The legacy of larval infection on immunological dynamics over metamorphosis

Abstract

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'.

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

“…It is also possible that sensitivity is driven by spatial considerations, for example the rate of bacterial dissemination throughout the haemocoel, but it is not clear why this would differ among species and populations. Finally, these experiments compare inducible immune parameters among populations within the larval life stage, but whether the observed patterns remain consistent across host ontogeny (Critchlow, Norris, & Tate, ), or among males and females (Khan, Prakash, & Agashe, ), remains an avenue for future study. Uncovering the mechanism(s) regulating inducible sensitivity to microbe density, coupled with experimental evolution of sensitivity, would allow the estimation of the relative costs and benefits of microbe density‐dependent and independent inducible immune responses.…”

“…It is also possible that sensitivity is driven by spatial considerations, for example the rate of bacterial dissemination throughout the haemocoel, but it is not clear why this would differ among species and populations. Finally, these experiments compare inducible immune parameters among populations within the larval life stage, but whether the observed patterns remain consistent across host ontogeny (Critchlow, Norris, & Tate, 2019), or among males and females (Khan, Prakash, & Agashe, 2016),…”

Coordinating Coronavirus Research: The COVID-19 Infectious Disease Ontology

“…while exhibiting pathogenic behavior towards others [57,58]. With respect to the latter, mature plants are often susceptible to different pathogens than developing plants [59,60,61,62]. We capture virus pathogenic behavior in VIDO in steps.…”

Larvae and adults exhibit contrasting patterns of immune gene expression and infection resistance in wild flour beetle populations

“…Collectively, previous research on infection susceptibility and immunity in holometabolous insects defies neat conclusions about relative immune investment across ontogeny. In honeybee workers ( Apis mellifera ), for example, the activity of the melanization enzyme phenoloxidase increases steadily over development from larva to adult [11], while in the tobacco hornworm ( Manduca sexta ), melanization activity peaks in the larval stage and declines thereafter [12] (see [13] for further examples). Most studies, however, employ insect populations reared in (and evolving under) lab conditions, sometimes for substantial periods of time.…”

“…To address this question, we turned to wild and lab-derived populations of flour beetles ( Tribolium castaneum and T. confusum ). Previous research in lab-reared T. castaneum has suggested that the regulation of immune [13] and cuticular [14] gene expression differs among life stages in uninfected individuals, while, in larvae specifically, different populations of both species exhibit natural variation in immune gene expression and resistance to bacterial infection [15]. To test whether immune gene expression and infection resistance in these populations differs among life stages, we injected larvae and adults from seven populations (four T. castaneum , three T. confusum ) with one of four increasing doses of the entomopathogenic bacterium Bacillus thuringiensis (Bt) or sterile media as a wounding control.…”