Competing for blood: the ecology of parasite resource competition in human malaria–helminth co‐infections

Ecological theory suggests that co‐infecting parasite species can interact within hosts directly, via host immunity and/or via resource competition. In mice, competition for red blood cells (RBCs) between malaria and bloodsucking helminths can regulate malaria population dynamics, but the importance of RBC competition in human hosts was unknown. We analysed infection density (i.e. the concentration of parasites in infected hosts), from a 2‐year deworming study of over 4000 human subjects. After accounting for resource‐use differences among parasites, we find evidence of resource competition, priority effects and a competitive hierarchy within co‐infected individuals. For example reducing competition via deworming increased Plasmodium vivax densities 2.8‐fold, and this effect is limited to bloodsucking hookworms. Our ecological, resource‐based perspective sheds new light into decades of conflicting outcomes of malaria–helminth co‐infection studies with significant health and transmission consequences. Beyond blood, investigating within‐human resource competition may bring new insights for improving human health.     

One stimulus—Two responses: Host and parasite life‐history variation in response to environmental stress

Climate change stressors will place different selective pressures on both parasites and their hosts, forcing individuals to modify their life‐history strategies and altering the distribution and prevalence of disease. Few studies have investigated whether parasites are able to respond to host stress and respond by varying their reproductive schedules. Additionally, multiple environmental stressors can limit the ability of a host to respond adaptively to parasite infection. This study compared both host and parasite life‐history parameters in unstressed and drought‐stressed environments using the human parasite, Schistosoma mansoni, in its freshwater snail intermediate host. Snail hosts infected with the parasite demonstrated a significant reproductive burst during the prepatent period (fecundity compensation), but that response was absent in a drought‐stressed environment. This is the first report of the elimination of host fecundity compensation to parasitism when exposed to additional environmental stress. More surprisingly, we found that infections in drought‐stressed snails had significantly higher parasite reproductive outputs than infections in unstressed snails. The finding suggests that climate change may alter the infection dynamics of this human parasite.     

Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

While the host immune system is often considered the most important physiological mechanism against parasites, precontact mechanisms determining exposure to parasites may also affect infection dynamics. For instance, chemical cues released by hosts can attract parasite transmission stages. We used the freshwater snail Lymnaea stagnalis and its trematode parasite Echinoparyphium aconiatum to examine the role of host chemical attractiveness, physiological condition, and immune function in determining its susceptibility to infection. We assessed host attractiveness through parasite chemo‐orientation behavior; physiological condition through host body size, food consumption, and respiration rate; and immune function through two immune parameters (phenoloxidase‐like and antibacterial activity of hemolymph) at an individual level. We found that, although snails showed high variation in chemical attractiveness to E. aconiatum cercariae, this did not determine their overall susceptibility to infection. This was because large body size increased attractiveness, but also increased metabolic activity that reduced overall susceptibility. High metabolic rate indicates fast physiological processes, including immune activity. The examined immune traits, however, showed no association with susceptibility to infection. Our results indicate that postcontact mechanisms were more likely to determine snail susceptibility to infection than variation in attractiveness to parasites. These may include localized immune responses in the target tissue of the parasite. The lack of a relationship between food consumption and attractiveness to parasites contradicts earlier findings that show food deprivation reducing snail attractiveness. This suggests that, although variation in resource level over space and time can alter infection dynamics, variation in chemical attractiveness may not contribute to parasite‐induced fitness variation within populations when individuals experience similar environmental conditions.     

Bottom–up regulation of parasite population densities in freshwater ecosystems

Theory predicts the bottom–up coupling of resource and consumer densities, and epidemiological models make the same prediction for host–parasite interactions. Empirical evidence that spatial variation in local host density drives parasite population density remains scarce, however. We test the coupling of consumer (parasite) and resource (host) populations using data from 310 populations of metazoan parasites infecting invertebrates and fish in New Zealand lakes, spanning a range of transmission modes. Both parasite density (no. parasites per m²) and intensity of infection (no. parasites per infected hosts) were quantified for each parasite population, and related to host density, spatial variability in host density and transmission mode (egg ingestion, contact transmission or trophic transmission). The results show that dense and temporally stable host populations are exploited by denser and more stable parasite populations. For parasites with multi‐host cycles, density of the ‘source’ host did not matter: only density of the current host affected parasite density at a given life stage. For contact‐transmitted parasites, intensity of infection decreased with increasing host density. Our results support the strong bottom–up coupling of consumer and resource densities, but also suggest that intraspecific competition among parasites may be weaker when hosts are abundant: high host density promotes greater parasite population density, but also reduces the number of conspecific parasites per individual host.     

Experimental warming drives a seasonal shift in the timing of host‐parasite dynamics with consequences for disease risk

Multi‐species experiments are critical for identifying the mechanisms through which climate change influences population dynamics and community interactions within ecological systems, including infectious diseases. Using a host–parasite system involving freshwater snails, amphibians and trematode parasites, we conducted a year‐long, outdoor experiment to evaluate how warming affected net parasite production, the timing of infection and the resultant pathology. Warming of 3 °C caused snail intermediate hosts to release parasites 9 months earlier and increased infected snail mortality by fourfold, leading to decreased overlap between amphibians and parasites. As a result, warming halved amphibian infection loads and reduced pathology by 67%, despite comparable total parasite production across temperature treatments. These results demonstrate that climate–disease theory should be expanded to account for predicted changes in host and parasite phenology, which may often be more important than changes in total parasite output for predicting climate‐driven changes in disease risk.     

Niche theory for within-host parasite dynamics: Analogies to food web modules via feedback loops

Why do parasites exhibit a wide dynamical range within their hosts? For instance, why does infecting dose either lead to infection or immune clearance? Why do some parasites exhibit boom-bust, oscillatory dynamics? What maintains parasite diversity, that is coinfection v single infection due to exclusion or priority effects? For insights on parasite dose, dynamics and diversity governing within-host infection, we turn to niche models. An omnivory food web model (IGP) blueprints one parasite competing with immune cells for host energy (PIE). Similarly, a competition model (keystone predation, KP) mirrors a new coinfection model (2PIE). We then drew analogies between models using feedback loops. The following three points arise: first, like in IGP, parasites oscillate when longer loops through parasites, immune cells and resource regulate parasite growth. Shorter, self-limitation loops (involving resources and enemies) stabilise those oscillations. Second, IGP can produce priority effects that resemble immune clearance. But, despite comparable loop structure, PIE cannot due to constraints imposed by production of immune cells. Third, despite somewhat different loop structure, KP and 2PIE share apparent and resource competition mechanisms that produce coexistence (coinfection) or priority effects of prey or parasites. Together, this mechanistic niche framework for within-host dynamics offers new perspective to improve individual health.     

Save your host,save yourself? Caste‐ratio adjustment in a parasite with division of labor and snail host survival following shell damage

Shell damage and parasitic infections are frequent in gastropods, influencing key snail host life‐history traits such as survival, growth, and reproduction. However, their interactions and potential effects on hosts and parasites have never been tested. Host–parasite interactions are particularly interesting in the context of the recently discovered division of labor in trematodes infecting marine snails. Some species have colonies consisting of two different castes present at varying ratios; reproductive members and nonreproductive soldiers specialized in defending the colony. We assessed snail host survival, growth, and shell regeneration in interaction with infections by two trematode species, Philophthalmus sp. and Maritrema novaezealandense, following damage to the shell in the New Zealand mud snail Zeacumantus subcarinatus. We concomitantly assessed caste‐ratio adjustment between nonreproductive soldiers and reproductive members in colonies of the trematode Philophthalmus sp. in response to interspecific competition and shell damage to its snail host. Shell damage, but not parasitic infection, significantly increased snail mortality, likely due to secondary infections by pathogens. However, trematode infection and shell damage did not negatively affect shell regeneration or growth in Z. subcarinatus; infected snails actually produced more new shell than their uninfected counterparts. Both interspecific competition and shell damage to the snail host induced caste‐ratio adjustment in Philophthalmus sp. colonies. The proportion of nonreproductive soldiers increased in response to interspecific competition and host shell damage, likely to defend the parasite colony and potentially the snail host against increasing threats. These results indicate that secondary infections by pathogens following shell damage to snails both significantly increased snail mortality and induced caste‐ratio adjustments in parasites. This is the first evidence that parasites with a division of labor may be able to produce nonreproductive soldiers according to environmental factors other than interspecific competition with other parasites.     

Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host

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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.     

Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts

Predators of parasites have recently gained attention as important parts of food webs and ecosystems. In aquatic systems, many taxa consume free‐living stages of parasites, and can thus reduce parasite transmission to hosts. However, the importance of the functional and numerical responses of parasite predators to disease dynamics is not well understood. We collected host–parasite–predator cooccurrence data from the field, and then experimentally manipulated predator abundance, parasite abundance, and the presence of alternative prey to determine the consequences for parasite transmission. The parasite predator of interest was a ubiquitous symbiotic oligochaete of mollusks, Chaetogaster limnaei limnaei, which inhabits host shells and consumes larval trematode parasites. Predators exhibited a rapid numerical response, where predator populations increased or decreased by as much as 60% in just 5 days, depending on the parasite:predator ratio. Furthermore, snail infection decreased substantially with increasing parasite predator densities, where the highest predator densities reduced infection by up to 89%. Predators of parasites can play an important role in regulating parasite transmission, even when infection risk is high, and especially when predators can rapidly respond numerically to resource pulses. We suggest that these types of interactions might have cascading effects on entire disease systems, and emphasize the importance of considering disease dynamics at the community level.     

Host resistance and tolerance of parasitic gut worms depend on resource availability

Resource availability can significantly alter host–parasite dynamics. Abundant food can provide more resources for hosts to resist infections, but also increase host tolerance of infections by reducing competition between hosts and parasites for food. Whether abundant food favors host resistance or tolerance (or both) might depend on the type of resource that the parasite exploits (e.g., host tissue vs. food), which can vary based on the stage of infection. In our study, we evaluated how low and high resource diets affect Cuban tree frog (Osteopilus septentrionalis) resistance and tolerance of a skin-penetrating, gut nematode Aplectana sp. at each stage of the infection. Compared to a low resource diet, a high resource diet enhanced frog resistance to worm penetration and tolerance while worms traveled to the gut. In contrast, a low resource diet increased resistance to establishment of the infection. After the infection established and worms could access food resources in the gut, a high resource diet enhanced host tolerance of parasites. On a high resource diet, parasitized frogs consumed significantly more food than non-parasitized frogs; when food was then restricted, mass of non-parasitized frogs did not change, whereas mass of parasitized frogs decreased significantly. Thus, a high resource diet increased frog tolerance of established worms because frogs could fully compensate for energy lost to the parasites. Our study shows that host–parasite dynamics are influenced by the effect of resource availability on host resistance and tolerance, which depends on when parasites have access to food and the stage of infection.     

Coinfecting parasites can modify fluctuating selection dynamics in host–parasite coevolution

Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host–parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.     

Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria‐phage system

Host–parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host–parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host–parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.     

Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction

Whether or not organisms become infected by parasites is likely to be a complex interplay between host and parasite genotypes, as well as the physiological condition of both species. Details of this interplay are very important because physiology‐driven susceptibility has the potential to confound genetic coevolutionary responses. Here we concentrate on how physiological aspects of infection may interfere with genetic‐based infectivity in a snail–trematode (Potamopyrgus antipodarum/Microphallus sp.) interaction by asking: (1) how does host condition affect susceptibility to infection? and (2) how does host condition affect the survival of infected individuals? We manipulated host condition by experimentally varying resources. Contrary to our expectation, host condition did not affect susceptibility to infection, suggesting that genetics are more important than physiology in this regard. However, hosts in poor condition had higher parasite‐induced mortality than hosts in good condition. Taken together, these results suggest that coevolutionary interactions with parasites may depend on host condition, not by altering susceptibility, but rather by affecting the likelihood of parasite transmission.     

Parasite consumption and host interference can inhibit disease spread in dense populations

Disease dynamics hinge on parasite transmission among hosts. However, canonical models for transmission often fit data poorly, limiting predictive ability. One solution involves building mechanistic yet general links between host behaviour and disease spread. To illustrate, we focus on the exposure component of transmission for hosts that consume their parasites, combining experiments, models and field data. Models of transmission that incorporate parasite consumption and foraging interference among hosts vastly outperformed alternatives when fit to experimental data using a zooplankton host (Daphnia dentifera) that consumes spores of a fungus (Metschnikowia bicuspidata). Once plugged into a fully dynamic model, both mechanisms inhibited epidemics overall. Foraging interference further depressed parasite invasion and prevalence at high host density, creating unimodal (hump‐shaped) relationships between host density and these indices. These novel results qualitatively matched a unimodal density–prevalence relationship in natural epidemics. Ultimately, a mechanistic approach to transmission can reveal new insights into disease outbreaks.     

Manipulation of host-resource dynamics impacts transmission of trophic parasites

Many complex life cycle parasites rely on predator–prey interactions for transmission, whereby definitive hosts become infected via the consumption of an infected intermediate host. As such, these trophic parasites are embedded in the larger community food web. We postulated that exposure to infection and, hence, parasite transmission are inherently linked to host foraging ecology, and that perturbation of the host-resource dynamic will impact parasite transmission dynamics. We employed a field manipulation experiment in which natural populations of the eastern chipmunk (Tamias striatus) were provisioned with a readily available food resource in clumped or uniform spatial distributions. Using replicated longitudinal capture-mark-recapture techniques, replicated supplemented and unsupplemented control sites were monitored before and after treatment for changes in infection levels with three gastro-intestinal helminth parasites. We predicted that definitive hosts subject to food supplementation would experience lower rates of exposure to infective intermediate hosts, presumably because they shifted their diet away from the intermediate host towards the more readily available resource (sunflower seeds). As predicted, prevalence of infection by the trophically transmitted parasite decreased in response to supplemental food treatment, but no such change in infection prevalence was detected for the two directly transmitted parasites in the system. The fact that food supplementation only had an impact on the transmission of the trophically transmitted parasite, and not the directly transmitted parasites, supports our hypothesis that host foraging ecology directly affects exposure to parasites that rely on the ingestion of intermediate hosts for transmission. We concluded that the relative availability of different food resources has important consequences for the transmission of parasites and, more specifically, parasites that are embedded in the food web. The broader implications of these findings for food web dynamics and disease ecology are discussed.     

Plant sex alters Allee effects in aggregating plant parasites

Species interactions are central to our understanding of population dynamics. While density typically strengthens competition, reducing absolute fitness, Allee effects can reverse this pattern, increasing fitness with density. Allee effects emerge in host–parasite systems when higher parasite densities dilute immune responses or increase resource‐mobilization. The optimal density of individuals in these systems should be influenced by how host quality alters the rates at which facilitative and competitive effects change across densities. We tested these ideas using sumac Rhus typhina and a gall‐forming parasite Melaphis rhois that attacks sumac leaves. Fitness peaked at intermediate densities, indicating an Allee effect, but the fitness peak depended on host sex. Patterns of abundance mirrored fitness patterns, with galls clustered on leaves and female hosts supporting greater numbers of galls. Within leaves, galls near the stem were more fit, and gall‐makers preferentially oviposited near to the stem. The patterns of fitness and abundance are consistent with Allee effects caused by increased resource mobilization at higher gall‐maker densities rather than diluted immune responses. Our results suggest that Allee effects in parasites can be described as the summative effects of competitive and facilitative processes and, because both are common, Allee effects are likely common in host–parasite systems.     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.     

On the capacity of macroparasites to control insect populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite-induced host mortality, reduction in host density as a result of parasite-induced host sterility, and competition among parasites within multiply-infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite-induced host sterility will control the insect populations below the level set by larval resources if the threshold host density for the parasites (N(T)) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite-induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters N(T), K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within-host competition, making the conditions for parasite control of the flies more stringent.     

Dose effects and density-dependent regulation of two microparasites of<Emphasis Type="Italic"> Daphnia magna</Emphasis>

Individual hosts constitute a limited resource for parasites, suggesting that density-dependent effects may play a role in within-host growth and parasite regulation. This hypothesis has been tested for several helminth parasites, but not for microparasites. We therefore examined dose-response patterns for the microparasitic bacterium Pasteuria ramosa and the fungus Metschnikowiella biscuspidata infecting the planktonic crustacean Daphnia magna. With increasing numbers of transmission stages administered to the host we found that host fecundity and survival and parasite transmission-stage production declined. Using a k-value analysis, a method that quantifies the strength of density dependence, we found for both parasites that density dependence acted at all doses, indicating the absence of a minimum density below which parasite fitness is density- independent. At low doses density was exactly compensated, but it was overcompensated at high doses. Overcompensation at high doses was weak for P. ramosa, but high for M. biscuspidata. At the two highest doses M. biscuspidata killed its hosts before any transmission stages were produced. Our data indicate that density dependence is expressed through retarded spore development in P. ramosa, but through both host mortality and reduced parasite fecundity in M. biscuspidata. A further experiment (P. ramosa only) revealed that in well-fed hosts more parasite transmission stages are produced than in poorly fed hosts, suggesting that competition for host resources retards P. ramosa development. Our data for P. ramosa, but not for M. biscuspidata, are largely consistent with assumptions made in models on microparasite epidemiology. We draw attention to the relevance of dose effects and within-host competition for the evolution of virulence. Received: 15 July 1999 / Accepted: 14 September 1999