Trans-generational Immune Priming in Invertebrates: Current Knowledge and Future Prospects

Abstract

Trans-generational immune priming (TGIP) refers to the transfer of the parental immunological experience to its progeny. This may result in offspring protection from repeated encounters with pathogens that persist across generations. Although extensively studied in vertebrates for over a century, this phenomenon has only been identified 20 years ago in invertebrates. Since then, invertebrate TGIP has been the focus of an increasing interest, with half of studies published during the last few years. TGIP has now been tested in several invertebrate systems using various experimental approaches and measures to study it at both functional and evolutionary levels. However, drawing an overall picture of TGIP from available studies still appears to be a difficult task. Here, we provide a comprehensive review of TGIP in invertebrates with the objective of confronting all the data generated to date to highlight the main features and mechanisms identified in the context of its ecology and evolution. To this purpose, we describe all the articles reporting experimental investigation of TGIP in invertebrates and propose a critical analysis of the experimental procedures performed to study this phenomenon. We then investigate the outcome of TGIP in the offspring and its ecological and evolutionary relevance before reviewing the potential molecular mechanisms identified to date. In the light of this review, we build hypothetical scenarios of the mechanisms through which TGIP might be achieved and propose guidelines for future investigations.

Honey Bee Queens and Virus Infections

“…Likewise, the test of immune priming was plagued by low sample size; studies of mortality dynamics require much higher sample sizes and replicates distributed across many replicates because of the intrinsic stochasticity of mortality, particularly in laboratory cage studies [101,102]. Finally, the sampling schedule for collecting offspring may also have prevented us from finding an effect because immune priming can be transient [103] and offspring should have been tested at multiple time points after queen inoculation with IAPV.…”

Relish as a Candidate Marker for Transgenerational Immune Priming in a Dampwood Termite (Blattodae: Archeotermopsidae)

“…Such context-dependent inheritance does not involve nucleotide changes in the genetic code [1][2][3]. Instead, the parental transfer of nutrients, hormones, cytoplasmic factors, small RNAs and other information-bearing molecules, as well as epigenetic tags that can modulate offspring gene expression [4][5][6], results in changes to offspring phenotype that anticipate environmental challenges and their demands. For example, differences in parental environments stemming from altered photoperiods [7], resource availability [8], temperatures [3], social environments [9], predation pressure [10], and parasite load [4] can potentially influence offspring phenotype in a manner that is independent of offspring genotype.…”

“…One example of potentially adaptive nongenetic inheritance is transgenerational immune priming (TGIP) whereby parents infected by a pathogen can immunologically prime their offspring against future infection [4]. TGIP is most likely to evolve when the pathogen is predictable in time and space (i.e., likely to persist into the next generation [5,14]) and when hosts exhibit either limited dispersal and/or overlapping generations [4,15]. If so, we expect TGIP to manifest via parental transfer of prefabricated immune proteins [16], immune-related transcripts [17], immune-elicitors [18,19], altered epigenetic markers [20,21], or combinations thereof, ultimately rendering progeny less susceptible to disease [4,5].…”

“…TGIP is most likely to evolve when the pathogen is predictable in time and space (i.e., likely to persist into the next generation [5,14]) and when hosts exhibit either limited dispersal and/or overlapping generations [4,15]. If so, we expect TGIP to manifest via parental transfer of prefabricated immune proteins [16], immune-related transcripts [17], immune-elicitors [18,19], altered epigenetic markers [20,21], or combinations thereof, ultimately rendering progeny less susceptible to disease [4,5]. For example, immune-primed mothers of Manduca sexta (Lepidoptera) can translocate pathogen-associated molecular patterns (PAMPs; molecular signatures unique to invading microbes) to their eggs [18,21] which, upon hatching, produce larvae with enhanced immune-related phenoloxidase expression and improved bacterial clearing capabilities [22,23].…”

“…Evidence for TGIP in insects predominantly comes from solitary, holometabolous insect species [4,5,18,19,[26][27][28]. However, social insects (mostly in the orders Hymenoptera and Blattodea [29]) live in densely populated groups of close relatives, rendering them highly vulnerable to the spread of contagion [30,31].…”