skip to main content


Title: Functional neurogenomic responses to acoustic threats, including a heterospecific referential alarm call and its referent, in the auditory forebrain of red-winged blackbirds
Abstract

In animal communication, functionally referential alarm calls elicit the same behavioral responses as their referents, despite their typically distinct bioacoustic traits. Yet the auditory forebrain in at least one songbird species, the black-capped chickadeePoecile atricapillus, responds similarly to threat calls and their referent predatory owl calls, as assessed by immediate early gene responses in the secondary auditory forebrain nuclei. Whether and where in the brain such perceptual and cognitive equivalence is processed remains to be understood in most other avian systems. Here, we studied the functional neurogenomic (non-) equivalence of acoustic threat stimuli perception by the red-winged blackbirdAgelaius phoeniceusin response to the actual calls of the obligate brood parasitic brown-headed cowbirdMolothrus aterand the referential anti-parasitic alarm calls of the yellow warblerSetophaga petechia,upon which the blackbird is known to eavesdrop. Using RNA-sequencing from neural tissue in the auditory lobule (primary and secondary auditory nuclei combined), in contrast to previous findings, we found significant differences in the gene expression profiles of both an immediate early gene, ZENK (egr-1), and other song-system relevant gene-products in blackbirds responding to cowbird vs. warbler calls. In turn, direct cues of threats (including conspecific intruder calls and nest-predator calls) elicited higher ZENK and other differential gene expression patterns compared to harmless heterospecific calls. These patterns are consistent with a perceptual non-equivalence in the auditory forebrain of adult male red-winged blackbirds in response to referential calls and the calls of their referents.

 
more » « less
Award ID(s):
2417581
NSF-PAR ID:
10487594
Author(s) / Creator(s):
; ; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Scientific Reports
Volume:
14
Issue:
1
ISSN:
2045-2322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Referential alarm calls that denote specific types of dangers are common across diverse vertebrate lineages. Different alarm calls can indicate a variety of threats, which often require specific actions to evade. Thus, to benefit from the call, listeners of referential alarm calls must be able to decode the signaled threat and respond to it in an appropriate manner. Yellow warblers ( Setophaga petechia ) produce referential “seet” calls that signal to conspecifics the presence of nearby obligate brood parasitic brown-headed cowbirds ( Molothrus ater ), which lay their eggs in the nests of other species, including yellow warblers. Our previous playback experiments have found that red-winged blackbirds ( Agelaius phoeniceus ), a species also parasitized by brown-headed cowbirds, eavesdrop upon and respond strongly to yellow warbler seet calls during the incubation stage of breeding with aggression similar to responses to both cowbird chatters and predator calls. To assess whether red-winged blackbird responses to seet calls vary with their own risk of brood parasitism, we presented the same playbacks during the nestling stage of breeding (when the risk of brood parasitism is lower than during incubation). As predicted, we found that blackbirds mediated their aggression toward both cowbird chatter calls and the warblers’ anti-parasitic referential alarm calls in parallel with the low current risk of brood parasitism during the nestling stage. These results further support that red-winged blackbirds flexibly respond to yellow warbler antiparasitic referential calls as a frontline defense against brood parasitism at their own nests. 
    more » « less
  2. Many avian species are negatively impacted by obligate avian brood parasites, which lay their eggs in the nests of host species. The yellow warbler (Setophaga petechia), which is host to the brood-parasitic brown-headed cowbird (Molothrus ater), represents one of the best-replicated study systems assessing antiparasitic host defenses. Over 15 prior studies on yellow warblers have used model-presentation experiments, whereby breeding hosts are exposed to models of brown-headed cowbirds or other nest threats, to test for anti-parasitic defenses unique to this species. Here we present results from our own quasi-replication study of the yellow warbler/brown-headed cowbird system, which used a novel design compared to previous experiments by pivoting to conduct acoustic playback treatments only, rather than presenting visual models with or without calls. We exposed active yellow warbler nests to playbacks of brown-headed cowbird chatters (brood parasite), blue jay (Cyanocitta cristata; nest predator) calls, conspecific “seet” calls (a referential alarm call for brood parasitism risk), conspecific “chip” calls (a generic alarm call), or control wood thrush (Hylocichla mustelina; harmless heterospecific) songs during the incubation stage. Similar to previous studies, we found that female yellow warblers seet called more frequently in response to playbacks of both brood parasitic chatter calls and conspecific seet calls whereas they produced more chip calls in response to the playback of nest predator calls. In contrast, female yellow warblers approached all playbacks to similar distances, which was different from the proximity patterns seen in previous studies. Our study demonstrates the importance of both replicating, and also pivoting, experimental studies on nest defense behaviors, as differences in experimental design can elicit novel behavioral response patterns in the same species. 
    more » « less
  3. Abstract

    Defending offspring incurs temporal and energetic costs and can be dangerous for the parents. Accordingly, the intensity of this costly behavior should reflect the perceived risk to the reproductive output. When facing costly brood parasitism by brown‐headed cowbirds (Molothrus ater), where cowbirds lay eggs in heterospecific nests and cause the hosts to care for their young, yellow warblers (Setophaga petechia) use referential “seet” calls to warn their mates of the parasitic danger. Yellow warblers of both sexes produce this call only in response to cowbirds or seet‐calling conspecifics. Seet calls are mainly produced during the laying and incubation stages of breeding, when risk of brood parasitism is highest, rather than during the nestling stage. On the other hand, general alarm calls (chips) are produced throughout the nesting cycle and are also used in conspecific interactions unrelated to nesting. We hypothesized that context shapes responses prior to breeding as well, such that yellow warblers without a mate and active nest would be less likely to respond to playbacks that simulate brood parasitism risk. To test this hypothesis, we presented playbacks of two nest threats, cowbirds (brood parasite) and blue jays (Cyanocitta cristata; nest predator), on territories of unmated male warblers (unpaired) and male warblers with a known mate (paired). We found that unpaired males were unresponsive toward playbacks indicating nest threats, whereas paired males were significantly more aggressive and vocal toward these playbacks compared to control playbacks. However, both paired and unpaired males were vocally responsive toward chip calls, which are informative for males regardless of pairing status. Male yellow warblers appear to adjust their responses during the earliest stages of breeding depending on the contextual relevance of specific threat stimuli, and together with prior studies, our work further supports that referential seet calls are associated with stage‐specific risk of brood parasitism.

     
    more » « less
  4. Abstract

    The recognition of and differential responses to salient stimuli are among the main drivers of behavioral plasticity, yet, how animals evolve and modulate functional responses to novel classes of antagonistic stimuli remain poorly understood. We studied free-living male red-winged blackbirds (Agelaius phoeniceus) to test whether gene expression responses in blood are distinct or shared between patterns of aggressive behavioral responses directed at simulated conspecific versus heterospecific intruders. In this species, males defend territories against conspecific males and respond aggressively to female brown-headed cowbirds (Molothrus ater), a brood parasite that commonly lays eggs in blackbird nests. Both conspecific songs and parasitic calls elicited aggressive responses from focal subjects and caused a downregulation in genes associated with immune system response, relative to control calls of a second, harmless heterospecific species. In turn, only the conspecific song treatment elicited an increase in singing behavior and an upregulation of genes associated with metabolic processes relative to the two heterospecific calls. Our results suggest that aspects of antagonistic behaviors to both conspecifics and brood parasites can be mediated by similar physiological responses, suggestive of shared molecular and behavioral pathways involved in the recognition and reaction to both evolutionarily old and new enemies.

     
    more » « less
  5. Sensory responses to courtship signals can be altered by reproductive hormones. In seasonally‐breeding female songbirds, for example, sound‐induced immediate early gene expression in the auditory pathway is selective for male song over behaviourally irrelevant sounds only when plasma oestradiol reaches breeding‐like levels. This selectivity has been hypothesised to be mediated by the release of monoaminergic neuromodulators in the auditory pathway. We previously showed that in oestrogen‐primed female white‐throated sparrows, exposure to male song induced dopamine and serotonin release in auditory regions. To mediate hormone‐dependent selectivity, this release must be (i) selective for song and (ii) modulated by endocrine state. Therefore, in the present study, we addressed both questions by conducting playbacks of song or a control sound to females in a breeding‐like or a nonbreeding endocrine state. We then used high‐performance liquid chromatography to measure turnover of dopamine, norepinephrine and serotonin in the auditory midbrain and forebrain. We found that sound‐induced turnover of dopamine and serotonin depended on endocrine state; hearing sound increased turnover in the auditory forebrain only in the birds in a breeding‐like endocrine state. Contrary to our expectations, these increases occurred in response to either song or artificial tones; in other words, they were not selective for song. The selectivity of sound‐induced monoamine release was thus strikingly different from that of immediate early gene responses described in previous studies. We did, however, find that constitutive monoamine release was altered by endocrine state; irrespective of whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding‐like state than in a nonbreeding endocrine state. The results of the present study suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated.

     
    more » « less