Long-term effects of prenatal sound experience on songbird behavior and their relation to song learning

Abstract

Across multiple taxa, prenatal exposure to rhythmic sound can promote neural development and alter postnatal behavior. In recent studies using zebra finches, stimulating embryos with parental “heat calls” affected their begging behavior as nestlings and song learning as adults. This song learning effect is potentially mediated by broader changes to offspring behavior that affect how they interact with potential song tutors; however, the long-term behavioral effects of prenatal sound are still poorly understood. In this study, therefore, we used captive wild-derived zebra finches to experimentally test (1) whether prenatal sound experience affected long-term behavioral traits and (2) whether these traits were correlated with song learning outcomes. Offspring that had experienced heat calls (treatment) or contact calls (control) in the egg were raised after hatching in a colony environment. We then used four assays to quantify different aspects of their adult behavior, including food neophobia, detour reaching, and exploration in a novel environment. Treatment offspring were less food neophobic (quicker to eat a novel food item), adding to increasing evidence that prenatal sound can affect long-term behavior. However, levels of food neophobia did not, in turn, predict song learning. Differences in offspring song learning may instead be explained by exploration behavior, as fast-exploring males produced more syllables from non-paternal tutors. While our findings do not support the hypothesis that behavior mediates the effects of prenatal sound on song learning, they nevertheless bring us closer to understanding the behavioral mechanisms through which prenatal sound might affect postnatal outcomes. Sounds experienced inside the egg can influence an individual’s behavior after hatching. In the zebra finch, exposing embryos to a parental “heat call” altered their song learning later in life, but the mechanism driving this effect is unknown. In this study, we tested whether prenatal playback of heat calls affected a suite of adult behavioral traits and whether any of these traits were associated with song learning. Exposure to heat calls produced adult zebra finches that were less neophobic towards a novel food item, but this trait was not itself correlated with song learning. Overall, these findings highlight the importance of the prenatal sound environment for shaping future offspring behavior, which may in turn have unappreciated fitness consequences.