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  • 1
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    Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution (2018)
    Nature Research
    In:  Heredity, 121 . pp. 225-238.
    Details
    Publication Date: 2021-02-08
    Description: 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.
    Type: Article , PeerReviewed
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  • 2
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    Grandparental immune priming in the pipefish Syngnathus typhle (2017)
    BioMed Central
    In:  BMC Evolutionary Biology, 17 (Art. Nr. 44).
    Details
    Publication Date: 2020-02-06
    Description: Background: 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). 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. Results: Grandparental 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. Conclusion: In 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.
    Type: Article , PeerReviewed
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  • 3
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    Male Pregnancy and Biparental Immune Priming (2012)
    University of Chicago Press
    In:  The American Naturalist, 180 (6). pp. 802-814.
    Details
    Publication Date: 2020-10-26
    Description: In vertebrates, maternal transfer of immunity via the eggs or the placenta provides offspring with crucial information on prevailing pathogens and parasites. Males contribute little to such trans-generational immune priming, either because they do not share the environment and parasite pressure of the offspring, or because sperm are suggested to be too small for transfer of immunity. In the teleost group of Syngnathids (pipefish, seahorses and sea dragons) males brood female eggs in a placenta-like structure. Such sex-role-reversed species provide a unique opportunity to test for adaptive plasticity in immune transfer. Here males in addition to females should influence offspring immunity. We experimentally tested paternal effects on offspring immunity by examining immune cell proliferation and immune gene expression. Maternal and paternal bacterial exposure induced the offspring's immune defence five weeks after hatching, and this effect persisted in four-month-old offspring. For several offspring immune traits double parental exposure (maternal and paternal) enhanced the response, while for another group of immune traits, the trans-generational induction already took place if only one parent was exposed. Our study shows that sex-role reversal in connection with male pregnancy opens the door for bi-parental influences on offspring immunity, and may represent one additional advantage for the evolution of male pregnancy.
    Type: Article , PeerReviewed
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  • 4
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    Biparental immune priming in the pipefish Syngnathus typhle (2016)
    Elsevier
    In:  Zoology, 119 (5). pp. 262-272.
    Details
    Publication Date: 2019-02-01
    Description: Highlights: • In a sex-role reversed pipefish, fathers have a major impact on offspring immunity. • Maternal effects are effective early in life but cease upon maturation. • Fathers provide long-term protection that comes with immunological specificity. • Long-term protection could be based on parental epigenetic traces. • Biparental immunological transfer comes with additive costs but lacks additive advantages. Abstract: The transfer of immunity from parents to offspring (trans-generational immune priming (TGIP)) boosts offspring immune defence and parasite resistance. TGIP is usually a maternal trait. However, if fathers have a physical connection to their offspring, and if offspring are born in the paternal parasitic environment, evolution of paternal TGIP can become adaptive. In Syngnathus typhle, a sex-role reversed pipefish with male pregnancy, both parents invest into offspring immune defence. To connect TGIP with parental investment, we need to know how parents share the task of TGIP, whether TGIP is asymmetrically distributed between the parents, and how the maternal and paternal effects interact in case of biparental TGIP. We experimentally investigated the strength and differences but also the costs of maternal and paternal contribution, and their interactive biparental influence on offspring immune defence throughout offspring maturation. To disentangle maternal and paternal influences, two different bacteria were used in a fully reciprocal design for parental and offspring exposure. In offspring, we measured gene expression of 29 immune genes, 15 genes associated with epigenetic regulation, immune cell activity and life-history traits. We identified asymmetric maternal and paternal immune priming with a dominating, long-lasting paternal effect. We could not detect an additive adaptive biparental TGIP impact. However, biparental TGIP harbours additive costs as shown in delayed sexual maturity. Epigenetic regulation may play a role both in maternal and paternal TGIP.
    Type: Article , PeerReviewed
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  • 5
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    Bacteria-type-specific biparental immune priming in the pipefishSyngnathus typhle (2016)
    Wiley
    In:  Ecology and Evolution, 6 (18). pp. 6735-6757.
    Details
    Publication Date: 2019-05-24
    Description: The transfer of acquired and specific immunity against previously encountered bacteria from mothers to offspring boosts the immune response of the next generation and supports the development of a successful pathogen defense. While most studies claim that the transfer of immunity is a maternal trait, in the sex-role-reversed pipefish Syngnathus typhle, fathers nurse the embryos over a placenta-like structure, which opens the door for additional paternal immune priming. We examined the potential and persistence of bacteria-type-specific parental immune priming in the pipefish S. typhle over maturation time using a fully reciprocal design with two different bacteria species (Vibrio spp. and Tenacibaculum maritimum). Our results suggest that S. typhle is able to specifically prime the next generation against prevalent local bacteria and to a limited extent even also against newly introduced bacteria species. Long-term protection was thereby maintained only against prevailing Vibrio bacteria. Maternal and paternal transgenerational immune priming can complement each other, as they affect different pathways of the offspring immune system and come with distinct degree of specificity. The differential regulation of DNA-methylation genes upon parental bacteria exposure in premature pipefish offspring indicates that epigenetic regulation processes are involved in transferring immune-related information across generations. The identified trade-offs between immune priming and reproduction determine TGIP as a costly trait, which might constrain the evolution of long-lasting TGIP, if parental and offspring generations do not share the same parasite assembly.
    Type: Article , PeerReviewed
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  • 6
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    Biparental immune priming in the Broad-nosed Pipefish (Syngnathus Typhle) (2016)
    In:  (PhD/ Doctoral thesis), Christian-Albrechts-Universität zu Kiel, Kiel, Germany, 223 pp
    Details
    Publication Date: 2022-01-17
    Description: All living organisms are permanently exposed to harmful parasites and pathogens. The immune system and with it sophisticated strategies arose to face challenging pathogens such as bacteria and viruses. One outstanding strategy is the transfer of immunity from mothers to offspring known as “trans-generational immune priming” (TGIP). Through the transfer of acquired immunological protection mothers can boost the immune defense of their offspring and facilitate resistance against bacteria present in the maternal environment. Commonly, TGIP is limited to females and was considered to be a maternal trait. Yet, in the sex-role reversed pipefish Syngnathus typhle fathers are closely connected to the embryos during male pregnancy over a placenta-like structure. This intimate physical connection between fathers and offspring may mechanistically facilitate additional paternal immune priming and provides an exclusive chance to study biparental investment into offspring immunity. In my thesis, I explored multi-generational biparental immune priming in the sex-role reversed pipefish S. typhle and discussed its evolutionary and ecological consequences as well as the mechanistic basis.
    Type: Thesis , NonPeerReviewed
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  • 7
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    Microbial embryonal colonization during pipefish male pregnancy (2019)
    Nature Research
    In:  Scientific Reports, 9 (1). Art.Nr. 3.
    Details
    Publication Date: 2022-01-31
    Description: While originally acquired from the environment, a fraction of the microbiota is transferred from parents to offspring. The immune system shapes the microbial colonization, while commensal microbes may boost host immune defences. Parental transfer of microbes in viviparous animals remains ambiguous, as the two transfer routes (transovarial vs. pregnancy) are intermingled within the maternal body. Pipefishes and seahorses (syngnathids) are ideally suited to disentangle transovarial microbial transfer from a contribution during pregnancy due to their maternal egg production and their unique male pregnancy. We assessed the persistency and the changes in the microbial communities of the maternal and paternal reproductive tracts over proceeding male pregnancy by sequencing microbial 16S rRNA genes of swabs from maternal gonads and brood pouches of non-pregnant and pregnant fathers. Applying parental immunological activation with heat-killed bacteria, we evaluated the impact of parental immunological status on microbial development. Our data indicate that maternal gonads and paternal brood pouches harbor distinct microbial communities, which could affect embryonal development in a sex-specific manner. Upon activation of the immune system, a shift of the microbial community was observed. The activation of the immune system induced the expansion of microbiota richness during late pregnancy, which corresponds to the time point of larval mouth opening, when initial microbial colonization must take place
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
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