Elsevier

Hormones and Behavior

Volume 69, March 2015, Pages 31-38
Hormones and Behavior

Regular article
Non-invasive administration of 17β-estradiol rapidly increases aggressive behavior in non-breeding, but not breeding, male song sparrows

https://doi.org/10.1016/j.yhbeh.2014.11.012Get rights and content

Highlights

  • Seasonal plasticity in the nongenomic effects of E2 on aggression was investigated.

  • E2 was administered non-invasively (via wax moth larvae).

  • E2 rapidly increased territorial aggression in non-breeding male song sparrows only.

  • Demonstrates influence of physical environment on molecular mechanisms of behavior

Abstract

17β-Estradiol (E2) acts in the brain via genomic and non-genomic mechanisms to influence physiology and behavior. There is seasonal plasticity in the mechanisms by which E2 activates aggression, and non-genomic mechanisms appear to predominate during the non-breeding season. Male song sparrows (Melospiza melodia) display E2-dependent territorial aggression throughout the year. Field studies show that song sparrow aggression during a territorial intrusion is similar in the non-breeding and breeding seasons, but aggression after an intrusion ends differs seasonally. Non-breeding males stop behaving aggressively within minutes whereas breeding males remain aggressive for hours. We hypothesize that this seasonal plasticity in the persistence of aggression relates to seasonal plasticity in E2 signaling. We used a non-invasive route of E2 administration to compare the non-genomic (within 20 min) effects of E2 on aggressive behavior in captive non-breeding and breeding season males. E2 rapidly increased barrier contacts (attacks) during an intrusion by 173% in non-breeding season males only. Given that these effects were observed within 20 min of E2 administration, they likely occurred via a non-genomic mechanism of action. The present data, taken together with past work, suggest that environmental cues associated with the non-breeding season influence the molecular mechanisms through which E2 influences behavior. In song sparrows, transient expression of aggressive behavior during the non-breeding season is highly adaptive: it minimizes energy expenditure and maximizes the amount of time available for foraging. In all, these data suggest the intriguing possibility that aggression in the non-breeding season may be activated by a non-genomic E2 mechanism due to the fitness benefits associated with rapid and transient expression of aggression.

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

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