Meghan A. Duffy

Selective Predation and Productivity Jointly Drive Complex Behavior in Host-Parasite Systems

Successful invasion of a parasite into a host population and resulting host‐parasite dynamics can depend crucially on other members of a host’s community such as predators. We do not fully understand how predation intensity and selectivity shape host‐parasite dynamics because the interplay between predator density, predator foraging behavior, and ecosystem productivity remains incompletely explored. By modifying a standard susceptible‐infected model, we show how productivity can modulate complex behavior induced by saturating and selective foraging behavior of predators in an otherwise stable host‐parasite system. When predators strongly prefer parasitized hosts, the host‐parasite system can oscillate, but predators can also create alternative stable states, Allee effects, and catastrophic extinction of parasites. In the latter three cases, parasites have difficulty invading and/or persisting in ecosystems. When predators are intermediately selective, these more complex behaviors become less important, but the host‐parasite system can switch from stable to oscillating and then back to stable states along a gradient of predator control. Surprisingly, at higher productivity, predators that neutrally select or avoid parasitized hosts can catalyze extinction of both hosts and parasites. Thus, synergy between two enemies can end disastrously for the host. Such diverse outcomes underscore the crucial importance of the community and ecosystem context in which host‐parasite interactions occur.

Quality matters: resource quality for hosts and the timing of epidemics

Epidemiologists increasingly realize that species interactions (e.g. selective predation) can determine when epidemics start and end. We hypothesize here that resource quality can also strongly influence disease dynamics: epidemics can be inhibited when resource quality for hosts is too poor and too good. In three lakes, resource quality for the zooplankton host (Daphnia dentifera) was poor when fungal epidemics (Metschnikowia bicuspidata) commenced and increased as epidemics waned. Experiments using variation in algal food showed that resource quality had conflicting effects on underlying epidemiology: high-quality food induced large production of infective propagules (spores) and high birth rate but also reduced transmission. A model then illustrated how these underlying correlations can inhibit the start of epidemics (when spore production/birth rate are too low) but also catalyse their end (when transmission becomes too low). This resource quality mechanism is likely to interface with other ones controlling disease dynamics and warrants closer evaluation.

Warmer does not have to mean sicker: temperature and predators can jointly drive timing of epidemics.

Ecologists and epidemiologists worry that global warming will increase disease prevalence. These fears arise because several direct and indirect mechanisms link warming to disease, and because parasite outbreaks are increasing in many taxa. However, this outcome is not a foregone conclusion, as physiological and community-interaction-based mechanisms may inhibit epidemics at warmer temperatures. Here, we explore this thermal-community-ecology-based mechanism, centering on fish predators that selectively prey upon Daphnia infected with a fungal parasite. We used an interplay between a simple model built around this systems biology and laboratory experiments designed to parameterize the model. Through this data-model interaction, we found that a given density of predators can inhibit epidemics as temperatures rise when thermal physiology of the predator scales more steeply than that of the host. This case is met in our fish-Daphnia-fungus system. Furthermore, the combination of steeply scaling parasite physiology and predation-induced mortality can inhibit epidemics at lower temperatures. This effect may terminate fungal epidemics of Daphnia as lakes cool in autumn. Thus, predation and physiology could constrain epidemics to intermediate temperatures (a pattern that we see in our system). More generally, these results accentuate the possibility that warmer temperatures might actually enhance predator control of parasites.

Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations.

Parasites are ubiquitous and often highly virulent, yet clear examples of parasite‐driven changes in host density in natural populations are surprisingly scarce. Here, we illustrate an example of this phenomenon and offer a theoretically reasonable resolution. We document the effects of two parasites, the bacterium Spirobacillus cienkowskii and the yeast Metschnikowia bicuspidata, on a common freshwater invertebrate, Daphnia dentifera. We show that while both parasites were quite virulent to individual hosts, only bacterial epidemics were associated with significant changes in host population dynamics and density. Our theoretical results may help explain why yeast epidemics did not significantly affect population dynamics. Using a model parameterized with data we collected, we argue that two prominent features of this system, rapid evolution of host resistance to the parasite and selective predation on infected hosts, both decrease peak infection prevalence and can minimize decline in host density during epidemics. Taken together, our results show that understanding the outcomes of host‐parasite interactions in this Daphnia‐microparasite system may require consideration of ecological context and evolutionary processes and their interaction.

PHYSICAL STRUCTURE OF LAKES CONSTRAINS EPIDEMICS IN DAPHNIA POPULATIONS

Parasites are integral parts of most ecosystems, yet attention has only recently focused on how community structure and abiotic factors impact host-parasite interactions. In lakes, both factors are influenced by habitat morphology. To investigate the role of habitat structure in mediating parasitism in the plankton, we quantified timing and prevalence of a common microparasite (Metschnikowia bicuspidata) in its host, Daphnia dentifera, in 18 lakes that vary in basin size and shape. Over three years, we found substantial spatial and temporal variation in the severity of epidemics. Although infection rates reached as high as 50% in some lakes, they did not occur in most lakes in most years. Host density, often considered to be a key determinant of disease spread, did not explain a significant amount of variation in the occurrence of epidemics. Furthermore, host resistance does not fully explain this parasites distribution, since we easily infected hosts in the laboratory. Rather, basin shape predicted epidemics well; epidemics occurred only in lakes with steep-sided basins. In these lakes, the magnitude of epidemics varied with year. We suggest that biological (predation) and physical (turbulence) effects of basin shape interact with annual weather patterns to determine the regional distribution of this parasite.

Ecological context influences epidemic size and parasite-driven evolution

Cost-Benefit Analysis Mounting resistance to infection is costly, requires energetic input, and may thus compromise fecundity. Duffy et al. (p. 1636; see the cover) tested the relationships between productivity, predation, and mortality in a combination of observations of a natural lake and an experimental replica of a clonal zooplankton-parasitic yeast population. In the wild, epidemics of the yeast could exceed 60% and cause significant host mortality. In this situation, the clonal zooplankton host faces the physiological dilemma of either increasing resistance to deal with infection or of safeguarding fecundity. Zooplankton that feed quickly can reproduce quickly, but also end up ingesting more yeast spores. However, because fish tend to cull infected hosts, fish predation counters infection. Ultimately, both wild and model systems showed that lakes with high productivity (more nitrogen) and/or few fish supported greater epidemics of yeast and more resistant hosts, whereas less productive lakes, or those with more fish, had smaller epidemics and hosts with higher susceptibility to the yeast. When the physiological cost of host resistance to a disease damages reproductive output, disease susceptibility can evolve. The occurrence and magnitude of disease outbreaks can strongly influence host evolution. In particular, when hosts face a resistance-fecundity trade-off, they might evolve increased resistance to infection during larger epidemics but increased susceptibility during smaller ones. We tested this theoretical prediction by using a zooplankton-yeast host-parasite system in which ecological factors determine epidemic size. Lakes with high productivity and low predation pressure had large yeast epidemics; during these outbreaks, hosts became more resistant to infection. However, with low productivity and high predation, epidemics remained small and hosts evolved increased susceptibility. Thus, by modulating disease outbreaks, ecological context (productivity and predation) shaped host evolution during epidemics. Consequently, anthropogenic alteration of productivity and predation might strongly influence both ecological and evolutionary outcomes of disease.

Parasite-mediated disruptive selection in a natural Daphnia population

BackgroundA mismatch has emerged between models and data of host-parasite evolution. Theory readily predicts that parasites can promote host diversity through mechanisms such as disruptive selection. Yet, despite these predictions, empirical evidence for parasite-mediated increases in host diversity remains surprisingly scant.ResultsHere, we document parasite-mediated disruptive selection on a natural Daphnia population during a parasite epidemic. The mean susceptibility of clones collected from the population before and after the epidemic did not differ, but clonal variance and broad-sense heritability of post-epidemic clones were significantly greater, indicating disruptive selection and rapid evolution. A maximum likelihood method that we developed for detecting selection on natural populations also suggests disruptive selection during the epidemic: the distribution of susceptibilities in the population shifted from unimodal prior to the epidemic to bimodal after the epidemic. Interestingly, this same bimodal distribution was retained after a generation of sexual reproduction.ConclusionThese results provide rare empirical support for parasite-driven increases in host genetic diversity, and suggest that this increase can occur rapidly.

Rapid evolution, seasonality, and the termination of parasite epidemics.

Why do epidemics end? This simple question has puzzled ecologists and epidemiologists for decades. Early explanations focused on drops in host density arising from highly virulent parasites and, later, on the effects of acquired immunity. More recently, however, two additional epidemic-ending mechanisms have surfaced: environmental change (including seasonality) and rapid evolution of increased resistance of hosts to infection. Both mechanisms, via either decreasing seasonal temperatures or evolution of resistance, act by altering transmission rates. To explore these possibilities, we tracked five epidemics of a virulent yeast parasite in lake populations of Daphnia dentifera from late summer through autumn. We then fit and compared performance of time-series models that included temperature-dependent and/or evolutionary changes in transmission rates. The analyses show evolution to be the better explanation of epidemic dynamics. Thus, by integrating data and models, this study highlights the potential role of evolution in driving the termination of epidemics in natural populations.

Variation in Resource Acquisition and Use among Host Clones Creates Key Epidemiological Trade-Offs

Parasites can certainly harm host fitness. Given such virulence, hosts should evolve strategies to resist or tolerate infection. But what governs those strategies and the costs that they incur? This study illustrates how a fecundity‐susceptibility trade‐off among clonally reared genotypes of a zooplankton (Daphnia dentifera) infected by a fungal parasite (Metschnikowia) arises due to variation in resource acquisition and use by hosts. To make these connections, we used lab experiments and theoretical models that link feeding with susceptibility, energetics, and fecundity of hosts. These feeding‐based mechanisms also produced a fecundity‐survivorship trade‐off. Meanwhile, a parasite spore yield–fecundity trade‐off arose from variation in juvenile growth rate among host clones (another index of resource use), a result that was readily anticipated and explained by the models. Thus, several key epidemiological trade‐offs stem from variation in resource acquisition and use among clones. This connection should catalyze the creation of new theory that integrates resource‐ and gene‐based responses of hosts to disease.

Ecological feedbacks and the evolution of resistance.

1. The idea that parasites can affect host diversity is pervasive, and the possibility that parasites can increase host diversity is of particular interest. In this review, we focus on diversity in the resistance of hosts to their parasites, and on the different ways in which parasites can increase or decrease this resistance diversity. 2. Theoretically, parasites can exert many different types of selection on host populations, which each have consequences for host diversity. Specifically, theory predicts that parasites can exert negative frequency-dependent selection (NFDS) and disruptive selection on resistance, both of which increase host diversity, as well as directional selection and stabilizing selection on resistance, both of which decrease host diversity. 3. Despite these theoretical predictions, most biologists think of only NFDS or directional selection for increased resistance in response to parasitism. Here, we present empirical support for all of these types of selection occurring in natural populations. Interestingly, several recent studies demonstrate that there is spatiotemporal variation in the type of selection that occurs (and, therefore, in the effects of parasitism on host diversity). 4. A key question that remains, then, is: What determines the type of parasite-mediated selection that occurs? Theory demonstrates that the answer to this question lies, at least in part, with trade-offs associated with resistance. Specifically, the type of evolution that occurs depends critically on the strength and shape of these trade-offs. This, combined with empirical evidence for a strong effect of environment on the shape and strength of trade-offs, may explain the observed spatiotemporal variation in parasite-mediated selection. 5. We conclude that spatiotemporal variation in parasite-driven evolution is likely to be common, and that this variation may be driven by ecological factors. We suggest that the feedback between ecological and evolutionary dynamics in host-parasite interactions is likely to be a productive area of research. In particular, studies addressing the role of ecological factors (e.g. productivity and predation regimes) in driving the outcome of parasite-mediated selection on host populations are warranted. Such studies are necessary if we are to understand the mechanisms underlying the observed variation in the effects of parasites on host diversity.