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 chickadee Poecile 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 blackbird Agelaius phoeniceus in response to the actual calls of the obligate brood parasitic brown-headed cowbird Molothrus ater and the referential anti-parasitic alarm calls of the yellow warbler Setophaga 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.
•Early exposure to salient cues can critically shape the development of social behaviors.•Different acoustic playbacks in ovo alter genome-wide methylation of the auditory forebrain in late-stage ...zebra finch embryos.•Immediate early gene activation is negatively correlated to relative global methylation in the same sample of individuals.•The data support a methylation-mediated embryonic acoustic programming hypothesis for songbird social and communicative behavioral development.
Early exposure to salient cues can critically shape the development of social behaviors. For example, both oscine birds and humans can hear and learn to recognize familiar sounds in ovo and in utero and recognize them following hatching and birth, respectively. Here we demonstrate that different chronic acoustic playbacks alter genome-wide methylation of the auditory forebrain in late-stage zebra finch (Taeniopygia guttata) embryos. Within the same subjects, immediate early gene activation in response to acute con- or heterospecific song exposure is negatively correlated with methylation extent in response to repeated daily prior exposure to the same type of stimuli. Specifically, we report less relative global methylation following playbacks of conspecific songs and more methylation following playbacks of distantly-related heterospecific songs. These findings offer a neuroepigenomic mechanism for the ontogenetic impacts of early acoustic experiences in songbirds.
Communication between parents and dependent offspring is critical not only during provisioning, but also in antipredator contexts. In altricial birds, a top cause of reproductive failure is nest ...predation, and alarm calls both by parents and chicks can serve to alert others and increase the likelihood of offspring escaping predation. Understanding the factors that determine the strength of parental antipredator responses to different nestling alarm calls can provide insight into parent–offspring recognition. The prothonotary warbler (
Protonotaria citrea
), a host of the obligate brood parasite, the brown-headed cowbird (
Molothrus ater
), never rejects cowbird young and raises the parasite together with its own offspring. To determine whether warbler parents learn cowbird nestling alarm calls, we presented experimentally parasitized or non-parasitized parents with playbacks of conspecific warbler, parasitic cowbird, and a harmless heterospecific control, eastern bluebird (
Sialis sialis
), nestling alarm calls. We recorded the latency to respond and the number of chips given by members of the resident warbler pair. We found that parents were most likely to respond to warbler nestling alarm calls, least likely to respond to bluebird calls, with a statistically intermediate likelihood of responding to cowbird calls. Critically, current and past parasitism status did not affect the likelihood of response to any playback or the number of chips given, however, currently parasitized parents had greater response latencies to playbacks than non-parasitized parents. These results suggest that warbler parents do not learn cowbird alarm calls from breeding experiences and, in turn, that cowbirds may employ a generalized, bet-hedging alarm call.
Generalist obligate brood parasites are excellent models for studies of developmental plasticity, as they experience a range of social and environmental variation when raised by one of their many ...hosts. Parasitic Brown-headed Cowbirds (Molothrus ater (Boddaert, 1783)) exhibit host-specific growth rates, yet Cowbird growth rates are not predicted by hosts’ incubation or brooding periods. We tested the novel “growth-tuning” hypothesis which predicts that total asynchrony between Cowbirds’ and hosts’ nesting periods results in faster parasitic growth in nests where host young fledge earlier than Cowbirds. We tested this prediction using previously published and newly added nestling mass data across diverse host species. Total nesting period asynchrony (summed across incubation and brooding stages) predicted Cowbird growth; 8-day-old Cowbirds were heavier in host nests with relatively shorter nesting periods. We further explored the drivers of variation in growth using mass measurements of Cowbirds in Song Sparrow (Melospiza melodia (A. Wilson, 1810)) and Red-winged Blackbird (Agelaius phoeniceus (Linnaeus, 1766)) nests. Our top models included host species (Cowbirds grew faster in Sparrow nests), numbers of nestmates (slowest when raised alone), and sex (males grew faster). These results confirm that multiple social and environmental factors predict directional patterns of developmental plasticity in avian generalist brood parasites.
•Zebra Finches show variability in their directional response to different song types.•fMRI results show subjects respond more to heterospecific songs.•fMRI responses are higher to heterospecific ...songs regardless of familiarity.•All other neural and behavioral metrics show higher responses to conspecific songs.•fMRI results are likely due to GABAergic inhibitory neurons responding to whydah song.
Species recognition is an essential behavioral outcome of social discrimination, flocking, mobbing, mating, and/or parental care. In songbirds, auditory species recognition cues are processed through specialized forebrain circuits dedicated to acoustic discrimination. Here we addressed the direction of behavioral and neural metrics of zebra finches’ (Taeniopygia guttata) responses to acoustic cues of unfamiliar conspecifics vs. heterospecifics. Behaviorally, vocal response rates were greater for conspecific male zebra finch songs over heterospecific Pin-tailed Whydah (Vidua macroura) songs, which paralleled greater multiunit spike rates in the auditory forebrain in response to the same type of conspecific over heterospecific auditory stimuli. In contrast, forebrain activation levels were reversed to species-specific song playbacks during two functional magnetic resonance imaging experiments: we detected consistently greater responses to whydah songs over finch songs and did so independently of whether subjects had been co-housed or not with heterospecifics. These results imply that the directionality of behavioral and neural response selectivity metrics are not always consistent and appear to be experience-independent in this set of stimulus-and-subject experimental paradigms.
All parental hosts of heterospecific brood parasites must pay the cost of rearing non-kin. Previous research on nest parasitism by brown-headed cowbirds (Molothrus ater) concluded that competitive ...superiority of the typically more intensively begging and larger cowbird chick leads to preferential feeding by foster parents and causes a reduction in the hosts' own brood. The larger size of cowbird nestlings can be the result of at least two causes: (1) cowbirds preferentially parasitize species with smaller nestlings and lower growth rates; and/or (2) cowbirds hatch earlier than hosts. I estimated the cost of cowbird parasitism for each of 29 species by calculating the difference between hosts' published brood sizes in nonparasitized and parasitized nests and using clutch size to standardize values. In this analysis, greater incubation length and lower adult mass, surrogate measures of the hatching asynchrony and size difference between parasite and hosts, were both related to greater costs of cowbird parasitism without bias owing to phylogeny. To establish causality, I manipulated clutch contents of eastern phoebes (Sayornis phoebe) and examined whether earlier hatching by a single cowbird or phoebe egg reduces the size of the rest of the original host brood. As predicted, greater hatching asynchrony increased the proportion of the original phoebe brood that was lost. This measure of the cost of parasitism was partially owing to increased hatching failure of the original eggs in asynchronous broods but was not at all related to the size differences of older and younger conspecific nestmates. However, proportional brood loss owing to an earlier hatching conspecific was consistently smaller than brood loss owing to asynchronous cowbirds in both naturally and experimentally parasitized phoebe nests. These results imply that although hatching asynchrony is an important cause of the reduction of host broods in parasitized clutches, competitive features of cowbird nestlings remain necessary to explain the full extent of hosts' reproductive costs caused by interspecific brood parasitism.
•We tested whether brood parasitism activates the HPA axis in adult accepter hosts.•Incubating female hosts showed no increase in baseline CORT when parasitized.•Females showed no CORT increase when ...parasitized with a non-mimetic vs mimetic egg.•Lack of CORT response is consistent with the “evolutionary lag” hypothesis.
Avian obligate brood parasitism, a reproductive strategy where a parasite lays its egg into the nest of another species, imposes significant fitness costs upon host parents and their offspring. To combat brood parasitism, many host species recognize and reject foreign eggs (rejecters), but others are accepters that raise the parasitic progeny. Some accepter hosts may be unable to grasp or pierce parasitic eggs even if they recognize them as foreign eggs in the clutch, whereas other accepters may not have evolved the cognitive skillsets to recognize dissimilar eggs in the nest. Here we assessed the endocrine responses of an accepter host species to model parasitic eggs to address these two alternatives. We experimentally parasitized nests of a locally common host of the brood-parasitic brown-headed cowbird (Molothrus ater), the prothonotary warbler (Protonotaria citrea; a cowbird-egg accepter), with a mimetic or non-mimetic model cowbird-sized egg. Our goal was to determine whether they perceived the non-mimetic egg as a greater stressor by measuring circulating corticosterone levels. We added eggs to nests during the incubation stage and obtained blood plasma samples from females on the nest 2 h later, using females with unmanipulated clutches as controls. Incubating females showed no differences in baseline plasma corticosterone levels between our different treatments. We conclude that exposure to foreign eggs does not activate the hypothalamic–pituitary–adrenal axis of prothonotary warbler hosts in this experimental paradigm.
Transitions between life history stages are fitness-limiting events that depend on environmental and individual characteristics. For altricial birds, fledging from the nest is a critical shift in ...development with direct impacts on survival, yet it remains one of the most understudied components of avian ontogeny. Even less is known about how brood parasitism affects the fledging process in host nestlings. The prothonotary warbler (
Protonotaria citrea
) is a host of the obligate brood parasitic brown-headed cowbird (
Molothrus ater
). We tested whether the presence of parasitic nestlings negatively alters host fledging by experimentally parasitizing nests with a cowbird (heterospecific parasite) or a warbler (conspecific parasite) egg, comparing them to non-manipulated control nests, and monitoring them using radio-frequency identification (RFID) systems. As expected, in heterospecifically parasitized nests, warblers were smaller, fledged at older ages, and had greater overall fledging latency compared to conspecifically parasitized nests. There was no such impact of conspecific parasitism relative to controls. Warbler nestling size predicted the age and order of fledging, with larger nestlings fledging earlier. Nestlings fledging at earlier ages fledged later during daytime hours. Cowbirds and last-fledged, smaller warbler chicks spent the most time in the nest entrance before fledging. Finally, although male warbler nestlings were larger than females, there were no sex effects or effects of extra-pair status on fledging. Our study shows that while conspecific parasitism has no detectable effect on host nestmates, heterospecific parasitism impacts host size and fledging phenology, which may influence post-fledging survival of parasitized broods.
Significance statement
In many species, juveniles undergo dramatic transitions in lifestyle as they age and become independent. For most birds, fledging from the nest is an important developmental shift, potentially impacted by their previous growth and early social experiences. One aspect that may affect fledging is brood parasitism, whereby birds lay their eggs into the nests of other birds who care for the unrelated young. Here, we determined experimentally if brood parasitism affects fledging of the prothonotary warbler, a species that always accepts eggs of the larger, obligate brood parasitic brown-headed cowbird. Our results show that while same-species parasitism has no statistical effect on the fledging of host warblers, cowbird parasitism causes delayed fledging in hosts, revealing a previously unappreciated, additional cost of brood parasitism upon host nestlings.
In most birds and mammals, young are raised in family groups. The phenotypes of nestmates and parents are thus reliable cues for recognition of conspecifics and kin. However, in some species, young ...develop alone, or in broods of mixed relatedness (e.g. because of multiple paternity or maternity), or among heterospecifics or unrelated conspecifics (brood parasites). Under these circumstances, the best referent (model) for discriminating close from distant kin and heterospecifics from conspecifics might be one's own self. This recognition process is known as self-referent phenotype matching. Here we review recent experimental evidence of self-referencing and suggest that behavioral neuroscience can provide new tools and insights into how it works (its proximate mechanistic and ontogenetic bases) and why it exists (its adaptive significance).
Repeatability is a measure of the amount of variation in a phenotype that is attributable to differences between individuals. This concept is important for any study of behaviour, as all traits of ...evolutionary interest must be repeatable in order to respond to selection. We investigated the repeatability of behavioural responses to experimental brood parasitism in American robins, a robust (100%) rejecter of parasitic brown-headed cowbird eggs. Because tests of repeatability require variation between individuals, we parasitized the same robin nests twice successively with model eggs dyed with colours known to elicit rejection at intermediate rates (58-70%). We calculated the repeatability of responses to parasitism, and used a generalized linear mixed model to also test for potentially confounding effects of ordinal date, presentation order, and clutch size. We found that repeatability in response to brood parasitism in this host species is high, and the best model predicting responses to sequential artificial parasitism includes only nest identity. This result is consistent with a critical assumption about egg rejection in this cowbird host as an evolved adaptation in response to brood parasitism.
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