Competitive interactions often occur in series; therefore animals may respond to social challenges in ways that prepare them for success in future conflict. Changes in the production of the steroid hormone testosterone (T) are thought to mediate phenotypic responses to competition, but research over the past few decades has yielded mixed results, leading to several potential explanations as to why T does not always elevate following a social challenge. Here, we measured T levels in tree swallows (Tachycineta bicolor), a system in which females compete for limited nesting cavities and female aggression is at least partially mediated by T. We experimentally induced social challenges in two ways: (1) using decoys to simulate territorial intrusions and (2) removing subsets of nesting cavities to increase competition among displaced and territory-holding females. Critically, these experiments occurred pre-laying, when females are physiologically capable of rapidly increasing circulating T levels. However, despite marked aggression in both experiments, T did not elevate following real or simulated social challenges, and in some cases, socially challenged females had lower T levels than controls. Likewise, the degree of aggression was negatively correlated with T levels following a simulated territorial intrusion. Though not in line with the idea that social challenges prompt T elevation in preparation for future challenges, these patterns nevertheless connect T to territorial aggression in females. Coupled with past work showing that T promotes aggression, these results suggest that T may act rapidly to allow animals to adaptively respond to the urgent demands of a competitive event.
Seasonal plasticity in aggression is likely to be shaped by the contexts in which aggression is beneficial, as well as the constraints inherent in its underlying mechanisms. In males, seasonal plasticity in testosterone (T) secretion is thought to underlie seasonal plasticity in conspecific aggression, but it is less clear how and why female aggression may vary across different breeding stages. Here, we integrate functional and mechanistic perspectives to begin to explore seasonal patterns of conspecific aggression in female tree swallows (
- Award ID(s):
- 1656109
- NSF-PAR ID:
- 10460425
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ethology
- Volume:
- 125
- Issue:
- 8
- ISSN:
- 0179-1613
- Page Range / eLocation ID:
- p. 555-564
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Periods of social instability can elicit adaptive phenotypic plasticity to promote success in future competition. However, the underlying molecular mechanisms have primarily been studied in captive and laboratory-reared animals, leaving uncertainty as to how natural competition among free-living animals affects gene activity. Here, we experimentally generated social competition among wild, cavity-nesting female birds (tree swallows,
Tachycineta bicolor ). After territorial settlement, we reduced the availability of key breeding resources (i.e., nest boxes), generating heightened competition; within 24 h we reversed the manipulation, causing aggressive interactions to subside. We sampled females during the peak of competition and 48 h after it ended, along with date-matched controls. We measured transcriptomic and epigenomic responses to competition in two socially relevant brain regions (hypothalamus and ventromedial telencephalon). Gene network analyses suggest that processes related to energy mobilization and aggression (e.g., dopamine synthesis) were up-regulated during competition, the latter of which persisted 2 d after competition had ended. Cellular maintenance processes were also down-regulated after competition. Competition additionally altered methylation patterns, particularly in pathways related to hormonal signaling, suggesting those genes were transcriptionally poised to respond to future competition. Thus, experimental competition among free-living animals shifts gene expression in ways that may facilitate the demands of competition at the expense of self-maintenance. Further, some of these effects persisted after competition ended, demonstrating the potential for epigenetic biological embedding of the social environment in ways that may prime individuals for success in future social instability. -
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Abstract Many animal species exhibit year‐round aggression, a behaviour that allows individuals to compete for limited resources in their environment (eg, food and mates). Interestingly, this high degree of territoriality persists during the non‐breeding season, despite low levels of circulating gonadal steroids (ie, testosterone [T] and oestradiol [E2]). Our previous work suggests that the pineal hormone melatonin mediates a ‘seasonal switch’ from gonadal to adrenal regulation of aggression in Siberian hamsters (
Phodopus sungorus ); solitary, seasonally breeding mammals that display increased aggression during the short, ‘winter‐like’ days (SDs) of the non‐breeding season. To test the hypothesis that melatonin elevates non‐breeding aggression by increasing circulating and neural steroid metabolism, we housed female hamsters in long days (LDs) or SDs, administered them timed or mis‐timed melatonin injections (mimic or do not mimic a SD‐like signal, respectively), and measured aggression, circulating hormone profiles and aromatase (ARO) immunoreactivity in brain regions associated with aggressive or reproductive behaviours (paraventricular hypothalamic nucleus [PVN], periaqueductal gray [PAG] and ventral tegmental area [VTA]). Females that were responsive to SD photoperiods (SD‐R) and LD females given timed melatonin injections (Mel‐T) exhibited gonadal regression and reduced circulating E2, but increased aggression and circulating dehydroepiandrosterone (DHEA). Furthermore, aggressive challenges differentially altered circulating hormone profiles across seasonal phenotypes; reproductively inactive females (ie, SD‐R and Mel‐T females) reduced circulating DHEA and T, but increased E2after an aggressive interaction, whereas reproductively active females (ie, LD females, SD non‐responder females and LD females given mis‐timed melatonin injections) solely increased circulating E2. Although no differences in neural ARO abundance were observed, LD and SD‐R females showed distinct associations between ARO cell density and aggressive behaviour in the PVN, PAG and VTA. Taken together, these results suggest that melatonin increases non‐breeding aggression by elevating circulating steroid metabolism after an aggressive encounter and by regulating behaviourally relevant neural circuits in a region‐specific manner. -
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Abstract Individuals of virtually all vertebrate species are exposed to annual fluctuations in the deterioration and renewal of their environments. As such, organisms have evolved to restrict energetically expensive processes and activities to a specific time of the year. Thus, the precise timing of physiology and behavior is critical for individual reproductive success and subsequent fitness. Although the majority of research on seasonality has focused on seasonal reproduction, pronounced fluctuations in other non‐reproductive social behaviors, including agonistic behaviors (e.g., aggression), also occur. To date, most studies that have investigated the neuroendocrine mechanisms underlying seasonal aggression have focused on the role of photoperiod (i.e., day length); prior findings have demonstrated that some seasonally breeding species housed in short “winter‐like” photoperiods display increased aggression compared with those housed in long “summer‐like” photoperiods, despite inhibited reproduction and low gonadal steroid levels. While fewer studies have examined how the hormonal correlates of environmental cues regulate seasonal aggression, our previous work suggests that the pineal hormone melatonin acts to increase non‐breeding aggression in Siberian hamsters (
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Abstract Territorial aggression in birds is widely observed and is commonly linked to sex, age, body size, physiology, seasonal cues, food resource, urbanization, and a variety of social contexts including conspecific audience effects. However, little is known about the heterospecific audience effects on territorial aggression.
Here, we address an emerging idea that heterospecific audience effects may be pervasive influences in the social lives of free‐living birds. We tested the hypothesis that the composition, number, and relative body size of heterospecific audiences observing an aggressive contest will influence the response probability and intensity of aggression displayed.
We subjected two Paridae species, tufted titmouse (TUTI,
Baeolophus bicolor ) and Carolina chickadee (CACH,Poecile carolinensis ), to playbacks of aggressive calls during a breeding season in north‐central Florida. At widely spaced playback sites (N = 134) in woodland habitats, we characterized the makeup of heterospecific audiences, aggression type (intra vs. interspecific territoriality), local population density, and various environmental factors (tree density, wind speed, and noise level) that are likely to influence territorial aggression.We found that the presence of heterospecific audiences increased TUTI aggression levels and that both parids were more likely to respond to playback stimuli when their audiences had higher heterospecific diversity (more heterospecific individuals and species). We also found TUTI were more likely to respond when CACH were present but not vice versa.
In conclusion, we found evidence that heterospecific audiences significantly influenced the metrics of territorial aggression of free‐living animals and we suggest that the definition of audience effects on the behavior of free‐living animals be expanded to incorporate heterospecific audiences.
