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 (ER α) gene expression are linked to differences in early growth and aggression; thus, maternal hormones may alter gene regulation, perhaps via DNA methylation, of ER α 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 ER α 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 ER α 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 ER α 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.
Highlights
The social environment experienced by females can have formative impacts on her survival and reproductive success, and on that of her offspring
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 estrogen receptor alpha (ERa) DNA methylation in offspring brain tissue to help inform and promote future experimental studies
The patterns we found between yolk testosterone, growth, and percent ERa DNA methylation in the diencephalon were not found in the telencephalon, and it is not clear why only the diencephalon would show these relationships
Summary
The social environment experienced by females can have formative impacts on her survival and reproductive success, and on that of her offspring. Several studies have shown that females breeding in high density and/or increased social interactions allocate more testosterone to their young prenatally (Whittingham and Schwabl 2001; Mazuc et al 2003; Pilz and Smith 2004; Dloniak et al 2006; Hargitai et al 2009; Bentz et al 2013; but see von Engelhardt and Groothuis 2011); these offspring display more-competitive traits like faster postnatal growth during the early phase of rapid mass gain (Schwabl 1996; Eising et al 2001; Pilz et al 2004; Navara et al 2005, 2006a; Cucco et al 2008; Bentz et al 2013; but see Gorman and Williams 2005) and increased aggressive, competitive behaviors
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