Early life conditions that impact song learning in male zebra finches also impact neural and behavioral responses to song in females

Abstract

Early life stressors can impair song in songbirds by negatively impacting brain development and subsequent learning. Even in species in which only males sing, early life stressors might also impact female behavior and its underlying neural mechanisms, but fewer studies have examined this possibility. We manipulated brood size in zebra finches to simultaneously examine the effects of developmental stress on male song learning and female behavioral and neural response to song. Although adult male HVC volume was unaffected, we found that males from larger broods imitated tutor song less accurately. In females, early condition did not affect the direction of song preference: all females preferred tutor song over unfamiliar song in an operant test. However, treatment did affect the magnitude of behavioral response to song: females from larger broods responded less during song preference trials. This difference in activity level did not reflect boldness per se, as a separate measure of this trait did not differ with brood size. Additionally, in females we found a treatment effect on expression of the immediate early gene ZENK in response to tutor song in brain regions involved in song perception (dNCM) and social motivation (LSc.vl, BSTm, TnA), but not in a region implicated in song memory (CMM). These results are consistent with the hypothesis that developmental stressors that impair song learning in male zebra finches also influence perceptual and/or motivational processes in females. However, our results suggest that the learning of tutor song by females is robust to disturbance by developmental stress. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018.

Early-life social environment predicts social network position in wild zebra finches

“…There is a clear body of evidence linking differences in earlylife developmental conditions to the social behaviour, and resulting social structure [21,28,86,87]. Developmental history could be a key factor underpinning consistent differences in individual behaviour [88][89][90][91][92][93]. For example, differences in brood size during early life can generate effects that are carried over into the following generations [94].…”

The multi-dimensional nature of vocal learning

“…While the overall modulation pattern of model whistles is produced accurately in these copies, multi-dimensional scaling of specific acoustic parameters of copies often result in substantial differences from the whistle that is being copied, suggesting a possible use of such mechanisms to make copies recognizable as such to eavesdroppers [97]. In some species of songbird, the ability to accurately imitate song elements or sequences of song elements may be targets of inter-and intra-sexual selection because it could signal aspects of individual quality and fitness [98][99][100][101], including motivation and/or ability to attend to social cues, use social information and form social bonds [102,103].…”

Meta-analyses reveal support for the Social Intelligence Hypothesis

“…Shultz & Dunbar, 2010; MacLean et al ., 2009; Dunbar & Shultz, 2007; Kverková et al ., 2018; Weisbecker et al ., 2015) and neocortex (Schillaci, 2008; Sandel et al ., 2016) vastly outnumbered studies on other brain regions] prevented us from analysing this relationship at a finer scale than comparing cognitive tests to neuroanatomy. Additionally, given that the SIH is based on the cognitive demands of sociality, it was surprising to see how few studies utilise social tests of cognition such as tactical deception (Byrne & Corp, 2004), theory of mind (Devaine et al ., 2017), social learning (Sewall et al ., 2018; Lefebvre, Palameta & Hatch, 1996) and inequity aversion (Wascher, 2015). Many intraspecific tests of the relationship between sociality and cognition use domain-general tasks, rather than socio-cognitive tasks to measure cognition, despite the explicit prediction that social pressures have driven the evolution of cognition (Dunbar, 1998; Jolly, 1966; Humphrey, 1976; Chance & Mead, 1953).…”