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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.

 

Variation in DNA methylation is associated with many ecological and life history traits, including niche breadth and lifespan. In vertebrates, DNA methylation occurs almost exclusively at “CpG” dinucleotides. Yet, how variation in the CpG content of the genome impacts organismal ecology has been largely overlooked. Here, we explore associations between promoter CpG content, lifespan and niche breadth among 60, amniote vertebrate species. The CpG content of 16 functionally relevant gene promoters was strongly, positively associated with lifespan in mammals and reptiles, but was not related to niche breadth. Possibly, by providing more substrate for CpG methylation to occur, high promoter CpG content extends the time taken for deleterious, age-related errors in CpG methylation patterns to accumulate, thereby extending lifespan. The association between CpG content and lifespan was driven by gene promoters with intermediate CpG enrichment—those known to be predisposed to regulation by methylation. Our findings provide novel support for the idea that high CpG content has been selected for in long-lived species to preserve the capacity for gene expression regulation by CpG methylation. Intriguingly, promoter CpG content was also dependent on gene function in our study; immune genes had on average 20% less CpG sites than metabolic- and stress-related genes.

 

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.

 

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. 

This record contains supplementary information for the article "Inheritance of DNA methylation differences in the mangrove Rhizophora mangle" published in Evolution&Development. It contains the barcodes (barcodes.txt), the reference contigs (contigs.fasta.gz), the annotation of the reference contigs (mergedAnnot.csv.gz), the SNPs (snps.vcf.gz), the methylation data (methylation.txt.gz), and the experimental design (design.txt). All data are unfiltered. Short reads are available on SRA (PRJNA746695). Note that demultiplexing of the pooled reads (SRX11452376) will fail because the barcodes are already removed and the header information is lost during SRA submission. Instead, use the pre-demultiplexed reads that are as well linked to PRJNA746695.

 

Table S13 (TableS13_DSSwithGeneAnnotation.offspringFams.csv.gz):

Differential cytosine methylation between families using the mother data set. The first three columns fragment number ("chr"), the position within the fragment ("pos"), and the sequence context ("context"). Columns with the pattern FDR_<X>_vs_<Y> contain false discovery rates of a test comparing population X with population Y. Average DNA methylation levels for each population are given in the columns "AC", "FD", "HI", "UTB", "WB", and "WI". The remaining columns contain the annotation of the fragment, for example whether it matches to a gene and if yes, the gene name ID and description are provided.

 

Here we characterize genetic patterns across the range of House Sparrows in Kenya using six microsatellite markers. We screened House Sparrows from two remote locations in northern Kenya, Marsabit (n = 24) and Wajir (n = 27), which are separated from other colonized areas in Kenya by minimally developed, arid habitat, and then compared these birds with House Sparrows in 10 more central and longer established Kenyan cities (n = 233) in this range. House Sparrows from Marsabit and Wajir originated from a separate source, probably Somalia and/or Ethiopia, from other Kenyan House Sparrows, probably Mombasa. Furthermore, the genetic characteristics of northern and southern populations indicate that they have not yet mixed, supporting a hypothesis that the large, minimally (human) developed, arid landscape spanning nearly all of northern Kenya, including the 100 000 km²Chalbi Desert, is a barrier to dispersal for House Sparrows.