistent with parasite‐mediated, frequency‐dependent selection. Reciprocal cross‐infection experiments have further shown that parasites are more infective to sympatric host snails than to allopatric snails, and that they are also more infective to common clones than rare clones within asexual host populations. Hence we suggest that sexual reproduction in these snails may be maintained, at least in part, by locally adapted parasites. Parasite‐mediated selection possibly also contributes to the maintenance of local clonal diversity within habitats, while clonal selection may be responsible for the distribution of clones among habitats. © 2003 The Linnean Society of London. Biological Journal of the Linnean Society 2003, 79 , 165–181.     

Genetic structure and host–parasite co‐divergence: evidence for trait‐specific local adaptation

Host–parasite co‐evolution can lead to genetic differentiation among isolated host–parasite populations and local adaptation between parasites and their hosts. However, tests of local adaptation rarely consider multiple fitness‐related traits although focus on a single component of fitness can be misleading. Here, we concomitantly examined genetic structure and co‐divergence patterns of the trematode Coitocaecum parvum and its crustacean host Paracalliope fluviatilis among isolated populations using the mitochondrial cytochrome oxidase I gene (COI). We then performed experimental cross‐infections between two genetically divergent host–parasite populations. Both hosts and parasites displayed genetic differentiation among populations, although genetic structure was less pronounced in the parasite. Data also supported a co‐divergence scenario between C. parvum and P. fluviatilis potentially related to local co‐adaptation. Results from cross‐infections indicated that some parasite lineages seemed to be locally adapted to their sympatric (home) hosts in which they achieved higher infection and survival rates than in allopatric (away) amphipods. However, local, intrinsic host and parasite characteristics (host behavioural or immunological resistance to infections, parasite infectivity or growth rate) also influenced patterns of host–parasite interactions. For example, overall host vulnerability to C. parvum varied between populations, regardless of parasite origin (local vs. foreign), potentially swamping apparent local co‐adaptation effects. Furthermore, local adaptation effects seemed trait specific; different components of parasite fitness (infection and survival rates, growth) responded differently to cross‐infections. Overall, data show that genetic differentiation is not inevitably coupled with local adaptation, and that the latter must be interpreted with caution in a multi‐trait context.     

The scaling of parasite biomass with host biomass in lake ecosystems: are parasites limited by host resources?

The standing crop biomass of different populations or trophic levels reflects patterns of energy flow through an ecosystem. The contribution of parasites to total biomass is often considered negligible; recent evidence suggests otherwise, although it comes from a narrow range of natural systems. Quantifying how local parasite biomass, whether that of a single species or an assemblage of species sharing the same host, varies across localities with host population biomass, is critical to determine what constrains parasite populations. We use an extensive dataset on all free‐living and parasitic metazoan species from multiple sites in New Zealand lakes to measure parasite biomass and test how it covaries with host biomass. In all lakes, trematodes had the highest combined biomass among parasite taxa, ranging from about 0.01 to 0.25 g m^?2, surpassing the biomass of minor free‐living taxa. Unlike findings from other studies, the life stage contributing the most to total trematode biomass was the metacercarial stage in the second intermediate host, and not sporocysts or rediae within snail first intermediate hosts, possibly due to low prevalence and small snail sizes. For populations of single parasite species, we found no relationship between host and parasite biomass for either juvenile or adult nematodes. In contrast, all life stages of trematodes had local biomasses that correlated positively with those of their hosts. For assemblages of parasite species sharing the same host, we found strong relationships between local host population biomass and the total biomass of parasites supported. In these host–parasite biomass relationships, the scaling factor (slope in log‐log space) suggests that parasites may not be making full use of available host resources. Host populations appear capable of supporting a little more parasite biomass, and may be open to expansion of existing parasites or invasion by new ones.     

Evaluating shell variation across different populations of a freshwater snail

The freshwater snail Potamopyrgus antipodarum has become a model system for studying invasion ecology, host–parasite coevolution, the maintenance of sexual reproduction and ecotoxicology. One understudied aspect of this snail is the variation in morphology within and among populations, which could provide insights into ecological differences across its native range. In this study of 17 New Zealand lake populations of P. antipodarum we used linear measurements and geometric morphometrics to compare several aspects of shell size and shape. We found that, except for those from Lake Te Anau, most lake populations of P. antipodarum differ slightly in shape, but differ significantly in size and in the presence of spines, where larger and spinier snails are found in deeper regions. These striking distinctions in size and shell armature, but not in shape, suggest that the various components of form are under different selective regimes. Snails from Lake Te Anau are different in both shape and size, implying that this population is diverging from the rest of the species in multiple ways, making it an interesting study population for further research.     

LOCAL MALADAPTATION IN THE ANTHER-SMUT FUNGUS MICROBOTRYUM VIOLACEUM TO ITS HOST PLANT SILENE LATIFOLIA: EVIDENCE FROM A CROSS-INOCULATION EXPERIMENT

Conventional wisdom holds that parasites evolve more rapidly than their hosts and are therefore locally adapted, that is, better at exploiting sympatric than allopatric hosts. We studied local adaptation in the insect-transmitted fungal pathogen Microbotryum violaceum and its host plant Silene latifolia. Infection success was tested in sympatric (local) and allopatric (foreign) combinations of pathogen and host from 14 natural populations from a metapopulation. Seedlings from up to 10 seed families from each population were exposed to sporidial suspensions from each of four fungal strains derived from the same population, from a near-by population (< 10 km distance), and from two populations at an intermediate (< 30 km) and remote (< 170 km) distance, respectively. We obtained significant pathogen X plant interactions in infection success (proportion of diseased plants) at both fungal population and strain level. There was an overall pattern of local maladaptation of this pathogen: average fungal infection success was significantly lower on sympatric hosts (mean proportion of diseased plants = 0.32 ± 0.03 SE) than on allopatric hosts (0.40 ± 0.02). Five of the 14 fungal populations showed no strong reduction in infection success on sympatric hosts, and three even tended to perform better on sympatric hosts. This pattern is consistent with models of time-lagged cycles predicting patterns of local adaptation in host-parasite systems to emerge only on average. Several factors may restrict the evolutionary potential of this pathogen relative to that of its host. First, a predominantly selfing breeding system may limit its ability to generate new virulence types by sexual recombination, whereas the obligately outcrossing host 5. latifolia may profit from rearrangement of resistance alleles by random mating. Second, populations often harbor only a few infected individuals, so virulence variation may be further reduced by drift. Third, migration rates among host plant populations are much higher than among pathogen populations, possibly because pollinators prefer healthy over diseased plants. Migration among partly isolated populations may therefore introduce novel host plant resistance variants more often than novel parasite virulence variants. That migration contributes to the coevolutionary dynamics in this system is supported by the geographic pattern of infectivity. Infection success increased over the first 10–km range of host-pathogen population distances, which is likely the natural range of gene exchange.     

Mate choice, frequency dependence, and the maintenance of resistance to parasitism in a simultaneous hermaphrodite

Biomphalaria glabrata are simultaneous hermaphroditic freshwatersnails that act as intermediate hosts for the macroparasitictrematode Schistosoma mansoni, a causative agent of schistosomiasis.Heritability and strain-specificity of both snail resistanceand susceptibility to schistosome infection have been demonstrated,genetic variability for which is maintained, in part, throughtrade-offs between high fitness costs associated with infectionand those associated with resistance. However, despite sucha high cost of resistance and a low prevalence of infectionin natural snail populations, genes for resistance are maintainedwithin snail populations over successive generations, includingin the complete absence of parasite pressure in laboratory populations.This may be indicative of alternative benefits of resistancegenes, in addition to parasite defense, such as differentialmating success between genotypes. Here we examined the mateand gender choice of snails across a multi-factorial range ofpotential partner combinations. These included host-resistanceor susceptibility genotype, host genotype frequency within thepopulation, current parasite infection status, and parasitegenotype. We demonstrate recognition and discrimination by hostsnails depending on host and/or parasite genotype for each ofthese factors. In particular, our results suggest that a raremating advantage to resistant genotypes may be a potential explanationfor the maintenance of highly costly resistance genes withinintermediate host populations under conditions of low or zeroparasite pressure.     

VARIATION BETWEEN POPULATIONS AND LOCAL ADAPTATION IN ACANTHOCEPHALAN‐INDUCED PARASITE MANIPULATION

Many trophically transmitted parasites manipulate their intermediate host phenotype, resulting in higher transmission to the final host. However, it is not known if manipulation is a fixed adaptation of the parasite or a dynamic process upon which selection still acts. In particular, local adaptation has never been tested in manipulating parasites. In this study, using experimental infections between six populations of the acanthocephalan parasite Pomphorhynchus laevis and its amphipod host Gammarus pulex, we investigated whether a manipulative parasite may be locally adapted to its host. We compared adaptation patterns for infectivity and manipulative ability. We first found a negative effect of all parasite infections on host survival. Both parasite and host origins influenced infection success. We found a tendency for higher infectivity in sympatric versus allopatric combinations, but detailed analyses revealed significant differences for two populations only. Conversely, no pattern of local adaptation was found for behavioral manipulation, but manipulation ability varied among parasite origins. This suggests that parasites may adapt their investment in behavioral manipulation according to some of their host's characteristics. In addition, all naturally infected host populations were less sensitive to parasite manipulation compared to a naive host population, suggesting that hosts may evolve a general resistance to manipulation.     

GENETIC VARIATION IN ASTERIONELLA FORMOSA (BACILLARIOPHYCEAE): IS IT LINKED TO FREQUENT EPIDEMICS OF HOST‐SPECIFIC PARASITIC FUNGI?1

Understanding of the genetic basis for susceptibility and resistance is still lacking for most aquatic host–parasite systems, for instance, for phytoplankton and their fungal parasites. Fungal parasites can have significant effects on phytoplankton populations, mainly through their ability to decimate algal host populations during epidemics. We used random amplified polymorphic DNA (RAPD) and amplified fragment length polymorphism (AFLP) analysis to study levels of genetic variation within a population of the freshwater diatom Asterionella formosa Hassall in relation to parasitism by the obligate, host‐specific, fungal parasite Zygorhizidium planktonicum Canter. The level of genetic variation within the A. formosa population in Lake Maarsseveen, The Netherlands was found to be high despite the presumed absence or very low frequency of sexual reproduction in this species, the limited gene flow, and the severity of parasite attack that would purge the population from susceptible genotypes. RAPD analysis revealed four distinct banding patterns, with 3 of 21 markers (14%) being polymorphic. In AFLP analysis, every single isolate of A. formosa showed a unique banding pattern, and 120 of the 210 AFLP markers (57%) were found to be polymorphic. Furthermore, character compatibility analysis revealed that sexual reproduction may be one of the mechanisms that generates and maintains genetic variation in the A. formosa population in Lake Maarsseveen. The presence of genetic variation in A. formosa was reflected in infection experiments, which showed that genetically different A. formosa strains differed in their susceptibility to various Z. planktonicum strains and that parasite strains differed in their ability to infect particular host strains.     

Evolutionary aspects of the metapopulation dynamics of Biomphalaria pfeifferi,the intermediate host of Schistosoma mansoni

Combining genetic and demographic data is a powerful approach to study adaptation process and evolutionary forces acting in natural populations. We focus on the freshwater snail Biomphalaria pfeifferi, the intermediate host of Schistosoma mansoni. Twenty‐one populations sampled in the south of Madagascar were genotyped at six microsatellite loci. Demographic parameters and parasitic prevalence were estimated monthly over the year preceding the genetic sampling. Our results indicate that populations experience recurrent bottlenecks and size fluctuations, which strongly depresses the genetic diversity within population. The recolonization of depleted sites involves genetically differentiated immigrants. We detected frequent migration events along rivers and rare migration events between watersheds. This explains the high level of differentiation observed among populations. The negative regression observed between the prevalence of S. mansoni and the genetic diversity of B. pfeifferi populations indicates that host consanguinity may affect prevalence through the genetic mechanisms involved in resistance. Coevolutionary outcomes are also influenced by the relative migration rates of snails and flukes, but the parasite local adaptation may be prevented by rare long distance dispersal in snails and the phylogeographical patterns of colonization of both hosts and snails.     

The hemolymph of Biomphalaria snail vectors of schistosomiasis supports a diverse microbiome

The microbiome - the microorganism community that is found on or within an organism's body - is increasingly recognized to shape many aspects of its host biology and is a key determinant of health and disease. Microbiomes modulate the capacity of insect disease vectors (mosquitoes, tsetse flies, sandflies) to transmit parasites and disease. We investigate the diversity and abundance of microorganisms within the hemolymph (i.e. blood) of Biomphalaria snails, the intermediate host for Schistosoma mansoni, using Illumina MiSeq sequencing of the bacterial 16S V4 rDNA. We sampled hemolymph from five snails from six different laboratory populations of B. glabrata and one population of B. alexandrina. We observed 279.84 ± 0.79 amplicon sequence variants per snail. There were significant differences in microbiome composition at the level of individual snails, snail populations and species. Snail microbiomes were dominated by Proteobacteria and Bacteroidetes while water microbiomes from snail tank were dominated by Actinobacteria. We investigated the absolute bacterial load using qPCR: hemolymph samples contained 2784 ± 339 bacteria/μl. We speculate that the microbiome may represent a critical, but unexplored intermediary in the snail–schistosome interaction as hemolymph is in very close contact with the parasite at each step of its development.     

The genetic population structure of the ant Plagiolepis xene-implications for genetic vulnerability of obligate social parasites

Obligatory social parasites, such as ant species that need colonies of other ant species for reproduction, are rare and many of them are classified as vulnerable. This is especially the case with highly adapted permanent inquilines that are specialised on one or a few host species. Their rarity may be due to reduced dispersal abilities, as a result of reduced body size, altered wing morphology, and curtailed nuptial flight, eventually leading to inbreeding. Furthermore, the host populations may differ in their ability to resist the parasite, yet the conditions of successful parasite invasion are largely unknown. Here we investigated the population structure of the inquiline ant Plagiolepis xene and its host P. pygmaea, using microsatellite data. Genetic differentiation, inbreeding, the effective population size and nest kin structure were analysed. We found that populations of P. xene are established by a single or at most a few individuals, and that the populations were genetically highly differentiated. However, within individual host populations the parasite is able to maintain panmixia, although data on the host suggests that the local distribution of the parasite also follows patterns of substructuring in the host population. Altogether our results suggest that inquiline parasite populations are genetically highly vulnerable.     

Experimental evolution of local parasite maladaptation

Sign and magnitude of local adaptation in host–parasite systems may vary with ecological, epidemiological or genetic parameters. To investigate the role of host genetic background, we established long‐term experimental populations of different genotypes of the protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. We observed the evolution of an overall pattern of parasite local maladaptation for infectivity, indicating a general coevolutionary disadvantage of this parasite. Maladaptation extended to host populations with the same genetic background, similar to extending from the local to a higher regional level in natural populations. Patterns for virulence were qualitatively similar, but with less statistical support. A nonsignificant correlation with levels of (mal)adaptation for infectivity suggests independent evolution of these traits. Our results indicate similar (co)evolutionary trajectories in populations with different genetic backgrounds. Nonetheless, the correlated clines of genetic distance and parasite performance illustrate how genetic background can shape spatial gradients of local adaptation.     

Effect of starvation on parasite-induced mortality in a freshwater snail (Potamopyrgus antipodarum)

The level of host exploitation is expected, under theory, to be selected to maximise (subject to constraints) the lifetime reproductive success of the parasite. Here we studied the effect of two castrating trematode species on their intermediate snail host, Potamopyrgus antipodarum. One of the trematode species, Microphallus sp., encysts in the snail host and the encysted larvae “hatch” following ingestion of infected snails by birds. The other species, Notocotylus gippyensis, by contrast, releases swimming larvae; ingestion of the snail host is not required for, and does not aid, transmission to the final host. We isolated field-collected snails for 3 months in the laboratory, and followed the survival of infected and uninfected snails under two conditions: not fed and fed ad libitum. Mortality of the infected hosts was higher than mortality of the uninfected ones, but the response to starvation treatment was parasite species specific. N. gippyensis induced significantly higher mortality in starved snails than did Microphallus. Based on these results, we suggest that host exploitation by different species of trematodes may depend on the type of transmission. Encysting in the snail host may select for a reduced rate of host exploitation so as to increase the probability of transmission to the final host. Received: 29 July 1998 / Accepted: 1 February 1999     

TEMPORAL DYNAMICS OF OUTCROSSING AND HOST MORTALITY RATES IN HOST–PATHOGEN EXPERIMENTAL COEVOLUTION

Cross‐fertilization is predicted to facilitate the short‐term response and the long‐term persistence of host populations engaged in antagonistic coevolutionary interactions. Consistent with this idea, our previous work has shown that coevolving bacterial pathogens (Serratia marcescens) can drive obligately selfing hosts (Caenorhabditis elegans) to extinction, whereas the obligately outcrossing and partially outcrossing populations persisted. We focused the present study on the partially outcrossing (mixed mating) and obligately outcrossing hosts, and analyzed the changes in the host resistance/avoidance (and pathogen infectivity) over time. We found that host mortality rates increased in the mixed mating populations over the first 10 generations of coevolution when outcrossing rates were initially low. However, mortality rates decreased after elevated outcrossing rates evolved during the experiment. In contrast, host mortality rates decreased in the obligately outcrossing populations during the first 10 generations of coevolution, and remained low throughout the experiment. Therefore, predominant selfing reduced the ability of the hosts to respond to coevolving pathogens compared to outcrossing hosts. Thus, we found that host–pathogen coevolution can generate rapid evolutionary change, and that host mating system can influence the outcome of coevolution at a fine temporal scale.     

A geographical mosaic of coevolution in a slave-making host-parasite system

Three different isolated populations of the slave‐making ant Rossomyrmex minuchae, sympatric with its obligate host Proformica longiseta, are known from the high mountains of southern Spain. To test the prediction that the slave‐maker and its host represent a coevolutionary geographical mosaic, we studied the variation in the cuticular hydrocarbons (CHCs) as the trait most likely to show the selection mosaic, plus trait remixing by the gene flow in the populations of each species by means of microsatellites. We found within populations, host and parasite had more similar CHC profiles than between the populations or between parasites and allopatric hosts. The differences between the CHC profiles of the host and parasite, which may be responsible for the level of tolerance towards the parasite, varied between the populations suggesting the existence of a selection mosaic of coevolution. Furthermore, P. longiseta showed higher gene flow than R. minuchae, which would allow local variation in the coevolution of the host and parasite while allowing some trait remixing.