Urban and rural male song sparrows (Melospiza melodia) differ in territorial aggression and activation of vasotocin neurons in response to song challenge.

When living in urban habitats, 'urban adapter' species often show greater aggression toward conspecifics, yet we do not understand the mechanisms underlying this behavioral shift. The neuroendocrine system regulates socio-sexual behaviors including aggression and thus could mediate behavioral responses to urbanization. Indeed, urban male song sparrows (Melospiza melodia), which are more territorially aggressive, also have greater abundance of the neuropeptide arginine vasotocin (AVT) in nodes of the brain social behavior network. Higher abundance of AVT could reflect long-term synthesis that underlies baseline territoriality or short-term changes that regulate aggression in response to social challenge. To begin to resolve the timeframe over which the AVT system contributes to habitat differences in aggression we used immediate early gene co-expression as a measure of the activation of AVT neurons. We compared Fos induction in AVT-immunoreactive neurons of the bed nucleus of the stria terminalis (BSTm) and paraventricular nucleus of the hypothalamus (PVN) between urban and rural male song sparrows in response to a short (< 5 min.) or long (> 30 min.) song playback to simulate territorial intrusion by another male. We found that urban males had a higher proportion of Fos-positive AVT neurons in both brain regions compared to rural males, regardless of the duration of song playback. Our results suggest that AVT neurons remain activated in urban males, independently of the duration of social challenge. These findings that Fos induction in AVT neurons differs between rural and urban male song sparrows further implicate this system in regulating behavioral responses to urbanization.

Migratory state and patterns of steroid hormone regulation in the pectoralis muscle of a nomadic migrant, the pine siskin (Spinus pinus).

The endocrine system is known to mediate responses to environmental change and transitions between different life stages (e.g., a non-breeding to a breeding life stage). Previous works from the field of environmental endocrinology have primarily focused on changes in circulating hormones, but a comprehensive understanding of endocrine signaling pathways requires studying changes in additional endocrine components (e.g., receptor densities) in a diversity of contexts and life stages. Migratory birds, for instance, can exhibit dramatic changes in their physiology and behavior, and both sex steroids as well as glucocorticoids are proposed mediators of the transition into a migratory state. However, the role of changes in endocrine signaling components within integral target tissues, such as flight muscles, in modulating the transition into a migratory state remains poorly understood. Here, we examined changes in gene expression levels of and correlational patterns (i.e., integration) between 8 endocrine signaling components associated with either glucocorticoids or sex steroid signaling in the pectoralis muscles of a nomadic migratory bird, the pine siskin (Spinus pinus). The pectoralis muscle is essential to migratory flight and undergoes conspicuous changes in preparation for migration, including hypertrophy. We focus on endocrine receptors and enzymes (e.g., 5α-reductase) that modulate the signaling capacity of circulating hormones within target tissues and may influence either catabolic or anabolic functioning within the pectoralis. Endocrine signaling components were compared between captive birds sampled prior to the expression of vernal migratory preparation and during the expression of a vernal migratory state. While birds exhibited differences in the size and color of the flight muscle and behavioral shifts indicative of a migratory state (i.e., zugunruhe), none of the measured endocrine components differed before and after the transition into the migratory state. Patterns of integration amongst all genes did, however, differ between the two life stages, suggesting the contrasting demands of different life stages may shape entire endocrine signaling networks within target tissues rather than individual components. Our work aligns with previous endocrine studies on pine siskins and, viewed together, suggest additional studies are needed to understand the endocrine system's role in mediating the development and progression of the vernal migratory state in this species. Further, the patterns observed in pine siskins, a nomadic migrant, differ from previous studies on obligate migrants and suggest that different mechanisms or interactions between endocrine signaling components may mediate the migratory transition in nomadic migrants.

Hypothalamic-pituitary-adrenal axis regulation and organization in urban and rural song sparrows.

Urban habitats present animals with persistent disturbances and acute stressors not present in rural habitats or present at significantly lower levels. Differences in the glucocorticoid stress response could underlie colonization of these novel habitats. Despite urban habitats characterization as more stressful, previous comparisons of urban and rural birds have failed to find consistent differences in baseline and stress induced glucocorticoid levels. Another aspect of glucocorticoid regulation that could underlie an animal's ability to inhabit novel habitats, but has yet to be well examined, is more efficient termination of the glucocorticoid stress response which would allow birds in urban habitats to recover more quickly after a disturbance. The glucocorticoid stress response is terminated by negative feedback achieved primarily through their binding of receptors in the hippocampus and hypothalamus and subsequent decreased synthesis and release from the adrenals. We investigated if male song sparrows (Melospiza melodia) in urban habitats show more efficient termination of the glucocorticoid stress response than their rural counterparts using two approaches. First, we measured glucocorticoid receptor, mineralocorticoid receptor and 11ß-HSD2 (an enzyme that inactivates corticosterone) mRNA expression in negative feedback targets of the brain (the hippocampus and hypothalamus) as a proxy measure of sensitivity to negative feedback. Second, we measured plasma corticosterone levels after standardized restraint and again following a challenge with the synthetic glucocorticoid, dexamethasone, as a means of assessing how quickly birds decreased glucocorticoid synthesis and release. Though there were no differences in the hypothalamus of urban and rural song sparrows, urban birds had lower glucocorticoid receptor and 11ß-HSD2 mRNA expression in the hippocampus. Further, urban and rural birds had similar reductions in corticosterone following the dexamethasone challenge, suggesting that they do not differ in how quickly they decrease glucocorticoid synthesis and release. Thus, urban and rural song sparrows display similar termination of the glucocorticoid stress response even though urban birds have decreased hippocampal glucocorticoid receptor and 11ß-HSD2 abundance.

Male zebra finches exposed to lead (Pb) during development have reduced volume of song nuclei, altered sexual traits, and received less attention from females as adults.

Lead (Pb) is a pervasive global contaminant that interferes with sensitive windows for neurological development and causes oxidative damage to tissues. The effects of moderate and high exposure to Pb have been well-studied in birds, but whether low-level early-life exposure to Pb influences adult phenotype remains unclear. Female songbirds use a male's song and coloration to discriminate between high- and low-quality males. Therefore, if early-life exposure to Pb disrupts song learning ability or shifts the allocation of antioxidant pigments away from colorful secondary sexual traits, male birds exposed to Pb may be less attractive to females. We exposed developing zebra finches (Taeniopygia guttata) to Pb-contaminated drinking water (100 or 1000 parts per billion [ppb]) after hatching (days 0-100). Once male finches reached adulthood (120-150 days post hatch), we measured song learning ability, coloration of bill and cheek patches, and volume of song nuclei in the brain. We also measured female preference for Pb-exposed males relative to control males. Finally, we measured motoric and spatial cognitive performance in male and female finches to assess whether cognitive traits differed in their sensitivity to Pb exposure. Male zebra finches exposed to 1000 ppb Pb had impaired song learning ability, reduced volume of song nuclei, bills with less redness and received less attention from females. Additionally, Pb exposure impaired motoric performance in both male and female finches but did not affect performance in a spatial cognitive task. Adult finches exposed to Pb-contaminated water had higher blood-Pb levels, though in all cases blood-Pb levels were below 7.0 µg dL-1. This study suggests that low-level exposure to Pb contributes to cognitive deficits that persist into adulthood and may indirectly influence fitness by altering secondary sexual traits and reducing male attractiveness.

Questioning the developmental effects of group size on cognitive abilities.

Australian magpies living in larger social groups learned quicker and made fewer errors across four cognitive tasks compared with birds living in smaller social groups, and this pattern may be driven by a developmental effect associated with the cognitive demands of living in larger groups. While Smulders (2018, Learning and Behavior, 1-2, doi:10.3758/s13420-018-0335-0) questioned whether this group size-cognitive performance pattern was driven by motivation rather than cognitive abilities, we question whether there is truly evidence of a developmental effect and whether the relationship between group size and cognitive performance can be explained in other ways. We highlight potential alternative explanations for the relationship between group size and cognitive performance and highlight some of the theoretical issues underlying the developmental effects of group size on cognitive abilities.

Territorial aggression in urban and rural Song Sparrows is correlated with corticosterone, but not testosterone.

Urban songbirds of several species more vigorously defend their territories in response to conspecific song playback than do their rural counterparts, but the hormonal basis of this behavioral difference is unclear. It is well established in vertebrates that both testosterone and corticosterone affect the intensity of territoriality. Previous studies have found no evidence that initial (i.e., immediately following territorial challenge, but prior to restraint) plasma testosterone accounts for the elevated territorial aggression of urban birds. Determining if testosterone still contributes to urban-rural differences in territoriality requires also assessing males' abilities to transiently increase plasma testosterone (in response to an injection of gonadotropin-releasing hormone). We tested whether these hormones are correlated with the territorial response to conspecific song playback in urban and rural male Song Sparrows (Melospiza melodia) in Montgomery County, Virginia. We found that the elevated territorial aggression of urban sparrows was not related to variation in either initial plasma testosterone or the ability to transiently increase testosterone. In contrast, despite no overall habitat difference in initial corticosterone, levels of this hormone were positively correlated with territoriality in urban and rural sparrows. Furthermore, for a given level of corticosterone, urban sparrows were more territorially aggressive. Our findings suggest that initial corticosterone may either play a role in the regulation of persistent differences in territorial behavior between free-ranging urban and rural male Song Sparrows or be affected by the intensity of behavioral response to territorial challenge.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Agonistic urban birds: elevated territorial aggression of urban song sparrows is consistent within a breeding period.

Urban birds often more vigorously defend their territories during simulated intrusions than do their rural counterparts, but the factors responsible remain unclear. To address this issue, we investigated whether the disparity in territorial aggression of urban and rural male song sparrows, Melospiza melodia, is individually consistent within a breeding period. Additionally, to better understand the physiological and ecological factors underlying this behavioural difference, we examined whether territoriality was associated with plasma testosterone, a hormone that contributes to elevated aggression in vertebrates, and/or conspecific density, a factor often positively related to aggression. The urbanization-related difference in territoriality was individually consistent within a breeding period. However, the elevated territorial aggression of urban birds was not associated with plasma testosterone and, counter to our predictions, conspecific density was lower in urban compared with rural areas. We suggest that other aspects of testosterone signalling and features of the socio-ecological environment, such as the availability of breeding sites, may underlie increased territorial aggression in urban birds.

Beeswax corticosterone implants produce long-term elevation of plasma corticosterone and influence condition.

Glucocorticoids can play a critical role in modulating life-history trade-offs. However, studying the effects of glucocorticoids on life-history often requires experimentally elevating plasma glucocorticoid concentrations for several weeks within normal physiological limits and without repeated handling of the animal. Recently, implants made of beeswax and testosterone (T) were shown to have release dynamics superior to some currently available T implants, and these beeswax implants dissolved, eliminating the need to recapture the animal. We evaluated the utility of beeswax implants containing four different dosages of corticosterone (CORT; the primary glucocorticoid in birds) and their effect on several condition indices in a captive colony of zebra finches (Taeniopygia guttata). The three implants with the greatest CORT doses (0.05, 0.1, and 0.5mg) produced spikes in plasma CORT concentrations 20h after treatment, but were within the limits that zebra finches may normally experience. The 0.5mg CORT implant elevated plasma CORT between typical baseline and restraint stress levels reported in other studies of zebra finches for the entire 35day experiment. Birds in the 0.5mg implant group were heavier, had greater furcular fat scores, and had lower hematocrit than birds in the control and other CORT implant groups. Beeswax CORT implants are a low cost method of elevating plasma CORT for a prolonged time. Furthermore, because there is no need to remove these implants at the end of a study, this method may be amenable to studies of free-ranging animals.

Potential trade-off between vocal ornamentation and spatial ability in a songbird.

Bird song is hypothesized to be a reliable indicator of cognition because it depends on brain structure and function. Song features have been found to correlate positively with measures of cognition, but the relationship between song and cognition is complicated because not all cognitive abilities are themselves positively correlated. If cognition is not a unitary trait, developmental constraints on brain growth could generate trade-offs between some aspects of cognition and song. To further clarify the relationship between song and cognition in song sparrows (Melospiza melodia), we examined repertoire size and performance on a spatial task. We found an inverse relationship between repertoire size and speed of spatial learning and suggest that a developmental trade-off between the hippocampus and song control nuclei could be responsible for this relationship. By attending to male song, females may learn about a suite of cognitive abilities; this study suggests that females may glean information about a male's cognitive weaknesses as well as his strengths.

What About Females? Urban Female Song Sparrows Elevate Aggressive Signaling Compared to Rural.

The costs and benefits of breeding behaviors are influenced by environmental conditions, and habitat variation can shift the degree to which behaviors are expressed. Novel urban habitats have been shown to differ significantly in disturbances such as noise, light at night, and human presence, as well as resource availability, compared to rural habitats. Perhaps because of these environmental differences, urban males of several species are consistently more aggressive than rural males, raising the hypothesis that greater territorial aggression is beneficial in urban habitats. Though often ignored, female songbirds of many species also perform aggressive territorial behaviors towards conspecifics during the breeding season. For socially monogamous songbirds, this aggression functions to ensure partner fidelity and secure resources for reproduction. Studies of the effects of urbanization on songbird behavior have yet to determine if urban females also express greater territorial aggression. Importantly, energetically demanding behaviors such as territoriality and parental care should constrain one another, leading to behavioral trade-offs during the breeding season. Though territorial aggression and parental care are inversely related in males of several species of songbird, this relationship is understudied in female songbirds, particularly those facing environmental change such as urbanization. In this study, we compared aggressive signaling and a measure of parental care (maternal nest visitation rates) between female song sparrows (Melospiza melodia), living in urban and rural habitats. We hypothesized that female aggressive signaling would be higher in urban environments compared to rural, and negatively correlated with maternal visitation rates. We found that urban females, like males, expressed increased aggressive signaling compared to rural. However, female aggressive signaling was not related to our measure of maternal care, suggesting females aren't facing a trade-off between these two behaviors. Collectively, our results are consistent with the hypothesis that urban habitats promote territorial aggression in female song sparrows. As urbanization continues to spread, understanding the behavioral changes animals employ in urban environments requires studying individuals of different sexes and age classes, and will help us understand how some species are able to cope with human induced rapid environmental change.

Infectious disease and cognition in wild populations.

Infectious disease is linked to impaired cognition across a breadth of host taxa and cognitive abilities, potentially contributing to variation in cognitive performance within and among populations. Impaired cognitive performance can stem from direct damage by the parasite, the host immune response, or lost opportunities for learning. Moreover, cognitive impairment could be compounded by factors that simultaneously increase infection risk and impair cognition directly, such as stress and malnutrition. As highlighted in this review, however, answers to fundamental questions remain unresolved, including the frequency, duration, and fitness consequences of infection-linked cognitive impairment in wild animal populations, the cognitive abilities most likely to be affected, and the potential for adaptive evolution of cognition in response to accelerating emergence of infectious disease.

Song environment affects singing effort and vasotocin immunoreactivity in the forebrain of male Lincoln's sparrows.

Male songbirds often establish territories and attract mates by singing, and some song features can reflect the singer's condition or quality. The quality of the song environment can change, so male songbirds should benefit from assessing the competitiveness of the song environment and appropriately adjusting their own singing behavior and the neural substrates by which song is controlled. In a wide range of taxa, social modulation of behavior is partly mediated by the arginine vasopressin or vasotocin (AVP/AVT) systems. To examine the modulation of singing behavior in response to the quality of the song environment, we compared the song output of laboratory-housed male Lincoln's sparrows (Melospiza lincolnii) exposed to 1 week of chronic playback of songs categorized as either high or low quality, based on song length, complexity, and trill performance. To explore the neural basis of any facultative shifts in behavior, we also quantified the subjects' AVT immunoreactivity (AVT-IR) in three forebrain regions that regulate sociosexual behavior: the medial bed nucleus of the stria terminalis (BSTm), the lateral septum (LS), and the preoptic area. We found that high-quality songs increased singing effort and reduced AVT-IR in the BSTm and LS, relative to low-quality songs. The effect of the quality of the song environment on both singing effort and forebrain AVT-IR raises the hypothesis that AVT within these brain regions plays a role in the modulation of behavior in response to competition that individual males may assess from the prevailing song environment.

Effects of low-density urbanization on genetic structure in the Song Sparrow.

Urbanization fragments landscapes and can impede the movement of organisms through their environment, which can decrease population connectivity. Reduction in connectivity influences gene flow and allele frequencies, and can lead to a reduction in genetic diversity and the fixation of certain alleles, with potential negative effects for populations. Previous studies have detected effects of urbanization on genetic diversity and structure in terrestrial animals living in landscapes that vary in their degree of urbanization, even over very short distances. We investigated the effects of low-intensity urbanization on genetic diversity and genetic structure in Song Sparrows (Melospiza melodia). We captured 208 Song Sparrows at seven sites along a gradient of urbanization in and around Blacksburg, VA, USA, then genotyped them using a panel of fifteen polymorphic microsatellite loci. We found that genetic diversity was comparable among the seven study sites, and there was no evidence of genetic structuring among sites. These findings suggest that over a gradient of urbanization characterized by low density urban development, Song Sparrows likely exist in a single panmictic population.

Environmental regulation of annual schedules in opportunistically-breeding songbirds: adaptive specializations or variations on a theme of white-crowned sparrow?

How birds use environmental cues to time breeding, migration and molt has been the subject of intensive study for nearly 90 years. Most work has focused on seasonal breeders; opportunistic breeders have been presumed to differ fundamentally from seasonal taxa in ways that facilitate coping with unpredictable environments. Understanding patterns and mechanisms of opportunists' responses to environmental cues can reveal the extent to which different environments require specialized adaptations of cue response systems. In this review we will present our perspective on how patterns and mechanisms of environmental cue response of three groups of opportunists--zebra finches, crossbills and Darwin's finches--compare with seasonal breeders. Long-standing predictions regarding tonic activity of the hypothalamic gonadotropin-releasing hormone system have been confirmed in at least some opportunists. However, opportunists resemble seasonal breeders in some surprising ways, illustrating basic similarity among taxa facing very different timing challenges. For instance, many opportunists completely regress the gonads outside breeding times, rely on initial predictive cues (both photic and non-photic) to regulate timing and rate of reproductive development, and in some cases even appear to display internal changes in responsiveness to environmental cues (i.e., cycles of reproductive refractoriness and sensitivity). Although advantages of unrestricted temporal flexibility are intuitively clear for animals coping with unpredictable habitats, the available data on these opportunists indicate that in all but the most extremely capricious situations the advantages of flexibility may be at least partly outweighed by contrasting advantages of following a reliable temporal schedule.

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

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.

Hatching asynchrony impacts cognition in male zebra finches.

Conditions experienced early in life can shape brain development and later cognition. Altricial songbirds are particularly vulnerable to early environmental perturbations. Research on "Developmental Stress" in songbirds has addressed how early-life conditions may impair song learning and has been extended to consider other components of adult phenotype. Early-life challenges ranging from ectoparasites to competition with siblings have been shown to compromise song learning and other measures of cognition, as well as behavioral strategy. Here, we examined both the effects of hatching asynchrony and early-life immune system challenge with lipopolysaccharide (LPS) on neophobia, song learning, motoric learning, and spatial cognition in male zebra finches (Taeniopygia guttata). We found that hatch order had a significant impact on motoric and spatial learning, such that later hatched males performed better than first and second hatched birds. In contrast, LPS treatment only impacted motoric learning and neither hatch order nor immune system challenge impacted song quality, song learning accuracy, or neophobia. These results are consistent with a growing body of evidence that conditions early in life can improve cognitive performance at adulthood. Moreover, these findings indicate that hatch order is an important factor to consider in developmental studies in asynchronously hatching birds.

Social calls provide novel insights into the evolution of vocal learning.

Learned song is among the best-studied models of animal communication. In oscine songbirds, where learned song is most prevalent, it is used primarily for intrasexual selection and mate attraction. Learning of a different class of vocal signals, known as contact calls, is found in a diverse array of species, where they are used to mediate social interactions among individuals. We argue that call learning provides a taxonomically rich system for studying testable hypotheses for the evolutionary origins of vocal learning. We describe and critically evaluate four nonmutually exclusive hypotheses for the origin and current function of vocal learning of calls, which propose that call learning (1) improves auditory detection and recognition, (2) signals local knowledge, (3) signals group membership, or (4) allows for the encoding of more complex social information. We propose approaches to testing these four hypotheses but emphasize that all of them share the idea that social living, not sexual selection, is a central driver of vocal learning. Finally, we identify future areas for research on call learning that could provide new perspectives on the origins and mechanisms of vocal learning in both animals and humans.

Social Complexity as a Driver of Communication and Cognition.

Cognition and communication both can be essential for effectively navigating the social environment and thus, social dynamics could select for enhanced abilities for communication and superior cognition. Additionally, social experience can influence both the ability to communicate effectively and performance in cognitive tasks within an individual's lifetime, consistent with phenotypic plasticity in these traits. Historically, research in animal cognition and animal communication has often addressed these traits independently, despite potential commonalities in social function and underlying mechanisms of the brain. Integrating research on animal communication and cognition will provide a more comprehensive understanding of how the social environment may shape behavior and specializations of the brain for sociality through both evolutionary and developmental processes. This selective review of research on the impacts of social dynamics on cognition and communication in animals aims to highlight areas for future research at both the ultimate and proximate levels. In particular, additional work on the effects of the social environment on cognitive performance over an individual's lifetime, and comparative studies of specialized abilities for communication, should be pursued.