Adaptive immunity in invertebrates: A straw house without a mechanistic foundation

Hauton, Chris; Smith, Valerie J.

doi:10.1002/bies.20650

Cited by 105 publications

(86 citation statements)

References 56 publications

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“…This result is particularly interesting because, despite increasing evidence supporting transfer of innate immunity in both vertebrates (fish and birds [62][63][64][65]) and invertebrates [9,33,34], there is still an ongoing debate regarding the validity, generality and interpretation of parental immune transfer in invertebrates [42,43,66,67]. Nonetheless, even without knowing the underlying immunological mechanism [42,43], the results generated in our study are consistent with the hypothesis that transgenerational transmission of innate immune factors does occur in D. melanogaster. This contention is based on the finding that daughters were better able to withstand an immune activation challenge (by maintaining high reproductive success) when produced by mothers that had also been immune-challenged prior to reproduction.…”

Section: Discussionsupporting

confidence: 85%

Transgenerational interactions involving parental age and immune status affect female reproductive success inDrosophila melanogaster

Nystrand

Dowling

2014

Proc. R. Soc. B.

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It is well established that the parental phenotype can influence offspring phenotypic expression, independent of the effects of the offspring's own genotype. Nonetheless, the evolutionary implications of such parental effects remain unclear, partly because previous studies have generally overlooked the potential for interactions between parental sources of non-genetic variance to influence patterns of offspring phenotypic expression. We tested for such interactions, subjecting male and female Drosophila melanogaster of two different age classes to an immune activation challenge or a control treatment. Flies were then crossed in all age and immune status combinations, and the reproductive success of their immune-and control-treated daughters measured. We found that daughters produced by two younger parents exhibited reduced reproductive success relative to those of other parental age combinations. Furthermore, immune-challenged daughters exhibited higher reproductive success when produced by immune-challenged relative to control-treated mothers, a pattern consistent with transgenerational immune priming. Finally, a complex interplay between paternal age and parental immune statuses influenced daughter's reproductive success. These findings demonstrate the dynamic nature of age-and immune-mediated parental effects, traceable to both parents, and regulated by interactions between parents and between parents and offspring.

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Section: Discussionsupporting

confidence: 85%

Transgenerational interactions involving parental age and immune status affect female reproductive success inDrosophila melanogaster

Nystrand

Dowling

2014

Proc. R. Soc. B.

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“…Despite the compelling evidence for its existence, our understanding of the mechanisms behind immune priming in invertebrates is still relatively poor [22]. As such, it is hard to specify the mechanisms that are critical to the evolutionary response of hosts in their level of priming, but it is clear that this may involve pathways in both the recognition of pathogens and the strength of the response.…”

Section: Modelmentioning

confidence: 99%

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

Best

Tidbury

White

et al. 2013

J. R. Soc. Interface.

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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.

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“…In addition to these examples of specific acquired resistance to reinfection, a wealth of observational evidence supporting increases in specific gene expression patterns, survival, and defense-related protein production is available for other invertebrates (10), suggesting that the capacity to acquire resistance is likely to be present in many invertebrate phyla. Unfortunately, to date very few data are available to suggest the mechanisms that underlie these phenomena (14).…”

mentioning

confidence: 99%

Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection

Hanington

Forys

Dragoo

et al. 2010

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

132

139

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Invertebrates lack adaptive immune systems homologous to those of vertebrates, yet it is becoming increasingly clear that they can produce diversified antigen recognition molecules. We have previously noted that the snail Biomphalaria glabrata produces a secreted lectin, fibrinogen-related protein 3 (FREP3), unusual among invertebrate defense molecules because it is somatically diversified by gene conversion and point mutation. Here we implicate FREP3 in playing a central role in resistance to a major group of snail pathogens, digenetic trematodes. FREP3 is up-regulated in three models of resistance of B. glabrata to infection with Schistosoma mansoni or Echinostoma paraensei, and functions as an opsonin favoring phagocytosis by hemocytes. Knock-down of FREP3 in resistant snails using siRNA-mediated interference resulted in increased susceptibility to E. paraensei, providing a direct link between a gastropod immune molecule and resistance to trematodes. FREP3 up-regulation is also associated with heightened responsiveness following priming with attenuated digenetic trematodes (acquired resistance) in this model invertebrate immune system. host-parasite interactions | evolution | immunology | parasitology | schistosomiasis

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Adaptive immunity in invertebrates: A straw house without a mechanistic foundation

Cited by 105 publications

References 56 publications

Transgenerational interactions involving parental age and immune status affect female reproductive success inDrosophila melanogaster

Transgenerational interactions involving parental age and immune status affect female reproductive success inDrosophila melanogaster

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

Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection

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