The visual ecology of selective predation: Are unhealthy hosts less stealthy hosts?

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.

Temperature and pathogen exposure act independently to drive host phenotypic trajectories

Natural populations are experiencing an increase in the occurrence of both thermal stress and disease outbreaks. How these two common stressors interact to determine host phenotypic shifts will be important for population persistence, yet a myriad of different traits and pathways are a target of both stressors, making generalizable predictions difficult to obtain. Here, using the host Daphnia magna and its bacterial pathogen Pasteuria ramosa , we tested how temperature and pathogen exposure interact to drive shifts in multivariate host phenotypes. We found that these two stressors acted mostly independently to shape host phenotypic trajectories, with temperature driving a faster pace of life by favouring early development and increased intrinsic population growth rates, while pathogen exposure impacted reproductive potential through reductions in lifetime fecundity. Studies focussed on extreme thermal stress are increasingly showing how pathogen exposure can severely hamper the thermal tolerance of a host. However, our results suggest that under milder thermal stress, and in terms of life-history traits, increases in temperature might not exacerbate the impact of pathogen exposure on host performance, and vice versa.

Disentangling non-specific and specific transgenerational immune priming components in host–parasite interactions

Exposure to a pathogen primes many organisms to respond faster or more efficiently to subsequent exposures. Such priming can be non-specific or specific, and has been found to extend across generations. Disentangling and quantifying specific and non-specific effects is essential for understanding the genetic epidemiology of a system. By combining a large infection experiment and mathematical modelling, we disentangle different transgenerational effects in the crustacean model Daphnia magna exposed to different strains of the bacterial parasite Pasteuria ramosa . In the experiment, we exposed hosts to a high dose of one of three parasite strains, and subsequently challenged their offspring with multiple doses of the same (homologous) or a different (heterologous) strain. We find that exposure of Daphnia to Pasteuria decreases the susceptibility of their offspring by approximately 50%. This transgenerational protection is not larger for homologous than for heterologous parasite challenges. Methodologically, our work represents an important contribution not only to the analysis of immune priming in ecological systems but also to the experimental assessment of vaccines. We present, for the first time, an inference framework to investigate specific and non-specific effects of immune priming on the susceptibility distribution of hosts—effects that are central to understanding immunity and the effect of vaccines.

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 infected hosts. 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 to uncover factors controlling epidemics in lakes, which is especially important given that water transparency is decreasing in many lakes.

Light exposure decreases infectivity of the Daphnia parasite Pasteuria ramosa

ABSTRACTClimate 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.

Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts?

Pathogens often rely on their host for dispersal. Yet, maximizing fitness via replication can cause damage to the host and an associated reduction in host movement, incurring a trade-off between transmission and dispersal. Here, we test the idea that pathogens might mitigate this trade-off between reproductive fitness and dispersal by taking advantage of sexual dimorphism in their host, tailoring responses separately to males and females. Using experimental populations of Daphnia magna and its bacterial pathogen Pasteuria ramosa as a test-case, we find evidence that this pathogen can use male hosts as a dispersal vector, and the larger females as high-quality resource patches for optimized production of transmission spores. As sexual dimorphism in dispersal and body size is widespread across the animal kingdom, this differential exploitation of the sexes by a pathogen might be an unappreciated phenomenon, possibly evolved in various systems.

Disentangling unspecific and specific transgenerational immune priming components in host-parasite interactions

Exposure to a pathogen primes many organisms to respond faster or more efficiently to subsequent exposures. Such priming can be unspecific or specific, and has been found to extend across generations. Disentangling and quantifying specific and unspecific effects is essential for understanding the genetic epidemiology of a system. By combining a large infection experiment and mathematical modeling, we disentangle different transgenerational effects in the crustacean model Daphnia magna exposed to different strains of the bacterial parasite Pasteuria ramosa. In the experiments, we exposed hosts to a high-dose of one of three parasite strains, and subsequently challenged their offspring with multiple doses of the same or a different strain, i. e. homologously or heterogously. We find that exposure to Pasteuria decreases the susceptibility of a host’s offspring by approximately 50%. This transgenerational protection is not larger for homologous than for heterologous parasite challenges. Our work represents an important contribution not only to the analysis of immune priming in ecological systems, but also to the experimental assessment of vaccines. We present for the first time an inference framework to investigate specific and unspecific effects of immune priming on the susceptibility distribution of hosts — effects that are central to understanding immunity and the effect of vaccines.Author summaryImmune memory is a feature of immune systems that forms the basis of vaccination. In opposition to textbook accounts, the ability to specifically remember previous exposures has been found to extend to invertebrates and shown to be able to be passed on from mother to off-spring, i. e. to be transgenerational. In this paper, we investigate the extent of this specificity in unprecedented detail in water fleas. We exposed water flea mothers to different strains of a bacterial pathogen and challenged their offspring with a wide range of doses of a strain that were either identical to (homologous) or different from (heterologous) the strain, to which the mother had been exposed. We find that, while exposure of the mother reduces the susceptibility of the offspring, this effect is not specific. This work outlines the limits of specific transgenerational immune memory in this invertebrate system.

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.We tested the influence of storage length (eight treatments ranging from 1 day to 1 year) and temperature (−20°C (freezer) vs. 4°C (refrigerator)) on spore infectivity and yield. We found that Pasteuria spores survived well at both −20°C and 4°C, and remained infective even after storage for one year. However, Pasteuria spore yields dropped over time, particularly at 4°C. In contrast, Metschnikowia spores were killed within days at −20°C. At 4°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.Scientists 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.

Host sexual dimorphism affects the outcome of within-host pathogen competition

Natural infections often consist multiple pathogens of the same or different species. In multiple infections, pathogens compete for access to host resources and fitness is determined by how well a pathogen can reproduce compared to its competitors. Given the propensity for males and females to exhibit variation in pathogen-induced reduction in lifespan or fecundity, we explore how host sex may modulate the competitive ability of pathogens, potentially favouring the transmission of different pathogen genotypes. Using the Daphnia magna - Pasteuria ramosa model system, we exposed male and female hosts to either a single genotype infection or coinfections consisting of two pathogen genotypes of varying levels of virulence, measured as pathogen-induced reduction in host lifespan. We found that co-infections within females generally favoured the transmission of the more virulent pathogen genotype. Conversely, co-infections within male hosts resulted in equal transmission of competing genotypes, or favoured the transmission of the less virulent pathogen genotype in treatments where it established prior to the more virulent competitor. These results suggest that sex is a form of host heterogeneity which may influence the evolution of virulence within co-infection contexts and that one sex may be a reservoir for pathogen genetic diversity in nature.

Parasite transmission in a natural multihost–multiparasite community

Understanding the transmission and dynamics of infectious diseases in natural communities requires understanding the extent to which the ecology, evolution and epidemiology of those diseases are shaped by alternative hosts. We performed laboratory experiments to test how parasite spillover affected traits associated with transmission in two co-occurring parasites: the bacterium Pasteuria ramosa and the fungus Metschnikowia bicuspidata . Both parasites were capable of transmission from the reservoir host ( Daphnia dentifera ) to the spillover host ( Ceriodaphnia dubia ), but this occurred at a much higher rate for the fungus than the bacterium. We quantified transmission potential by combining information on parasite transmission and growth rate, and used this to compare parasite fitness in the two host species. For both parasites, transmission potential was lower in the spillover host. For the bacterium, virulence was higher in the spillover host. Transmission back to the original host was high for both parasites, with spillover influencing transmission rate of the fungus but not the bacterium. Thus, while inferior, the spillover host is not a dead-end for either parasite. Overall, our results demonstrate that the presence of multiple hosts in a community can have important consequences for disease transmission, and host and parasite fitness. This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.