Immune Response to Parasitic Attack: Evolution of a Pulsed Character

Frank, Steven A.

doi:10.1006/jtbi.2002.3122

Cited by 26 publications

(23 citation statements)

References 23 publications

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“…The main function of TLRs is to detect and begin to coordinate responses to diverse parasites [9,19]. High constitutive TLR expression could thus enable sparrows to detect microbes quickly [48], tolerate their endotoxins more effectively [49] and/or initiate clearance processes before microbes incite pathology [50]. These hypotheses are consistent empirically with observations in rodents [48,51] and consistent theoretically with regards to the costs and benefits of immune defences [52].…”

Section: Discussionsupporting

confidence: 74%

Surveillance for microbes and range expansion in house sparrows

et al. 2014

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Interactions between hosts and parasites influence the success of host introductions and range expansions post-introduction. However, the physiological mechanisms mediating these outcomes are little known. In some vertebrates, variation in the regulation of inflammation has been implicated, perhaps because inflammation imparts excessive costs, including high resource demands and collateral damage upon encounter with novel parasites. Here, we tested the hypothesis that variation in the regulation of inflammation contributed to the spread of house sparrows ( Passer domesticus ) across Kenya, one of the world's most recent invasions of this species. Specifically, we asked whether inflammatory gene expression declines with population age (i.e. distance from Mombasa (dfM), the site of introduction around 1950). We compared expression of two microbe surveillance molecules (Toll-like receptors, TLRs-2 and 4) and a proinflammatory cytokine (interleukin-6, IL-6) before and after an injection of an immunogenic component of Gram-negative bacteria (lipopolysaccharide, LPS) among six sparrow populations. We then used a best-subset model selection approach to determine whether population age (dfM) or other factors (e.g. malaria or coccidian infection, sparrow density or genetic group membership) best-explained gene expression. For baseline expression of TLR-2 and TLR-4 , population age tended to be the best predictor with expression decreasing with population age, although other factors were also important. Induced expression of TLRs was affected by LPS treatment alone. For induced IL-6 , only LPS treatment reliably predicted expression; baseline expression was not explained by any factor. These data suggest that changes in microbe surveillance, more so than downstream control of inflammation via cytokines, might have been important to the house sparrow invasion of Kenya.

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Section: Discussionsupporting

confidence: 74%

Surveillance for microbes and range expansion in house sparrows

et al. 2014

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“…In any case, there may be too many intermediate or system-specific steps between helminth-induced immune responses and their bystander effects on microparasites to be detected in such an analysis. What is remarkable here is that a detectable general rule about top-down control of microparasites during helminth coinfection emerged, despite the dynamic complexities of immune responses (34). It is important to highlight such cases of functional simplicity in complex systems, particularly in this era of high-throughput data collection in biomedicine (27).…”

Section: Discussionmentioning

confidence: 96%

Ecological rules governing helminth–microparasite coinfection

Graham

2008

Proc. Natl. Acad. Sci. U.S.A.

339

396

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Coinfection of a host by multiple parasite species has important epidemiological and clinical implications. However, the direction and magnitude of effects vary considerably among systems, and, until now, there has been no general framework within which to explain this variation. Community ecology has great potential for application to such problems in biomedicine. Here, metaanalysis of data from 54 experiments on laboratory mice reveals that basic ecological rules govern the outcome of coinfection across a broad spectrum of parasite taxa. Specifically, resource-based (''bottomup'') and predator-based (''top-down'') control mechanisms combined to determine microparasite population size in helminthcoinfected hosts. Coinfection imposed bottom-up control (resulting in decreased microparasite density) when a helminth that causes anemia was paired with a microparasite species that requires host red blood cells. At the same time, coinfection impaired top-down control of microparasites by the immune system: the greater the helminth-induced suppression of the inflammatory cytokine interferon (IFN)-␥, the greater the increase in microparasite density. These results suggest that microparasite population growth will be most explosive when underlying helminths do not impose resource limitations but do strongly modulate IFN-␥ responses. Surprisingly simple rules and an ecological framework within which to analyze biomedical data thus emerge from analysis of this dataset. Through such an interdisciplinary lens, predicting the outcome of coinfection may become tractable.cytokine ͉ disease ecology ͉ metaanalysis ͉ predation ͉ resource limitation

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“…The parasites to which hosts are exposed, the frequency of exposure, and the costs and benefits associated with mounting defences against those parasites, are all expected to contribute to the evolution of inducible immune responses (Cressler et al, 2015;Frank, 2002;Hamilton et al, 2008;Mayer, Mora, Rivoire, & Walczak, 2016). The dynamics of immunity during the acute infection phase are particularly important for host fitness, as modest levels of variation in early responses could lead to drastic variation in host mortality and parasite persistence (Duneau et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Natural variation in the contribution of microbial density to inducible immune dynamics

et al. 2019

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Immune responses evolve to balance the benefits of microbial killing against the costs of autoimmunity and energetic resource use. Models that explore the evolution of optimal immune responses generally include a term for constitutive immunity, or the level of immunological investment prior to microbial exposure, and for inducible immunity, or investment in immune function after microbial challenge. However, studies rarely consider the functional form of inducible immune responses with respect to microbial density, despite the theoretical dependence of immune system evolution on microbe‐ versus immune‐mediated damage to the host. In this study, we analyse antimicrobial peptide (AMP) gene expression from seven wild‐caught flour beetle populations (Tribolium spp.) during acute infection with the virulent bacteria Bacillus thuringiensis (Bt) and Photorhabdus luminescens (P.lum) to demonstrate that inducible immune responses mediated by the humoral IMD pathway exhibit natural variation in both microbe density‐dependent and independent temporal dynamics. Beetle populations that exhibited greater AMP expression sensitivity to Bt density were also more likely to die from infection, while populations that exhibited higher microbe density‐independent AMP expression were more likely to survive P. luminescens infection. Reduction in pathway signalling efficiency through RNAi‐mediated knockdown of the imd gene reduced the magnitude of both microbe‐independent and dependent responses and reduced host resistance to Bt growth, but had no net effect on host survival. This study provides a framework for understanding natural variation in the flexibility of investment in inducible immune responses and should inform theory on the contribution of nonequilibrium host‐microbe dynamics to immune system evolution.

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Immune Response to Parasitic Attack: Evolution of a Pulsed Character

Cited by 26 publications

References 23 publications

Surveillance for microbes and range expansion in house sparrows

Surveillance for microbes and range expansion in house sparrows

Ecological rules governing helminth–microparasite coinfection

Natural variation in the contribution of microbial density to inducible immune dynamics

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