Behavioral phenotypes persist after gonadal steroid manipulation in white-throated sparrows

Maney, Donna L.; Lange, Henry S.; Raees, Madiha Q.; Reid, Allison; Sanford, Sara E.

doi:10.1016/j.yhbeh.2008.09.002

Cited by 39 publications

(61 citation statements)

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“…Therefore, we might expect morph differences in social behavior to be driven by T alone. Exogenous administration of sex steroids, however, stimulates more singing in WS than TS birds of both sexes, despite producing identical plasma levels (9). This result strongly suggests that sensitivity to plasma steroid manipulations differs between the morphs.…”

Section: Discussionmentioning

confidence: 88%

“…In songbirds, territorial and parental behaviors typically depend on sex steroids; during the breeding season, WS birds have higher plasma testosterone (T) than do their same-sex TS counterparts (7,8). Morph differences in behavior cannot be entirely explained by these hormones, however, because the differences persist even when plasma levels are experimentally equalized (9). Individual variation in steroid-dependent behavior may be better explained by neural sensitivity to the hormones, for example by variation in the distribution and abundance of steroid receptors (10,11).…”

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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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103

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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: Discussionmentioning

confidence: 88%

mentioning

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.

Self Cite

103

136

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“…Because plasma E2 profoundly affects behavioral responses to song (Moore, 1983;Maney et al, 2006Maney et al, , 2008Maney et al, , 2009) and thus presumably alters behavioral relevance, we hypothesized that it may affect song-induced genomic responses in NCM. In support of this hypothesis, we showed previously that zenk responses in this region were selective for song over behaviorally nonrelevant tones only when plasma E2 exceeded nonbreeding levels (Maney et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…Like Maney et al (2006), we worked with whitethroated sparrows because they have a simple song consisting only of relatively pure-tone whistles, because they are highly seasonal breeders exhibiting large changes in hormonal profiles and behavior from fall to spring (Falls and Kopachena, 1994;Spinney et al, 2006), and because their behavioral responses to song are easily manipulated by E2-treatment in the lab (Maney et al, 2006(Maney et al, , 2008(Maney et al, , 2009. As is the case for many species, plasma E2 in wild-caught female white-throated sparrows does not reach breeding levels in captivity even under long day lengths; we therefore manipulated plasma E2 by administration of exogenous E2 in nonbreeding females held on a winter-like photoperiod.…”

Section: Introductionmentioning

confidence: 99%

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Sanford

Lange

Maney

2009

Developmental Neurobiology

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Sex steroids facilitate dramatic changes in behavioral responses to sociosexual signals and are increasingly implicated in the sensory processing of those signals. Our previous work demonstrated that in female white-throated sparrows, which are seasonal breeders, genomic responses in the auditory forebrain are selective for conspecific song over frequency-matched tones only when plasma estradiol (E2) reaches breeding levels. Here, we sought to map this E2-dependent selectivity in the best-studied area of the auditory forebrain, the caudomedial nidopallium (NCM). Nonbreeding females with low endogenous levels of E2 were treated with E2 or a placebo and exposed to conspecific song, tones, or no sound playback. Immunoreactive protein product of the immediate early gene zenk (egr-1) was then quantified within seven distinct subregions, or domains, of NCM. We report three main findings: (1) regardless of hormone treatment, the zenk response is significantly higher in dorsal than in ventral NCM, and higher in medial than in lateral NCM; (2) E2-dependent selectivity of the response is limited to the rostral and medial domains of NCM; in the more caudal domains, song induces more zenk expression than tones regardless of hormone treatment; (3) even when no sound stimuli were presented, E2 treatment significantly increased zenk expression in the rostral, but not the caudal, domains of NCM. Together, the latter two findings suggest that E2-dependent plasticity in NCM is concentrated in rostral NCM, which is hodologically and neurochemically distinct from caudal NCM. Activity in rostral NCM may therefore be seasonally regulated in this species.

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“…In our twinning case, the female that laid the egg was a white morph mated to a tan male. Previous studies have shown some variation in gonadal steroid levels between females of both morphs (Maney et al 2009, Horton et al 2014), though others have only shown differences between males (Spinney et al 2006, Swett andBreuner 2009), and none have demonstrated a connection to egg production and embryo development. Tan males tend to provide more assistance with nesting attempts as well as guard their mate during the fertile period (Tuttle 2003).…”

Section: Discussionmentioning

confidence: 97%

Genetic Verification of Dizygotic Twin Embryos in the White-throated Sparrow (Zonotrichia albicollis)

Betuel

Tuttle

Gonser

2015

The Wilson Journal of Ornithology

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Behavioral phenotypes persist after gonadal steroid manipulation in white-throated sparrows

Cited by 39 publications

References 63 publications

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

Topography of estradiol‐modulated genomic responses in the songbird auditory forebrain

Genetic Verification of Dizygotic Twin Embryos in the White-throated Sparrow (Zonotrichia albicollis)

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