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ABSTRACT Animals encounter many novel and unpredictable challenges when moving into new areas, including pathogen exposure. Because effective immune defenses against such threats can be costly, plastic immune responses could be particularly advantageous, as such defenses can be engaged only when context warrants activation. DNA methylation is a key regulator of plasticity via its effects on gene expression. In vertebrates, DNA methylation occurs exclusively at CpG dinucleotides and, typically, high DNA methylation decreases gene expression, particularly when it occurs in promoters. The CpG content of gene regulatory regions may therefore represent one form of epigenetic potential (EP), a genomic means to enable gene expression and hence adaptive phenotypic plasticity. Non-native populations of house sparrows (Passer domesticus) – one of the world's most cosmopolitan species – have high EP in the promoter of a key microbial surveillance gene, Toll-like receptor 4 (TLR4), compared with native populations. We previously hypothesized that high EP may enable sparrows to balance the costs and benefits of inflammatory immune responses well, a trait critical to success in novel environments. In the present study, we found support for this hypothesis: house sparrows with high EP in the TLR4 promoter were better able to resist a pathogenic Salmonella enterica infection than sparrows with low EP. These results support the idea that high EP contributes to invasion and perhaps adaptation in novel environments, but the mechanistic details whereby these organismal effects arise remain obscure.
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Microbial surveillance versus cytokine responsiveness in native and non-native house sparrows
The success of introduced species often relies on flexible traits, including immune system traits. While theories predict non-natives will have weak defences due to decreased parasite pressure, effective parasite surveillance remains crucial, as infection risk is rarely zero and the evolutionary novelty of infection is elevated in non-native areas. This study examines the relationship between parasite surveillance and cytokine responsiveness in native and non-native house sparrows, hypothesizing that non-natives maintain high pathogen surveillance while avoiding costly inflammation. We made this specific prediction, as this pattern could enable invaders to effectively mitigate pathogen risk in a manner commensurate with the life-history priorities of a colonizing organism (i.e. rapid maturation and high reproductive effort). To test this hypothesis, we measuredTLR-2 andTLR-4 expression, markers of pathogen surveillance and cytokine responses (changes inIL-1βandIL-10), regulators of inflammation, to a simulated bacterial infection. In non-native sparrows, we found that asTLR-4 expression increased,IL-1βandIL-10responses decreased, a relationship not observed in native sparrows. Additionally, higher body condition predicted largerIL-1βandIL-10responses in all birds. These findings suggest that highTLR-4surveillance may mitigate strong inflammatory responses in non-native sparrows, with pathological and resource-based costs driving immune variation among and within populations.
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- Award ID(s):
- 2027054
- PAR ID:
- 10661058
- Publisher / Repository:
- Biology Letters
- Date Published:
- Journal Name:
- Biology Letters
- Volume:
- 21
- Issue:
- 1
- ISSN:
- 1744-957X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1098/rsbl.2024.0431
