Abstract
BackgroundMaternal hormones, like testosterone, can strongly influence developing offspring, even generating long-term organizational effects on adult behavior; yet, the mechanisms facilitating these effects are still unclear. Here, we experimentally elevated prenatal testosterone in the eggs of zebra finches (Taeniopygia guttata) and measured male aggression in adulthood along with patterns of neural gene expression (RNA-seq) and DNA methylation (MethylC-Seq) in two socially relevant brain regions (hypothalamus and nucleus taenia of the amygdala). We used enrichment analyses and protein-protein interaction networks to find candidate processes and hub genes potentially affected by the treatment. We additionally identified differentially expressed genes that contained differentially methylated regions.ResultsWe found that males from testosterone-injected eggs displayed more aggressive behaviors compared to males from control eggs. Hundreds of genes were differentially expressed, particularly in the hypothalamus, including potential aggression-related hub genes (e.g., brain derived neurotrophic factor). There were also enriched processes with well-established links to aggressive phenotypes (e.g., somatostatin and glutamate signaling). Furthermore, several highly connected genes identified in protein-protein interaction networks also showed differential methylation, including adenylate cyclase 2 and proprotein convertase 2.ConclusionsThese results highlight genes and processes that may play an important role in mediating the effects of prenatal testosterone on long-term phenotypic outcomes, thereby providing insights into the molecular mechanisms that facilitate hormone-mediated maternal effects.
Highlights
Maternal hormones, like testosterone, can strongly influence developing offspring, even generating long-term organizational effects on adult behavior; yet, the mechanisms facilitating these effects are still unclear
Aggression was assayed in 15 min same-sex conspecific intrusion trials in adult males, during which the number of aggressive actions performed by the subject toward the intruder were recorded
Repeatability of aggression was significant across the two behavioral trials (R = 0.64 ± 0.18 SE; p = 0.005), suggesting individuals were moderately consistent in the way they responded to conspecific intruders
Summary
Like testosterone, can strongly influence developing offspring, even generating long-term organizational effects on adult behavior; yet, the mechanisms facilitating these effects are still unclear. Methylation patterns are established in early development and may be one way for hormone-induced changes to last into adulthood. Examples of this are evident in the methylation patterns produced by steroid-mediated sex differentiation in mammals [17] and fetal exposure to endocrine disrupters [18]. Candidate-gene analyses suggest that variation in the maternal environment can result in altered DNA methylation patterns in juvenile birds [19, 20]. The proposed mechanism, starting with prenatal T and leading to long-term phenotypic changes in adults, along with the potential intervening transcriptomic/epigenomic steps, has yet to be tested
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