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Relationship between maternal environment and DNA methylation patterns of estrogen receptor alpha in wild Eastern Bluebird ( Sialia sialis ) nestlings: a pilot study

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ABSTRACT

There is mounting evidence that, across taxa, females breeding in competitive environments tend to allocate more testosterone to their offspring prenatally and these offspring typically have more aggressive and faster‐growing phenotypes. To date, no study has determined the mechanisms mediating this maternal effect's influence on offspring phenotype. However, levels of estrogen receptor alpha (ERα) gene expression are linked to differences in early growth and aggression; thus, maternal hormones may alter gene regulation, perhaps via DNA methylation, of ERα in offspring during prenatal development. We performed a pilot study to examine natural variation in testosterone allocation to offspring through egg yolks in wild Eastern Bluebirds (Sialia sialis) in varying breeding densities and percent DNA methylation of CG dinucleotides in the ERα promoter in offspring brain regions associated with growth and behavior. We hypothesized that breeding density would be positively correlated with yolk testosterone, and prenatal exposure to maternal‐derived yolk testosterone would be associated with greater offspring growth and decreased ERα promoter methylation. Yolk testosterone concentration was positively correlated with breeding density, nestling growth rate, and percent DNA methylation of one out of five investigated CpG sites (site 3) in the diencephalon ERα promoter, but none in the telencephalon (n = 10). Percent DNA methylation of diencephalon CpG site 3 was positively correlated with growth rate. These data suggest a possible role for epigenetics in mediating the effects of the maternal environment on offspring phenotype. Experimentally examining this mechanism with a larger sample size in future studies may help elucidate a prominent way in which animals respond to their environment. Further, by determining the mechanisms that mediate maternal effects, we can begin to understand the potential for the heritability of these mechanisms and the impact that maternal effects are capable of producing at an evolutionary scale.

No MeSH data available.


Picture of (A) male and (B) female Eastern Bluebirds, Sialia sialis (photo courtesy of Geoffrey E. Hill).
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ece32162-fig-0001: Picture of (A) male and (B) female Eastern Bluebirds, Sialia sialis (photo courtesy of Geoffrey E. Hill).

Mentions: In the present pilot study, we investigated relationships between natural variation in the competitive environment experienced by Eastern Bluebirds (Sialia sialis; Fig. 1) and their yolk testosterone allocation, offspring growth, and ERα DNA methylation in offspring brain tissue to help inform and promote future experimental studies. Eastern Bluebirds are obligate secondary cavity nesters and are limited by available cavities, causing intense competition for cavities in high breeding densities (Pinkowski 1976; Parren 1991; Gowaty and Plissner 1998). Because yolk testosterone concentrations have been linked to competitive environment and influence offspring growth rates and aggression in other species (von Engelhardt and Groothuis 2011), we hypothesized that (1) higher breeding densities would be positively correlated with testosterone allocation to egg yolks and (2) that exposure to high yolk testosterone concentrations would be related to faster growth rates in Eastern Bluebirds. Further, because previous work cited above indicates that testosterone may affect offspring phenotype via aromatization to estrogen, we further hypothesized that (3) higher yolk testosterone concentrations would be associated with decreased ERα DNA methylation in the diencephalon and posterior telencephalon in offspring and (4) patterns of ERα DNA methylation would negatively correlate with offspring growth rates.


Relationship between maternal environment and DNA methylation patterns of estrogen receptor alpha in wild Eastern Bluebird ( Sialia sialis ) nestlings: a pilot study
Picture of (A) male and (B) female Eastern Bluebirds, Sialia sialis (photo courtesy of Geoffrey E. Hill).
© Copyright Policy - creativeCommonsBy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4979703&req=5

ece32162-fig-0001: Picture of (A) male and (B) female Eastern Bluebirds, Sialia sialis (photo courtesy of Geoffrey E. Hill).
Mentions: In the present pilot study, we investigated relationships between natural variation in the competitive environment experienced by Eastern Bluebirds (Sialia sialis; Fig. 1) and their yolk testosterone allocation, offspring growth, and ERα DNA methylation in offspring brain tissue to help inform and promote future experimental studies. Eastern Bluebirds are obligate secondary cavity nesters and are limited by available cavities, causing intense competition for cavities in high breeding densities (Pinkowski 1976; Parren 1991; Gowaty and Plissner 1998). Because yolk testosterone concentrations have been linked to competitive environment and influence offspring growth rates and aggression in other species (von Engelhardt and Groothuis 2011), we hypothesized that (1) higher breeding densities would be positively correlated with testosterone allocation to egg yolks and (2) that exposure to high yolk testosterone concentrations would be related to faster growth rates in Eastern Bluebirds. Further, because previous work cited above indicates that testosterone may affect offspring phenotype via aromatization to estrogen, we further hypothesized that (3) higher yolk testosterone concentrations would be associated with decreased ERα DNA methylation in the diencephalon and posterior telencephalon in offspring and (4) patterns of ERα DNA methylation would negatively correlate with offspring growth rates.

View Article: PubMed Central - PubMed

ABSTRACT

There is mounting evidence that, across taxa, females breeding in competitive environments tend to allocate more testosterone to their offspring prenatally and these offspring typically have more aggressive and faster‐growing phenotypes. To date, no study has determined the mechanisms mediating this maternal effect's influence on offspring phenotype. However, levels of estrogen receptor alpha (ERα) gene expression are linked to differences in early growth and aggression; thus, maternal hormones may alter gene regulation, perhaps via DNA methylation, of ERα in offspring during prenatal development. We performed a pilot study to examine natural variation in testosterone allocation to offspring through egg yolks in wild Eastern Bluebirds (Sialia sialis) in varying breeding densities and percent DNA methylation of CG dinucleotides in the ERα promoter in offspring brain regions associated with growth and behavior. We hypothesized that breeding density would be positively correlated with yolk testosterone, and prenatal exposure to maternal‐derived yolk testosterone would be associated with greater offspring growth and decreased ERα promoter methylation. Yolk testosterone concentration was positively correlated with breeding density, nestling growth rate, and percent DNA methylation of one out of five investigated CpG sites (site 3) in the diencephalon ERα promoter, but none in the telencephalon (n = 10). Percent DNA methylation of diencephalon CpG site 3 was positively correlated with growth rate. These data suggest a possible role for epigenetics in mediating the effects of the maternal environment on offspring phenotype. Experimentally examining this mechanism with a larger sample size in future studies may help elucidate a prominent way in which animals respond to their environment. Further, by determining the mechanisms that mediate maternal effects, we can begin to understand the potential for the heritability of these mechanisms and the impact that maternal effects are capable of producing at an evolutionary scale.

No MeSH data available.