Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle,Tenebrio molitor

Abstract

A primary infection by a parasite may indicate a higher risk of being reinfected in the near future (since infection may indicate that enemies are becoming more abundant). Acquired immunity does not exist in invertebrates despite the fact that they also face increased risks of reinfection following primary exposure. However, when subjected to immune insult, insects can produce immune responses that persist for long enough to provide prophylaxis. Because these immune responses are costly, persistence must be maintained through a selective advantage. We tested for the possibility that these long-lasting immune responses provided increased resistance to later infections by experimentally mimicking a primary immune insult (pre-challenge) in larvae of the mealworm beetle, Tenebrio molitor, with lipopolysaccharides (LPS) prior to early or late exposure to spores of the entomopathogenic fungus Metarhizium anisopliae. We found that pre-challenged larvae produced a long-lasting antimicrobial response, which provided a survival benefit when the larvae were exposed to fungal infection. These results suggest that the observed response is functionally 'adaptive'.

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

“…These claims for functionally adaptive immunity have been based largely on observations of only a few species and a limited selection of phenomena. Nonetheless, they have been presented as evidence for innate immune memory or priming, (2)(3)(4)(5)(6)(7)(8)(9) innate immune specificity (2,5,8) or the inheritance of immune genotype within invertebrate lineages (i.e. vertical transfer from mother to offspring).…”

“…They bind to molecules within the host immune system, the pattern recognition receptors (PRRs), to form a complex that then initiates a series of events, such as signal transduction or activation of enzyme cascades that result in the liberation of bioactive molecules. What actually happens when protostome invertebrates are injected with PAMPs is that a full-blown immune response occurs, involving activation of particular enzyme cascades, such as the prophenoloxidase system, the regulated exocytosis of aggressive molecules, (4,13) an increase in the expression of genes coding for antimicrobial proteins (17,20,23) and /or other related proteins (see Table 1 and Smith et al (33) ), and the initiation of encapsulation reactions leading to haemocytopenia. Experiments in which presentation of PAMPs to the protostome immune system has been claimed to 'prime' the immune system, measure not immune parameters, as might be expected, but survival, (5) temporary increases in growth (34,35) or reproductive capacity.…”

Lepidopteran species have a variety of defence strategies against bacterial infections

“…Recent research shows that invertebrate defences against pathogens are more complex and sophisticated than previously thought (Little & Kraaijeveld 2004, Criscitiello & de Figueiredo 2013. The innate immune system, consisting of humoral and cellular subdivisions, has also an adaptive aspect, which allows a more efficient response in the case of a recurring infection (Moret & Siva-Jothy 2003, Kurtz 2005, Sadd & Schmid-Hempel 2006. Mechanistic studies usually concentrate on model species such as Drosophila melanogaster and have been proven extremely valuable for understanding the regulation of host immunity in these species.…”

“…Although invertebrates lack an anti-body based immunological memory, adaptivelike immune functions have been reported in several cases (Moret & Siva-Jothy 2003, Criscitiello & de Figueiredo 2013. The innate immune system seems to have an inducible dimension, immune priming, functionally analogous to the adaptive immune defence in vertebrates (Cristiciello & de Figueiredo 2013).…”

“…The innate immune system seems to have an inducible dimension, immune priming, functionally analogous to the adaptive immune defence in vertebrates (Cristiciello & de Figueiredo 2013). Whether the observations of protection against a recurring infection are mainly due to a prolonged, persistent immune reaction that stays up regulated (Moret & Siva-Jothy 2003, Mikonranta et al 2014, or an enhanced re-up regulation of defences during the secondary pathogen encounter still remains somewhat controversial (Sadd & Schmid-Hempel 2006). This makes studying a larger variety of hosts and pathogens even more important.…”