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: 9.81). 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.

Download full-text


Available from: Leah C Wilson, Aug 15, 2015
    • "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. "
    [Show abstract] [Hide abstract]
    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 · 3.51 Impact Factor
  • Source
    • "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]. "
    [Show abstract] [Hide abstract]
    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 · 3.39 Impact Factor
  • Source
    • "n to ' lactation ' [ Péczely and Kiss , 1988 ] . These chang - es are correlated with changes in the GnRH system of the preoptic areas [ Deviche et al . , 2000 ] . Reduction in VIP immunoreactivity is also observed in the BNST of the field sparrow and song sparrow during winter , when they are less aggressive and display no territorial behaviour [ Goodson et al . , 2012b ] . However , the role of VIP in social bonding remains unknown . As the modulatory role of VIP differs with the type of social behaviour , the question arises whether its distribution pattern may be influenced by the social bonding pattern related to breeding systems ( mono - / polygamous ) ."
    [Show abstract] [Hide abstract]
    ABSTRACT: Vasopressin influences social behaviour in mammals, in particular social recognition and bonding. However, much less is known about its avian analogue, vasotocin, although vasotocin appears to modulate singing behaviour and agonistic interactions together with vasoactive intestinal peptide (VIP) in some songbirds. The objectives of our study were to compare the expression of vasotocin and VIP in brain nuclei hypothetised to be part of the social behavioural network, i.e. septal areas, bed nucleus of the stria terminalis and medial preoptic nucleus (POM), in two songbird species in the wild: the blue tit (Cyanistes caeruleus) and European penduline tit (Remiz pendulinus). These two closely related passerine birds differ in their pair bonding and mating systems: blue tits are socially monogamous with extensive pair bond lasting for several months, whereas in the European penduline tit, pair bond is short and it dissolves during or after laying of the eggs. The two species did not differ in the distribution of vasotocin in the observed brain regions; however, VIP was more abundant in all three regions of penduline tits than in blue tits. We found a sex difference in favour of males in the distribution of vasotocin- and VIP-immunoreactive neurones, fibres and terminals in all three regions in penduline tits. In blue tits, such gender differences were only observed in the POM. The limited differences between the two species suggest that the levels of vasotocin and VIP in the socially relevant brain regions are likely influenced by many other social or environmental factors than just by differences in the duration of pair bonding. © 2014 S. Karger AG, Basel.
    Brain Behavior and Evolution 04/2014; 83(2):140-9. DOI:10.1159/000357831 · 4.29 Impact Factor
Show more