Immune stress and facultative sex in a parasitic nematode

It has been suggested that sexual reproduction in parasites may be advantageous because it helps evade genotype‐specific host immune responses. Indirect support for this hypothesis has recently come from work on Strongyloides ratti, a parasitic nematode of rats that develops and reproduces sexually or asexually. In this species, host immune responses against S. ratti lead to a higher proportion of individuals reproducing sexually. However, an alternative explanation for these results is that sex is favoured by general environmental stress, including host responses against antigen sources other than S. ratti. Here we test this hypothesis, by determining how host immunity against two other parasitic nematode species (Nippostrongylus brasiliensis & Strongyloides venezuelensis) and commonly used mammalian antigens (sheep red blood cells) affects the likelihood of S. ratti larvae developing sexually. Our results show that increased levels of sex occur in response to immune responses generated against these other species, and not just host immunity elicited by S. ratti. This is consistent with the idea that sex is favoured under stressful conditions, and does not support the immune evasion hypothesis.     

The control of morph development in the parasitic nematode Strongyloides ratti.

The parasitic nematode Strongyloides ratti has a complex life cycle. The progeny of the parasitic females can develop into three distinct morphs, namely directly developing infective third-stage larvae (iL3s), free-living adult males and free-living adult females. We have analysed of the effect of host immune status (an intra-host factor), environmental temperature (an extra-host factor) and their interaction on the proportion of larvae that develop into these three morphs. The results are consistent with the developmental decision of larvae being controlled by at least two discrete developmental switches. One is a sex-determination event that is affected by host immune status and the other is a switch between alternative female morphs that is affected by both host immune status and environmental temperature. These findings clarify the basis of the life cycle of S. ratti and demonstrate how such complex life cycles can result from a combination of simple developmental switches.     

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 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.     

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.     

The contrariwise life of a parasitic, pedomorphic copepod with a non-feeding adult: ontogenesis, ecology, and evolution

Abstract. The extraordinary parasitic metanauplius larva of Caribeopsyllus amphiodiae is sexually dimorphic, with conspicuous gonads, and elaborate lens-bearing eyes. The parasites usually occur singly within their host, and grow for ≤5 months within the stomach of burrowing ophiuroids ( Amphiodia urtica ). They transform into free-living, semelparous, non-feeding adults that live only 2 weeks. The species' life-history pattern, with a larval period ∼10 × longer than the adult life span, is contrariwise to that of other copepods but not for animals with non-feeding adults of both sexes. It appears that the life cycle of C. amphiodiae is pedomorphic, and probably evolved through a delay of metamorphosis regulated by developmental hormones. We attribute the dominance of the larval phase to the greater potential for survival and growth of the enterozoic parasitic stages than of the free-living, post-metamorphic stages. We note that among marine invertebrates, non-feeding adults of both sexes occur exclusively in taxa with a complex life cycle, and that non-feeding adults of both sexes are never found in taxa that have small larvae and delayed maturation. They occur only when there is a large larva that can provide the adult stage with sufficient nutrient reserves for reproduction.     

Parasitic castration of plants by fungi

If the production of genetically variable offspring is a mechanism of host defense against parasites, then parasites capable of suppressing sexual reproduction in hosts may gain a selective advantage over parasites that do not do so. Recent work has shown that a range of systemic fungi infecting plants sterilize their hosts, effectively preventing coevolutionary responses by host populations to avoid infection, while stimulating clonal spread of the infected plant. Indeed, parasitic castration of plants may represent a widespread fungal adaptation.     

Assessing immunocompetence in red palm weevil adult and immature stages in response to bacterial challenge and entomopathogenic nematode infection

Parasites and pathogens can follow different patterns of infection depending on the host developmental stage or sex. In fact, immune function is energetically costly for hosts and trade‐offs exist between immune defenses and life history traits as growth, development and reproduction and organisms should thus optimize immune defense through their life cycle according to their developmental stage. Identifying the most susceptible target and the most virulent pathogen is particularly important in the case of insect pests, in order to develop effective control strategies targeting the most vulnerable individuals with the most effective control agent. Here, we carried out laboratory tests to identify the most susceptible target of infection by infecting different stages of the red palm weevil Rhynchophorus ferrugineus (larvae, pupae, male, and female adults) with both a generic pathogen, antibiotic‐resistant Gram‐negative bacteria Escherichia coli XL1‐Blue, and two specific strains of entomopathogenic nematodes (EPNs), Steinernema carpocapsae ItS‐CAO1 and Heterorhabditis bacteriophora ItH‐LU1. By evaluating bacterial clearance, host mortality and parasite progeny release, we demonstrate that larvae are more resistant than adults to bacterial challenge and they release less EPNs progeny after infection despite a higher mortality compared to adults. Considering the two EPN strains, S. carpocapsae was more virulent than H. bacteriophora both in terms of host mortality and more abundant progeny released by hosts after death. The outcomes attained with unspecific and specific pathogens provide useful information for a more efficient and sustainable management of this invasive pest.     

Effect of the digenean parasites of fish on the fauna of Mediterranean lagoons

Attention is drawn to the effects of parasites on their hosts, taking as a model the digenean parasites of teleosts (hereafter: fish) from lagoons along the French Mediterranean coast. Because digeneans have a heteroxenic life cycle, their impact is not limited to the definitive host, which harbours the sexual adults, but is extended to the first host (mollusc) and to the second host ("invertebrate" or fish). Adult parasites, in order to ensure efficient sexual reproduction, never cause excessive damage to their definitive host, usually only exploiting the intestinal fluids; however, the host must intensify its search for prey, which results in a diminished fitness. Within the first host, 'larval' stages of digenean parasites invade the gonads, resulting in its castration, then exhaustion and eventually death. The diversion of energy from the second hosts towards the parasites forces them to intensify their search for food, resulting in decreased fitness and an increased risk of being eaten; in addition, manipulation of the host's behaviour by parasites drives this host into the food chain of the definitive host. In lagoons, many individuals of almost all species of fish and invertebrates act as first, second and/or definitive hosts for digeneans. Obviously, parasites have a severe impact on the population dynamics of key taxa, on the food web and therefore also on the functioning of the whole lagoon ecosystem. Yet this impact has been largely overlooked or underestimated in functioning models, by ecologists, who tend to prioritize more apparent trophic relationships.     

Population genetics of complex life-cycle parasites: an illustration with trematodes

Accurate inferences on population genetics data require a sound underlying theoretical null model. Organisms alternating sexual and asexual reproduction during their life-cycle have been largely neglected in theoretical population genetic models, thus limiting the biological interpretation of population genetics parameters measured in natural populations. In this article, we derive the expectations of those parameters for the life-cycle of monoecious trematodes, a group comprising several important human and livestock parasites that obligatorily alternate sexual and asexual reproduction during their life-cycle. We model how migration rates between hosts, sexual and asexual mutation rates, adult selfing rate and the variance in reproductive success of parasites during the clonal phase affect the amount of neutral genetic diversity of the parasite (effective population size) and its apportionment within and between definitive hosts (using F-statistics). We demonstrate, in particular, that variance in reproductive success of clones, a parameter that has been completely overlooked in previous population genetics models, is very important in shaping the distribution of the genetic variability both within and among definitive hosts. Within definitive hosts, the parameter F(IS) (a measure of the deviation from random mating) is decreased by high variance in clonal reproductive success of larvae but increased by high adult self-fertilisation rates. Both clonal multiplication and selfing have similar effects on between-host genetic differentiation (F(ST)). Migration occurring before and after asexual reproduction can have different effects on the patterns of F(IS), depending on values of the other parameters such as the mutation rate. While the model applies to any hermaphroditic organism alternating sexual and clonal reproduction (e.g. many plants), the results are specifically discussed in the light of the limited population genetic data on monoecious trematodes available to date and their previous interpretation. We hope that our model will encourage more empirical population genetics studies on monoecious trematodes and other organisms with similar life-cycles.     

Evolution of complex life cycles in trophically transmitted helminths. I. Host incorporation and trophic ascent

Links between parasites and food webs are evolutionarily ancient but dynamic: life history theory provides insights into helminth complex life cycle origins. Most adult helminths benefit by sexual reproduction in vertebrates, often high up food chains, but direct infection is commonly constrained by a trophic vacuum between free‐living propagules and definitive hosts. Intermediate hosts fill this vacuum, facilitating transmission to definitive hosts. The central question concerns why sexual reproduction, and sometimes even larval growth, is suppressed in intermediate hosts, favouring growth arrest at larval maturity in intermediate hosts and reproductive suppression until transmission to definitive hosts? Increased longevity and higher growth in definitive hosts can generate selection for larger parasite body size and higher fecundity at sexual maturity. Life cycle length is increased by two evolutionary mechanisms, upward and downward incorporation, allowing simple (one‐host) cycles to become complex (multihost). In downward incorporation, an intermediate host is added below the definitive host: models suggest that downward incorporation probably evolves only after ecological or evolutionary perturbations create a trophic vacuum. In upward incorporation, a new definitive host is added above the original definitive host, which subsequently becomes an intermediate host, again maintained by the trophic vacuum: theory suggests that this is plausible even under constant ecological/evolutionary conditions. The final cycle is similar irrespective of its origin (upward or downward). Insights about host incorporation are best gained by linking comparative phylogenetic analyses (describing evolutionary history) with evolutionary models (examining selective forces). Ascent of host trophic levels and evolution of optimal host taxa ranges are discussed.     

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Climate change is expected to alter the dynamics of host–parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the ‘shelter effect’. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid‐summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature‐dependent parasite life history components in a single measure of fitness, R₀. It allows quantitative predictions of climate change impacts, and is easily generalized to many host–parasite systems.     

Effect of a nuclear polyhedrosis virus on the relationship between Trichoplusia ni (Lepidoptera: Noctuidae) and the parasite, Hyposoter exiguae (hymenoptera: Ichneumonidae)

The effect of a nuclear polyhedrosis virus on the relationship between Trichoplusia ni and the parasite, Hyposoter exiguae, was investigated to determine if the virus could invade and multiply in the tissues of the parasites, if parasites which emerged from virus-infected T. ni larvae had normal emergence, fecundity, and longevity, and if the parasite could serve as a vector for the virus. Light microscopy revealed particles which appeared to be polyhedra within the lumen of the midgut of parasite larvae from virus-infected hosts. Transmission electron microscopy confirmed the presence of polyhedra and free virions within the midgut of the larvae. Polyhedra or free virions were never found within any parasite tissues. Parasite larvae within hosts exposed to virus before parasitization perished when their hosts died of virus infection. Parasite larvae in hosts exposed to virus after parasitization completed their development before their hosts died of virus infection. The proportion of parasites which survived increased as the time between host parasitization and host virus exposure increased. Parasite larvae which developed in hosts exposed to the virus soon after parasitization spent significantly less time in their hosts than did parasites which developed in noninfected hosts. There was no significant difference in time spent in the pupal stage, percent adult emergence, adult longevity with and without food and water, and fecundity of parasites which developed in virus-infected hosts and those which developed in noninfected hosts. Female parasites laid as many eggs in virus-infected hosts as they did in noninfected hosts. Sixty percent of the female parasites which oviposited in virus-infected hosts vectored infective doses of virus to an average of 6% of the healthy hosts subsequently exposed to them. None of the healthy host larvae exposed to male parasites which had been exposed to virus-infected host larvae became infected with the virus. Forty percent of the female parasites which developed in virus-infected hosts transmitted infective doses of the virus to an average of 65% of the healthy host larvae exposed to them. Ninety percent of the male parasites which developed in virus-infected hosts transferred infective doses of the virus to an average of 21% of the healthy host larvae exposed to them.     

Life history and virulence are linked in the ectoparasitic salmon louse Lepeophtheirus salmonis

Models of virulence evolution for horizontally transmitted parasites often assume that transmission rate (the probability that an infected host infects a susceptible host) and virulence (the increase in host mortality due to infection) are positively correlated, because higher rates of production of propagules may cause more damages to the host. However, empirical support for this assumption is scant and limited to microparasites. To fill this gap, we explored the relationships between parasite life history and virulence in the salmon louse, Lepeophtheirus salmonis, a horizontally transmitted copepod ectoparasite on Atlantic salmon Salmo salar. In the laboratory, we infected juvenile salmon hosts with equal doses of infective L. salmonis larvae and monitored parasite age at first reproduction, parasite fecundity, area of damage caused on the skin of the host, and host weight and length gain. We found that earlier onset of parasite reproduction was associated with higher parasite fecundity. Moreover, higher parasite fecundity (a proxy for transmission rate, as infection probability increases with higher numbers of parasite larvae released to the water) was associated with lower host weight gain (correlated with lower survival in juvenile salmon), supporting the presence of a virulence–transmission trade‐off. Our results are relevant in the context of increasing intensive farming, where frequent anti‐parasite drug use and increased host density may have selected for faster production of parasite transmission stages, via earlier reproduction and increased early fecundity. Our study highlights that salmon lice, therefore, are a good model for studying how human activity may affect the evolution of parasite virulence.     

Facultative symbiont infections affect aphid reproduction

Some bacterial symbionts alter their hosts reproduction through various mechanisms that enhance their transmission in the host population. In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum harbors several facultative symbionts influencing several aspects of host ecology. Aphids reproduce by cyclical parthenogenesis whereby clonal and sexual reproduction alternate within the annual life cycle. Many species, including the pea aphid, also show variation in their reproductive mode at the population level, with some lineages reproducing by cyclical parthenogenesis and others by permanent parthenogenesis. While the role of facultative symbionts has been well studied during the parthenogenetic phase of their aphid hosts, very little is known on their possible influence during the sexual phase. Here we investigated whether facultative symbionts modulate the capacity to produce sexual forms in various genetic backgrounds of the pea aphid with controlled symbiont composition and also in different aphid genotypes from natural populations with previously characterized infection status and reproductive mode. We found that most facultative symbionts exhibited detrimental effects on their hosts fitness under sex-inducing conditions in comparison with the reference lines. We also showed that the loss of sexual phase in permanently parthenogenetic lineages of A. pisum was not explained by facultative symbionts. Finally, we demonstrated that Spiroplasma infection annihilated the production of males in the host progeny by inducing a male-killing phenotype, an unexpected result for organisms such as aphids that reproduce primarily through clonal reproduction.     

Evolution of trophic transmission in parasites: why add intermediate hosts?

Although multihost complex life cycles (CLCs) are common in several distantly related groups of parasites, their evolution remains poorly understood. In this article, we argue that under particular circumstances, adding a second host to a single-host life cycle is likely to enhance transmission (i.e., reaching the target host). For instance, in several situations, the propagules of a parasite exploiting a predator species will achieve a higher host-finding success by encysting in a prey of the target predator than by other dispersal modes. In such a case, selection should favor the transition from a single- to a two-host life cycle that includes the prey species as an intermediate host. We use an optimality model to explore this idea, and we discuss it in relation to dispersal strategies known among free-living species, especially animal dispersal. The model found that selection favored a complex life cycle only if intermediate hosts were more abundant than definitive hosts. The selective value of a complex life cycle increased with predation rates by definitive hosts on intermediate hosts. In exploring trade-offs between transmission strategies, we found that more costly trade-offs made it more difficult to evolve a CLC while less costly trade-offs between traits could favor a mixed strategy.     

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.     

核型多角体病毒与侧沟茧蜂对斜纹夜蛾幼虫的协同作用

研究了斜纹夜蛾幼虫体内的斜纹夜蛾侧沟茧蜂存活率、发育历期、寄主感染病毒时间、病毒浓度之间的关系,并测定了斜纹夜蛾侧沟茧蜂的传毒效率．结果表明,病毒对寄主体内寄生蜂历期无明显影响,寄生在幼虫体内的寄生蜂能在寄主病死前完成发育,存活比例因寄主感染病毒的时间和浓度而异．斜纹夜蛾被寄生后接种病毒(SINPV),距离寄生时间越长,饲毒浓度越低,寄生蜂完成发育的比例越大,但饲毒时间是主要影响因素．从感病幼虫体内发育成的侧沟茧蜂或曾经在感病寄主上产过卵的寄生蜂,以及通过人工方式使产卵器被病毒污染的寄生蜂,均能携带一定数量的病毒．通过产卵活动,侧沟茧蜂成蜂能在寄主幼虫个体间传递病毒．当寄生蜂在感病的寄主幼虫上产卵带毒后,平均可传递病毒给2．14头幼虫;发育于感病幼虫体内的寄生蜂,平均可传递病毒给2．45头幼虫．通过用病毒液浸茧或用混有病毒的蜂蜜饲喂成蜂等方式使产卵器污染病毒的寄生蜂,传毒效率随饲毒浓度增加而提高,平均可传递病毒1．45头和0．94头幼虫     

Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito

Plasmodium spp. undergo a complex obligate developmental cycle within their invertebrate vectors that enables transmission between vertebrate hosts. This developmental cycle involves sexual reproduction and then asexual multiplication, separated by phases of invasion and colonization of distinct vector tissues. As with other stages in the Plasmodium life cycle, there is exquisite adaptation of the malaria parasite to its changing environment as it transforms within the blood of its vertebrate host, through the different tissues of its mosquito vector and onwards to infect a new vertebrate host. Despite the intricacies inherent in these successive transformations, malaria parasites remain staggeringly successful at disseminating through their vertebrate host populations.