Grandparental immune priming in the pipefish Syngnathus typhle

Anne Beemelmanns,Olivia Roth

doi:10.1186/s12862-017-0885-3

Abstract

BackgroundPhenotypic changes in response to environmental influences can persist from one generation into the next. In many systems parental parasite experience influences offspring immune responses, known as transgenerational immune priming (TGIP). TGIP in vertebrates is mainly maternal and short-term, supporting the adaptive immune system of the offspring during its maturation. However, if fathers and offspring have a close physical connection, evolution of additional paternal immune priming can be adaptive. Biparental TGIP may result in maximized immunological protection. Here, we investigate multigenerational biparental TGIP in the sex-role reversed pipefish Syngnathus typhle by exposing grandparents to an immune challenge with heat-killed bacteria and assessing gene expression (44 target genes) of the F2-generation.ResultsGrandparental immune challenge induced gene expression of immune genes in one-week-old grandoffspring. Similarly, genes mediating epigenetic regulation including DNA-methylation and histone modifications were involved in grandparental immune priming. While grand-maternal impact was strong on genes of the complement component system, grand-paternal exposure changed expression patterns of genes mediating innate immune defense.ConclusionIn a system with male pregnancy, grandparents influenced the immune system of their grandoffspring in a sex-specific manner, demonstrating multigenerational biparental TGIP. The involvement of epigenetic effects suggests that TGIP via the paternal line may not be limited to the pipefish system that displays male pregnancy. While the benefits and costs of grandparental TGIP depend on the temporal heterogeneity of environmental conditions, multigenerational TGIP may affect host-parasite coevolution by dampening the amplitude of Red Queen Dynamics.

Highlights

Phenotypic changes in response to environmental influences can persist from one generation into the
We evaluated with a Permutational Multivariate Analysis of Variance (PERMANOVA) whether gene expression (44 target genes) of F2-juvenile pipefish revealed grandparental sex-specific influences (‘F0-sex’) and grandoffspring bacteria treatment effects (‘F2-bacteria’) including their interaction (‘F0-sex x F2-bacteria’), while setting the family structure as random term
The multivariate PERMANOVA model was based on an Euclidean distance matrix and applied for 29 immune genes and 15 genes associated to epigenetic regulation, and divided into following specific functional gene categories: (i) innate immune system

Summary

Introduction

Phenotypic changes in response to environmental influences can persist from one generation into the next. In many systems parental parasite experience influences offspring immune responses, known as transgenerational immune priming (TGIP). An offspring phenotype is influenced by a plethora of environmental factors experienced during its ontogeny and by its parents [1,2,3] Such transgenerational plasticity of phenotypes is often adaptive, can promote efficient and rapid acclimatization to environmental changes, and even has the potential to modify evolutionary dynamics [4,5,6]. Environmental variation can result in heterogeneous parasite distributions across environments [21] persisting through host generations Under such matching environmental conditions where host-dispersal is limited and hosts have a long lifespan, selection for TGIP is predicted to be strong and evolutionarily adaptive [22, 23]

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