Species-Specific Auditory Forebrain Responses to Non-Learned Vocalizations in Juvenile Blackbirds

Abstract

Species recognition mediates the association of individuals with conspecifics. Learned cues often facilitate species recognition via early social experience with parents and siblings. Yet, in some songbirds, the production of species-typical vocalizations develops in the absence of early social experiences. Here, we investigate the auditory-evoked neural responses of juvenile red-winged blackbirds (Agelaius phoeniceus), a nonparasitic (parental) species within the Icterid family and contrast these results with a closely related Icterid parasitic species that lacks parental care, the brown-headed cowbird (Molothrus ater). We demonstrate that immediate early gene (IEG) activity in the caudomedial mesopallium (CMM) is selectively evoked in response to conspecific non-learned vocalizations in comparison to 2 types of heterospecific non-learned vocalizations, independent of the acoustic similarity patterns between the playback stimuli. This pattern, however, was not detected in the caudomedial nidopallium (NCM). Because the red-winged blackbird is a parental species, the conspecific non-learned vocalization is presumably a familiar sound to the juvenile red-winged blackbird, whereas the heterospecific non-learned vocalizations are novel. We contrast results reported here with our recent demonstration of selective IEG induction in response to non-learned conspecific vocalizations in juvenile parasitic brown-headed cowbirds, in which conspecific non-learned vocalizations are presumably novel. In this case, selective IEG induction from conspecific non-learned vocalization occurred within NCM but not within CMM. By comparing closely related species with stark differences in the early exposure to conspecifics, we demonstrate that CMM and NCM respond to familiar vs. novel non-learned vocalizations in a manner that parallel previously reported regional responses to learned vocalizations such as conspecific songs.

Neural mechanisms of auditory species recognition in birds

“…Taken together, these results support a model of neural activation to represent stimulus‐dependent neural selectivity of specific content of the playback types (e.g. conspecific versus heterospecific), rather than the acoustic contrasts between stimulus sounds (Lynch et al , ).…”

“…Thus, neural response selectivity could depend purely on the acoustic dis/similarities between conspecific and heterospecific sounds used as stimuli (Mendelson et al, 2016). However, IEG activation in red-winged blackbirds (Agelaius phoeniceus) did not reflect acoustic similarities between the call used as the conspecific stimulus versus heterospecific stimulus calls of two different species (Lynch, Louder, & Hauber, 2018). Similarly, Hauber et al (2013) found the neural firing rates of zebra finches responded at similarly lower levels to the heterospecific songs of Bengalese finch (Lonchura striata domestica) and Parson's finch (Poephila cincta) versus conspecific songs, and Poirier et al (2009) found greater neural responses in zebra finches upon hearing conspecific songs versus multiple exemplars of canary (Serinus canaria domestica) and European starling (Sturnus vulgaris) songs, despite the contrasting acoustic structures of each set of heterospecific stimuli.…”

“…Accordingly, young males of the brood‐parasitic brown‐headed cowbird ( Molothrus ater ), a species that lacks parental care and relies on a foster species to raise their offspring, exhibited increased ZENK induction within the CMM following exposure to familiar songs, regardless of whether the recently exposed song was conspecific or heterospecific (Lynch et al , ). In the brains of immature male red‐winged blackbirds, a non‐parasitic parental species closely related to cowbirds, playbacks also evoke conspecific selectivity for familiar non‐learned female chatter calls in the CMM but not in the NCM (Lynch et al , ). By contrast, young male cowbirds showed conspecific‐selective ZENK expression within the NCM, but not the CMM, for a conspecific female non‐learned call, the chatter (Lynch et al , ), suggesting that the chatter call is a species‐specific password to cue species recognition in juvenile brood parasites (Hauber, Russo, & Sherman, ).…”

“…Mello et al, 1992;Hernandez & MacDougall-Shackleton, 2004;Farrell et al, 2015), suggestive of parallel neural substrates for the representation of species-typical sounds. However, the two regions may have functional differences for the various types of auditory signals encountered by an individual based on context, including sex (Bolhuis & Gahr, 2006) and prior experience (Lynch et al, 2017(Lynch et al, , 2018. Accordingly, young males of the brood-parasitic brown-headed cowbird (Molothrus ater), a species that lacks parental care and relies on a foster species to raise their offspring, exhibited increased ZENK induction within the CMM following exposure to familiar songs, regardless of whether the recently exposed song was conspecific or heterospecific (Lynch et al, 2017).…”

Shared transcriptional responses to con- and heterospecific behavioral antagonists in a wild songbird

“…What constitutes the physiological basis of anti-parasite responses remains largely unknown in avian host-parasite systems 10 . For example, recent work in wild-caught juvenile male red-winged blackbirds (Agelaius phoeniceus; hereafter: redwings) found no differences in immediate early gene (IEG) expression levels within the auditory forebrain in response to the calls of adult female brood parasites (brown-headed cowbirds Molothrus ater; hereafter: cowbirds) versus a harmless control species (mourning dove Zenaida macroura; hereafter: doves), whereas responses were stronger to conspecific adult female calls 11 . In the wild, however, juvenile redwings do not hold territories and may not (yet) have been exposed to parasitism by cowbirds.…”