Interactions between environmental stressors: the influence of salinity on host–parasite interactions between Daphnia magna and Pasteuria ramosa

Matthew D. Hall; Andrea Vettiger; Dieter Ebert

doi:10.1007/s00442-012-2452-3

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

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.2386 ◽

2020 ◽

Vol 287 (1920) ◽

pp. 20192386

Author(s):

Frida Ben-Ami ◽

Christian Orlic ◽

Roland R. Regoes

Keyword(s):

Genetic Epidemiology ◽

Ecological Systems ◽

High Dose ◽

Immune Priming ◽

Specific Effects ◽

Host Parasite Interactions ◽

Pasteuria Ramosa ◽

Different Strains ◽

Host Parasite ◽

First Time

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.

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The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle

Epidemiology and Infection ◽

10.1017/s0950268803008793 ◽

2003 ◽

Vol 131 (2) ◽

pp. 957-966 ◽

Cited By ~ 58

Author(s):

R. R. REGOES ◽

J. W. HOTTINGER ◽

L. SYGNARSKI ◽

D. EBERT

Keyword(s):

Daphnia Magna ◽

Infection Rate ◽

Infection Process ◽

Action Principle ◽

Mass Action ◽

Infection Model ◽

Susceptibility To Infection ◽

Pasteuria Ramosa ◽

Simple Mass ◽

Host Parasite

In simple epidemiological models that describe the interaction between hosts with their parasites, the infection process is commonly assumed to be governed by the law of mass action, i.e. it is assumed that the infection rate depends linearly on the densities of the host and the parasite. The mass-action assumption, however, can be problematic if certain aspects of the host–parasite interaction are very pronounced, such as spatial compartmentalization, host immunity which may protect from infection with low doses, or host heterogeneity with regard to susceptibility to infection. As deviations from a mass-action infection rate have consequences for the dynamics of the host–parasite system, it is important to test for the appropriateness of the mass-action assumption in a given host–parasite system. In this paper, we examine the relationship between the infection rate and the parasite inoculum for the water flee Daphnia magna and its bacterial parasite Pasteuria ramosa. We measured the fraction of infected hosts after exposure to 14 different doses of the parasite. We find that the observed relationship between the fraction of infected hosts and the parasite dose is largely consistent with an infection process governed by the mass-action principle. However, we have evidence for a subtle but significant deviation from a simple mass-action infection model, which can be explained either by some antagonistic effects of the parasite spores during the infection process, or by heterogeneity in the hosts' susceptibility with regard to infection.

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

10.1101/429498 ◽

2018 ◽

Cited By ~ 1

Author(s):

Frida Ben-Ami ◽

Christian Orlic ◽

Roland R. Regoes

Keyword(s):

Bacterial Pathogen ◽

Immune Memory ◽

High Dose ◽

Immune Priming ◽

Host Parasite Interactions ◽

Pasteuria Ramosa ◽

Wide Range ◽

Different Strains ◽

Host Parasite ◽

First Time

AbstractExposure 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.

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Four QTL underlie resistance to a microsporidian parasite that may drive genome evolution in its Daphnia host

10.1101/847194 ◽

2019 ◽

Author(s):

Devon Keller ◽

Devin Kirk ◽

Pepijn Luijckx

Keyword(s):

Immune Response ◽

Daphnia Magna ◽

Genetic Architecture ◽

Pivotal Role ◽

Parasite Resistance ◽

Microsporidian Parasite ◽

Ecological Processes ◽

Host Parasite Interactions ◽

Host Parasite ◽

General Immune Response

AbstractDespite its pivotal role in evolutionary and ecological processes the genetic architecture underlying host-parasite interactions remains understudied. Here we use a quantitative trait loci approach to identify regions in the Daphnia magna genome that provide resistance against its microsporidium parasite Ordospora colligata. The probability that Daphnia became infected was affected by a single locus and an interaction between two additional loci. A fourth locus influenced the number of spores that grew within the host. Comparing our findings to previously published genetic work on Daphnia magna revealed that two of these loci may be the same as detected for another microsporidium parasite, suggesting a general immune response to this group of pathogens. More importantly, this comparison revealed that two regions previously identified to be under selection coincided with parasite resistance loci, highlighting the pivotal role parasites may play in shaping the host genome.

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Genetic variation in the cellular response of Daphnia magna (Crustacea: Cladocera) to its bacterial parasite

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2010.0772 ◽

2010 ◽

Vol 277 (1698) ◽

pp. 3291-3297 ◽

Cited By ~ 32

Author(s):

Stuart K. J. R. Auld ◽

Jennifer A. Scholefield ◽

Tom J. Little

Keyword(s):

Genetic Variation ◽

Daphnia Magna ◽

Cellular Response ◽

Cell Types ◽

Parasite Fitness ◽

Pasteuria Ramosa ◽

Cellular Immune ◽

Genetically Determined ◽

Host Parasite ◽

Parasite Exposure

Linking measures of immune function with infection, and ultimately, host and parasite fitness is a major goal in the field of ecological immunology. In this study, we tested for the presence and timing of a cellular immune response in the crustacean Daphnia magna following exposure to its sterilizing endoparasite Pasteuria ramosa . We found that D. magna possesses two cell types circulating in the haemolymph: a spherical one, which we call a granulocyte and an irregular-shaped amoeboid cell first described by Metchnikoff over 125 years ago. Daphnia magna mounts a strong cellular response (of the amoeboid cells) just a few hours after parasite exposure. We further tested for, and found, considerable genetic variation for the magnitude of this cellular response. These data fostered a heuristic model of resistance in this naturally coevolving host–parasite interaction. Specifically, the strongest cellular responses were found in the most susceptible hosts, indicating resistance is not always borne from a response that destroys invading parasites, but rather stems from mechanisms that prevent their initial entry. Thus, D. magna may have a two-stage defence—a genetically determined barrier to parasite establishment and a cellular response once establishment has begun.

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