scholarly journals Experimental Evolution of Insect Immune Memory VS. Pathogen Resistance

2017 ◽  
Author(s):  
Imroze Khan ◽  
Arun Prakash ◽  
Deepa Agashe

ABSTRACTUnder strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (‘immune priming’), whereby sub-lethal exposure to a pathogen enhances survival after secondary infection. To understand the evolution and consequences of these immune responses, we imposed strong pathogen selection on flour beetles (Tribolium castaneum), infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt each generation evolved high basal resistance against multiple Bt strains. In contrast, all populations injected only with a high dose of live Bt evolved less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Thus, pathogens can select for rapid modulation of insect priming ability, leading to divergent immune strategies (generalized resistance vs. specific immune priming) with distinct mechanisms and adaptive benefits.

2017 ◽  
Vol 284 (1869) ◽  
pp. 20171583 ◽  
Author(s):  
Imroze Khan ◽  
Arun Prakash ◽  
Deepa Agashe

Under strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (immune priming), whereby sublethal exposure to a pathogen enhances survival after secondary infection. Theory predicts that immune memory should evolve when the pathogen is highly virulent, or when pathogen exposure is relatively rare. However, there are no empirical tests of these hypotheses, and the adaptive benefits of immune memory relative to direct resistance against a pathogen are poorly understood. To determine the selective pressures and ecological conditions that shape immune evolution, we imposed strong pathogen selection on flour beetle ( Tribolium castaneum ) populations, infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt evolved high basal resistance against multiple Bt strains. By contrast, populations injected only with a high dose of live Bt evolved a less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Intriguingly, one replicate population first evolved priming and subsequently evolved basal resistance, suggesting the potential for dynamic evolution of different immune strategies. Our work is the first report showing that pathogens can select for rapid modulation of insect priming ability, allowing hosts to evolve divergent immune strategies (generalized resistance versus specific immune memory) with potentially distinct mechanisms.


2019 ◽  
Author(s):  
Arun Prakash ◽  
Deepa Agashe ◽  
Imroze Khan

ABSTRACTInsects exhibit various forms of immune responses, including basal resistance to pathogens and a form of immune memory (“priming”) that can act within or across generations. The evolutionary drivers of such diverse immune functions remain poorly understood. Previously, we found that in the beetle Tribolium castaneum, both resistance and priming evolved as mutually exclusive strategies against the pathogen Bacillus thuringiensis. However, since evolved resistance improved survival far more than priming, the evolution of priming in some populations was puzzling. Was resistance more costly in these populations, or did priming provide added benefits? To test this, we revisited our evolved beetles and analyzed the costs and benefits of evolved priming vs. resistance. Surprisingly, resistant beetles increased reproduction after infection, with no measurable costs. In contrast, mounting a priming response reduced offspring early survival, development rate and reproduction. Even added trans-generational survival benefits of evolved priming could not tilt the balance in favor of priming. Hence, resistance is consistently more beneficial than priming; and the evolution and persistence of costly priming rather than resistance remains a mystery. Nevertheless, our work provides the first detailed comparison of the complex fitness consequences of distinct insect immune strategies, opening new questions about their evolutionary dynamics.


2018 ◽  
Author(s):  
Frida Ben-Ami ◽  
Christian Orlic ◽  
Roland R. Regoes

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.


2021 ◽  
Author(s):  
Lai Ka Lo ◽  
Reshma R ◽  
Lisa-Johanna Tewes ◽  
Barbara Milutinović ◽  
Caroline Müller ◽  
...  

Rapid recognition of disease cues is essential for preventing pathogenic infections and for disease management in group-living animals. Healthy individuals across taxa can detect illness in other conspecifics and adjust their responses to limit further infections of themselves and the group. However, little is known about potential changes in chemical phenotypes due to disease, which may mediate these responses. We here asked whether individual immune experience resulting from wounding or the injection of heat-killed bacteria of Bacillus thuringiensis (i.e., immune priming) leads to changes in the chemical profiles of adult red flour beetles (Tribolium castaneum). This group-living insect species is a well-studied example for both immune priming as a form of innate immune memory and niche construction via 'external immunity', i.e., the secretion of quinone-containing antimicrobials into the flour. Upon interaction with wounded conspecifics, naive beetles were previously found to not only up-regulate immunity, but moreover reduce gene expression of the evolutionary capacitor HSP90, an effect that has the potential to enhance adaptability. We here used gas chromatography-flame-ionisation detection (GC-FID) to study the composition of stink gland secretions and cuticular hydrocarbons (CHCs) of immune-primed and wounded beetles compared to controls. The overall profiles as well as target compounds of the stink gland secretions showed transient, slight changes after these treatments, particularly in wounded females. Priming and wounding led to pronounced changes in CHC profiles with increases in the proportion of methyl-branched alkanes. Furthermore, we found sex-specific differences, that were particularly pronounced in the CHCs, although the changes due to immune stimulation were overall similar in both sexes. We suggest that CHCs are potential candidates for the transfer of information related to individual immunological experience into the group.


2021 ◽  
Vol 6 (1) ◽  
pp. 79
Author(s):  
Etis Duhita Rahayuningtyas ◽  
Indah Suasani Wahyuni ◽  
Irna Sufiawati

ABSTRACTBackground: Stevens-Johnson syndrome (SSJ) is a hypersensitivity reaction that is often triggered by drugs but this case is rare. These reactions result in uncontrolled keratinocyte damage to the skin and mucosa throughout the body, including the oral mucosa, and are often life-threatening. The use of high doses of corticosteroids is a treatment that is often given but it can trigger secondary infections of fungal and viral in the oral cavity. Purpose: This case report discusses the management of oral manifestations and secondary infections in SSJ patients, and becomes guidance for health professionals. Case: A-42-years-old male patient was consulted from the Department of Dermatology and Venereology (DV) due to oral pain and eating difficulties. The severity-of-illness-score for toxic-epidermal-necrolysis (SCORTEN) was 1. Erosive serosanguinous crusts, tend to bleed were found on the lips. Intraoral clinically presented wide erosive lesions and multiple ulcers, accompanied by a pseudomembranous plaque, and teeth decay. Hematologic examination showed an increase in leukocytes, neutrophil segments, monocytes, SGOT, urea, and creatinine as well as decreased hemoglobin, hematocrit, erythrocytes, MCHC, protein, and albumin. Anti-HSV1 IgG increased almost 6 times than normal values. The patient was diagnosed with SJS with oral involvement, secondary infections of pseudomembranous candidiasis, and herpetic stomatitis. Case Management: Systemic therapy given were intravenous dexamethasone, ranitidine, calcium, and cetirizine, from the DV Department, while hydrocortisone lip ointment, Chlorhexidine digluconate 0.12%, and Nystatin oral suspension for oral problems. The lesions progressed in 24 days. Conclusion: Oral secondary infections may occur in SJS patients due to high-dose corticosteroid therapy.Keywords: Herpetic Stomatitis, Oral Manifestation, Oral Secondary Infection, Pseudomembranous Candidiasis, Stevens-Johnson Syndrome.


2007 ◽  
Vol 76 (2) ◽  
pp. 664-670 ◽  
Author(s):  
Ze Hua Fan ◽  
Xiao Wei Wang ◽  
Jinhua Lu ◽  
Bow Ho ◽  
Jeak Ling Ding

ABSTRACT The family of NF-κB transcription factors essentially regulates immune-related gene expression. Recently, we isolated and characterized the classical NF-κB/inhibitor κB (IκB) homologues from a “living fossil,” the horseshoe crab, Carcinoscorpius rotundicauda. Interestingly, this ancient species also harbors another class I NF-κB p100 homologue, C. rotundicauda Relish (CrRelish). Similar to Drosophila Relish and the mammalian p100, CrRelish contains both the Rel-homology domains (RHD) and the IκB-like domain. In this study, we found that the RHD of CrRelish can recognize horseshoe crab and human κB response elements and activate the downstream reporter in vitro, thereby suggesting the evolutionary conservation of this molecule. Pseudomonas aeruginosa infection transcriptionally upregulates CrRelish, which exhibits a dynamic protein profile over the time course of infection. Surprisingly, secondary infection reinduced an upsurge in CrRelish protein expression to a level which overrode the protein degradation at 12 h postinfection. These observations strongly suggest the involvement of CrRelish in antibacterial defense. Secondary infection causes (i) the maintenance of a favorable expression-competent sequence context of the CrRelish gene and/or (ii) the derepression or stabilization of the CrRelish transcript resulting from the primary infection to enable the more rapid expression and accumulation of the CrRelish protein, reflecting apparent signal/immune priming in a repeated infection.


2021 ◽  
Author(s):  
Arun Prakash ◽  
imroze khan

Until recently, it was assumed that insects lack immune memory since they do not have vertebrate-like specialized memory cells. Therefore, their most well studied evolutionary response against pathogens was increased basal immunity. However, growing evidence suggests that many insects also exhibit a form of immune memory (immune priming), where prior exposure to a low dose of infection confers protection against subsequent infection by the same pathogen that acts both within and across generations. Most strikingly, they can rapidly evolve as a highly parallel and mutually exclusive strategy from basal immunity, under different selective conditions and with divergent evolutionary trade-offs. However, the relative importance of priming as an optimal immune strategy also has contradictions, primarily because supporting mechanisms are still unclear. In this review, we adopt a comparative approach to highlight several emerging evolutionary, ecological and mechanistic features of priming vs basal immune responses that warrant immediate attention for future research.


2021 ◽  
pp. 159-182
Author(s):  
Paul Schmid-Hempel

infect a number of host species. This host range is given by an ecological filter (the possibility of encounter) and a physiological one (the capacity of establishing an infection). Host ranges typically are right-skewed, with most parasites infecting only a few, but few infecting very many hosts. There is no universally valid hypothesis that explains host range. However, a number of factors contribute to host range, such as geographical range, phylogenetic distance, host predictability, and parasite virulence. Specificity and cross-reactivity of immune defences are important mechanisms. Moreover, immune memory is based on specificity; transgenerational immune priming protects offspring when parents have already been exposed to the same or similar parasites.


2020 ◽  
Vol 287 (1920) ◽  
pp. 20192386
Author(s):  
Frida Ben-Ami ◽  
Christian Orlic ◽  
Roland R. Regoes

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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