Hybrid fitness in a locally adapted parasite

The parasite (Red Queen) hypothesis for the maintenance of sexual reproduction and genetic diversity assumes that host-parasite interactions result from tight genetic specificity. Hence, hybridization between divergent parasite populations would be expected to disrupt adaptive gene combinations, leading to reduced infectivity on exposure to parental sympatric hosts, as long as gene effects are nonadditive. In contrast, hybridization would not cause reduced infectivity on allopatric hosts unless the divergent parasite populations possess alleles that are intrinsically incompatible when they are combined. In three different experiments, we compared the infectivity of locally adapted parasite (trematode) populations with that of F(1) hybrid parasites when exposed to host (snail) populations that were sympatric to one of the two parasite populations. We tested for intrinsic genetic incompatibilities in two experiments by including one host population that was allopatric to both parasite populations. As predicted, when the target host populations were sympatric to the parasite populations, the hybrids were significantly less infective than the parental average, while hybrid parasites on allopatric hosts were not, thereby ruling out intrinsic genetic incompatibilities. The results are consistent with nonadditive gene effects and tightly specific host-driven selection underlying parasite divergence, as envisioned by coevolutionary theory and the Red Queen hypothesis.     

Parasites, sex, and clonal diversity in natural snail populations

Under the Red Queen hypothesis, host-parasite coevolution selects against common host genotypes. Although this mechanism might underlie the persistence of sexual reproduction, it might also maintain high clonal diversity. Alternatively, clonal diversity might be maintained by multiple origins of parthenogens from conspecific sexuals, a feature in many animal groups. Herein, we addressed the maintenance of overall genetic diversity by coevolving parasites, as predicted by the Red Queen hypothesis. We specifically examined the contribution of parasites to host clonal diversity and the frequency of sexually reproducing individuals in natural stream populations of Potamopyrgus antipodarum snails. We also tested the alternative hypothesis that clonal diversity is maintained by the input of clones by mutation from sympatric sexuals. Clonal diversity and the frequency of sexual individuals were both positively related to infection frequency. Surprisingly, although clones are derived by mutation from sexual snails, parasites explained more of the genotypic variation among parthenogenetic subpopulations. Our findings thus highlight the importance of parasites as drivers of clonal diversity, as well as sex.     

Interspecific antagonism and virulence in hosts exposed to two parasite species

Co-infection of host organisms by multiple parasite species has evolutionary consequences for all participants in the symbiosis. In this study, we co-exposed aquatic-snails (Biomphalaria glabrata) to two of their trematode parasites, Schistosoma mansoni and Echinostoma caproni. In co-exposed snails, E. caproni prevalence was 63% compared to only 23% for S. mansoni. Co-exposed E. caproni-infected snails exhibited reduced fecundity, higher mortality, and higher parasite reproduction (higher virulence) compared to hosts exposed to echinostomes alone. Conversely, co-exposed S. mansoni-infected snails released fewer parasites and produced greater numbers of eggs compared to hosts exposed to S. mansoni alone. These results suggest that co-exposure not only influences the establishment (presence or absence) of particular parasite species, but also impacts host life history, parasite reproduction, and the virulence of the interaction.     

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.     

Effects of interspecific competition on asexual proliferation and clonal genetic diversity in larval trematode infections of snails

Interactions among different parasite species within hosts can be important factors shaping the evolution of parasite and host populations. Within snail hosts, antagonistic interactions among trematode species, such as competition and predation, can influence parasite abundance and diversity. In the present study we examined the strength of antagonistic interactions between 2 marine trematodes (Maritrema novaezealandensis and Philophthalmus sp.) in naturally infected Zeacumantus subcarinatus snails. We found approximately the same number of snails harbouring both species as would be expected by chance given the prevalence of each. However, snails infected with only M. novaezealandensis and snails with M. novaezealandensis and Philophthalmus sp. co-occurring were smaller than snails harbouring only Philophthalmus sp. In addition, the number of Philophthalmus sp. rediae was not affected by the presence of M. novaezealandensis sporocysts and the within-host clonal diversity of M. novaezealandensis was not influenced by the presence of Philophthalmus sp. Our results suggest that antagonistic interactions may not be a major force influencing the evolution of these trematodes and that characteristics such as host size and parasite infection longevity are shaping their abundance and population dynamics.     

HybHyp—hybridizing the host: the long reach of parasite genes. A new hypothesis to explain host–parasite interrelationships in plant hybrid complexes

Ever since existence of sexuality in plants was accepted in around 1700, questions centred about the role and maintenance of sexual reproduction in general, leading to a number of hypotheses like the Vicar of Bray, the Ratchet or the Hitch-hiker theory. Bell (The masterpiece of nature. The evolution and genetics of sexuality. University of California Press, Berkeley, LA, 1982) formulated the Red Queen Hypothesis (RQH) which explains the persistence of sexual reproduction as an outcome of a coevolutionary arms race between hosts and parasites. By sexual recombination and genetic diversification hosts minimize the risk of pathogen infection. Since virulence of pathogens is genetically determined and often species specific, parasites are mostly adapted to common host genotypes, whereas rare and divergent genotypes are less infected and therefore have a selective advantage. Employing Dawkins (The extended phenotype. The long reach of the gene, 1999) central theorem of the extended phenotype to the RQH, mating systems in hosts might be a result of the long reach of the parasites genes. Here now the hypothesis is proposed, that evolution by hybridisation and polyploidy in host plants is an extended phenotype of parasites, a response of hosts triggered by the parasites genes to slow down the effects of the Red Queen strategy of plants. Thus, hybridisation and polyploidy might have evolved by parasite pressure and not by host strategy. This hypothesis is called the “hybridisation-of-the-host-hypothesis”.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

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.     

Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges

Aim To use a comparative approach to understand parasite demographic patterns in native versus introduced populations, evaluating the potential roles of host invasion history and parasite life history. Location North American east and west coasts with a focus on San Francisco Bay (SFB). Methods Species richness and prevalence of trematode parasites were examined in the native and introduced ranges of two gastropod host species, Ilyanassa obsoleta and Littorina saxatilis. We divided the native range into the putative source area for introduction and areas to the north and south; we also sampled the overlapping introduced range in SFB. We dissected 14,781 snails from 103 populations and recorded the prevalence and identity of trematode parasites. We compared trematode species richness and prevalence across the hosts’ introduced and native ranges, and evaluated the influence of host availability on observed patterns. Results Relative to the native range, both I. obsoleta and L. saxatilis have escaped (lost) parasites in SFB, and L. saxatilis demonstrated a greater reduction of trematode diversity and infection prevalence than I. obsoleta. This was not due to sampling inequalities between the hosts. Instead, rarefaction curves suggested complete capture of trematode species in native source and SFB subregions, except for L. saxatilis in SFB, where infection was extremely rare. For I. obsoleta, infection prevalence of trematodes using fish definitive hosts was significantly lower in SFB compared to the native range, unlike those using bird hosts. Host availability partly explained the presence of introduced trematodes in SFB. Main conclusions Differential losses of parasite richness and prevalence for the two gastropod host species in their introduced range is probably the result of several mechanistic factors: time since introduction, propagule pressure, vector of introduction, and host availability. Moreover, the recent occurrence of L. saxatilis’ invasion and its active introduction vector suggest that its parasite diversity and distribution will probably increase over time. Our study suggests that host invasion history and parasite life history play key roles in the extent and diversity of trematodes transferred to introduced populations. Our results also provide vital information for understanding community‐level influences of parasite introductions, as well as for disease ecology in general.     

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.     

The role of epistasis on the evolution of recombination in host-parasite coevolution

Antagonistic coevolution between hosts and parasites is known to affect selection on recombination in hosts. The Red Queen Hypothesis (RQH) posits that genetic shuffling is beneficial for hosts because it quickly creates resistant genotypes. Indeed, a large body of theoretical studies have shown that for many models of the genetic interaction between host and parasite, the coevolutionary dynamics of hosts and parasites generate selection for recombination or sexual reproduction. Here we investigate models in which the effect of the host on the parasite (and vice versa) depend approximately multiplicatively on the number of matched alleles. Contrary to expectation, these models generate a dynamical behavior that strongly selects against recombination/sex. We investigate this atypical behavior analytically and numerically. Specifically we show that two complementary equilibria are responsible for generating strong linkage disequilibria of opposite sign, which in turn causes strong selection against sex. The biological relevance of this finding stems from the fact that these phenomena can also be observed if hosts are attacked by two parasites that affect host fitness independently. Hence the role of the Red Queen Hypothesis in natural host parasite systems where infection by multiple parasites is the rule rather than the exception needs to be reevaluated.     

HOST-PARASITE COEVOLUTION: EVIDENCE FOR RARE ADVANTAGE AND TIME-LAGGED SELECTION IN A NATURAL POPULATION

In theory, parasites can create time-lagged, frequency-dependent selection in their hosts, resulting in oscillatory gene-frequency dynamics in both the host and the parasite (the Red Queen hypothesis). However, oscillatory dynamics have not been observed in natural populations. In the present study, we evaluated the dynamics of asexual clones of a New Zealand snail, Potamopyrgus antipodarum, and its trematode parasites over a five-year period. During the summer of each year, we determined host-clone frequencies in random samples of the snail to track genetic changes in the snail population. Similarly, we monitored changes in the parasite population, focusing on the dominant parasite, Microphallus sp., by calculating the frequency of clones in samples of infected individuals from the same collections. We then compared these results to the results of a computer model that was designed to examine clone frequency dynamics for various levels of parasite virulence. Consistent with these simulations and with ideas regarding dynamic coevolution, parasites responded to common clones in a time-lagged fashion. Finally, in a laboratory experiment, we found that clones that had been rare during the previous five years were significantly less infectible by Microphallus when compared to the common clones. Taken together, these results confirm that rare host genotypes are more likely to escape infection by parasites; they also show that host-parasite interactions produce, in a natural population, some of the dynamics anticipated by the Red Queen hypothesis.     

Escape from the Red Queen: an overlooked scenario in coevolutionary studies

Almost all eukaryotic organisms undergo sexual recombination at some stage of their life history. However, strictly asexual organisms should have higher per capita rate of reproduction compared with those that have sex, so the latter must convey some advantage which overrides the reproductive benefit of asexuality. For example, sexual reproduction and recombination may play an important role in allowing organisms to evolutionarily ‘keep up’ with parasites. Host–parasite coevolution can operate via negative frequency‐dependent selection whereby parasite genotypes adapt to infect host genotypes as they become locally common. By producing more genetically diverse offspring with unique genotypes, sexual organisms have an advantage over asexual counterparts. Essentially, sexual hosts are more difficult for coevolving parasites to ‘track’ over time. This scenario has been named the “Red Queen hypothesis”. It refers to a passage in Lewis Carroll's ‘Through the Looking Glass’ in which the Red Queen tells Alice: ‘it takes all the running you can do, to keep in the same place’; this statement resembles the negative frequency‐dependent dynamics of host–parasite coevolution.     

Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails

Using field surveys and experimental infections, we investigated the influence of a trematode parasite on life history traits of adult Lymnaea elodes snails. We found that parasitism significantly affected the growth, fecundity, and survival of host snails. Within five of the six natural L. elodes populations we sampled, shell length of echinostome-infected hosts was significantly greater than for uninfected conspecifics. Furthermore, we show that gigantism occurs among experimentally infected snails due to an accelerated growth rate and size-selective mortality following an Echinostoma revolutum infection. The fecundity of infected snails sharply decreased beginning at 3 weeks post exposure (PE) and all egg production eventually ceased for most hosts by 5–6 weeks PE. Energy constraints, imposed by parasite development, alter the host energy budget. Early in the infection, parasite depletion of host energy reserves reduces host reproduction, but sufficient resources remain to allow accelerated host growth. Mortality was increased among host snails at two distinct stages: shortly after exposure and several weeks after cercariae were first released. We did not observe tissue degradation in snails during the first 4 weeks after exposure to the parasite, but destruction of host tissues was noted among snails dying later in the infection. Received: 5 September 1997 / Accepted: 19 November 1997     

Advice of the rose: experimental coevolution of a trematode parasite and its snail host

Understanding host-parasite coevolution requires multigenerational studies in which changes in both parasite infectivity and host susceptibility are monitored. We conducted a coevolution experiment that examined six generations of interaction between a freshwater snail (Potamopyrgus antipodarum) and one of its common parasites (the sterilizing trematode, Microphallus sp.). In one treatment (recycled), the parasite was reintroduced into the same population of host snails. In the second treatment (lagged), the host snails received parasites from the recycled treatment, but the addition of these parasites did not begin until the second generation. Hence any parasite-mediated genetic changes of the host in the lagged treatment were expected to be one generation behind those in the recycled treatment. The lagged treatment thus allowed us to test for time lags in parasite adaptation, as predicted by the Red Queen model of host-parasite coevolution. Finally, in the third treatment (control), parasites were not added. The results showed that parasites from the recycled treatment were significantly more infective to snails from the lagged treatment than from the recycled treatment. In addition, the hosts from the recycled treatment diverged from the control hosts with regard to their susceptibility to parasites collected from the field. Taken together, the results are consistent with time lagged, frequency-dependent selection and rapid coevolution between hosts and parasites.     

Host condition as a constraint for parasite reproduction

Environmental stress has been suggested to increase host susceptibility to infections and reduce host ability to resist parasite growth and reproduction, thus benefiting parasites. This prediction stems from expected costs of immune defence; hosts in poor condition should have less resources to be allocated to immune function. However, the alternative hypothesis for response to environmental stress is that hosts in poor condition provide less resources for parasites and/or suffer higher mortality, leading to reduced parasite growth, reproduction and survival. We contrasted these alternative hypotheses in a trematode–snail ( Diplostomum spathaceum – Lymnaea stagnalis ) system by asking: (1) how host condition affects parasite reproduction (amount and quality of produced transmission stages) and (2) how host condition affects the survival of infected host individuals. We experimentally manipulated host condition by starving the snails, and found that parasites produced fewer and poorer quality transmission stages in stressed hosts. Furthermore, starvation increased snail mortality. These findings indicate that in well-established trematode infections, reduced ability of immune allocation has no effect on host exploitation by parasites. Instead, deteriorating resources for the snail host can directly limit the amount of resources available for the parasite. This, together with increased host mortality, may have negative effects on parasite populations in the wild.     

On the track of the Red Queen: bark beetles, their nematodes, local climate and geographic parthenogenesis

Geographic parthenogenesis has been explained as resulting from parasite pressure (Red Queen hypothesis): several studies have found high degrees of sexuals where the prevalence of parasites is high. However, it is important to address whether prevalence of parasites mirrors risk of infection. We explored geographic parthenogenesis of Ips acuminatus bark beetles and their nematodes. Local climate is crucial for nematode stages outside the host, in spring and summer, and prevalence should thus be associated with those temperatures if prevalence reliably reflects exposure risk across populations. This was the case; however, high prevalence of a virulent nematode species was not associated with many sexuals, whereas highly sexual populations were characterized by high infection risk of benign nematodes. Low virulence of the latter makes Red Queen dynamics unlikely. Geographical patterns of parthenogenesis were instead associated with winter temperature and variance in temperature.     

Within‐population covariation between sexual reproduction and susceptibility to local parasites

Evolutionary biology has yet to reconcile the ubiquity of sex with its costs relative to asexual reproduction. Here, we test the hypothesis that coevolving parasites maintain sex in their hosts. Specifically, we examined the distributions of sexual reproduction and susceptibility to local parasites within a single population of freshwater snails (Potamopyrgus antipodarum). Susceptibility to local trematode parasites (Microphallus sp.) is a relative measure of the strength of coevolutionary selection in this system. Thus, if coevolving parasites maintain sex, sexual snails should be common where susceptibility is high. We tested this prediction in a mixed population of sexual and asexual snails by measuring the susceptibility of snails from multiple sites in a lake. Consistent with the prediction, the frequency of sexual snails was tightly and positively correlated with susceptibility to local parasites. Strikingly, in just two years, asexual females increased in frequency at sites where susceptibility declined. We also found that the frequency of sexual females covaries more strongly with susceptibility than with the prevalence of Microphallus infection in the field. In linking susceptibility to the frequency of sexual hosts, our results directly implicate spatial variation in coevolutionary selection in driving the geographic mosaic of sex.     

Do Parasitic Trematode Cercariae Demonstrate a Preference for Susceptible Host Species?

Many parasites are motile and exhibit behavioural preferences for certain host species. Because hosts can vary in their susceptibility to infections, parasites might benefit from preferentially detecting and infecting the most susceptible host, but this mechanistic hypothesis for host-choice has rarely been tested. We evaluated whether cercariae (larval trematode parasites) prefer the most susceptible host species by simultaneously presenting cercariae with four species of tadpole hosts. Cercariae consistently preferred hosts in the following order: Anaxyrus ( = Bufo) terrestris (southern toad), Hyla squirella (squirrel tree frog), Lithobates ( = Rana) sphenocephala (southern leopard frog), and Osteopilus septentrionalis (Cuban tree frog). These host species varied in susceptibility to cercariae in an order similar to their attractiveness with a correlation that approached significance. Host attractiveness to parasites also varied consistently and significantly among individuals within a host species. If heritable, this individual-level host variation would represent the raw material upon which selection could act, which could promote a Red Queen “arms race” between host cues and parasite detection of those cues. If, in general, motile parasites prefer to infect the most susceptible host species, this phenomenon could explain aggregated distributions of parasites among hosts and contribute to parasite transmission rates and the evolution of virulence. Parasite preferences for hosts belie the common assumption of disease models that parasites seek and infect hosts at random.     

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.