Grandparental immune priming in the pipefish Syngnathus typhle

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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0885-3) contains supplementary material, which is available to authorized users.

Trans‐generational plasticity in response to immune challenge is constrained by heat stress

“…On May 22, animals from the cold and the hot group were either exposed to an immune challenge with heat‐killed Vibrio bacteria (peritoneal injection of 50 μl of 10 9 bacteria/ml) of an Italian Vibrio isolate I9K1 (Beemelmanns & Roth, , ; Roth, Keller, Landis, Salzburger, & Reusch, ; Roth, Klein, et al., ), or they were left naïve. In each aquarium, one female and one male were placed that were either both immune‐challenged but kept at cold temperatures (VC), both immune‐challenged but exposed to elevated temperatures (VH), both not immune‐challenged and kept at cold temperatures (NC) or both not immune‐challenged and exposed to elevated temperatures (NH).…”

“…The small aquaria were swimming in the large tanks of the aquaria system due to their polystyrene surrounding, and water exchange was permitted over two circular sections that were cut and covered with fine‐mesh nets. Eight days after birth, juveniles of each half‐clutch were again split and either exposed to an immune challenge with heat‐killed Vibrio bacteria over a pricking with a needle dipped in a solution of 10 10 heat‐killed Vibrio bacteria/ml, or stayed without an immunological treatment (naïve) as described in Beemelmanns and Roth (, ). For this treatment, four families per parental treatment (16 families in total) with an equal distribution of five replicates per each of the four offspring treatment groups (NC, NH, VC, VH) were used (20 offspring per family resulting in 16 × 20 = 320 animals).…”

“…If environmental change induces a shift in the parasite assemblage, this host plasticity promotes an efficient response that mediates acclimatization (Lazzaro & Little, ). The plasticity can be transferred from the parents to the offspring in invertebrates and vertebrates (trans‐generational immune priming, TGIP; Beemelmanns & Roth, , , ; Grindstaff, Brodie, & Ketterson, ; Hasselquist & Nilsson, ; Roth, Klein, Beemelmanns, Scharsack, & Reusch, ; Sadd, Kleinlogel, Schmid‐Hempel, & Schmid‐Hempel, ). TGIP boosts offspring immunity and is in vertebrates of particular importance during early life stages, when mortality selection is high due to the immature adaptive immune system (Hasselquist & Nilsson, ).…”

“…Trans‐generational plasticity has been shown to buffer single abiotic and biotic changes (Beemelmanns & Roth, ; Donelson et al., ; Roth, Klein, et al., ; Salinas & Munch, ; Shama et al., ). However, whether TGP also has the potential to compensate multiple environmental modifications simultaneously remains unknown.…”

“…Alternatively, we hypothesize that parental immune challenge and temperature change do not interact but involve separate physiological mechanisms relying on segregated resource pools. Focusing on these two hypotheses, we assessed expression of a limited gene set (44) involved in immune defence or DNA modification and histone modification with a known role in TGIP (Beemelmanns & Roth, , ; Roth, Klein, et al., ). As life‐history responses, we measured duration of male pregnancy, clutch size and offspring size.…”