1. Secondary metabolites produced by primary producers have a wide range of functions as well as indirect effects outside the scope of their direct target. Research suggests that protease inhibitors produced by cyanobacteria influence grazing by herbivores and may also protect against parasites of cyanobacteria. In this study we asked whether those same protease inhibitors produced by cyanobacteria also can influence interactions of herbivores with their parasites. 2. We used the Daphnia-Metschnikowia zooplankton host-fungal parasite system to address this question because it is well documented that cyanobacteria protease inhibitors suppress trypsin and chymotrypsin in the gut of Daphnia, and because it is known that Metschnikowia infects via the gut. We tested the hypothesis that Daphnia gut proteases are necessary for Metschnikowia spores to be released from their asci. We then also tested whether diets that decrease trypsin and chymotrypsin activity in the guts of Daphnia lead to lower levels of infection. 3. Our results show that chymotrypsin promotes release of the fungal spores from their asci. Moreover, a diet that strongly inhibited chymotrypsin activity in Daphnia decreased infection levels, particularly in the most susceptible Daphnia clones. 4. Our results support the growing literature that cyanobacterial diets can be beneficial to zooplankton hosts when challenged by parasites and uncover a mechanism that contributes to the protective effect of cyanobacterial diets. Specifically, we demonstrate that host chymotrypsin enzymes promote dehiscence of Metschnikowia spores; when cyanobacteria inhibit activity of chymotrypsin in hosts, this most likely traps the spore inside the ascus, preventing the parasite from puncturing the gut and beginning the infection process. 5. This study illustrates how secondary metabolites of phytoplankton can protect herbivores against their own enemies.

Most parasite species infect multiple host species, and reciprocally, most hosts are infected by multiple parasites. This leads to complex webs of interactions that influence disease within the community, making it challenging to understand and predict disease spread within the community and epidemics. Here, we used network approaches to analyze a multi-year time series dataset that includes eight zooplankton host species (in the Daphnia and Ceriodaphnia genera) and seven microparasite species to examine patterns of cross-species transmission. These analyses suggest that parasite species varied in their ability to infect multiple host species and in which host species they most commonly infected. Three parasites (the bacteria Pasteuria ramosa and Spirobacillus cienkowskii and the oomycete Blastulidium paedophthorum) showed signatures of relatively high cross species transmission, while the others seemed more restricted. Even for the three common multihost parasites, our approach also revealed differences in patterns of potential cross species transmission. For P. ramosa, two host species, Daphnia dentifera and D. retrocurva, seem particularly likely to transmit across species; in contrast, for S. cienkowskii, no host species stands out as particularly important for cross species transmission. Additionally, these patterns matched those describing epidemic size, suggesting that infected host density may drive cross-species transmission. These results are based on observations of patterns of infection in natural communities, and therefore we cannot draw definitive conclusions about interspecific transmission in lakes. However, some of the patterns are supported by additional lines of evidence, and others point to interesting avenues for future research. Together, these findings provide additional evidence that network approaches can provide valuable insights into patterns of transmission in complex multihost-multiparasite communities in nature.

Myriad ecological and evolutionary factors can influence whether a particular parasite successfully transmits to a new host during a disease outbreak, with consequences for the structure and diversity of parasite populations. However, even though the diversity and evolution of parasite populations is of clear fundamental and applied importance, we have surprisingly few studies that track how genetic structure of parasites changes during naturally occurring outbreaks in non-human populations. Here, we used population genetic approaches to reveal how genotypes of a bacterial parasite, Pasteuria ramosa, change over time, focusing on how infecting P. ramosa genotypes change during the course of epidemics in Daphnia populations in two lakes. We found evidence for genetic change – and, therefore, evolution – of the parasite during outbreaks. In one lake, P. ramosa genotypes structured by sampling date; in both lakes, genetic distance between groups of P. ramosa isolates increased with time between sampling. Diversity in parasite populations remained constant over epidemics, though one epidemic (which was large) had low genetic diversity while the other epidemic (which was small) had high genetic diversity. Our findings demonstrate that patterns of parasite evolution differ between outbreaks; future studies exploring the feedbacks between epidemic size, host diversity, and parasite genetic diversity would improve our understanding of parasite dynamics and evolution.

Organisms are increasingly facing multiple stressors, which can simultaneously interact to cause unpredictable impacts compared to a single stressor alone. Recent evidence suggests that phenotypic plasticity can allow for rapid responses to altered environments, including biotic and abiotic stressors, both within a generation and across generations (transgenerational plasticity). Parents can potentially ‘prime’ their offspring to better cope with similar stressors, or, alternatively, might produce offspring that are less fit because of energetic constraints. At present, it remains unclear exactly how biotic and abiotic stressors jointly mediate the responses of transgenerational plasticity, and whether this plasticity is adaptive. Here we test the effects of biotic and abiotic environmental changes on within- and trans-generational plasticity using a Daphnia-Metschnikowia zooplankton-fungal parasite system. By exposing parents and their offspring consecutively to the single and combined effects of temperature elevation and parasite infection, we showed that transgenerational plasticity induced by temperature and parasite stress influenced host fecundity and lifespan; offspring of mothers that were exposed to one of the stressors were better able to tolerate temperature elevation, compared to offspring of mothers that were exposed to neither or both stressors. Yet the negative effects caused by parasite infection were much stronger, and this greater reduction in host fitness was not mitigated by transgenerational plasticity. We also showed that temperature elevation led to a lower average immune response, but the nature of its relationship with fecundity reversed under elevated temperatures; this suggests that parents that were exposed to parasites can potentially prime their offspring to respond to the joint stressors of both temperature elevation and parasite infection. Together, our results highlight the need to address questions at the interface of multiple stressors and transgenerational plasticity, and the importance of considering multiple fitness-associated traits when evaluating the adaptive value of transgenerational plasticity under changing 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 towards being able to predict how changes in predation will influence parasite dynamics.

Predators can strongly influence disease transmission and evolution, particularly when they prey selectively on infected hosts. Although selective predation has been observed in numerous systems, why predators select infected prey remains poorly understood. Here, we use a model of predator vision to test a longstanding hypothesis as to the mechanistic basis of selective predation in a Daphnia-microparasite system, which serves as a model for the ecology and evolution of infectious diseases. Bluegill sunfish feed selectively on Daphnia with a variety of parasites, particularly in water uncolored by dissolved organic carbon. The leading hypothesis for selective predation in this system is that infection-induced changes in the appearance of Daphnia render them more visible to bluegill. Rigorously evaluating this hypothesis requires that we quantify the effect of infection on the visibility of prey from the predator’s perspective, rather than our own. Using a model of the bluegill visual system, we show that the three common parasites, Metschnikowia bicuspidata, Pasteuria ramosa and Spirobacillus cienkowskii, increase the opacity of Daphnia, rendering infected Daphnia darker against the background of downwelling light. As a result of this increased brightness contrast, bluegill can see infected Daphnia at greater distances than uninfected Daphnia – between 19-33% further, depending on the parasite. Pasteuria and Spirobacillus also increase the chromatic contrast of Daphnia. Contrary to expectations, the visibility Daphnia was not strongly impacted by water color in our model. Our work generates hypotheses about which parasites are most likely affected by selective predation in this important model system and establishes visual models as a valuable tool for understanding ecological interactions that impact disease transmission.

A document by Meghan Duffy. Click on the document to view its contents.

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 three 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.

A document by Meghan Duffy. Click on the document to view its contents.