Search for: All records

Parasites often coinfect host populations, and, by interacting within hosts, might change the trajectory of multi-parasite epidemics. However, host-parasite interactions often change with host age, raising the possibility that within-host interactions between parasites might also change, influencing the spread of disease. We measured how heterospecific parasites interacted within zooplankton hosts and how host age changed these interactions. We then parameterized an epidemiological model to explore how age-effects altered the impact of coinfection on epidemic dynamics. In our model, we found that in populations where epidemiologically relevant parameters did not change with age, the presence of a second parasite altered epidemic dynamics. In contrast, when parameters varied with host age (based on our empirical measures), there was no longer a difference in epidemic dynamics between singly and coinfected populations, indicating that variable age structure within a population eliminates the impact of coinfection on epidemic dynamics. Moreover, infection prevalence of both parasites was lower in populations where epidemiologically relevant parameters changed with age. Given that hostpopulation age structure changes over time and space, these results indicate that age-effects are important for understanding epidemiological processes in coinfected systems and that studies focused on a single age group could yield inaccurate insights. 

Theory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a “resistance is futile” outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts’ resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, “transmission rate”) along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations. 

Abstract Transgenerational plasticity can help organisms respond rapidly to changing environments. Most prior studies of transgenerational plasticity in host–parasite interactions have focused on the host, leaving us with a limited understanding of transgenerational plasticity of parasites. We tested whether exposure to elevated temperatures while spores are developing can modify the ability of those spores to infect new hosts, as well as the growth and virulence of the next generation of parasites in the new host. We exposed Daphnia dentifera to its naturally co-occurring fungal parasite Metschnikowia bicuspidata , rearing the parasite at cooler (20°C) or warmer (24°C) temperatures and then, factorially, using those spores to infect at 20 and 24°C. Infections by parasites reared at warmer past temperatures produced more mature spores, but only when the current infections were at cooler temperatures. Moreover, the percentage of mature spores was impacted by both rearing and current temperatures, and was highest for infections with spores reared in a warmer environment that infected hosts in a cooler environment. In contrast, virulence was influenced only by current temperatures. These results demonstrate transgenerational plasticity of parasites in response to temperature changes, with fitness impacts that are dependent on both past and current environments. 

Disease ecologists now recognize the limitation behind examining host–parasite interactions in isolation: community members—especially predators—dramatically affect host–parasite dynamics. Although the initial paradigm was that predation should reduce disease in prey populations (“healthy herds hypothesis”), researchers have realized that predators sometimes increase disease in their prey. These “predator–spreaders” are now recognized as critical to disease dynamics, but empirical research on the topic remains fragmented. In a narrow sense, a “predator–spreader” would be defined as a predator that mechanically spreads parasites via feeding. However, predators affect their prey and, subsequently, disease transmission in many other ways such as altering prey population structure, behavior, and physiology. We review the existing evidence for these mechanisms and provide heuristics that incorporate features of the host, predator, parasite, and environment to understand whether or not a predator is likely to be a predator–spreader. We also provide guidance for targeted study of each mechanism and quantifying the effects of predators on parasitism in a way that yields more general insights into the factors that promote predator spreading. We aim to offer a better understanding of this important and underappreciated interaction and a path toward being able to predict how changes in predation will influence parasite dynamics.

 

Virulence, the degree to which a pathogen harms its host, is an important but poorly understood aspect of host-pathogen interactions. Virulence is not static, instead depending on ecological context and potentially evolving rapidly. For instance, at the start of an epidemic, when susceptible hosts are plentiful, pathogens may evolve increased virulence if this maximizes their intrinsic growth rate. However, if host density declines during an epidemic, theory predicts evolution of reduced virulence. Although well-studied theoretically, there is still little empirical evidence for virulence evolution in epidemics, especially in natural settings with native host and pathogen species. Here, we used a combination of field observations and lab assays in theDaphnia-Pasteuriamodel system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak ofPasteuria ramosainDaphnia dentifera, where infection prevalence peaked at ~ 40% of the population infected and host density declined precipitously during the outbreak. In controlled infections in the lab, lifespan and reproduction of infected hosts was lower than that of unexposed control hosts and of hosts that were exposed but not infected. We did not detect any significant changes in host resistance or parasite infectivity, nor did we find evidence for shifts in parasite virulence (quantified by host lifespan and number of clutches produced by hosts). However, over the epidemic, the parasite evolved to produce significantly fewer spores in infected hosts. While this finding was unexpected, it might reflect previously quantified tradeoffs: parasites in high mortality (e.g., high predation) environments shift from vegetative growth to spore production sooner in infections, reducing spore yield. Future studies that track evolution of parasite spore yield in more populations, and that link those changes with genetic changes and with predation rates, will yield better insight into the drivers of parasite evolution in the wild.

 

Infectious disease can threaten host populations. Hosts can rapidly evolve resistance during epidemics, with this evolution often modulated by fitness trade-offs (e.g., between resistance and fecundity). However, many organisms switch between asexual and sexual reproduction, and this shift in reproductive strategy can also alter how resistance in host populations persists through time. Recombination can shuffle alleles selected for during an asexual phase, uncoupling the combinations of alleles that facilitated resistance to parasites and altering the distribution of resistance phenotypes in populations. Furthermore, in host species that produce diapausing propagules (e.g., seeds, spores, or resting eggs) after sex, accumulation of propagules into and gene flow out of a germ bank introduce allele combinations from past populations. Thus, recombination and gene flow might shift populations away from the trait distribution reached after selection by parasites. To understand how recombination and gene flow alter host population resistance, we tracked the genotypic diversity and resistance distributions of two wild populations of cyclical parthenogens. In one population, resistance and genetic diversity increased after recombination whereas, in the other, recombination did not shift already high resistance and genetic diversity. In both lakes, resistance remained high after temporal gene flow. This observation surprised us: due to costs to resistance imposed by a fecundity-resistance trade-off, we expected that high population resistance would be a transient state that would be eroded through time by recombination and gene flow. Instead, low resistance was the transient state, while recombination and gene flow re-established or maintained high resistance to this virulent parasite. We propose this outcome may have been driven by the joint influence of fitness trade-offs, genetic slippage after recombination, and temporal gene flow via the egg bank.