Parents invest in their offspring by transmitting acquired resistance against pathogens that only the parents have encountered, a phenomenon known as trans-generational immune priming (TGIP). Examples of TGIP are widespread in the animal kingdom. Female vertebrates achieve TGIP by passing antibodies to their offspring, but the mechanisms of sex-specific TGIP in invertebrates are unclear despite increasing evidence suggesting that both male-specific and female-specific TGIP occurs in insects. We used the tobacco hornworm (Manduca sexta) to investigate sex-specific TGIP in insects because it is a model host for the analysis of insect immunity and the complete genome sequence is available. We found that feeding larvae with non-pathogenic Escherichia coli or the entomopathogen Serratia entomophila triggered immune responses in the infected host associated with shifts in both DNA methylation and histone acetylation. Maternal TGIP was mediated by the translocation of bacterial structures from the gut lumen to the eggs, resulting in the microbe-specific transcriptional reprogramming of genes encoding immunity-related effector molecules and enzymes involved in the regulation of histone acetylation as well as DNA methylation in larvae of the F1 generation. The third-instar F1 larvae displayed sex-specific differences in the expression profiles of immunity-related genes and DNA methylation. We observed crosstalk between histone acetylation and DNA methylation, which mediated sex-specific immune responses in the F1 generation derived from parents exposed to a bacterial challenge. Multiple routes for TGIP seem to exist in M. sexta and – partially sex-specific – effects in the offspring depend on the microbial exposure history of their parents. Crucially, the entomopathogen S. entomophila appears to be capable of interfering with TGIP in the host.
The bivoltine European map butterfly (Araschnia levana) displays seasonal polyphenism characterized by the formation of two remarkably distinct dorsal wing phenotypes: The spring generation (A. levana levana) is predominantly orange with black spots and develops from diapause pupae, whereas the summer generation (A. levana prorsa) has black, white, and orange bands and develops from subitaneous pupae. The choice between spring or summer imagoes is regulated by the photoperiod during larval and prepupal development, but polyphenism in the larvae has not been investigated before. Recently, it has been found that the prepupae of A. levana display differences in immunity‐related gene expression, so we tested whether larvae destined to become spring (short‐day) or summer (long‐day) morphs also display differences in innate immunity. We measured larval survival following the injection of a bacterial entomopathogen (Pseudomonas entomophila), the antimicrobial activity in their hemolymph and the induced expression of selected genes encoding antimicrobial peptides (AMPs). Larvae of the short‐day generation died significantly later, exhibited higher antibacterial activity in the hemolymph, and displayed higher induced expression levels of AMPs than those of the long‐day generation. Our study expands the seasonal polyphenism of A. levana beyond the morphologically distinct spring and summer imagoes to include immunological larval polyphenism that reveals the photoperiodic modulation of immunity. This may reflect life‐history traits that manifest as trade‐offs between immunity and fecundity.
The European map butterfly (Araschnia levana) is a well‐known example of seasonal polyphenism because the spring and summer imagoes exhibit distinct morphological phenotypes. The day length and temperature during larval and prepupal development determine whether spring or summer imagoes emerge after metamorphosis. Inspired by the fundamentally different transcriptomic profiles in prepupae developing from larvae exposed to long days or short days, we postulate that posttranscriptional epigenetic regulators such as microRNAs (miRNAs) may contribute to the epigenetic control of seasonal polyphenism in A. levana. To test this hypothesis, we used microarrays containing over 2,000 insect miRNAs to identify candidate regulators that are differentially expressed in last‐instar larvae or pupae developing under long‐day or short‐day conditions. We used our transcriptomic database to identify potential 3′‐untranslated regions of messenger RNAs to predict miRNA targets by considering both base pair complementarity and minimum free energy hybridization. This approach resulted in the identification of multiple targets of miRNAs that were differentially regulated in polyphenic morphs of A. levana including a candidate (miR‐2856‐3p) regulating the previously identified diapause bioclock protein gene. In conclusion, the expression profiling of miRNAs provided insights into their possible involvement in seasonal polyphenism of A. levana and offer an important resource for further studies.
The European map butterfly Araschnia levana is a well-known example of seasonal polyphenism. Spring and summer imagoes exhibit distinct morphological phenotypes. Key environmental factors responsible for the expression of different morphs are day length and temperature. Larval exposure to light for more than 16 h per day entails direct development and results in the adult f. prorsa summer phenotype. Less than 15.5 h per day increasingly promotes diapause and the adult f. levana spring phenotype. The phenotype depends on the timing of the release of 20-hydroxyecdysone in pupae. Release within the first days after pupation potentially inhibits the default “levana-gene-expression-profile” because pre-pupae destined for diapause or subitaneous development have unique transcriptomic programs. Moreover, multiple microRNAs and their targets are differentially regulated during the larval and pupal stages, and candidates for diapause maintenance, duration, and phenotype determination have been identified. However, the complete pathway from photoreception to timekeeping and diapause or subitaneous development remains unclear. Beside the wing polyphenism, the hormonal and epigenetic modifications of the two phenotypes also include differences in biomechanical design and immunocompetence. Here, we discuss research on the physiological and molecular basis of polyphenism in A. levana, including hormonal control, epigenetic regulation, and the effect of ecological parameters on developmental fate.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.