Regular articleNon-invasive administration of 17β-estradiol rapidly increases aggressive behavior in non-breeding, but not breeding, male song sparrows
Introduction
17β-estradiol (E2) acts in the brain via both genomic and non-genomic signaling mechanisms to influence physiology and behavior (Vasudevan and Pfaff, 2008). In the genomic model of steroid action, E2 binds to cytosolic estrogen receptors (ERs), and the hormone-receptor complex translocates to the cell nucleus, and binds to estrogen response elements in the DNA to alter gene expression (Jensen et al., 1968, McCarthy, 2009, Vasudevan and Pfaff, 2008). These effects generally take several hours or days to develop (Zangenehpour and Chaudhuri, 2002), and lead to persistent changes in physiology and behavior (McCarthy, 2009, McEwen, 2001). However, E2 also acts on a timescale that is too short to be attributed to changes in gene transcription (Cornil and Charlier, 2010). In this non-genomic model of E2 action, E2 binds to plasma membrane-associated ERs, which activate signal transduction cascades including mobilization of cytosolic calcium and phosphorylation of cAMP response element binding (CREB) and mitogen-activated protein kinase (MAPK) (Ivanova et al., 2002, Kelly et al., 1999, Singer et al., 1999). These rapid, non-genomic effects typically occur within minutes and lead to more transient changes in physiology and behavior (Laredo et al., 2014).
Recent data suggest that the signaling mechanisms by which E2 regulates aggressive behavior are modulated by photoperiod. Specifically, in Peromyscus mice, acute E2 administration rapidly alters aggressive behavior in male subjects housed on short (non-breeding season-like) photoperiods but not those housed on long (breeding season-like) photoperiods (Trainor et al., 2007a, Trainor et al., 2008). Further, microarray and real-time PCR analyses indicate that estrogen response element-dependent gene expression is higher in animals housed on long photoperiods as compared to those housed on short photoperiods (Trainor et al., 2007a). Taken together, these data indicate that the non-genomic effects of E2 on aggressive behavior may be more prominent during the non-breeding season, whereas the genomic effects of E2 on aggression may be more prominent during the breeding season (Trainor et al., 2007a).
Like Peromyscus, male song sparrows (Melospiza melodia) display E2-dependent territorial aggression throughout the year (except for a brief period during molt) (Wingfield and Soma, 2002). Territorial aggression in song sparrows is measured in the field via simulated territorial intrusion (STI) whereby a live caged decoy and conspecific song playback are used to elicit aggressive behavior in residents (Soma et al., 2000). Territorial aggression during a STI is both qualitatively and quantitatively similar in the breeding and non-breeding seasons (Wingfield and Hahn, 1994). However, territorial aggression after a STI is terminated changes seasonally. In the breeding season, residents continue patrolling their territories and exhibit spontaneous song for hours (even days) after a STI, whereas in the non-breeding season, residents stop behaving aggressively within minutes (Wingfield, 1994). It appears that once the behavior is elicited, breeding territorial aggression is persistent, whereas non-breeding territorial aggression is transient.
Acute inhibition of E2 synthesis significantly inhibits aggressive behavior in male song sparrows in the non-breeding season only (Soma et al., 2000). Further, acute administration of E2 lowers CREB phosphorylation in the medial preoptic nucleus, a brain area implicated in aggression in songbirds, in the non-breeding season only (Heimovics et al., 2012b). These data, taken together with the Peromyscus studies, raise the hypothesis that non-breeding territorial aggression in male song sparrows is transient because it is activated by non-genomic E2 signaling mechanisms. We test this hypothesis here using a non-invasive route of E2 administration to compare the rapid (within 20 min) non-genomic effects of E2 on aggressive behavior in captive male song sparrows during the non-breeding versus breeding season.
Section snippets
Subjects and housing
In the Pacific Northwest, song sparrows do not migrate, and males defend territories throughout the year (Arcese, 1989, Wingfield and Monk, 1992). Thus, conspecific song playback and mist nets were used to capture free-living adult male song sparrows both in late October/early November (non-breeding season) and in May (breeding season) near Vancouver, British Columbia (49° 12′N, 123° 01′W). After capture, subjects were transported to the University of British Columbia's Animal Care Centre Annex
Results
The mean (± standard error) latency to consume larva was 6. 8 ± 0. 1 sec (min = 0 sec, max = 22 sec). Latency to consume larva did not differ significantly between seasons or treatments.
Discussion
This study tested the hypothesis that non-breeding (but not breeding) season territorial aggression in male song sparrows is activated by non-genomic E2 signaling mechanisms. Consistent with this hypothesis, acute, non-invasive E2 administration significantly increased the number of barrier contacts made during a 10 min L-STI in non-breeding season subjects only. Because the effect of E2 on barrier contacts was seen less than 20 min after administration, it is likely that E2 acted via non-genomic
Conclusions
Animals living at temperate latitudes experience profound seasonal changes in physiology and behavior, but it is not uncommon for behaviors such as territorial aggression to be observed throughout the year. However, the function of and underlying motivational state accompanying these behaviors differ seasonally, and the present data taken with past work shows that the proximate mechanisms regulating these behaviors can differ seasonally as well. Non-genomic activation of E2-dependent behavior
Acknowledgments
We thank Nora Prior and Annika Sun for help with field work, Tal Kaikov for help with behavioral testing, the University of British Columbia Animal Care Centre Annex staff for help with animal care, Dr. Cathy Ma for assistance with the E2 assays, and Dr. Joanne Weinberg for the use of her gamma counter. This work was supported by postdoctoral fellowships to S. A. H. from the Canadian Institutes of Health Research (CIHR) and the Michael Smith Foundation for Heath Research and a CIHR Operating
References (68)
Territory acquisition and loss in male song sparrows
Anim. Behav.
(1989)- et al.
Plasma DHEA levels in wild, territorial red squirrels: seasonal variation and effect of ACTH
Gen. Comp. Endocrinol.
(2008) - et al.
Rapid behavioral response to corticosterone varies with photoperiod and dose
Horm. Behav.
(2000) - et al.
Noninvasive corticosterone treatment rapidly increases activity in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii)
Gen. Comp. Endocrinol.
(1998) - et al.
17beta-Estradiol levels in male zebra finch brain: combining Palkovits punch and an ultrasensitive radioimmunoassay
Gen. Comp. Endocrinol.
(2010) - et al.
Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain
Behav. Brain Res.
(2006) The vertebrate social behavior network: evolutionary themes and variations
Horm. Behav.
(2005)- et al.
Membrane-initiated estrogen signaling in hypothalamic neurons
Mol. Cell. Endocrinol.
(2008) - et al.
Estrogen modulation of G-protein-coupled receptors
Trends Endocrinol. Metab.
(1999) - et al.
Rapid effects of estrogen to modulate G protein-coupled receptors via activation of protein kinase A and protein kinase C pathways
Steroids
(1999)
Nongenomic effects of estradiol on aggression under short day photoperiods
Horm. Behav.
Rapid effects of estrogens on behavior: environmental modulation and molecular mechanisms
Front. Neuroendocrinol.
Estrogen receptors stimulate brain region specific metabotropic glutamate receptors to rapidly initiate signal transduction pathways
J. Chem. Neuroanat.
Membrane estradiol signaling in the brain
Front. Neuroendocrinol.
Role of brain norepinephrine in the behavioral response to stress
Prog. Neuropsychopharmacol. Biol. Psychiatry
Genotype/age interactions on aggressive behavior in gonadally intact estrogen receptor beta knockout (betaERKO) male mice
Horm. Behav.
Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season
Horm. Behav.
From social behavior to neural circuitry: steroid hormones rapidly modulate advertisement calling via a vocal pattern generator
Horm. Behav.
Rapid effects of corticosterone on cache recovery in mountain chickadees (Parus gambeli)
Horm. Behav.
Neurosteroids, immunosteroids, and the balkanization of endocrinology
Gen. Comp. Endocrinol.
Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression
Gen. Comp. Endocrinol.
Novel mechanisms for neuroendocrine regulation of aggression
Front. Neuroendocrinol.
The role of androgen receptors in regulating territorial aggression in male song sparrows
Horm. Behav.
Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice
Horm. Behav.
Gonadotropin-inhibitory hormone inhibits aggressive behavior of male quail by increasing neuroestrogen synthesis in the brain beyond its optimum concentration
Gen. Comp. Endocrinol.
Non-genomic actions of estrogens and their interaction with genomic actions in the brain
Front. Neuroendocrinol.
Combined effects of DHEA and fadrozole on aggression and neural VIP immunoreactivity in the non-breeding male song sparrow
Horm. Behav.
Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna
Horm. Behav.
Testosterone and territorial behavior in sedentary and migratory sparrows
Anim. Behav.
Differential induction and decay curves of c-fos and zif268 revealed through dual activity maps
Brain Res. Mol. Brain Res.
Characterization of the G-protein-coupled membrane-bound estrogen receptor GPR30 in the zebra finch brain reveals a sex difference in gene and protein expression
Dev. Neurobiol.
Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings
Endocrinology
Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain
J. Neuroendocrinol.
Rapid effects of aggressive interactions on aromatase activity and oestradiol in discrete brain regions of wild male white-crowned sparrows
J. Neuroendocrinol.
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