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ABSTRACT Epigenetic mechanisms may play a central role in mediating phenotypic plasticity, especially during range expansions, when populations face a suite of novel environmental conditions. Individuals may differ in their epigenetic potential (EP; their capacity for epigenetic modifications of gene expression), which may affect their ability to colonize new areas. One form of EP, the number of CpG sites, is higher in introduced house sparrows (Passer domesticus) than in native birds in the promoter region of a microbial surveillance gene, Toll-like Receptor 4 (TLR4), which may allow invading birds to fine-tune their immune responses to unfamiliar parasites. Here, we compared TLR4 gene expression from whole blood, liver and spleen in house sparrows with different EP, first challenging some birds with lipopolysaccharide (LPS), to increase gene expression by simulating a natural infection. We expected that high EP would predict high inducibility and reversibility of TLR4 expression in the blood of birds treated with LPS, but we did not make directional predictions regarding organs, as we could not repeatedly sample these tissues. We found that EP was predictive of TLR4 expression in all tissues. Birds with high EP expressed more TLR4 in the blood than individuals with low EP, regardless of treatment with LPS. Only females with high EP exhibited reversibility in gene expression. Further, the effect of EP varied between sexes and among tissues. Together, these data support EP as one regulator of TLR4 expression.
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Temperature predictability and introduction history affect the expression of genes regulating DNA methylation in a globally distributed songbird
Phenotypic plasticity is a major mechanism whereby organisms adjust their traits within‐generations to changes in environmental conditions. In the context of range expansions, plasticity is thought to be especially important, as plastic changes in traits can lead to rapid adaptation. One epigenetic process in particular, DNA methylation, enables organisms to adjust gene expression contingent on the environment, which suggests it may play a role in range expansions. At present, we know little about how methylation is regulated in wildlife, especially expression of the enzymes responsible for altering methyl marks on the genome. In this study, we compared expression of three epigenetic regulator genes (DNA methyltransferase 1, DNMT1; DNA methyltransferase 3, DNMT3; and one ten‐eleven translocation methylcytosine dioxygenase, TET2) in three tissues (gut, liver, and spleen) of house sparrowsPasser domesticusfrom nine countries. Some countries are in the native range of the species (Israel, the Netherlands, Norway, Spain, and Vietnam) whereas others are sites the species has colonized in the last 150 years (i.e. Australia, Canada, New Zealand, and Senegal). In this exploratory study, we asked whether non‐native birds and/or birds from sites with comparatively unpredictable climates would express different levels of these genes. We found that all three genes were expressed more in sparrows from the native range and from areas with more stable temperatures. Expression of all three genes was also strongly correlated among‐locations and within‐individuals, but mean expression was quite different among tissues. Many factors (e.g. urbanization of the capture site, sex of the bird) did not significantly affect gene expression, but others surprisingly did (e.g. latitude). Our results suggest that these enzymes could be important in range expansions or geographic distribution generally, but more detailed investigations will be insightful.
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- Award ID(s):
- 2027054
- PAR ID:
- 10661060
- Publisher / Repository:
- Journal of Avian Biology
- Date Published:
- Journal Name:
- Journal of Avian Biology
- Volume:
- 2025
- Issue:
- 6
- ISSN:
- 0908-8857
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Synopsis Epigenetic potential, defined as the capacity for epigenetically-mediated phenotypic plasticity, may play an important role during range expansions. During range expansions, populations may encounter relatively novel challenges while experiencing lower genetic diversity. Phenotypic plasticity via epigenetic potential might be selectively advantageous at the time of initial introduction or during spread into new areas, enabling introduced organisms to cope rapidly with novel challenges. Here, we asked whether one form of epigenetic potential (i.e., the abundance of CpG sites) in three microbial surveillance genes: Toll-like receptors (TLRs) 1B (TLR1B), 2A (TLR2A), and 4 (TLR4) varied between native and introduced house sparrows (Passer domesticus). Using an opportunistic approach based on samples collected from sparrow populations around the world, we found that introduced birds had more CpG sites in TLR2A and TLR4, but not TLR1B, than native ones. Introduced birds also lost more CpG sites in TLR1B, gained more CpG sites in TLR2A, and lost fewer CpG sites in TLR4 compared to native birds. These results were not driven by differences in genetic diversity or population genetic structure, and many CpG sites fell within predicted transcription factor binding sites (TFBS), with losses and gains of CpG sites altering predicted TFBS. Although we lacked statistical power to conduct the most rigorous possible analyses, these results suggest that epigenetic potential may play a role in house sparrow range expansions, but additional work will be critical to elucidating how epigenetic potential affects gene expression and hence phenotypic plasticity at the individual, population, and species levels.more » « less
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Synopsis Epigenetic mechanisms are increasingly understood to have major impacts across ecology. However, one molecular epigenetic mechanism, DNA methylation, currently dominates the literature. A second mechanism, histone modification, is likely important to ecologically relevant phenotypes and thus warrants investigation, especially because molecular interplay between methylation and histone acetylation can strongly affect gene expression. There are a limited number of histone acetylation studies on non-model organisms, yet those that exist show that it can impact gene expression and phenotypic plasticity. Wild birds provide an excellent system to investigate histone acetylation, as free-living individuals must rapidly adjust to environmental change. Here, we screen histone acetylation in the house sparrow (Passer domesticus); we studied this species because DNA methylation was important in the spread of this bird globally. This species has one of the broadest geographic distributions in the world, and part of this success is related to the way that it uses methylation to regulate its gene expression. Here, we verify that a commercially available assay that was developed for mammals can be used in house sparrows. We detected high variance in histone acetylation among individuals in both liver and spleen tissue. Further, house sparrows with higher epigenetic potential in the Toll Like Receptor-4 (TLR-4) promoter (i.e., CpG content) had higher histone acetylation in liver. Also, there was a negative correlation between histone acetylation in spleen and TLR-4 expression. In addition to validating a method for measuring histone acetylation in wild songbirds, this study also shows that histone acetylation is related to epigenetic potential and gene expression, adding a new study option for ecological epigenetics.more » « less
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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.more » « less
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vonHoldt, Bridgett (Ed.)Abstract As a highly successful introduced species, house sparrows (Passer domesticus) respond rapidly to their new habitats, generating phenotypic patterns across their introduced range that resemble variation in native regions. Epigenetic mechanisms likely facilitate the success of introduced house sparrows by aiding particular individuals to adjust their phenotypes plastically to novel conditions. Our objective here was to investigate patterns of DNA methylation among populations of house sparrows at a broad geographic scale that included different introduction histories: invading, established, and native. We defined the invading category as the locations with introductions less than 70 years ago and the established category as the locations with greater than 70 years since introduction. We screened DNA methylation among individuals (n = 45) by epiRADseq, expecting that variation in DNA methylation among individuals from invading populations would be higher when compared with individuals from established and native populations. Invading house sparrows had the highest variance in DNA methylation of all three groups, but established house sparrows also had higher variance than native ones. The highest number of differently methylated regions were detected between invading and native populations of house sparrow. Additionally, DNA methylation was negatively correlated to time-since introduction, which further suggests that DNA methylation had a role in the successful colonization’s of house sparrows.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1002/jav.03468
