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Duffy, M. A.

Publications and source records attributed to Duffy, M. A..

13 recordsLinked to original sources

Symbiont virulence is a poor predictor of impacts on host population dynamics

Symbionts are classified as parasites or mutualists based on their impacts on host individuals, but timescale, ecological context, and level of biological organization can all influence symbiosis outcomes, and hence whether they are deemed harmful or beneficial. We designed experiments exposing the key freshwater grazer Daphnia dentifera to two symbionts varying in virulence, to test how well individual-level effects translate into population-level patterns. We found that a seemingly mildly virulent microsporidian strongly reduced host population size, with consequences for primary production, while a yeast that was highly virulent to individuals had no detectable negative effects on host population size. Our experiments show that studies that fail to consider the impacts of symbionts at multiple scales risk focusing mitigation and control measures on the wrong symbionts.

ecology↗

Resource Quality Differentially Impacts Daphnia Interactions with Two Parasites

Resource quality can have conflicting effects on host-parasite interactions; for example, higher resource quality might increase host investment in immune function, or conversely, might permit greater parasite reproduction. Thus, anticipating the impact of changing resource quality on host- parasite interactions is challenging, especially because we often lack a mechanistic understanding of how resource quality influences host physiology and fitness to alter infection outcomes. We investigated whether there are generalizations in how resource quality affects multiple host clones interactions with different parasites. We used the Daphnia freshwater zooplankton model system to experimentally investigate how a resource quality gradient from high-quality green algae to poor-quality cyanobacteria diets influences host fitness, physiology, and infection by two parasites: a bacterium, Pasteuria ramosa, and a fungus, Metschnikowia bicuspidata. We ran a separate experiment for each parasite using a factorial design with four diets, two Daphnia dentifera host clones, and parasite-inoculated and uninoculated treatments (16 treatments per experiment). Diet strongly influenced infection by the fungus but not the bacterium. These relationships between diet and infection cannot be explained by changes in feeding rate (and, therefore, parasite exposure). Instead, the impact of diet on fungal infection was associated with impacts of diet on the earliest stage of infection: hosts that fed on poor quality diets had very few attacking spores in their guts. Diet did not significantly influence host immune responses. Diet influenced spore production differently for the two parasites, with reduced resource quality limiting the number of fungal spores and the size (but not number) of bacterial spores. Diet, host clone, and infection all affected host fitness. Interestingly, diet influenced the impact of the bacterium, a parasitic castrator that induces gigantism; for one clone, infected hosts fed high quality diets still produced a substantial number of offspring, whereas resource limitation hindered gigantism. Finally, there were often costs of resisting infection, though these generally were not affected by diet. Overall, we show that resource quality differentially impacts the exposure, infection, and proliferation processes for different parasites and host clones, which highlights the need to use multi-genotype and multi-parasite studies to better understand these complex interactions.

ecology↗

Microsporidian coinfection reduces fitness of a fungal pathogen due to rapid host mortality

Infection outcomes can be strongly context-dependent, shifting a host-symbiont relationship along a parasitism-mutualism continuum. Numerous studies show that under stressful conditions, symbionts that are typically mutualistic can become parasitic. The reverse possibility - a parasite becoming mutualistic - has received much less study. We investigated whether the parasitic microsporidium Ordospora pajunii can become beneficial for its host Daphnia dentifera in the presence of the more virulent fungal pathogen Metschnikowia bicuspidata. We found that, even though infection with O. pajunii reduces the frequency of penetration of M. bicuspidata spores into the host body cavity, it does not improve the survival or reproduction of the host; conversely, coinfection increased the mortality of Daphnia. However, the shorter lifespan of coinfected hosts disrupted the life cycle of M. bicuspidata, greatly reducing its fitness. Thus, coinfection with both pathogens was detrimental to the host at the individual level, but might be beneficial for the host population as a result of greatly reduced production of M. bicuspidata spores. If so, this would mean that O. pajunii outbreaks should delay or prevent M. bicuspidata outbreaks. In support of this, in an analysis of dynamics of naturally occurring outbreaks in two lakes where these pathogens co-occur, we found a time lag in occurrence between O. pajunii and M. bicuspidata, with M. bicuspidata epidemics only occurring after the collapse of O. pajunii epidemics. Thus, these results suggest that the interaction between co-occurring symbionts - and the net impact of a symbiont on a host - might be qualitatively different at different scales. ImportanceUnderstanding the factors that modify infection probability and virulence is crucial for identifying the drivers of infection outbreaks and modeling disease epidemic progression, and increases our ability to control diseases and reduce the harm they cause. One factor that can strongly influence infection probability and virulence is the presence of other pathogens. However, while coexposures and coinfections are incredibly common, we still have only a limited understanding of how pathogen interactions alter infection outcomes, or whether their impacts are scale-dependent. We used a system of one host and two pathogens to show that sequential coinfection can have a tremendous impact on the host and on the infecting pathogens, and that the outcome of (co-)infection can be negative or positive depending on the focal organization level.

ecology↗

Virulence and transmission biology of the widespread, ecologically important pathogen of zooplankton, Spirobacillus cienkowskii

Spirobacillus cienkowskii (Spirobacillus, hereafter) is a widely distributed bacterial pathogen that has significant impacts on the population dynamics of zooplankton (Daphnia spp.), particularly in months when Daphnia are asexually reproducing. Yet little is known about Spirobacillus virulence, transmission mode and dynamics. As a result, we cannot explain the dynamics of Spirobacillus epidemics in nature or use Spirobacillus as a model pathogen, despite Daphnias tractability as a model-host. Here, we work to fill these knowledge gaps experimentally. We found that Spirobacillus is among the most virulent of Daphnia pathogens, killing its host within a week and reducing host fecundity. We further found that Spirobacillus did not transmit horizontally among hosts unless the host died or was destroyed (i.e., it is an "obligate killer"). In experiments aimed at quantifying the dynamics of horizontal transmission among asexually reproducing Daphnia, we demonstrated that Spirobacillus transmits poorly in the laboratory. In mesocosms, Spirobacillus failed to generate epidemics; in experiments wherein individual Daphnia were exposed, Spirobacillus transmission success was low. In the (limited) set of conditions we considered, Spirobacillus transmission success did not change with host density or pathogen dose and declined following environmental incubation. Lastly, we conducted a field survey of Spirobacillus prevalence within egg-cases (ephippia) made by sexually reproducing Daphnia. We found Spirobacillus DNA in [~]40% of ephippia, suggesting that, in addition to transmitting horizontally among asexually reproducing Daphnia, Spirobacillus may transmit vertically from sexually reproducing Daphnia. Our work fills critical gaps in the biology of Spirobacillus and illuminates new hypotheses vis-a-vis its life-history. ImportanceSpirobacillus cienkowskii is a bacterial pathogen of zooplankton, first described in the 19th Century and recently placed in a new family of bacteria, the Silvanigrellaceae. Spirobacillus causes epidemics in lake zooplankton populations and increases the probability that zooplankton will be eaten by predators. However, little is known about how Spirobacillus transmits among hosts, its impact on host survival and reproduction (i.e., how virulent it is) in laboratory conditions and what role virulence plays in Spirobacillus life cycle. Here, we experimentally quantified Spirobacillus virulence and showed that Spirobacillus must kill its host to transmit horizontally. We also found evidence that Spirobacillus may transmit vertically via Daphnias seed-like egg cases. Our work will help scientists to (i) understand Spirobacillus epidemics, (ii) use Spirobacillus as a model pathogen for the study of host-parasite interactions and (iii) better understand the unusual group of bacteria to which Spirobacillus belongs.

microbiology↗

Phylogeny, morphology, virulence, ecology, and host range of Ordospora pajunii (Ordosporidae),a microsporidian symbiont of Daphnia spp.

Impacts of microsporidia on host individuals are frequently subtle and can be context dependent. A key example of the latter comes from a recently discovered microsporidian symbiont of Daphnia, the net impact of which was found to shift from negative to positive based on environmental context. Given this, we hypothesized low baseline virulence of the microsporidian; here, we investigated the impact of infection on hosts in controlled conditions and the absence of other stressors. We also investigated its phylogenetic position, ecology and host range. The genetic data indicates that the symbiont is Ordospora pajunii, a newly described microsporidian parasite of Daphnia. We show that O. pajunii infection damages the gut, causing infected epithelial cells to lose microvilli and then rupture. The prevalence of this microsporidian could be high (up to 100% in the lab and 77% of adults in the field). Its overall virulence was low in most cases, but some genotypes suffered reduced survival and/or reproduction. Susceptibility and virulence were strongly host-genotype dependent. We found that North American O. pajunii were able to infect multiple Daphnia species, including the European species D. longispina, as well as Ceriodaphnia spp. Given the low, often undetectable virulence of this microsporidian, and potentially far reaching consequences of infections for the host when interacting with other pathogens or food, this Daphnia - O. pajunii symbiosis emerges as a valuable system for studying the mechanisms of context-dependent shifts between mutualism and parasitism, as well as for understanding how symbionts might alter host interactions with resources. ImportanceThe net outcome of symbiosis depends on the costs and benefits to each partner. Those can be context dependent, driving the potential for an interaction to change between parasitism and mutualism. Understanding the baseline fitness impact in an interaction can help us understand those shifts; for an organism that is generally parasitic, it should be easier for it to become a mutualist if its baseline virulence is relatively low. Recently, a microsporidian was found to become beneficial to its Daphnia hosts in certain ecological contexts, but little was known about the symbiont (including its species identity). Here, we identify it as the microsporidium Ordospora pajunii. Despite the parasitic nature of microsporidia, we found O. pajunii to be, at most, mildly virulent; this helps explain why it can shift towards mutualism in certain ecological contexts and helps establish O. pajunii is a valuable model for investigating shifts along the mutualism-parasitism continuum.

ecology↗

Transgenerational virulence: Maternal pathogen exposure reduces offspring fitness

Pathogens can alter the phenotype not only of exposed hosts, but also of future generations. Transgenerational immune priming, where parental infection drives reduced susceptibility of offspring, has been particularly well explored, but pathogens can also alter life history traits of offspring. Here, we examined the potential for transgenerational impacts of a microsporidian pathogen, Ordospora pajunii, by experimentally measuring the impact of maternal exposure on offspring fitness in the presence and absence of parasites, and then developing mathematical models that explored the population-level impacts of these transgenerational effects. We did not find evidence of transgenerational immune priming: offspring of exposed mothers became infected at high rates, similar to offspring of unexposed mothers, and the infection burden did not differ between these two groups. We also did not find any evidence of transgenerational tolerance, where daughters of exposed mothers have higher fitness after infection. Instead, we found evidence for negative transgenerational impacts of infection: uninfected offspring of exposed mothers had substantially greater early life mortality than uninfected offspring of unexposed mothers. Offspring of exposed mothers also had reduced growth rate, fewer clutches, and fewer offspring. We propose that these observations should be considered transgenerational virulence, where a pathogen reduces the fitness of the offspring of infected hosts. Our parameterized mathematical model allowed us to explore the impacts of transgenerational virulence at the population level. If transgenerational virulence manifests as decreased reproduction or increased mortality in offspring, as we saw in the empirical portion of our study, this reduces total host density, infection prevalence, and infected host density, which could have implications for both host conservation and spillover risk. We propose that transgenerational virulence might be common and is a concept worthy of further empirical and theoretical exploration.

ecology↗

Temperature modifies trait-mediated infection outcomes in a Daphnia-fungal parasite system

One major concern related to climate change is that elevated temperatures will drive increases in parasite outbreaks. Increasing temperature is known to alter host traits and host-parasite interactions, but we know relatively little about how these are connected mechanistically - that is, about how elevated temperatures impact the relationship between epidemiologically relevant host traits and infection outcomes. Here, we used a zooplankton-fungus (Daphnia dentifera-Metschnikowia bicuspidata) disease system to investigate whether temperature interacted with host susceptibility traits in determining infection outcomes. We did this by exposing D. dentifera to M. bicuspidata or leaving them unexposed at either control (20{degrees}C) or warming temperatures (24{degrees}C) in a fully factorial design. We found that elevated temperatures altered the physical barrier and immune responses to parasites during the initial infection process, and that infected hosts at elevated temperatures suffered a greater reduction of fecundity and lifespan. Furthermore, the relationship between a key trait - gut epithelium thickness, which is a physical barrier - and the likelihood of terminal infection reversed at warmer temperatures. Together, our results highlight the complex ways that temperatures can modulate host-parasite interactions, and the importance of considering key host susceptibility traits when predicting disease dynamics in a warmer world. This article is part of the theme issue Infectious disease and evolution in a changing world.

ecology↗

'Resistance is futile': Weaker selection for resistance during larger epidemics further increases prevalence and depresses host density

What determines how much resistance hosts evolve? One might intuit that hosts evolve higher resistance when parasites are more abundant. However, the opposite pattern can arise due to costs of resistance. Here we illustrate with mathematical, experimental, and field approaches how ecological context can increase parasite abundance and select for lower resistance. Resistance is futile when all host genotypes become sufficiently infected. To make this argument, we first analyzed an eco-evolutionary model of parasites, hosts, and hosts resources. We determined eco-evolutionary outcomes for resistance (mathematically, transmission rate) and densities along gradients that drive epidemic size. When epidemic drivers are high, hosts evolve lower resistance, amplifying epidemics and decreasing host density. Experimental mesocosms qualitatively agreed. In the experiment, higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites. Evolving zooplankton hosts were less resistant at high nutrients than at low. Less resistance, in turn, was associated with higher infection prevalence and lower host density. We also analyzed the size of naturally occurring epidemics, finding a broad, bimodal distribution of epidemic sizes consistent with the eco-evolutionary model. Together, our three approaches supported predictions that high epidemic drivers lead to evolution of lower resistance which drives higher prevalence and lower host density.

evolutionary biology↗

Virulent disease epidemics can increase host density by depressing foraging of hosts

All else equal, parasites that harm host fitness should depress densities of their hosts. However, parasites that alter host traits may increase host density via indirect ecological interactions. Here, we show how depression of infected host foraging rate can produce such a hydra effect. Using a foraging assay, we quantified reduced foraging rates of a zooplankton host infected with a virulent fungal parasite. We then parameterized a dynamical model of hosts, parasites, and resources with this foraging function, showing how foraging depression can create a hydra effect. Mathematically, the hydra arose when increased resource productivity exceeded any increase in resource consumption per host. Therefore, the foraging-mediated hydra effect more likely emerged (1) for hosts which strongly control logistic-like resources and (2) during larger epidemics of moderately virulent parasites. We then analyzed epidemics from 13 fungal epidemics in nature. We found evidence for a foraging-mediated hydra effect: large outbreaks depressed foraging rate and correlated with increased densities of both algae and hosts. Therefore, depression of foraging rate of infected hosts can produce higher host densities even during epidemics of parasites that increase host mortality. Such hydras might prevent collapse of host populations but also could produce higher densities of infected hosts.Competing Interest StatementThe authors have declared no competing interest.View Full Text

ecology↗

Toward a unified dilution effect theory: How competence, competition, and the transmission mechanism influence disease-diversity relationships

Biodiversity in communities is changing globally, including the gain and loss of host species in host-pathogen communities. Increased host diversity can cause infection prevalence in a focal host to increase (amplification) or decrease (dilution). However, it is unclear what general rules govern the context dependent effects, in part because theories for pathogens with different transmission modes have developed largely independently. Using a two-host model, we explore how the pathogen transmission mode and characteristics of a second host (disease competence and competitive ability) influence disease prevalence in a focal host. Our work shows how the theories for pathogens with environmental transmission, density-dependent direct transmission, and frequency-dependent direct transmission can be unified. Our work also identifies general rules about how host and pathogen characteristics affect amplification/dilution. For example, higher competence hosts promote amplification, unless they are strong interspecific competitors; strong interspecific competitors promote dilution, unless they are large sources of new infections; and dilution occurs under frequency-dependent direct transmission more than density-dependent direct transmission, unless interspecific host competition is sufficiently strong. Our work helps explain how the characteristics of the pathogen and a second host affect disease prevalence in a focal host.

ecology↗

Light exposure decreases infectivity of the Daphnia parasite Pasteuria ramosa

Climate change is altering light regimes in lakes, which should impact disease outbreaks, since sunlight can harm aquatic pathogens. However, some bacterial endospores are resistant to damage from light, even surviving exposure to UV-C. We examined the sensitivity of Pasteuria ramosa endospores, an aquatic parasite infecting Daphnia zooplankton, to biologically relevant wavelengths of light. Laboratory exposure to increasing intensities of UV-B, UV-A, and visible light significantly decreased P. ramosa infectivity, though there was no effect of spore exposure on parasitic castration of the host. P. ramosa is more sensitive than its Daphnia host to damage by longer wavelength UV-A and visible light; this may enable Daphnia to seek an optimal light environment in the water column where both UV-B damage and parasitism are minimal. Studies of pathogen light sensitivity help us uncover factors controlling epidemics in lakes, which is especially important given that water transparency is decreasing in many lakes.

ecology↗

Storage length and temperature influence infectivity and spore yield of two common Daphnia parasites

Daphnia and their parasites have emerged as a model system for understanding the ecology and evolution of infectious diseases. Two of the most commonly studied Daphnia parasites are the bacterium Pasteuria ramosa and the fungus Metschnikowia bicuspidata. In addition to being the focus of numerous field studies, these two parasites have been used in many laboratory experiments. However, there is little information in the scientific literature about how the conditions under which these parasites are stored influence the infectivity and yield of transmission stages (\"spores\"). This is problematic because such information is critical for experiment design and data interpretation.\n\nWe tested the influence of storage length (eight treatments ranging from 1 day to 1 year) and temperature (-20{degrees}C (freezer) vs. 4{degrees}C (refrigerator)) on spore infectivity and yield. We found that Pasteuria spores survived well at both -20{degrees}C and 4{degrees}C, and remained infective even after storage for one year. However, Pasteuria spore yields dropped over time, particularly at 4{degrees}C. In contrast, Metschnikowia spores were killed within days at -20{degrees}C. At 4{degrees}C, Metschnikowia infectivity declined steadily over a period of two months and, by four months, spores were no longer infective. Spore yield from Metschnikowia-infected hosts was not significantly impacted by storage length, but trended downwards.\n\nScientists working with Pasteuria should be aware that spore yield declines during storage, particularly in the refrigerator. Scientists working with Metschnikowia should be aware that it is killed by freezer storage and that, even if it is stored in the refrigerator, infectivity declines within a few months. These results might have implications for parasite distributions in the field; for example, the high sensitivity of Metschnikowia to freezing might help explain why it tends to be more common in deep lakes than in ponds or rock pools.

epidemiology↗

Last And Corresponding Authorship Practices In Ecology

Authorship is intended to convey information regarding credit and responsibility for manuscripts. However, while there is general agreement within ecology that the first author is the person who contributed the most to a particular project, there is less agreement regarding whether being last author is a position of significance and regarding what is indicated by someone being the corresponding author on a manuscript. Using an analysis of papers published in American Naturalist, Ecology, Evolution, and Oikos, I found that: 1) the number of authors on papers is increasing over time; 2) the proportion of first authors as corresponding author has increased over time, as has the proportion of last authors as corresponding author; 3) 84% of papers published in 2016 had the first author as corresponding author; and 4) geographic regions differed in the likelihood of having the first (or last) author as corresponding author. I also carried out an online survey to better understand views on last and corresponding authorship. This survey revealed that most ecologists view the last author as the \"senior\" author on a paper (that is, the person who runs the research group in which most of the work was carried out), and most ecologists view the corresponding author as the person taking full responsibility for a paper. However, there was substantial variation in views on authorship, especially corresponding authorship. Given these results, I suggest that discussions of authorship have as their starting point that the first author will be corresponding author and the senior author will be last author. I also suggest ways of deciding author order in cases where two senior authors contributed equally.

ecology↗