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Food availability may be an environmental factor that modulates the expression of territorial aggression through neuropeptide Y (NPY) and neurosteroid signaling. A seasonal decrease in food availability increases NPY in the social behavior network (SBN). NPY may stimulate non-breeding territorial aggression directly, or via the production of neuroestrogens. In addition, a decrease in food availability may increase circulating precursors to neuroestrogens. Agonistic encounters also affect the neuroendocrine state as dominants show an increase in NPY and aromatase expression, which may reinforce the defense of the foraging territory.
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Aggression is an adaptive behavior that plays an important role in gaining access to limited resources. Aggression may occur uncoupled from reproduction, thus offering a valuable context to further understand its neural and hormonal regulation. This review focuses on the contributions from song sparrows (Melospiza melodia) and the weakly electric b...
Citations
... Angel Caputi, Ruben Budelli and their colleagues have applied a cognitive approach to understand the computations made by the brain to create and interpret electric images (Caputi et al., 1998;Budelli and Caputi, 2000). Gymnotus omarorum is also recognized as the best-understood teleost model for the study of neuroendocrine mechanisms of aggression uncoupled from reproduction (Silva et al., 2013;Quintana et al., 2021). The path embarked upon by the Omars was indeed expanded by the three generations of scientists who were trained under their influence and who keep their legacy alive (Fig. 2C). ...
South America is a vast continent endowed with extraordinary biodiversity that offers abundant opportunities for neuroethological research. Although neuroethology is still emerging in the region, the number of research groups studying South American species to unveil the neural organization of natural behaviors has grown considerably during the last decade. In this Perspective, we provide an account of the roots and strategies that led to the present state of neuroethology in the Southern Cone of America, with a forward-looking vision of its role in education and its international recognition. Hopefully, our Perspective will serve to further promote the study of natural behaviors across South America, as well as in other scarcely explored regions of the world.
... Endocrine and neuroendocrine systems play a crucial role in the regulation of social behaviour, including aggressiveness and the acquisition of social status (dominance vs. submission) in fish [44,[48][49][50]. However, the involvement of the melanocortin system in the regulation of social behaviour has been scarcely studied. ...
Simple Summary
Enhanced feeding can be associated with aggressive behaviour since food resources are the main reason for agonistic behaviour (any social behaviour related to fighting). The overexpression of the gene agouti-signalling protein (Asip1) in transgenic zebrafish (asip1-Tg) results in enhanced food intake and linear growth. Our next question was if asip1-Tg animals exhibit a dominant phenotype associated with the feeding-enhanced levels when compared to wild-type (WT) fish. To address this question, we quantified the aggressive behaviour by conducting dyadic fights with real opponents as well as by exposing the animals to their specular image using mirrors. The results indicate that asip1-Tg are less aggressive than WT zebrafish in both dyadic fights and mirror-stimulus tests. These findings provide direct evidence of the role of the melanocortin system in the regulation of fish behaviour. The subordinate personality observed in asip1-Tg suggests that this transgene would be non-threatening to native populations in the event of an escape from aquaculture facilities. These results provide a genetic modification strategy to enhance growth in fish through high feeding motivation without promoting aggressiveness. This suggests that inhibiting the melanocortin system could be a viable target for genetically engineered fish. It is worth noting that the regulatory approval for such genetically engineered fish would be subject to the guidelines and regulations of the U.S. Food and Drug Association.
Abstract
Feeding motivation plays a crucial role in food intake and growth. It closely depends on hunger and satiation, which are controlled by the melanocortin system. Overexpression of the inverse agonist agouti-signalling protein (ASIP) and agouti-related protein (AGRP) leads to enhanced food intake, linear growth, and weight. In zebrafish, overexpression of Agrp leads to the development of obesity, in contrast to the phenotype observed in transgenic zebrafish that overexpress asip1 under the control of a constitutive promoter (asip1-Tg). Previous studies have demonstrated that asip1-Tg zebrafish exhibit larger sizes but do not become obese. These fish display increased feeding motivation, resulting in a higher feeding rate, yet a higher food ration is not essential in order to grow larger than wild-type (WT) fish. This is most likely attributed to their improved intestinal permeability to amino acids and enhanced locomotor activity. A relationship between high feeding motivation and aggression has been previously reported in some other transgenic species showing enhanced growth. This study aims to elucidate whether the hunger observed in asip1-Tg is linked to aggressive behaviour. Dominance and aggressiveness were quantified using dyadic fights and mirror-stimulus tests, in addition to the analysis of basal cortisol levels. The results indicate that asip1-Tg are less aggressive than WT zebrafish in both dyadic fights and mirror-stimulus tests.
... In song sparrows, aromatase is highly expressed in the SBN and varies seasonally (Soma et al., 2003;Wacker, 2019). Altogether, these data suggest that seasonal changes in neuroestrogen synthesis contribute to seasonal changes in territorial aggression in song sparrows (Jalabert et al., 2018;Quintana et al., 2021). To measure estrogens in specific regions of the SBN, a highly specific and sensitive method is required. ...
Neuroestrogens are synthesized within the brain and regulate social behavior, learning and memory, and cognition. In song sparrows, Melospiza melodia, 17β-estradiol (17β-E2) promotes aggressive behavior, including during the nonbreeding season when circulating steroid levels are low. Estrogens are challenging to measure because they are present at very low levels, and current techniques often lack the sensitivity required. Furthermore, current methods often focus on 17β-E2 and disregard other estrogens. Here, we developed and validated a method to measure four estrogens [estrone (E1), 17β-E2, 17α-estradiol (17α-E2), estriol (E3)] simultaneously in microdissected songbird brain, with high specificity, sensitivity, accuracy, and precision. We used liquid chromatography tandem mass spectrometry (LC-MS/MS), and to improve sensitivity, we derivatized estrogens using 1,2-dimethylimidazole-5-sulfonyl-chloride (DMIS). The straightforward protocol improved sensitivity by 10-fold for some analytes. There is substantial regional variation in neuroestrogen levels in brain areas that regulate social behavior in male song sparrows. For example, the auditory area NCM, which has high aromatase levels, has the highest E1 and 17β-E2 levels. In contrast, estrogen levels in blood are very low. Estrogen levels in both brain and circulation are lower in the nonbreeding season than in the breeding season. This technique will be useful for estrogen measurement in songbirds and potentially other animal models.
... Aggression is perhaps one of the most extensively studied social behaviors with respect to seasonal changes in the brain and behavior (fishesreviewed in Quintana et al., 2021;Silva et al., 2020; amphibians and reptilesreviewed in Wilczynski et al., 2017;birdsreviewed in Heimovics et al., 2018;Wingfield et al., 2018;mammalsreviewed in Munley et al., 2018;Soma et al., 2015). Aggressive behavior is universally exhibited across animal taxa and enables individuals to compete for access to limited resources in their environment (e.g., territories, mates, and food; Jalabert et al., 2018;Nelson, 2006). ...
... Although fewer studies have investigated the neural actions of sex steroids on seasonal aggression in fishes, there is some support that these neuroendocrine mechanisms may be evolutionarily conserved across vertebrates, particularly in weakly electric fish (reviewed in Quintana et al., 2021;Silva et al., 2020). In the solitary species Gymnotus omarorum, non-breeding males display high levels of aggression despite low plasma 11-KT levels, and this behavioral phenotype is independent of gonadal steroids. ...
Many animals show pronounced changes in physiology and behavior across the annual cycle, and these adaptations enable individuals to prioritize investing in the neuroendocrine mechanisms underlying reproduction and/or survival based on the time of year. While prior research has offered valuable insight into how seasonal variation in neuroendocrine processes regulates social behavior, the majority of these studies have investigated how a single hormone influences a single behavioral phenotype. Given that hormones are synthesized and metabolized via complex biochemical pathways and often act in concert to control social behavior, these approaches provide a limited view of how hormones regulate seasonal changes in behavior. In this review, we discuss how seasonal influences on hormones, the brain, and social behavior can be studied using liquid chromatography-tandem mass spectrometry (LC-MS/MS), an analytical chemistry technique that enables researchers to simultaneously quantify the concentrations of multiple hormones and the activities of their synthetic enzymes. First, we examine studies that have investigated seasonal plasticity in brain-behavior interactions, specifically by focusing on how two groups of hormones, sex steroids and nonapeptides, regulate sexual and aggressive behavior. Then, we explain the operations of LC-MS/MS, highlight studies that have used LC-MS/MS to study the neuroendocrine mechanisms underlying social behavior, both within and outside of a seasonal context, and discuss potential applications for LC-MS/MS in the field of behavioral neuroendocrinology. We propose that this cutting-edge technology will provide a more comprehensive understanding of how the multitude of hormones that comprise complex neuroendocrine networks affect seasonal variation in the brain and behavior.
Individual variation in the timing of activities is increasingly being reported for a wide variety of species, often measured as the timing of activity onset in the morning. However, so far, the adaptive significance of consistent variation in temporal phenotypes (i.e. the chronotype) remains largely elusive. Potentially, differences in timing of activities may arise as a result of competition among individuals for resources. Less aggressive individuals may try to avoid competition by becoming active earlier during the day when other individuals are still inactive, leading to a positive correlation between chronotype and aggressive personality type (i.e. a behavioural syndrome). To investigate this, we assessed the chronotype of female great tits, Parus major, by measuring emergence time from the nestbox in the morning and experimentally tested their levels of same-sex aggression through simulated territorial intrusion tests. Contradicting our initial hypothesis, consistently more aggressive females became active earlier during the day compared to less aggressive females, which could be caused by shared underlying mechanisms, like pleiotropic effects of sex hormones or gene pleiotropy, which potentially impose constraints on the independent evolution of both traits. Surprisingly, on the within-individual level we found an opposing correlation between emergence time and aggression. Our findings highlight the need for further investigations into the interplay between chronotype and aggression that take the underlying mechanisms into account in order to understand the adaptive significance of this trait association.
Sex is ubiquitous and variable throughout the animal kingdom. Historically, scientists have used reductionist methodologies that rely on a priori sex categorizations, in which two discrete sexes are inextricably linked with gamete type. However, this binarized operationalization does not adequately reflect the diversity of sex observed in nature. This is due, in part, to the fact that sex exists across many levels of biological analysis, including genetic, molecular, cellular, morphological, behavioral, and population levels. Furthermore, the biological mechanisms governing sex are embedded in complex networks that dynamically interact with other systems. To produce the most accurate and scientifically rigorous work examining sex in neuroendocrinology and to capture the full range of sex variability and diversity present in animal systems, we must critically assess the frameworks, experimental designs, and analytical methods used in our research. In this perspective piece, we first propose a new conceptual framework to guide the integrative study of sex. Then, we provide practical guidance on research approaches for studying sex-associated variables, including factors to consider in study design, selection of model organisms, experimental methodologies, and statistical analyses. We invite fellow scientists to conscientiously apply these modernized approaches to advance our biological understanding of sex and to encourage academically and socially responsible outcomes of our work. By expanding our conceptual frameworks and methodo-logical approaches to the study of sex, we will gain insight into the unique ways that sex exists across levels of biological organization to produce the vast array of variability and diversity observed in nature.
Steroids play a crucial role in modulating brain and behavior. While traditionally it is thought that the brain is a target of sex steroids produced in endocrine glands (e.g. gonads), the brain itself produces steroids, known as neurosteroids. Neurosteroids can be produced in regions involved in the regulation of social behaviors and may act locally to regulate social behaviors, such as reproduction and aggression. Our model species, the weakly electric fish Gymnotus omarorum , displays non-breeding aggression in both sexes. This is a valuable natural behavior to understand neuroendocrine mechanisms that differ from those underlying breeding aggression. In the non-breeding season, circulating sex steroid levels are low, which facilitates the study of neurosteroids. Here, for the first time in a teleost fish, we used liquid chromatography-tandem mass spectrometry (LC-MS/MS) to quantify a panel of 8 steroids in both plasma and brain to characterize steroid profiles in wild non-breeding adult males and females. We show that: 1) systemic steroid levels in the non-breeding season are similar in both sexes, although only males have detectable circulating 11-ketotestosterone, 2) brain steroid levels are sexually dimorphic, as females display higher levels of androstenedione, testosterone and estrone, and only males had detectable 11-ketotestosterone, 3) systemic androgens such as androstenedione and testosterone in the non-breeding season are potential precursors for neuroestrogen synthesis, and 4) estrogens, which play a key role in non-breeding aggression, are detectable in the brain (but not the plasma) in both sexes. These data are consistent with previous studies of G . omarorum that show non-breeding aggression is dependent on estrogen signaling, as has also been shown in bird and mammal models. Overall, our results provide a foundation for understanding the role of neurosteroids, the interplay between central and peripheral steroids and potential sex differences in the regulation of social behaviors.
Many animals live in highly social environments, in which individuals must behave in a way that enables them to survive and live harmoniously among conspecifics. Dominance hierarchies are typical among social species and are essential for determining and preserving stability within social groups. Although there is considerable evidence that sex steroid hormones regulate behaviors associated with dominance, such as aggression and mating, fewer studies have examined the role of these hormones in controlling social status, especially in species that exhibit social hierarchies. Furthermore, despite this research, we know remarkably little about the precise neural and molecular mechanisms through which sex steroids modulate traits associated with social rank. Here, we review the neuroendocrine regulation of social status by sex steroids in teleost fishes, the largest and most diverse vertebrate group that shows extensive variation in reproductive systems and social structures between species. First, we describe the function of sex steroids and novel steroid-related genes that teleost fishes possess due to a lineage-specific whole-genome duplication event. Then, we discuss correlational, pharmacological, and molecular genetic studies on the control of social status by sex steroids in teleost fishes, including recent studies that have implemented gene editing technologies, such as CRISPR/Cas9. Finally, we argue that gene editing approaches in teleost studies, within both integrative and comparative frameworks, will be vital for elucidating the role of sex steroids in controlling social rank and characterizing their neural and molecular mechanisms of action. Collectively, ongoing and future research in these species will provide novel insight into the evolution of the regulation of social status by sex steroids and other neuroendocrine substrates across vertebrates.
