Challenges of metamorphosis in invertebrate hosts: maintaining parasite resistance across life‐history stages

Abstract

Abstract. 1. Insects lack the acquired immune system of vertebrates, but there is some evidence that insect immunity can be primed against an encountered pathogen to mitigate the intensity of future infections within a life stage.2. Many invertebrates have multiple life-history stages separated by complete metamorphosis, but different life stages can often be infected by the same pathogens, and the potential loss of immune priming during metamorphosis could therefore have detrimental effects on the host. Evidence that invertebrate immune priming can persist through metamorphosis is still missing, and consequently it is unclear how host-parasite interactions change across different life-history stages in the context of infection history.3. By experimentally manipulating the infection history of the flour beetle Tribolium confusum, we show that intestinal gregarine parasite infections during the larval stage reduced parasite load in adults, demonstrating that a host-controlled mechanism for parasite resistance can persist through complete metamorphosis in insects.4. Infections reduced larval developmental rates and increased host mortality but only during the crucial metamorphic stage, indicating that parasites impact multiple life stages. In general, our results demonstrate that invertebrates can show surprisingly robust immune priming despite dramatic physiological changes and protect hosts across completely different life-history stages.

Insect immunology and hematopoiesis

“…The length of the protection may last the lifetime of the insect (although most of these studies have been performed in short-lived insects), or may last only for only a few days (Moret and Siva-Jothy, 2003; Pham et al, 2007). In addition, protection from infection may be conferred to the offspring (Moret and Schmid-Hempel, 2001; Trauer-Kizilelma and Hilker, 2015), may be passed along to the nestmates (Traniello et al, 2002; Ugelvig and Cremer, 2007), and may persist across molts (Bargielowski and Koella, 2009; Thomas and Rudolf, 2010). …”

Evolution of transgenerational immunity in invertebrates

“…It has been documented in a range of invertebrate species, including Decapoda [5], Branchiopoda [6], Lepidoptera [7], Coleoptera [8], Diptera [9], and Hymenoptera [10]. Interestingly, in some cases, immune priming has been shown to persist not only throughout the lifespan of the animal [11,12], but also across generations [13][14][15]. Transgenerational immunity has been thus far reported in a dozen invertebrate species [13,14,16 -24].…”

Methylation on RNA: A Potential Mechanism Related to Immune Priming within But Not across Generations

“…This phenomenon has been reported in ctenophores, sponges, mollusks, crustaceans and insects, among others (Milutinović and Kurtz, 2016). Within generations, immune priming is strain or species specific (Roth et al, 2009) and long lasting (it can persist across different life developmental stages; Thomas and Rudolf, 2010). In addition, immune priming not only occurs within generations but also across generations: parents can protect their offspring against the same parasites or pathogens that they confronted (Sadd and Schmid-Hempel, 2007).…”