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  • 1
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    Immunostimulatory effects of dietary poly-β-hydroxybutyrate in European sea bass postlarvae (2017)
    Wiley
    In:  Aquaculture Research, 48 (12). pp. 5707-5717.
    Details
    Publication Date: 2020-02-06
    Description: The stable production of high-quality fry in marine aquaculture is still hampered by unpredictable mortality caused by infectious diseases during larval rearing. Consequently, the development of new biocontrol agents is crucial for a viable aquaculture industry. The bacterial energy storage compound poly-β-hydroxybutyrate (PHB) has been shown to exhibit beneficial properties on aquatic organisms such as enhanced survival, growth, disease resistance and a controlling effect on the gastrointestinal microbiota. However, the effect of PHB on the developing immune system of fish larvae has so far not been investigated. In this study, the effect of feeding PHB-enriched Artemia nauplii on survival, growth and immune response in European sea bass (Dicentrarchus labrax) postlarvae was examined. Amorphous PHB was administered to 28-day-old sea bass postlarvae over a period of 10 days. The survival and growth performance were monitored, and the expression of 29 genes involved in immunity, growth, metabolism and stress-response was measured. While the expression of the insulin-like growth factor 1 (igf1), an indicator of relative growth, was upregulated in response to feeding PHB, the larval survival and growth performance remained unaffected. After 10 days of PHB treatment, the expression of the antimicrobial peptides dicentracin (dic) and hepcidin (hep) as well as mhc class IIa and mhc class IIb was elevated in the PHB fed postlarvae. This indicates that PHB is capable of stimulating the immune system of fish early life stages, which may be the cause of the increased resistance to diseases and robustness observed in previous studies.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/are.13393
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  • 2
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    Demography and genome divergence of lake and stream populations of an East African cichlid fish (2017)
    Wiley
    In:  Molecular Ecology, 26 (19). 5016-5030 .
    Details
    Publication Date: 2020-02-06
    Description: Disentangling the processes and mechanisms underlying adaptive diversification is facilitated by the comparative study of replicate population pairs that have diverged along a similar environmental gradient. Such a setting is realized in a cichlid fish from southern Lake Tanganyika, Astatotilapia burtoni, which occurs within the lake proper as well as in various affluent rivers. Previously, we demonstrated that independent lake and stream populations show similar adaptations to the two habitat regimes. However, little is known about the evolutionary and demographic history of the A. burtoni populations in question and the patterns of genome divergence among them. Here, we apply restriction site-associated DNA sequencing (RADseq) to examine the evolutionary history, the population structure and genomic differentiation of lake and stream populations in A. burtoni. A phylogenetic reconstruction based on genome-wide molecular data largely resolved the evolutionary relationships among populations, allowing us to re-evaluate the independence of replicate lake-stream population clusters. Further, we detected a strong pattern of isolation by distance, with baseline genomic divergence increasing with geographic distance and decreasing with the level of gene flow between lake and stream populations. Genome divergence patterns were heterogeneous and inconsistent among lake-stream population clusters, which is explained by differences in divergence times, levels of gene flow and local selection regimes. In line with the latter, we only detected consistent outlier loci when the most divergent lake-stream population pair was excluded. Several of the thus identified candidate genes have inferred functions in immune and neuronal systems and show differences in gene expression between lake and stream populations.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
    Format: text
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    DOI: 10.1111/mec.14248
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  • 3
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    Effects of parental care on resource allocation into immune defense and buccal microbiota in mouthbrooding cichlid fishes (2018)
    Wiley
    In:  Evolution, 72 (5). pp. 1109-1123.
    Details
    Publication Date: 2021-02-08
    Description: Sexual dimorphism is founded upon a resource allocation trade-off between investments in reproduction versus other life-history traits including the immune system. In species with conventional parental care roles, theory predicts that males maximize their lifetime reproductive success by allocating resources toward sexual selection, while females achieve this through prolonging their lifespan. Here, we examine the interrelation between sexual dimorphism and parental care strategies in closely related maternal and biparental mouthbrooding cichlid fishes from East African Lake Tanganyika. We measured cellular immune parameters, examined the relative expression of 28 immune system and life history-related candidate genes and analyzed the microbiota composition in the buccal cavity. According to our predictions, maternal mouthbrooders are more sexually dimorphic in immune parameters than biparental mouthbrooders, which has possibly arisen through a differential resource allocation into parental care versus secondary sexual traits. Biparental mouthbrooders, on the other hand, which share the costs of parental care, feature an upregulated adaptive immune response and stronger antiviral properties, while their inflammation response is reduced. Overall, our results suggest a differential resource allocation trade-off between the two modes of parental investment.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/evo.13452
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  • 4
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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
    Format: text
    Format: text
    DOI: 10.1002/ece3.2391
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  • 5
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    Male mate choice relies on major histocompatibility complex class I in a sex-role-reversed pipefish (2014)
    Wiley
    In:  Journal of Evolutionary Biology, 27 (5). pp. 929-938.
    Details
    Publication Date: 2019-07-09
    Description: Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC-based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex-role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence-based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex-role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/jeb.12365
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  • 6
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    Experimental evolution of external immune defences in the red flour beetle (2014)
    Wiley
    In:  Journal of Evolutionary Biology, 27 (8). pp. 1562-1571.
    Details
    Publication Date: 2017-07-10
    Description: The red flour beetle, Tribolium castaneum, secretes quinones that control the microbial flora in the surrounding environment. These secretions act as an external immune defence that provides protection against pathogens. At high concentrations, however, these secretions are harmful to the host itself, and selection may thus have optimized the level of expression under natural conditions. Here, we show that the expression of external immunity responded to selection during experimental evolution within a few generations. At the same time, one component of internal immune defence (phenoloxidase activity) was compromised in beetles selected for either high or low external defences. Intriguingly, offspring protection against a natural pathogen was reduced in flour obtained from beetle lines selected for low amounts of secretions. Altogether, this suggests that external and internal immune defences work together efficiently under natural conditions, whereas every manipulation on the side of external immune defence comes with costs to the internal immune defence.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/jeb.12406
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  • 7
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    Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum (2010)
    Wiley
    In:  Journal of Animal Ecology, 79 (2). pp. 403-413.
    Details
    Publication Date: 2017-06-09
    Description: Summary 1. Parasitized females in mammals, fish and birds can enhance the immune defence of their offspring by transferring specific antibodies for the embryo. Likewise, social insect mothers transfer immunity despite the fact that invertebrates lack antibodies. 2.  Female trans-generational immune priming is consistent with parental investment theory, because mothers invest more into rearing their offspring than fathers. However, when immune priming is not directly linked to parental care, as is often the case in insects that abandon their eggs after oviposition, both sexes might benefit from protecting their offspring. 3. Using the red flour beetle, Tribolium castaneum, we show that after parental exposure to heat-killed bacteria, trans-generational immune priming occurs through fathers as well as mothers. 4. This novel finding challenges the traditional view that males provide only genes to their offspring in species without paternal care, and raises the possibility of a division of tasks with respect to immune protection between parents.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/j.1365-2656.2009.01617.x
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  • 8
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    Variation of anal fin egg-spots along an environmental gradient in a haplochromine cichlid fish (2017)
    Wiley
    In:  Evolution, 71 (3). pp. 766-777.
    Details
    Publication Date: 2020-10-26
    Description: Male secondary sexual traits are targets of inter- and/or intrasexual selection, but can vary due to a correlation with life-history traits or as by-product of adaptation to distinct environments. Trade-offs contributing to this variation may comprise conspicuousness towards conspecifics versus inconspicuousness towards predators, or between allocating resources into coloration versus the immune system. Here, we examine variation in expression of a carotenoid-based visual signal, anal-fin egg-spots, along a replicate environmental gradient in the haplochromine cichlid fish Astatotilapia burtoni. We quantified egg-spot number, area, and coloration; applied visual models to estimate the trait's conspicuousness when perceived against the surrounding tissue under natural conditions; and used the lymphocyte ratio as a measure for immune activity. We find that (i) males possess larger and more conspicuous egg-spots than females, which is likely explained by their function in sexual selection; (ii) riverine fish generally feature fewer but larger and/or more intensively colored egg-spots, which is probably to maintain signal efficiency in intraspecific interactions in long-wavelength shifted riverine light conditions; and (iii) egg-spot number and relative area correlate with immune defense, suggesting a trade-off in the allocation of carotenoids. Taken together, haplochromine egg-spots feature the potential to adapt to the respective underwater light environment, and are traded-off with investment into the immune system
    Type: Article , PeerReviewed
    Format: text
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    DOI: 10.1111/evo.13166
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  • 9
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    Bateman's principle and immunity in a sex-role reversed pipefish (2011)
    Wiley
    In:  Journal of Evolutionary Biology, 24 (7). pp. 1410-1420.
    Details
    Publication Date: 2017-07-10
    Description: In diverse animal species, from insects to mammals, females display a more efficient immune defence than males. Bateman’s principle posits that males maximize their fitness by increasing mating frequency whereas females gain fitness benefits by maximizing their lifespan. As a longer lifespan requires a more efficient immune system, these implications of Bateman’s principle may explain widespread immune dimorphism among animals. Because in most extant animals, the provisioning of eggs and a higher parental investment are attributes of the female sex, sex-role reversed species provide a unique opportunity to assess whether or not immune dimorphism depends on life history and not on sex per se. In the broad-nosed pipefish Syngnathus typhle, males brood and nourish the eggs in a ventral pouch and thus invest more into reproduction than females. We found males to have a more active immune response both in field data from four populations and also in an experiment under controlled laboratory conditions. This applied to different measures of immunocompetence using innate as well as adaptive immune system traits. We further determined the specificity of immune response initiation after a fully factorial primary and secondary exposure to a common marine pathogen Vibrio spp. Males not only had a more active but also a more specific immune defence than females. Our results thus indeed suggest that the sex that invests more into the offspring has the stronger immune defence.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/j.1420-9101.2011.02273.x
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  • 10
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    Hosts are ahead in a marine host-parasite coevolutionary arms race: innate immune system adaptation in pipefish Syngnathus typhle against Vibrio phylotypes (2012)
    Wiley
    In:  Evolution, 66 (8). pp. 2528-2539.
    Details
    Publication Date: 2017-01-04
    Description: Microparasites have a higher evolutionary potential than their hosts due to an increased mutation rate and a shorter generation time that usually results in parasites being locally adapted to their sympatric hosts. This pattern may not apply to generalist pathogens as adaptation to sympatric host genotypes is disadvantageous due to a narrowing of the host range, in particular under strong gene flow among host populations. Under this scenario, we predict that the immune defense of hosts reveals adaptation to locally common pathogen phylotypes. This was tested in four host populations of the pipefish Syngnathus typhle and associated bacteria of the genus Vibrio. We investigated the population divergence among host and bacteria populations and verified that gene flow is higher among host populations than among parasite populations. Next, we experimentally assessed the strength of innate immune defense of pipefish hosts using in vitro assays that measured antimicrobial activity of blood plasma against sympatric and allopatric Vibrio phylotypes. Pipefish plasma displays stronger antimicrobial activity against sympatric Vibrio phylotypes compared to allopatric ones. This suggests that host defense is genetically adapted against local bacteria with a broad and unspecialized host spectrum, a situation that is typical for marine systems with weak host population structure.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/j.1558-5646.2012.01614.x
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