The evolution of juvenile susceptibility to infectious disease

Ashby, Ben; Bruns, Emily

doi:10.1098/rspb.2018.0844

Cited by 50 publications

(70 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…If most hosts have only a few parasites while a few hosts have many parasites [22], parasite aggregation could induce heterogeneity in the impact of infection on host demography through mortality or developmental effects. Connecting empirical patterns of infection and immunity across ontogeny with mathematical models of age- and stage-structured immune system evolution [2,7,23] could provide a unifying framework for understanding patterns of immunological variation in nature.…”

Section: Discussionmentioning

confidence: 99%

The legacy of larval infection on immunological dynamics over metamorphosis

Critchlow

Norris

Tate

2019

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

Insect metamorphosis promotes the exploration of different ecological niches, as well as exposure to different parasites, across life stages. Adaptation should favour immune responses that are tailored to specific microbial threats, with the potential for metamorphosis to decouple the underlying genetic or physiological basis of immune responses in each stage. However, we do not have a good understanding of how early-life exposure to parasites influences immune responses in subsequent life stages. Is there a developmental legacy of larval infection in holometabolous insect hosts? To address this question, we exposed flour beetle ( Tribolium castaneum ) larvae to a protozoan parasite that inhabits the midgut of larvae and adults despite clearance during metamorphosis. We quantified the expression of relevant immune genes in the gut and whole body of exposed and unexposed individuals during the larval, pupal and adult stages. Our results suggest that parasite exposure induces the differential expression of several immune genes in the larval stage that persist into subsequent stages. We also demonstrate that immune gene expression covariance is partially decoupled among tissues and life stages. These results suggest that larval infection can leave a lasting imprint on immune phenotypes, with implications for the evolution of metamorphosis and immune systems. This article is part of the theme issue ‘The evolution of complete metamorphosis'.

show abstract

Section: Discussionmentioning

confidence: 99%

The legacy of larval infection on immunological dynamics over metamorphosis

Critchlow

Norris

Tate

2019

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

show abstract

“…Although most of the theory of evolution of virulence (defined in this literature as the increased death rate due to infection) focuses on homogeneous host populations, heterogeneity within host populations is ubiquitous in nature (Anderson & May 1992, Chapter 8-11). One typical form of host heterogeneity is stage-related structure (e.g., juveniles and adults), and a number of recent ecological studies have examined the impacts of host populations' stage-related heterogeneity on disease epidemiology (e.g., Dwyer 1991;Fleming-Davies et al 2015;Hite et al 2016; for theory, Ashby & Bruns 2018). In these studies, the differences in virulence across life stages have been explained as age-related variation in tolerance, resistance, exposure, immunocompetence, and susceptibility and affected by maternal and acquired immunity (Hudson & Dobson 1995;Wilson et al 2002).…”

Section: Introductionmentioning

confidence: 99%

The evolution of stage-specific virulence: differential selection of parasites in juveniles

Iritani

Visher

Boots

2018

Preprint

View full text Add to dashboard Cite

The impact of infectious disease is often very different in juveniles and adults, but theory has focused on the drivers of stage-dependent defense in hosts rather than the potential for stage-dependent virulence evolution. Stage-structure has the potential to be important to the evolution of pathogens because it exposes parasites to heterogeneous environments in terms of both host characteristics and transmission routes. We develop a stage-structured (juvenile-adult) epidemiological model and examine the evolutionary outcomes of stage-specific virulence under the classic assumption of a transmission-virulence trade-off. We show that selection on virulence against adults remains consistent with the classic theory. However, the evolution of juvenile virulence is sensitive to both demography and transmission pathway with higher virulence against juveniles being favored either when the transmission pathway is assortative (juveniles preferentially interact together) and the juvenile stage is short, or in contrast when the transmission pathway is disassortative and the juvenile stage is long.These results highlight the potentially profound effects of host stage-structure on determining parasite virulence in nature. This new perspective may have broad implications for both understanding and managing disease severity. Impact summaryUnderstanding the evolution of parasite virulence remains one of the most important questions in evolutionary ecology. Virulence is often very different in young and old hosts, but previous theory has presumed that these differences are attributed to adaptation in host defense rather than parasite adaptation. However, stage-structure within host populations can expose parasites to heterogeneous environments, which may lead to differential selection on parasite virulence (stage-specific virulence). Surprisingly, no study has investigated the effects of hosts' stage-structure on the evolution of stage-specific virulence. We present a theoretical analysis to examine when selection can favor higher virulence against juveniles (juvenile-virulence) versus adults (adult-virulence). Our key result is that higher juvenile-virulence is selected for either when the transmission is assortative within age classes and maturation is slow, or when the transmission is disassortative (occurring predominantly between-classes) and maturation is relatively fast. These at first sight contrasting outcomes can be understood as adaptation to the exploitation of the more available host stage. Although the data on assortativity in infectious disease systems is limited, empirical studies for the virulence of Great Island Virus in guillemots (Uria aalge) and for salmon louse in pink salmon (Oncorhynchus gorbuscha) are consistent with our predictions. Our work provides testable predictions for stage-specific virulence and presents a novel mechanism that may explain variation in virulence in nature. There are also management implications for conservation, public health, vaccination programs, and farming to understanding the...

show abstract

“…developmental stages lack immune-competency and thus have higher susceptibility to infectious pathogens [4][5][6][7][8][9][10][11] is not supported by current evidence. An increasing number of studies demonstrate that insect embryos are capable of mounting immune-defences [12][13][14][15][16][17][18][19][20][21].…”

mentioning

confidence: 99%

Young but not defenceless: antifungal activity during embryonic development of a social insect

2020

View full text Add to dashboard Cite

Termites live in environments heavily colonized by diverse microorganisms, including pathogens. Eggs laid within the nest are likely to experience similar pathogenic pressures as those experienced by older nest-mates. Consequently, eggs may be under selective pressures to be immune-competent. Through in vitro experiments using developing embryos of the dampwood termite, Zootermopsis angusticollis , we tested the ontogeny, location and strength of their antifungal activity against the fungus, Metarhizium brunneum . Exterior washes of the chorion (extra-chorionic) and components within the chorion (intra-chorionic) were incubated with fungal conidia, which were then scored for viability. The fungistatic activity was location and developmental stage dependent. Extra-chorionic washes had relatively weak antifungal activity. Intra-chorionic homogenates were highly antifungal, exhibiting increased potency through development. The positive correlation between intra-chorionic fungistasis and developmental stage is probably due to the expression of endogenous proteins during embryogenesis. Boiling of both the extra-chorionic washes and the intra-chorionic contents rescued conidia viability, indicating the antifungal agent(s) is (are) heat-sensitive and probably proteinaceous. This study is the first to address embryonic antifungal activity in a hemimetabolous, eusocial taxon. Our results support the hypothesis that microbes have been significant agents of selection in termites, fostering the evolution of antifungal properties even in the most immature stage of development.

show abstract

The evolution of juvenile susceptibility to infectious disease

Cited by 50 publications

References 44 publications

The legacy of larval infection on immunological dynamics over metamorphosis

The legacy of larval infection on immunological dynamics over metamorphosis

The evolution of stage-specific virulence: differential selection of parasites in juveniles

Young but not defenceless: antifungal activity during embryonic development of a social insect

Contact Info

Product

Resources

About