The Ratchet and the Red Queen: the maintenance of sex in parasites

The adaptive significance of sexual reproduction remains as an unsolved problem in evolutionary biology. One promising hypothesis is that frequency‐dependent selection by parasites selects for sexual reproduction in hosts, but it is unclear whether such selection on hosts would feed back to select for sexual reproduction in parasites. Here we used individual‐based computer simulations to explore this possibility. Specifically, we tracked the dynamics of asexual parasites following their introduction into sexual parasite populations for different combinations of parasite virulence and transmission. Our results suggest that coevolutionary interactions with hosts would generally lead to a stable coexistence between sexual parasites and a single parasite clone. However, if multiple mutations to asexual reproduction were allowed, we found that the interaction led to the accumulation of clonal diversity in the asexual parasite population, which led to the eventual extinction of the sexual parasites. Thus, coevolution with sexual hosts may not be generally sufficient to select for sex in parasites. We then allowed for the stochastic accumulation of mutations in the finite parasite populations (Muller's Ratchet). We found that, for higher levels of parasite virulence and transmission, the population bottlenecks resulting from host–parasite coevolution led to the rapid accumulation of mutations in the clonal parasites and their elimination from the population. This result may explain the observation that sexual reproduction is more common in parasitic animals than in their free‐living relatives.     

Parasitism and breeding system variation in North American populations of Daphnia pulex

The Red Queen hypothesis proposes that frequency-dependent selection by parasites may be responsible for the evolutionary maintenance of sexual reproduction. We sought to determine whether parasites could be responsible for variation in the occurrence of sexual reproduction in 21 populations of Daphnia pulex (Crustacea; Cladocera) that previous studies have shown to consist of either cyclical parthenogens, obligate parthenogens, or a mixture of both. We measured parasite prevalence over a four-week period (which essentially encompasses an entire season for the temporary snow-melt habitats we sampled) and regressed three different measures of sexuality against mean levels of parasite prevalence. Levels of parasitism were low and we found no relationship between levels of sexuality and mean parasite prevalence. Genetic variation with infection level was detected in 2 of the 21 populations, with several different clones showing signs of overparasitism or underparasitism. Overall, however, our results suggest that parasites are not a major source of selection in these populations and it thus seems unlikely they are responsible for maintaining breeding system variation across the study region.     

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.     

Mixed infections and hybridisation in monogenean parasites

Theory predicts that sexual reproduction promotes disease invasion by increasing the evolutionary potential of the parasite, whereas asexual reproduction tends to enhance establishment success and population growth rate. Gyrodactylid monogeneans are ubiquitous ectoparasites of teleost fish, and the evolutionary success of the specious Gyrodactylus genus is thought to be partly due to their use of various modes of reproduction. Gyrodactylus turnbulli is a natural parasite of the guppy (Poecilia reticulata), a small, tropical fish used as a model for behavioural, ecological and evolutionary studies. Using experimental infections and a recently developed microsatellite marker, we conclusively show that monogenean parasites reproduce sexually. Conservatively, we estimate that sexual recombination occurs and that between 3.7-10.9% of the parasites in our experimental crosses are hybrid genotypes with ancestors from different laboratory strains of G. turnbulli. We also provide evidence of hybrid vigour and/or inter-strain competition, which appeared to lead to a higher maximum parasite load in mixed infections. Finally, we demonstrate inbreeding avoidance for the first time in platyhelminths which may influence the distribution of parasites within a host and their subsequent exposure to the host's localized immune response. Combined reproductive modes and inbreeding avoidance may explain the extreme evolutionary diversification success of parasites such as Gyrodactylus, where host-parasite coevolution is punctuated by relatively frequent host switching.     

A bit of sex stabilizes host-parasite dynamics

To date, only a few studies have focused on the effects of sex on population dynamics. Previous models have typically found that sexual reproduction dampens population fluctuations. Although asexual and sexual reproduction are just the two endpoints along a continuum of varying rates of sex, previous work has ignored the effects of intermediate degrees of sex on population dynamics. Here we study the effects of partial sexual reproduction (i.e. sex occurs only every few generations or with small probability in each generation) on the coupled population dynamics of a Nicholson-Bailey host-parasite model. We show that complex dynamics are simplified for high host population growth rates if the frequency of sex is sufficiently high in both host and parasite: sex decreases fluctuations in population density, and leads to non-chaotic dynamics for population growth rates that would result in chaotic dynamics in the absence of sexual reproduction. However, the simplification does not increase gradually with an increasing frequency of sex but appears abruptly at low-to-intermediate frequencies of sex. For some parameter settings, intermediate frequencies of sexual reproduction can simplify the dynamics more than lower or higher frequencies. Thus, in agreement with earlier results, sexual reproduction typically stabilizes complex population dynamics in our models. Additionally, our results suggest that low-to-intermediate frequencies of sex may often be as (or even more) stabilizing as high frequencies.     

Triggers and tricks of Plasmodium sexual development

Irrespective of the tremendous suffering caused by malaria, a Plasmodium infection by pathogenic blood stages is only transient and an obligate step toward the Anopheles vector where sexual reproduction and genetic recombination of the unicellular parasite takes place. Recent expression profiling studies identified the molecular make-up of female and male gametocytes. Differential promoters and translational repression through mRNA binding by a female-specific helicase help to fine-tune the expression of these sexual stage-specific genes. However, we are only just beginning to discover the triggers that initiate gametocytogenesis and the developmental programs that drive sexual development.     

Parasites in sexual and asexual mollies (Poecilia, Poeciliidae, Teleostei): a case for the Red Queen?

The maintenance of sexual reproduction in the face of its supposed costs is a major paradox in evolutionary biology. The Red Queen hypothesis, which states that sex is an adaptation to fast-evolving parasites, is currently one of the most recognized explanations for the ubiquity of sex and predicts that asexual lineages should suffer from a higher parasite load if they coexist with closely related sexuals. We tested this prediction using four populations of the sexual fish species Poecilia latipinna and its asexual relative Poecilia formosa. Contrary to expectation, no differences in parasite load could be detected between the two species.     

The coevolution of parasites with host-acquired immunity and the evolution of sex

Abstract. Here I present a deterministic model of the coevolution of parasites with the acquired immunity of their hosts, a system in which coevolutionary oscillations can be maintained. These dynamics can confer an advantage to sexual reproduction within the parasite population, but the effect is not strong enough to outweigh the twofold cost of sex. The advantage arises primarily because sexual reproduction impedes the response to fluctuating epistasis and not because it facilitates the response to directional selection—in fact, sexual reproduction often slows the response to directional selection. Where the cost of sexual reproduction is small, a polymorphism can be maintained between the sexuals and the asexuals. A polymorphism is maintained in which the advantage gained due to recombination is balanced by the cost of sex. At much higher costs of sex, a polymorphism between the asexual and sexual populations can still be maintained if the asexuals do not have a full complement of genotypes available to them, because the asexuals only outcompete those sexuals with which they share the same selected alleles. However, over time we might expect the asexuals to amass the full array of genotypes, thus permanently eliminating sexuals from the population. The sexuals may avoid this fate if the parasite population is finite. Although the model presented here describes the coevolution of parasites with the acquired immune responses of their hosts, it can be compared with other host-parasite models that have more traditionally been used to investigate Red Queen theories of the evolution of sex.     

The maintenance of sex in parasites

The maintenance of sex is an unresolved paradox in evolutionary biology, given the inherent twofold fitness advantage for asexuals. Parasitic helminths offer a unique opportunity to address this enigma. Parasites that can create novel antigenic strains are able to escape pre-existing host immunity. Viruses produce diversity through mutation with rapid clonal proliferation. The long generation times of helminth parasites prevent them from adopting this strategy. Instead, we argue that sexual reproduction enables parasitic helminths to rapidly generate strain diversity. We use both a stochastic, individual-based model and a simple analytical model to assess the selective value of sexual versus asexual reproduction in helminth parasites. We demonstrate that sexual reproduction can more easily produce and maintain strain diversity than asexual reproduction for long-lived parasites. We also show that sexual parasite populations are resistant to invasion by rare asexual mutants. These results are robust to high levels of cross-immunity between strains. We suggest that the enhancement of strain diversity, despite stochastic extinction of strains, may be critical to the evolutionary success of sex in long-lived parasites.     

Geographic variation in sterilizing parasite species and the Red Queen

The Red Queen hypothesis predicts that sexual reproduction should be favoured in locations where the risk of infection by virulent parasites is consistently high. When hosts are exposed to multiple parasites over their geographic range, the coevolving parasite species may vary among host populations. We surveyed 26 streams on the South Island of New Zealand to determine whether the frequency of snails ( Potamopyrgus antipodarum ) infected by various sterilizing trematode parasite species was correlated with the frequency of sexual individuals. We compared the results with a survey conducted over 20 years ago to determine whether the associations were consistent. We also evaluated different measures of parasite-mediated selection among populations, including prevalence of the most common local parasite (MCLP) species and parasite diversity to assess the best predictor of sexual reproduction among stream populations. The results showed that the relationship between male frequency and parasite infection is more geographically widespread than previously recorded. Additionally, we found that the prevalence of the MCLP was the best predictor of sex in habitats where hosts populations are infected with multiple parasites (approximately 15 trematode species). This study provides evidence that sexual snails occur more often in environments with high infection levels, and that the pattern of parasite-imposed selection is geographically variable. Support for the Red Queen may be strengthened by focussing on the MCLP, which may vary among host populations.     

Density,parasitism, and sexual reproduction are strongly correlated in lake Daphnia populations

Many organisms can reproduce both asexually and sexually. For cyclical parthenogens, periods of asexual reproduction are punctuated by bouts of sexual reproduction, and the shift from asexual to sexual reproduction has large impacts on fitness and population dynamics. We studied populations of Daphnia dentifera to determine the amount of investment in sexual reproduction as well as the factors associated with variation in investment in sex. To do so, we tracked host density, infections by nine different parasites, and sexual reproduction in 15 lake populations of D. dentifera for 3 years. Sexual reproduction was seasonal, with male and ephippial female production beginning as early as late September and generally increasing through November. However, there was substantial variation in the prevalence of sexual individuals across populations, with some populations remaining entirely asexual throughout the study period and others shifting almost entirely to sexual females and males. We found strong relationships between density, prevalence of infection, parasite species richness, and sexual reproduction in these populations. However, strong collinearity between density, parasitism, and sexual reproduction means that further work will be required to disentangle the causal mechanisms underlying these relationships.     

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.     

Parasites and sexual reproduction in psychid moths

Persistence of sexual reproduction among coexisting asexual competitors has been a major paradox in evolutionary biology. The number of empirical studies is still very limited, as few systems with coexisting sexual and strictly asexual lineages have been found. We studied the ecological mechanisms behind the simultaneous coexistence of a sexually and an asexually reproducing closely related species of psychid moth in Central Finland between 1999 and 2001. The two species compete for the same resources and are often infected by the same hymenopteran parasitoids. They are extremely morphologically and behaviorally similar and can be separated only by their reproductive strategy (sexual vs. asexual) or by genetic markers. We compared the life-history traits of these species in two locations where they coexist to test predictions of the cost-of-sex hypothesis. We did not find any difference in female size, number of larvae, or offspring survival between the sexuals and asexuals, indicating that sexuals are subject to cost of sex. We also used genetic markers to check and exclude the possibility of Wolbachia bacteria infection inducing parthenogenesis. None of the samples was infected by Wolbachia and, thus, it is unlikely that these bacteria could affect our results. We sampled 38 locations to study the prevalence of parasitoids and the moths' reproductive strategy. We found a strong positive correlation between prevalence of sexual reproduction and prevalence of parasitoids. In locations where parasitoids are rare asexuals exist in high densities, whereas in locations with a high parasitoid load the sexual species was dominant. Spatial distribution alone does not explain the results. We suggest that the parasite hypothesis for sex may offer an explanation for the persistence of sexual moths in this system.     

Stress,drugs and the evolution of reproductive restraint in malaria parasites

Life-history theory predicts that sexually reproducing organisms have evolved to resolve resource-allocation trade-offs between growth/survival versus reproduction, and current versus future reproduction. Malaria parasites replicate asexually in their vertebrate hosts, but must reproduce sexually to infect vectors and be transmitted to new hosts. As different specialized stages are required for these functions, the division of resources between these life-history components is a fundamental evolutionary problem. Here, we test how drug-sensitive and drug-resistant isolates of the human malaria parasite Plasmodium falciparum resolve the trade-off between in-host replication and between-host transmission when exposed to treatment with anti-malarial drugs. Previous studies have shown that parasites increase their investment in sexual stages when exposed to stressful conditions, such as drugs. However, we demonstrate that sensitive parasites facultatively decrease their investment in sexual stages when exposed to drugs. In contrast to previous studies, we tested parasites from a region where treatment with anti-malarial drugs is common and transmission is seasonal. We hypothesize that when exposed to drugs, parasites invest in their survival and future transmission by diverting resources from reproduction to replication. Furthermore, as drug-resistant parasites did not adjust their investment when exposed to drugs, we suggest that parasites respond to changes in their proliferation (state) rather the presence of drugs.     

Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.)

Local adaptation within host-parasite systems can evolve by several non-exclusive drivers (e.g., host species-genetic adaptation; ecological conditions-ecological adaptation, and time-temporal adaptation). Social insects, especially bumblebees, with an annual colony life history not only provide an ideal system to test parasite transmission within and between different host colonies, but also parasite adaptation to specific host species and environments. Here, we study local adaptation in a multiple-host parasite characterized by high levels of horizontal transmission. Crithidia bombi occurs as a gut parasite in several bumblebee species. Parasites were sampled from five different host species in two subsequent years. Population genetic tools were used to test for the several types of adaptation. Although we found no evidence for local adaptation of the parasite toward host species, there was a slight temporal differentiation of the parasite populations, which might have resulted from severe bottlenecks during queen hibernation. Parasite populations were in Hardy-Weinberg equilibrium and showed no signs of linkage disequilibrium suggesting that sexual reproduction is an alternative strategy in this otherwise clonal parasite. Moreover, high levels of multiple infections were found, which might facilitate sexual genetic exchange. The detection of identical clones in different host species suggested that horizontal transmission occurs between host species and underpins the lack of host-specific adaptation.     

PARASITIC CASTRATION PROMOTES COEVOLUTIONARY CYCLING BUT ALSO IMPOSES A COST ON SEX

Antagonistic coevolution between hosts and parasites is thought to drive a range of biological phenomena including the maintenance of sexual reproduction. Of particular interest are conditions that produce persistent fluctuations in the frequencies of genes governing host–parasite specificity (coevolutionary cycling), as sex may be more beneficial than asexual reproduction in a constantly changing environment. Although many studies have shown that coevolutionary cycling can lead to the maintenance of sex, the effects of ecological feedbacks on the persistence of these fluctuations in gene frequencies are not well understood. Here, we use a simple deterministic model that incorporates ecological feedbacks to explore how parasitic reductions in host fecundity affect the maintenance of coevolutionary cycling. We demonstrate that parasitic castration is inherently destabilizing and may be necessary for coevolutionary cycling to persist indefinitely, but also reduces the likelihood that sexually reproducing individuals will find a fertile partner, which may select against sex. These findings suggest that castrators can play an important role in shaping host evolution and are likely to be good targets for observing fluctuations in gene frequencies that govern specificity in host–parasite interactions.     

Sexual reproduction and diversity: Connection between sexual selection and biological communities via population dynamics

Sexual reproduction is a mysterious phenomenon. Most animals and plants invest in sexual reproduction, even though it is more costly than asexual reproduction. Theoretical studies suggest that occasional or conditional use of sexual reproduction, involving facultative switching between sexual and asexual reproduction, is the optimal reproductive strategy. However, obligate sexual reproduction is common in nature. Recent studies suggest that the evolution of facultative sexual reproduction is prevented by males that coerce females into sexual fertilization; thus, sexual reproduction has the potential to enforce costs on a given species. Here, the effect of sex on biodiversity is explored by evaluating the reproductive costs arising from sex. Sex provides atypical selection pressure that favors traits that increase fertilization success, even at the expense of population growth rates, that is, sexual selection. The strength of sexual selection depends on the density of a given species. Sexual selection often causes strong negative effects on the population growth rates of species that occur at high density. Conversely, a species that reduces its density is released from this negative effect, and so increases its growth rate. Thus, this negative density-dependent effect on population growth that arises from sexual selection could be used to rescue endangered species from extinction, prevent the overgrowth of common species and promote the coexistence of competitive species. Recent publications on sexual reproduction provide several predictions related to the evolution of reproductive strategies, which is an important step toward integrating evolutionary dynamics, demographic dynamics and community dynamics.     

Reappraising the theme of breeding systems in Echinococcus: is outcrossing a rare phenomenon?

Selfing has been considered the most common mode of reproduction in Echinococcus flatworms. However, population genetic studies on the asexual larval stage involving nuclear co-dominant markers have not always revealed significant heterozygote deficiencies--the expected outcome of a regularly and highly inbred population. In this study, we analysed the genetic structure of Echinococcus granulosus sensu lato populations from Southern Brazil during their adult (sexual) stage using 1 mitochondrial and 1 nuclear marker (cox 1 and mdh, respectively). We show that parasite genetic differentiation is largest among definitive hosts (domestic dogs) from different farms, suggesting that transmission is mostly maintained within a farm. Moreover, we show that heterozygote deficiencies are not significant, and we suggest that outbreeding is the most common mode of reproduction of the parasite in that region.     

Determining the optimal developmental route of Strongyloides ratti: an evolutionarily stable strategy approach

Understanding the processes that drive parasite evolution is crucial to the development of management programs that sustain long-term, effective control of infectious disease in the face of parasite adaptation. Here we present a novel evolutionarily stable strategy (ESS) model of the developmental decisions of a nematode parasite, Strongyloides ratti. The genus Strongyloides exhibits an unusual developmental plasticity such that progeny from an individual may either develop via a direct (homogonic) route, where the developing larvae are infective to new hosts, or an indirect (heterogonic) route, where the larvae develop into free-living, dioecious adults that undergo at least one bout of sexual reproduction outside the host, before producing offspring that develop into infective larvae. The model correctly predicts a number of observed features of the parasite's behavior and shows that this plasticity may be adaptive such that pure homogonic development, pure heterogonic development, or a mixed strategy may be optimal depending on the prevailing environmental conditions, both within and outside the host. Importantly, our results depend only on the benefits of an extra round of reproduction in the environment external to the host and not on benefits to sexual reproduction through the purging of deleterious mutation or the generation of novel, favorable genotypes. The ESS framework presented here provides a powerful, general approach to predict how macroparasites, the agents of many of the world's most important infectious diseases, will evolve in response to the various selection pressures imposed by different control regimes in the future.     

The life cycle of Ascogregarina taiwanensis (Apicomplexa:Lecudinidae).

A number of features, including large size of the trophozoite, host-specificity, developmental synchrony and evident migration behavior, of Ascogregarina taiwanensis make it suitable as a model for studies of parasite-host relationships. In this article, Wei June Chen describes the life cycle of As. taiwanensis; and raises some areas for future work, including the interaction between the parasite and its host, inhibition of sexual reproduction by non-natural hosts and their mutual effects during the development.