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 one 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 socio-sexual 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

Indirect effects of urbanization: consequences of increased aggression in an urban male songbird for mates and offspring

Behavioral traits are often the first response to changing environmental conditions, including human induced rapid environmental change. For example, animals living in urban areas are often more aggressive than rural animals. This is especially evident in songbirds; males of several species display elevated aggression in urban habitats. Increased male aggression has been associated with reduced parental care, but the consequences of this trade-off for males, social partners, and offspring in the context of urbanization remains unclear. We explored the effects of increased urban male aggression on the life history traits, parental care, and offspring outcomes of song sparrows (Melospiza melodia). We predicted that urban males would reduce paternal investment and result in urban females providing greater nestling care or reduced fledging success in urban habitats compared to rural. Contrary to our prediction, aggressive urban males did not decrease care but visited the nest more often compared to rural males. Additionally, urban birds had higher nest and fledging success compared to rural, though this was largely due to higher nest predation in rural habitats. Our study is among the first to evaluate trade-offs associated with elevated aggression expressed by urban animals and adds to a growing body of evidence that urban habitats provide benefits to some species

The evolution of self-control

This work was supported by the National Evolutionary Synthesis Center (NESCent) through support of a working group led by C.L.N. and B.H. NESCent is supported by the National Science Foundation (NSF) EF-0905606. For training in phylogenetic comparative methods, we thank the AnthroTree Workshop (supported by NSF BCS-0923791). Y.S. thanks the National Natural Science Foundation of China (Project 31170995) and National Basic Research Program (973 Program: 2010CB833904). E.E.B. thanks the Duke Vertical Integration Program and the Duke Undergraduate Research Support Office. J.M.P. was supported by a Newton International Fellowship from the Royal Society and the British Academy. L.R.S. thanks the James S. McDonnell Foundation for Award 220020242. L.J.N.B. and M.L.P. acknowledge the National Institutes of Mental Health (R01-MH096875 and R01-MH089484), a Duke Institute for Brain Sciences Incubator Award (to M.L.P.), and a Duke Center for Interdisciplinary Decision Sciences Fellowship (to L.J.N.B.). E.V. and E.A. thank the Programma Nazionale per la Ricerca–Consiglio Nazionale delle Ricerche (CNR) Aging Program 2012–2014 for financial support, Roma Capitale–Museo Civico di Zoologia and Fondazione Bioparco for hosting the Istituto di Scienze e Tecnologie della Cognizione–CNR Unit of Cognitive Primatology and Primate Centre, and Massimiliano Bianchi and Simone Catarinacci for assistance with capuchin monkeys. K.F. thanks the Japan Society for the Promotion of Science (JSPS) for Grant-in-Aid for Scientific Research 20220004. F. Aureli thanks the Stages in the Evolution and Development of Sign Use project (Contract 012-984 NESTPathfinder) and the Integrating Cooperation Research Across Europe project (Contract 043318), both funded by the European Community’s Sixth Framework Programme (FP6/2002–2006). F. Amici was supported by Humboldt Research Fellowship for Postdoctoral Researchers (Humboldt ID 1138999). L.F.J. and M.M.D. acknowledge NSF Electrical, Communications, and Cyber Systems Grant 1028319 (to L.F.J.) and an NSF Graduate Fellowship (to M.M.D.). C.H. thanks Grant-in-Aid for JSPS Fellows (10J04395). A.T. thanks Research Fellowships of the JSPS for Young Scientists (21264). F.R. and Z.V. acknowledge Austrian Science Fund (FWF) Project P21244-B17, the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement 311870 (to F.R.), Vienna Science and Technology Fund Project CS11-026 (to Z.V.), and many private sponsors, including Royal Canin for financial support and the Game Park Ernstbrunn for hosting the Wolf Science Center. S.M.R. thanks the Natural Sciences and Engineering Research Council (Canada). J.K.Y. thanks the US Department of Agriculture–Wildlife Services–National Wildlife Research Center. J.F.C. thanks the James S. McDonnell Foundation and Alfred P. Sloan Foundation. E.L.M. and B.H. thank the Duke Lemur Center and acknowledge National Institutes of Health Grant 5 R03 HD070649-02 and NSF Grants DGE-1106401, NSF-BCS-27552, and NSF-BCS-25172. This is Publication 1265 of the Duke Lemur Center.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.PostprintPeer reviewe

Two Neural Measures Differ between Urban and Rural Song Sparrows after Conspecific Song Playback

Urbanization is a critical form of environmental change that can affect the physiology and behavior of wild animals and, notably, birds. One behavioral difference between birds living in urban and rural habitats is that urban males show elevated boldness or territorial aggression in response to simulated social challenge. This pattern has been described in several populations of song sparrow, Melospiza melodia. Such behavioral differences must be underpinned by differences in the brain, yet little work has explored how urbanization and neural function may be interrelated. We explored the relationship between urbanization and neural activation within a network of brain regions, collectively called the social behavior network, which contributes to the regulation of territorial aggression. Specifically, we captured free-living, territorial male song sparrows by playing them conspecific songs for 6–11 min, and then collected their brains. We estimated recent neural activation, as indicated by the immediate early gene FOS, and measured levels of a neuropeptide, arginine vasotocin (AVT), which is involved in the regulation of social behavior. Based on previous studies we expected urban males, which are generally more territorially aggressive, to have lower FOS expression in a node of the social behavior network implicated in regulating territoriality, the lateral septum (LS). Additionally, we expected urban males to have lower AVT expression in a brain region involved in the regulation of sociality, the medial bed nucleus of the stria terminalis (BSTm). We found that, compared to rural males, urban male song sparrows did have lower FOS expression in the LS. This pattern suggests that lower neural activation in the LS could contribute to behavioral adjustments to urbanization in male song sparrows. Additionally, counter to our predictions, urban male song sparrows had higher AVT-like immunoreactivity in the BSTm. Future work building upon these findings is needed to determine the causal role of such neural differences across rural and urban habitats. Understanding the mechanisms impacted by urbanization will inform our understanding of the reversibility and consequences of this form of habitat change

Female Lincoln's sparrows modulate their behavior in response to variation in male song quality

Sexually reproducing organisms should mate with the highest quality individuals that they can. When female songbirds choose a mate, they are thought to use several aspects of male song that reflect his quality. Under resource-limited environmental conditions, male Lincoln's sparrows (Melospiza lincolnii) vary among one another in several aspects of song quality, including song length, song complexity, and trill performance. In a 2-pronged approach, we tested whether variation in song quality of male Lincoln's sparrows influences the behavior of females that are in a reproductive-like state. Over two trials, we exposed females to songs from the high and low ends of the distribution of naturally occurring song quality variation and found a higher level of behavioral activity in females exposed to high-quality songs, especially when they had first been exposed to low-quality songs. We also examined female phonotaxis toward antiphonally played songs with experimentally elevated and reduced trill performance and found that females moved preferentially toward the songs with elevated trill performance. Contrary to most studies investigating the behavioral responses of wild, female songbirds to variation in male song, we obtained our results without administering exogenous estradiol, which can artificially perturb the female's physiology. Our results demonstrate that the behavior of female Lincoln's sparrows is modulated by the quality of male songs to which they are exposed and that trill performance plays a significant role in this behavioral modulation. Furthermore, as the order of song quality presentation matters, it appears that recent song experience also influences female behavior. Copyright 2010, Oxford University Press.

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

Migratory state is not associated with differences in neural glucocorticoid or mineralocorticoid receptor expression in pine siskins

Although the endocrine system likely plays an important role in orchestrating the transition to a migratory state, the specific mechanisms by which this occurs remain poorly understood. Changes in glucocorticoid signaling are one proposed mechanism that may be important in migratory transitions. Although previous work has focused on the role of changes in circulating glucocorticoids, another potential mechanism is changes in the expression of its cognate receptors. Here, we test this hypothesis by comparing mRNA expression of the genes for the mineralocorticoid receptor ( ) and glucocorticoid receptor ( ) in two brain regions implicated in the regulation of migratory behavior (the hippocampus and hypothalamus) in pine siskins ( ) sampled before or after the transition to a spring nomadic migratory state. Compared to pre-migratory birds, migratory birds had body conditions more indicative of physiological preparations for migration (e.g., larger body mass), and greater levels of nocturnal migratory restlessness. However, we found no differences between pre-migratory and migratory birds in the expression of or mRNA in either the hippocampus or hypothalamus. Thus, differences in expression of receptors for glucocorticoids do not appear to underly the observed differences in physiology and behavior across a migratory transition. Taken together with previous results showing no change in circulating corticosterone levels during this transition, our findings provide no evidence for a role of glucocorticoid signaling in the spring migratory transition of this species

Placement of Tissue Punches.

<p>Photomicrographs of sagittal brain sections approximately 300 µm (upper panel) and 900 µm (lower panel) from the midline illustrating where micropunches of tissue were taken to quantify levels of norepinephrine, dopamine, serotonin, and their primary metabolites in the caudomedial mesopallium (CMM), the caudomedial nidopallium (NCM), area X, and the robust nucleus of the arcopallium (RA; lower image). Images generated for illustration only.</p

Treatment effects on forebrain monoamines.

<p>The effects of the level of song challenge on the amount (mean pg/mg of protein ± SEM) of (a) norepinephrine metabolite in the caudomedial mesopallium (CMM) and (b) serotonin in the robust nucleus of the arcopallium (RA).</p