Estradiol modulates neural responses to song in a seasonal songbird

Maney, Donna L.; Goode, Christopher T.; Lange, Henry S.; Sanford, Sara E.; Solomon, Benjamin L.

doi:10.1002/cne.21830

Cited by 107 publications

(146 citation statements)

References 69 publications

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“…In females the c path was satisfied for singing [t (8) = 2.501; P = 0.037]. As in previous studies (22), however, we did not detect a morph difference in female provisioning rate [t (18) = 0.616; P = 0.546]. Thus, the c path was satisfied in females only for song.…”

Section: Erα Gene Expression Predicts Territorial Song and Parental Bsupporting

confidence: 58%

“…To test for such regulation in vivo, we quantified ERα mRNA expression in the brains of 79 free-living, behaviorally characterized white-throated sparrows during the breeding season near Argyle, Maine. We focused our analysis on nine distinct brain regions, several of which make up an E2-sensitive social behavior network (17,18). To control for type I error due to multiple tests, we first conducted an omnibus multiple analysis of covariance (MANCOVA) on all of the ERα values for each sex.…”

Section: Erα Gene Expression Depends On Morph In a Free-living Populamentioning

confidence: 99%

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Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

Horton

Hudson

Ortlund

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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136

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The evolution of behavior relies on changes at the level of the genome; yet the ability to attribute a behavioral change to a specific, naturally occurring genetic change is rare in vertebrates. In the white-throated sparrow (Zonotrichia albicollis), a chromosomal polymorphism (ZAL2/2 m ) is known to segregate with a behavioral phenotype. Individuals with the ZAL2 m haplotype engage in more territorial aggression and less parental behavior than individuals without it. These behaviors are thought to be mediated by sensitivity to sex steroids, and the chromosomal rearrangement underlying the polymorphism has captured a prime candidate gene: estrogen receptor 1 (ESR1), which encodes estrogen receptor α (ERα). We therefore hypothesized that the behavioral effects of the ZAL2 m rearrangement are mediated by polymorphism in ESR1. We report here that (i) the ESR1 promoter region contains fixed polymorphisms distinguishing the ZAL2 m and ZAL2 alleles; (ii); those polymorphisms regulate transcription efficiency in vitro and therefore potentially do the same in vivo (iii); the local expression of ERα in the brain depends strongly on genotype in a freeliving population; and (iv) ERα expression in the medial amygdala and medial preoptic area may fully mediate the effects of genotype on territorial aggression and parenting, respectively. Thus, our study provides a rare glimpse of how a chromosomal polymorphism has affected the brain and social behavior in a vertebrate. Our results suggest that in this species, differentiation of ESR1 has played a causal role in the evolution of phenotypes with alternative life-history strategies.estradiol | testosterone | morph | reproductive tactics B ecause the genetic basis of social behavior is complex and involves many genes throughout the genome, it has been difficult to link behavior with specific genes-particularly in vertebrates. The white-throated sparrow (Zonotrichia albicollis), a common North American songbird, represents a unique model for connecting genetic sequence with behavior (1). This species occurs in two plumage morphs (Fig. 1) that segregate absolutely with a rearranged chromosome 2 called ZAL2 m (2). ZAL2 m consists of at least two pericentric inversions (3) and is present in all white-striped (WS) individuals but never in tan-striped (TS) individuals. The rearrangement occurs equally in males and females, and almost all breeding pairs consist of one individual with and one without it (4). This disassortative mating system is the mechanism by which balancing selection acts to maintain ZAL2/2 m in the population, and consequently, homozygosity for ZAL2 m is rare (4,5). Recombination between ZAL2 and ZAL2 m is profoundly suppressed (3), and this genetic isolation has resulted in the differentiation of alternative chromosome types (6).Genetic differentiation of ZAL2/2 m is associated with a behavioral phenotype (1, 4); WS males engage in more territorial aggression and mate-finding than do TS males. In contrast, TS males show more nestling provisioning and mate guarding....

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Section: Erα Gene Expression Predicts Territorial Song and Parental Bsupporting

confidence: 58%

Section: Erα Gene Expression Depends On Morph In a Free-living Populamentioning

confidence: 99%

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

Horton

Hudson

Ortlund

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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100

136

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“…Thus, winning might alter the network's functional connectivity and neurochemical release by adjusting how specific network nodes detect and respond to androgen hormones (see ref. 36 for example). Indeed, activation of AR in adult animals plays a critical role in aspects of reproduction and parenting (37,38), which implies that these behaviors might be adjusted in winners as a result of changes to neural AR expression.…”

Section: Functional Significance Of Increased Ar In the Limbic And Mementioning

confidence: 99%

Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression

Fuxjager

Forbes-Lorman²,

Coss³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

190

120

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Winning aggressive disputes can enhance future fighting ability and the desire to seek out additional contests. In some instances, these effects are long lasting and vary in response to the physical location of a fight. Thus, in principle, winning aggressive encounters may cause long-term and context-dependent changes to brain areas that control the output of antagonistic behavior or the motivation to fight (or both). We examined this issue in the territorial California mouse (Peromyscus californicus) because males of this species are more likely to win fights after accruing victories in their home territory but not after accruing victories in unfamiliar locations. Using immunocytochemistry and real-time quantitative PCR, we found that winning fights either at home or away increases the expression of androgen receptors (AR) in the medial anterior bed nucleus of the stria terminalis, a key brain area that controls social aggression. We also found that AR expression in brain regions that mediate motivation and reward, nucleus accumbens (NAcc) and ventral tegmental area (VTA), increases only in response to fights in the home territory. These effects of winning were likely exclusive to the neural androgenic system because they have no detectible impact on the expression of progestin receptors. Finally, we demonstrated that the observed changes in androgen sensitivity in the NAcc and VTA are positively associated with the ability to win aggressive contests. Thus, winning fights can change brain phenotype in a manner that likely promotes future victory and possibly primes neural circuits that motivate individuals to fight.aggression | androgen and progestin receptors | behavioral reinforcement | neurobiology | winner effect S ocial experiences that individuals accrue throughout life can modify the brain's morphology and hormonal milieu (1, 2). These changes are often thought to adjust future social behavior because they occur in brain areas that control affective state, arousal, and motivation (3). However, less is known about how the environment of a given social encounter modulates its subsequent effects on the brain. We examined this issue here by testing (i) whether winning fights modifies neural circuits that control social aggression and motivation and (ii) whether a fight's environment, in turn, modulates any of these effects.Winning aggressive disputes or competitions can affect future behavior (4, 5). For example, individuals that win fights are more likely to win later in life (6). In some species, this so-called winner effect is long lasting and forms only in response to victories in certain locations (6). Although mechanistic studies of the winner effect focus on how postencounter changes in steroid hormones adjust future winning behavior (7), this physiological model is less suitable for species in which the winner effect either persists well after excess hormones are cleared from circulation or depends on a fight's environment (8, 9). Thus, it is possible that the experience of victory induces long-term ...

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“…Â 17.00 mm; sealed with silicone at both ends) packed with crystalline 17b-oestradiol (Steraloids Inc., Newport, RI, USA) to elevate sensitivity to song [6].…”

Section: Methodsmentioning

confidence: 99%

Song in the cold is ‘hot’: memory of and preference for sexual signals perceived under thermal challenge

Beaulieu

Sockman

2012

Biol. Lett.

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The environmental conditions under which signals are perceived can affect receiver responses. Many songbird populations produce a song chorus at dawn, when, in cold habitats, they would experience thermal challenge. We recorded temperature and the song activity of Lincoln's sparrows (Melospiza lincolnii ) on a high-elevation meadow, and determined that song behaviour is concentrated around the coldest time of the day, at dawn. We hypothesized that this is because male song in the cold is more attractive to females than song in the warm. To test this, we exposed laboratory-housed Lincoln's sparrow females to songs at 18 8 8 8 8C and 168 8 8 8 8C, which they naturally experience in the wild. Females spent 40 per cent more time close to the speaker during playback at 18 8 8 8 8C than at 168 8 8 8 8C. When tested at 168 8 8 8 8C 1-2 days later, females biased their movement towards the speaker playing songs previously heard at 18 8 8 8 8C over 168 8 8 8 8C. Thus, female Lincoln's sparrows remembered and affiliated with songs they heard under thermal challenge, indicating that the thermal environment can affect the attractiveness of a sexual signal.

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Estradiol modulates neural responses to song in a seasonal songbird

Cited by 107 publications

References 69 publications

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression

Song in the cold is ‘hot’: memory of and preference for sexual signals perceived under thermal challenge

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