To flock or fight: Neurochemical signatures of divergent life histories in sparrows

Department of Biology, Indiana University, Bloomington, IN 47405, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 06/2012; 109 Suppl 1(Supplement_1):10685-92. DOI: 10.1073/pnas.1203394109
Source: PubMed

ABSTRACT Many bird species exhibit dramatic seasonal switches between territoriality and flocking, but whereas neuroendocrine mechanisms of territorial aggression have been extensively studied, those of seasonal flocking are unknown. We collected brains in spring and winter from male field sparrows (Spizella pusilla), which seasonally flock, and male song sparrows (Melospiza melodia), which are territorial year-round in much of their range. Spring collections were preceded by field-based assessments of aggression. Tissue series were immunofluorescently multilabeled for vasotocin, mesotocin (MT), corticotropin-releasing hormone (CRH), vasoactive intestinal polypeptide, tyrosine hydroxylase, and aromatase, and labeling densities were measured in many socially relevant brain areas. Extensive seasonal differences are shared by both species. Many measures correlate significantly with both individual and species differences in aggression, likely reflecting evolved mechanisms that differentiate the less aggressive field sparrow from the more aggressive song sparrow. Winter-specific species differences include a substantial increase of MT and CRH immunoreactivity in the dorsal lateral septum (LS) and medial amygdala of field sparrows but not song sparrows. These species differences likely relate to flocking rather than the suppression of winter aggression in field sparrows, because similar winter differences were found for two other emberizids that are not territorial in winter--dark-eyed juncos (Junco hyemalis), which seasonally flock, and eastern towhees (Pipilo erythropthalmus), which do not flock. MT signaling in the dorsal LS is also associated with year-round species differences in grouping in estrildid finches, suggesting that common mechanisms are targeted during the evolution of different life histories.

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Available from: Leah C Wilson, Sep 29, 2015
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    • "During the time of year in which flocking occurs, field sparrows have greater CRF immunoreactivity in the lateral septum (Goodson et al., 2012), a region in which CRF 1 receptor binding has been associated with increased social huddling in meadow voles (Beery et al., 2014). Naked mole-rats have low to undetectable CRF 1 receptor binding in the lateral septum, but showed status differences in other brain regions. "
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    ABSTRACT: Naked mole-rats (Heterocephalus glaber) live in groups that are notable for their large size and caste structure, with breeding monopolized by a single female and small number of males. Recent studies have demonstrated substantial differences between the brains of breeders and subordinates induced by changes in social standing. CRF receptors-which bind the hormone corticotropin-releasing factor as well as related peptides-are important regulators of stress and anxiety, and are emerging as factors affecting social behavior. We conducted autoradiographic analyses of CRF1 and CRF2 receptor binding densities in female and male naked mole-rats varying in breeding status. Both globally and in specific brain regions, CRF1 receptor densities varied with breeding status. CRF1 receptor densities were higher in subordinates across brain regions, and particularly in the piriform cortex and cortical amygdala. Sex differences were present in CRF2 receptor binding densities, as is the case in multiple vole species. CRF2 receptor densities were higher in females, both globally and in the cortical amygdala and lateral amygdalar nucleus. These results provide novel insights into the neurobiology of social hierarchy in naked mole-rats, and add to a growing body of work that links changes in the CRF system with social behavior. This article is protected by copyright. All rights reserved. © 2015 Wiley Periodicals, Inc.
    The Journal of Comparative Neurology 06/2015; DOI:10.1002/cne.23834 · 3.23 Impact Factor
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    • "Species that have the highest visual acuity (relative to body mass) most commonly prey on flying insects (Eastern towhee, white-throated sparrow and American tree sparrow; supplementary material Table S1). Additionally, species with relatively higher visual acuity (towhees and song sparrows) tend to be more territorial compared with species with relatively lower acuity (hence, with lower probabilities of detecting predators from far away; Tisdale and Fernández-Juricic, 2009), which tend to flock more (field sparrows, dark-eyed juncos; Goodson et al., 2012). The implication is that the benefits of flocking (dilution and collective detection effects; Krause and Ruxton, 2002) might compensate for some sensory constraints. "
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    ABSTRACT: Avian species vary in their visual system configuration, but previous studies have often compared single visual traits between 2-3 distantly related species. However, birds use different visual dimensions that cannot be maximized simultaneously to meet different perceptual demands, potentially leading to trade-offs between visual traits. We studied the degree of inter-specific variation in multiple visual traits related to foraging and anti-predator behaviors in nine species of closely related emberizid sparrows, controlling for phylogenetic effects. Emberizid sparrows maximize binocular vision, even seeing their bill tips, which may enhance the detection of prey and facilitate food handling. Sparrows have a single retinal center of acute vision (i.e., fovea) projecting fronto-laterally (but not into the binocular field). The foveal projection close to the edge of the binocular field may shorten the time to gather and process both monocular and binocular visual information from the foraging substrate. Contrary to previous work, we found that species with larger visual fields had higher visual acuity, which may compensate for larger blind spots (i.e., pectens) above the center of acute vision, enhancing predator detection. Finally, species with a steeper change in ganglion cell density across the retina had higher eye movement amplitude likely due to a more pronounced reduction in visual resolution away from the fovea, which would need to be moved around more frequently. The visual configuration of emberizid passive prey foragers is substantially different from that of previously studied avian groups (e.g., sit-and-wait and tactile foragers). © 2015. Published by The Company of Biologists Ltd.
    Journal of Experimental Biology 03/2015; 218(9). DOI:10.1242/jeb.108613 · 2.90 Impact Factor
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    • "These cell groups have been studied primarily in relation to motor function, incentive motivation, and prolactin secretion, respectively, although other DA cell groups in the brain are known to be relevant to social behavior [15] [16] [17] [18], hormonal regulation [19], and responses to stress [19] [20] [21]. In songbirds, the various DA cell groups exhibit distinct patterns of Fos response (a proxy marker of neural activity) to various social stimuli [18], and both individual and species differences are reflected in DA anatomy and/or socially induced Fos response, as shown in relation to affiliation (for the A10 cell group and the A11 cell group of midbrain central gray, CG) [7] and aggression (for the A10 cell group, A12 cell group; and A14 cell group of the medial hypothalamus and preoptic area, POA) [22]. "
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    ABSTRACT: Dopamine (DA) is well known for its involvement in novelty-seeking, learning, and goal-oriented behaviors such as social behavior. However, little is known about how DA modulates social processes dif-ferentially in relation to sex and behavioral phenotype (e.g., personality). Importantly, the major DA cell groups (A8–A15) are conserved across all amniote vertebrates, and thus broadly relevant insights may be obtained through investigations of avian species such as zebra finches (Taeniopygia guttata), which express a human-like social organization based on biparental nuclear families that are embedded within larger social groups. We here build upon a previous study that quantified multidimensional personal-ity structures in male and female zebra finches using principal components analysis (PCA) of extensive behavioral measures in social and nonsocial contexts. These complex dimensions of behavioral phenotype can be characterized as Social competence/dominance, Gregariousness, and Anxiety. Here we analyze Fos protein expression in DA neuronal populations in response to social novelty and demonstrate that the Fos content of multiple dopamine cell groups is significantly predicted by sex, personality, social context, and their interactions. In order to further investigate coordinated neuromodulation of behavior across multiple DA cell groups, we also conducted a PCA of neural variables (DA cell numbers and their phasic Fos responses) and show that behavioral PCs are associated with unique suites of neural PCs. These find-ings demonstrate that personality and sex are reflected in DA neuron activity and coordinated patterns of neuromodulation arising from multiple DA cell groups.
    Behavioural Brain Research 12/2014; 280:101-112. DOI:10.1016/j.bbr.2014.12.004 · 3.03 Impact Factor
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