Vocal matching and intensity of begging calls are associated with a forebrain song circuit in a generalist brood parasite

Abstract

Vocalizations produced by developing young early in life have simple acoustic features and are thought to be innate. Complex forms of early vocal learning are less likely to evolve in young altricial songbirds because the forebrain vocal-learning circuit is underdeveloped during the period when early vocalizations are produced. However, selective pressure experienced in early postnatal life may lead to early vocal learning that is likely controlled by a simpler brain circuit. We found the food begging calls produced by fledglings of the brown-headed cowbird (Molothrus ater), a generalist avian brood parasite, induced the expression of several immediate early genes and early circuit innervation in a forebrain vocal-motor pathway that is later used for vocal imitation. The forebrain neural activity was correlated with vocal intensity and variability of begging calls that appears to allow cowbirds to vocally match host nestmates. The begging-induced forebrain circuits we observed in fledgling cowbirds were not detected in nonparasitic passerines, including species that are close relatives to the cowbird. The involvement of forebrain vocal circuits during fledgling begging and its association with vocal learning plasticity may be an adaptation that provides young generalist brood parasites with a flexible signaling strategy to procure food from a wide range of heterospecific host parents.

Innate development of acoustic signals for host parent–offspring recognition in the brood‐parasitic Screaming CowbirdMolothrus rufoaxillaris

“…Such apparent refinement of vocal mimicry in older Screaming Cowbird nestlings had no detectable effects on host responsiveness to playbacks, but we cannot dismiss the possibility that it becomes more important after fledging, when exhibiting Baywing-like acoustic signals seems to be critical to elicit parental care and avoid host discrimination (De M arsico et al 2012). A recent study in the Brown-Headed Cowbird shows that begging calls of parasite fledglings, but not nestlings, consistently match the peak frequency of host's begging calls, suggesting that social experience may shape some vocal modifications that help parasites to procure resources after fledging (Liu et al 2016). Nevertheless, it is worthwhile to note that we have observed Screaming Cowbird young recently fledged from Mockingbird nests being called and escorted by two or more adult Baywings from neighbouring territories (De M arsico & Reboreda 2008).…”

“…This pattern suggests that parasitic nestlings could refine some host-specific acoustic cues during vocal development, for example if host parents reinforce mimetic calls by increasing food provisioning (Langmore et al 2008). A recent study in the Brown-Headed Cowbird shows that begging calls of parasite fledglings, but not nestlings, consistently match the peak frequency of host's begging calls, suggesting that social experience may shape some vocal modifications that help parasites to procure resources after fledging (Liu et al 2016). S3).…”

“…The mechanisms underlying begging call development and the resulting level of vocal plasticity in parasitic nestlings may have evolutionary implications for host-parasite interactions (Liu et al 2016). For instance, the ability to learn and exploit their host's sensory preferences may provide brood parasites with the potential to colonize new hosts successfully (Agrawal 2001, Rold an et al 2013.…”

A neural basis for password-based species recognition in an avian brood parasite

“…We also predict that neural responses to the password will vary across juvenile and adult stages. Such malleability in neural responses has been described in forebrain vocal circuits in brood parasites but not in related parental taxa (Liu et al, 2016). In experiment 2, juvenile cowbirds were either exposed to recent experience or no recent experience with either conspecific or heterospecific songs, which are both learned vocalizations.…”

Vocal imitation of mother's calls by begging Red-backed Fairywren nestlings increases parental provisioning

“…We suggest that if higher element similarity between mother and young is the consequence of superior development during the embryonic stage, then females could use element similarity as a signal to invest in nestlings of higher quality (Haig 1990). Similarly, if females in better condition were able to call more and provision their nestlings at a greater rate, they may also produce offspring that could expend more resources on brain areas associated with vocal learning (e.g., Nowicki et al 2002, Liu et al 2015. This again would lead to greater element similarity and could serve as a signal for mothers to invest in higher-quality offspring.…”