Age Structure Eliminates the Impact of Coinfection on Epidemic Dynamics in a Freshwater Zooplankton System

Clay, P. A.; Gattis, Sabrina; Garcia, Jade; Hernandez, Vincent; Ben‐Ami, Frida; Duffy, Meghan A.

doi:10.1086/726897

Cited by 6 publications

(4 citation statements)

References 63 publications

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“…Unfortunately, experimental tests of this in this system seem unlikely to be successful, as multiple attempts to select M. bicuspidata for a variety of conditions have failed (37, 39, 40). Instead, we propose that studies that quantify how the age and health state of the host (41, 42), the timing and order of exposures (11, 43) and the genotype of each organism (42, 44) influence outcomes during coinfections would likely be more fruitful.…”

Section: Discussionmentioning

confidence: 99%

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

Dziuba,

McIntire,

Davenport

et al. 2024

Preprint

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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 microsporidiumOrdospora pajuniican become beneficial for its hostDaphnia dentiferain the presence of the more virulent fungal pathogenMetschnikowia bicuspidata. We found that, even though infection withO. pajuniireduces the frequency of penetration ofM. bicuspidataspores into the host body cavity, it does not improve the survival or reproduction of the host; conversely, coinfection increased the mortality ofDaphnia. However, the shorter lifespan of coinfected hosts disrupted the life cycle ofM. 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 ofM. bicuspidataspores. If so, this would mean thatO. pajuniioutbreaks should delay or preventM. bicuspidataoutbreaks. 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 betweenO. pajuniiandM. bicuspidata, withM. bicuspidataepidemics only occurring after the collapse ofO. pajuniiepidemics. 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. Importance: Understanding 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.

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Section: Discussionmentioning

confidence: 99%

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

Dziuba,

McIntire,

Davenport

et al. 2024

Preprint

Self Cite

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“…A similar pattern of higher susceptibility of a younger host was found in D. magna exposed to the bacterium P. ramosa , and the proposed explanation was that immune defense mechanisms are less efficient in younger instars of Daphnia ( 76 ). In contrast, older D. dentifera are more susceptible to the fungus Metschnikowia bicuspidata ; this is partially due to the higher feeding rates of older (and, therefore, larger) hosts ( 77 ), but also due to other factors, with the per spore infectivity of M. bicuspidata increasing as hosts age ( 44 ). Because Daphnia encounter parasites while foraging for phytoplankton, feeding rates determine the contact rate of the host with many parasites, including bacteria, fungi, and microsporidia ( 75 , 77 – 79 ).…”

Section: Discussionmentioning

confidence: 99%

“…We used two different exposure times in our experiment. Our preliminary work on this parasite had suggested that younger hosts might be more susceptible, and there is substantial evidence that age can influence infection outcomes ( 44 , 45 ).…”

Section: Methodsmentioning

confidence: 99%

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

Dziuba,

McIntire,

Seto

et al. 2024

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The 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 indicate 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 Daphnia 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. IMPORTANCE The 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 toward mutualism in certain ecological contexts and helps establish O. pajunii is a valuable model for investigating shifts along the mutualism-parasitism continuum.

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“…A similar pattern of higher susceptibility of a younger host was found in D. magna exposed to the bacterium P. ramosa , and the proposed explanation was that immune defense mechanisms are less efficient in younger instars of Daphnia (76). In contrast, older D. dentifera are more susceptible to the fungus Metschnikowia bicuspidata ; this is partially due to the higher feeding rates of older (and, therefore, larger) hosts (77), but also due to other factors, with the per spore infectivity of M. bicuspidata increasing as hosts age (44). Because Daphnia encounter parasites while foraging for phytoplankton, feeding rates determine the contact rate of the host with many parasites, including bacteria, fungi and microsporidia (75, 77–79).…”

Section: Discussionmentioning

confidence: 99%

Phylogeny, morphology, virulence, ecology, and host range ofOrdospora pajunii(Ordosporidae), a microsporidian symbiont ofDaphniaspp

Dziuba

McIntire

Seto

et al. 2023

Preprint

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Symbiosis is increasingly recognized as a dynamic relationship, with the net outcome falling along a continuum from mutualism to parasitism. A key example of this comes from a recently discovered microsporidian symbiont ofDaphnia, the net impact of which was found to vary from negative to positive. We investigated the taxonomic position of this microsporidian and the morphology of infected hosts, as well as the virulence, ecology and host range of the symbiont; we also provide information about its culturing methods. The genetic data indicates that the microsporidian symbiont belongs toOrdospora pajunii, a newly described microsporidian parasite ofDaphnia. We show thatO. pajuniiinfection damages the gut, causing infected epithelial cells to lose microvilli and then rupture. The prevalence of this microsporidian can be high (up to 100% in the lab and 77% of adults in the field). Its overall virulence seems low in most cases, but some genotypes suffer reduced survival and reproduction. Susceptibility and virulence are strongly host-genotype dependent. We found that North AmericanO. pajuniiare able to infect multipleDaphniaspecies, including the European speciesD. longispina, as well as the genusCeriodaphnia. We propose theDaphnia-O. pajuniisymbiosis 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.

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Age Structure Eliminates the Impact of Coinfection on Epidemic Dynamics in a Freshwater Zooplankton System

Cited by 6 publications

References 63 publications

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

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

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

Phylogeny, morphology, virulence, ecology, and host range ofOrdospora pajunii(Ordosporidae), a microsporidian symbiont ofDaphniaspp

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