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ABSTRACT Studies of symbiosis employ the term “parasitism” to connote different sorts of relationships. Within the context of mutualistic symbioses, parasites are otherwise cooperative individuals or strains that appropriate a disproportionate amount of the synergistic products. In the context of antagonistic symbioses, there is no pretence of cooperation, and instead parasites are defined as individuals or strains that derive fitness benefits at a fitness cost to their hosts. In both cases, parasitism is selected for at the lower level (that of the individual symbiont) but selected against at the higher level (the group of symbionts in a single host). Despite these similarities, these different sorts of parasitism likely evolve by different pathways. Once a host–symbiont relationship initiates, if functional synergy is lacking, the relationship will remain exploitative, although parasites may differ in their detrimental effects on the host and the higher‐level unit. If functional synergy is present, however, cooperation may develop with benefits for both host and symbionts (i.e. mutualism). Nevertheless, parasites may still evolve from within these incipient relationships when individuals or strains of symbionts act parasitically by defecting from the common good to further their selfish replication. Levels‐of‐selection dynamics thus underlie both forms of parasitism, but only in the case of latent functional synergy can true symbiotic complexity at the higher level emerge.
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Phylogeny, morphology, virulence, ecology, and host range of Ordospora pajunii (Ordosporidae), a microsporidian symbiont of Daphnia spp.
ABSTRACT 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 ofDaphnia, 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 isOrdospora 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 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 AmericanO. pajuniiwere able to infect multipleDaphniaspecies, including the European speciesDaphnia longispina, as well asCeriodaphniaspp. 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, thisDaphnia–O. pajuniisymbiosis 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 itsDaphniahosts in certain ecological contexts, but little was known about the symbiont (including its species identity). Here, we identify it as the microsporidiumOrdospora pajunii. Despite the parasitic nature of microsporidia, we foundO. pajuniito be, at most, mildly virulent; this helps explain why it can shift toward mutualism in certain ecological contexts and helps establishO. pajuniiis a valuable model for investigating shifts along the mutualism-parasitism continuum.
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- Award ID(s):
- 1929738
- PAR ID:
- 10508465
- Editor(s):
- Pujol, Nathalie; Sinkins, Steven P
- Publisher / Repository:
- ASM Press
- Date Published:
- Journal Name:
- mBio
- ISSN:
- 2150-7511
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/mbio.00582-24
