The epidemiological consequences of immune priming

Tidbury, Hannah J.; Best, Alex; Boots, Mike

doi:10.1098/rspb.2012.1841

Cited by 60 publications

(90 citation statements)

References 42 publications

(51 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Transgenerational immune priming is predicted to have not only a strong effect on disease prevalence [65,66], but also on the age structure [65] and population dynamics of invertebrates [66]. Our theoretical model shows that, beyond the effect of host lifespan and host dispersal, several other life-history parameters play a key role in the evolution of transgenerational immunity.…”

Section: Discussionmentioning

confidence: 98%

Evolution of transgenerational immunity in invertebrates

et al. 2016

View full text Add to dashboard Cite

Over a decade ago, the discovery of transgenerational immunity in invertebrates shifted existing paradigms on the lack of sophistication of their immune system. Nonetheless, the prevalence of this trait and the ecological factors driving its evolution in invertebrates remain poorly understood. Here, we develop a theoretical host -parasite model and predict that long lifespan and low dispersal should promote the evolution of transgenerational immunity. We also predict that in species that produce both philopatric and dispersing individuals, it may pay to have a plastic allocation strategy with a higher transgenerational immunity investment in philopatric offspring because they are more likely to encounter locally adapted pathogens. We review all experimental studies published to date, comprising 21 invertebrate species in nine different orders, and we show that, as expected, longevity and dispersal correlate with the transfer of immunity to offspring. The validity of our prediction regarding the plasticity of investment in transgenerational immunity remains to be tested in invertebrates, but also in vertebrate species. We discuss the implications of our work for the study of the evolution of immunity, and we suggest further avenues of research to expand our knowledge of the impact of transgenerational immune protection in host -parasite interactions.

show abstract

Section: Discussionmentioning

confidence: 98%

Evolution of transgenerational immunity in invertebrates

et al. 2016

View full text Add to dashboard Cite

show abstract

“…As well as potentially suffering reduced fecundity, infected hosts suffer through a further death rate (defined here as virulence) a. For analytical ease, we make two notable simplifications to the model of Tidbury et al [18]: we do not include maternal priming and we assume that priming is permanent (the impact of these assumptions is considered in §4).…”

Section: Modelmentioning

confidence: 99%

“…However, as of yet there has been no theoretical study of the evolution of immune priming. Two recent papers have, however, investigated the impact on host population dynamics, finding that immune priming can reduce the prevalence of infection considerably [17,18]. Furthermore, Tidbury et al [18] found that the population dynamics of hosts with primed immunity are more complex than in classic models with acquired immunity, with the potential for bistability between disease-free and endemic states as well as for endemic cycles.…”

Section: Introductionmentioning

confidence: 99%

The evolutionary dynamics of within-generation immune priming in invertebrate hosts

Best

Tidbury

White

et al. 2013

J. R. Soc. Interface.

Self Cite

View full text Add to dashboard Cite

While invertebrates lack the machinery necessary for 'acquired immunity', there is increasing empirical evidence that exposure to low levels of disease may 'prime' an invertebrate's immune response, increasing its defence to subsequent exposure. Despite this increasing empirical data, there has been little theoretical attention paid to immune priming. Here, we investigate the evolution of immune priming, focusing on the role of the unique feedbacks generated by a newly developed susceptible -primed -infected epidemiological model. Contrasting our results with previous models on the evolution of acquired immunity, we highlight that there are important implications to the evolution of immunity through priming owing to these different epidemiological feedbacks. In particular, we find that in contrast to acquired immunity, priming is strongly selected for at high as well as intermediate pathogen virulence. We also find that priming may be greatest at either intermediate or high host lifespans depending on the severity of disease. Furthermore, hosts faced with more severe pathogens are more likely to evolve diversity in priming. Finally, we show when the evolution of priming leads to the exclusion of the pathogens or hosts experiencing population cycles. Overall the model acts as a baseline for understanding the evolution of priming in host -pathogen systems.

show abstract

“…This persistent priming also has broad implications for understanding the epidemiological consequences of priming. For example, Tidbury et al (Tidbury et al, 2012) showed that immune priming may increase the persistence of the pathogen and destabilise host-pathogen dynamics. We suggest that the linked effects of the phenomena reported here -age effects, maternal effects and priming -merit further study as major drivers of disease spread and host-pathogen evolution in this and other systems.…”

Section: Research Articlementioning

confidence: 99%

The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations

Garbutt

O'Donoghue

McTaggart

et al. 2014

Journal of Experimental Biology

View full text Add to dashboard Cite

Immunity in vertebrates is well established to develop with time, but the ontogeny of defence in invertebrates is markedly less studied. Yet, age-specific capacity for defence against pathogens, coupled with age structure in populations, has widespread implications for disease spread. Thus, we sought to determine the susceptibility of hosts of different ages in an experimental invertebrate host-pathogen system. In a series of experiments, we show that the ability of Daphnia magna to resist its natural bacterial pathogen Pasteuria ramosa changes with host age. Clonal differences make it difficult to draw general conclusions, but the majority of observations indicate that resistance increases early in the life of D. magna, consistent with the idea that the defence system develops with time. Immediately following this, at about the time when a daphnid would be most heavily investing in reproduction, resistance tends to decline. Because many ecological factors influence the age structure of Daphnia populations, our results highlight a broad mechanism by which ecological context can affect disease epidemiology. We also show that a previously observed protective effect of restricted maternal food persists throughout the entire juvenile period, and that the protective effect of prior treatment with a small dose of the pathogen ('priming') persists for 7 days, observations that reinforce the idea that immunity in D. magna can change over time. Together, our experiments lead us to conclude that invertebrate defence capabilities have an ontogeny that merits consideration with respect to both their immune systems and the epidemic spread of infection.

show abstract

The epidemiological consequences of immune priming

Cited by 60 publications

References 42 publications

Evolution of transgenerational immunity in invertebrates

Evolution of transgenerational immunity in invertebrates

The evolutionary dynamics of within-generation immune priming in invertebrate hosts

The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations

Contact Info

Product

Resources

About