Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution

Abstract

Parental experience with parasites and pathogens can lead to increased offspring resistance to infection, through a process known as transgenerational immune priming (TGIP). Broadly defined, TGIP occurs across a wide range of taxa, and can be viewed as a type of phenotypic plasticity, with hosts responding to the pressures of relevant local infection risk by altering their offspring's immune defenses. There are ever increasing examples of both invertebrate and vertebrate TGIP, which go beyond classical examples of maternal antibody transfer. Here we critically summarize the current evidence for TGIP in both invertebrates and vertebrates. Mechanisms underlying TGIP remain elusive in many systems, but while it is unlikely that they are conserved across the range of organisms with TGIP, recent insight into epigenetic modulation may challenge this view. We place TGIP into a framework of evolutionary ecology, discussing costs and relevant environmental variation. We highlight how the ecology of species or populations should affect if, where, when, and how TGIP is realized. We propose that the field can progress by incorporating evolutionary ecology focused designs to the study of the so far well chronicled, but mostly descriptive TGIP, and how rapidly developing -omic methods can be employed to further understand TGIP across taxa.

Fig. 1

A simple schematic representing the base expectations of the existence of TGIP when accounting for the predictability of the parasite environment between generations and the costs associated with elevated immunity. In the absence of associated costs, all offspring will be expected to display increased resistance, irrespective of parental experience with parasites and the predictability of the environment across generations. When costs for increased resistance are present, increased resistance is only predicted when the parental environment predicts the parasite environment of offspring, and when parents are exposed to infection (TGIP). Under a framework of specific costs of resistance, parasite-specific TGIP is only expected to evolve when the predictability of the environment across generations is also specific to the parasite types