Pathogen‐induced maternal effects result in enhanced immune responsiveness across generations

Abstract

Parental investment theory postulates that adults can accurately perceive cues from their surroundings, anticipate the needs of future offspring based on those cues, and selectively allocate nongenetic resources to their progeny. Such context‐dependent parental contributions can result in phenotypically variable offspring. Consistent with these predictions, we show that bacterially exposed Manduca sexta mothers oviposited significantly more variable embryos (as measured by mass, volume, hatching time, and hatching success) relative to naïve and control mothers. By using an in vivo “clearance of infection” assay, we also show that challenged larvae born to heat‐killed‐ or live‐Serratia‐injected mothers, supported lower microbial loads and cleared the infection faster than progeny of control mothers. Our data support the notion that mothers can anticipate the future pathogenic risks and immunological needs of their unborn offspring, providing progeny with enhanced immune protection likely through transgenerational immune priming. Although the inclusion of live Serratia into oocytes does not appear to be the mechanism by which mothers confer protection to their young, other mechanisms, including epigenetic modifications in the progeny due to maternal pathogenic stress, may be at play. The adaptive nature of maternal effects in the face of pathogenic stress provides insights into parental investment, resource allocation, and life‐history theories and highlights the significant role that pathogen‐induced maternal effects play as generators and modulators of evolutionary change.

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

“…In addition, depending on the system, only specific types of pathogens may trigger TGIP. For example, in mealworm beetles priming against grampositive bacteria was shown to be more efficient than against gram-negative bacteria (Dhinaut et al 2018), although in the moth Manduca sexta, TGIP was shown upon inoculation with gram-negative Serratia marcescens (Rosengaus et al 2017). Concerning the afforded protection, highly specific protection on a strain level (Roth et al 2010) and cross-reactivity (Dhinaut et al 2018) have both been shown in related flour beetle systems, indicating that the specificity of protection given by TGIP may also vary greatly among pathogen types and hosts.…”

“…In honey bees this may be achieved by the nutrition protein vitellogenin acting in a novel role as a potential carrier of an immune priming signal to offspring by binding to PAMPs and transporting bacteria fragments into eggs (Salmela et al 2015). However, it remains to be investigated if this transfer alone is sufficient to elicit the substantial TGIP responses seen in several insects, and no transfer of bacterial fragments was shown to be associated with TGIP against bacteria in M. sexta moths (Rosengaus et al 2017).…”

Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor

“…To date, TGIP has been reported in all major invertebrate phyla (insects [10][11][12]21,36,37], crustaceans [1,38,39], molluscs [20,40]), except annelids. The present study filled this gap by evidencing TGIP in a marine polychaete.…”

“…In invertebrates, which are deprived of such immune effectors, modalities appear more diverse, and underpinning mechanisms often remain elusive [2]. Indeed, many studies have evidenced that an immune challenge of one or both parents enhances the immune performance of the offspring, measured as higher resistance to infection/parasitism or higher immune activity [9][10][11][12][13][14][15][16]. However, in most cases, so many processes occur between the stage of the manipulation (parent immune challenge) and the endpoint measure (immune efficiency in eggs, larvae, or adults produced by the primed parent) that the physiological mechanisms underlying TGIP cannot be properly evidenced.…”

Limb ablation and regeneration in Harmonia axyridis: costs for regenerators, but benefits for their progeny

“…For example, restriction of larval diet diminishes the maternal effects normally conferred by female Hippodamia convergens Guerin-Meneville to their progeny (Vargas et al, 2012a). However, there is evidence that insects challenged by bacterial infection can use epigenetic mechanisms to improve the immunological resistance of their progeny, for example in tobacco hornworm (Rosengaus et al, 2017), although immunological challenges resulting in negative maternal effects have been also observed in mosquitoes (Vantaux et al, 2014).…”