Forebrain Transcriptional Response to Transient Changes in Circulating Androgens in a Cichlid Fish

Abstract

21It has been hypothesized that androgens respond to the social interactions as a way to adjust 22 the behaviour of individuals to the challenges of the social environment in an adaptive 23 manner. 24 Therefore, it is expected that transient changes in circulating androgen levels within 25 physiological scope should impact the state of the brain network that regulates social 26 behavior, which should translate into adaptive behavioural changes. Here, we examined the 27 effect that a transient peak in androgen circulating levels, which mimics socially driven 28 changes in androgen levels, has on the forebrain state, which harbors most nuclei of the social 29 decision-making network. For this purpose, we successfully induced transient changes in 30 circulating androgen levels in an African cichlid fish (Mozambique tilapia, Oreochromis 31 mossambicus) commonly used as a model in behavioral neuroendocrinology by injecting 11-32 ketotestosterone or testosterone, and compared the forebrain transcriptome of these 33 individuals to control fish injected with vehicle. Forebrain samples were collected 30 min and 34 60 min after injection and analyzed using RNAseq. Our results showed that a transient peak in 35 11-ketotestosterone drives more accentuated changes in forebrain transcriptome than 36 testosterone, and that transcriptomic impact was greater at the 30 min than at the 60 min post-37 androgen administration. Several genes involved in the regulation of translation, steroid 38 metabolism, ion channel membrane receptors, and genes involved in epigenetic mechanisms 39 were differentially expressed after 11-ketotestosterone or testosterone injection. In summary, 40 this study identified specific candidate genes that may regulate socially driven changes in 41 behavioural flexibility mediated by androgens. 42 130 Animals and housing 131O. mossambicus adult males from a stock held at ISPA were used in this experiment. Fish 132 were maintained in glass tanks (120 x 40 x 50 cm, 240 l) with a fine gravel substrate. Tanks 133 were supplied with a double filtering system (gravel and external biofilter) and constant 134 aeration. Water quality was analyzed twice per month for nitrites (0.2-0.5 ppm), ammonia 135 (<0.5 ppm, Pallintest kit) and pH (6.0 -6.2). Fish were kept at a temperature of 26 ± 2 ºC, a 136 12L:12D photoperiod, and fed with commercial cichlid floating sticks. Ninety-nine focal 137

From silence to song: Testosterone triggers extensive transcriptional changes in the female canary HVC

“…The scale of gene regulation observed in this study far exceeds previous reports in CNS literature, which typically identify fewer than 2,000 differentially expressed genes 13,14,[40][41][42][43][44][45][46][47][48][49][50] . This discrepancy may be attributed to the high expression of androgen and estrogen receptors in HVC neurons 21,22,51,52 and the cellular diversity of the HVC 53 .…”

“…The extensive effects of testosterone on HVC gene expression surpassed our expectations, as we did not expect such a large number of differentially expressed genes. A comparison of our results with other studies on the effects of testosterone treatment or seasonal phenotypes on the transcriptomes of both peripheral tissues and the central nervous system in other animals, including birds, amphibians, fish, and rodents, revealed that typically far fewer differentially expressed genes are reported, with most studies reporting fewer than 2000 genes (Bao et al, 2019; Bissegger et al, 2014; Carrier et al, 2015; Cheviron and Swanson, 2017; Dopico et al, 2015; Faber-Hammond et al, 2015; Félix et al, 2020; Morey et al, 2016; Peterson et al, 2013; Quintela et al, 2015; Sharma et al, 2019; Zhang et al, 2016; Zhao et al, 2021). A comparably large effect was only reported for seasonal changes in the testes (Tian et al, 2019).…”

Aggressive but not reproductive boldness in male green anole lizards correlates with baseline vasopressin activity

“…The mechanisms that underlie boldness during social encounters likely involve the social decision-making network (Newman, 1999;Hofmann, 2012, 2011) and its various neuroendocrine mediators (Baugh et al, 2012;Félix et al, 2020;Ketterson and Nolan Val, 1999) that are conserved across vertebrates. The mediators linked to individual variability in behavioral phenotype include steroid hormones (Koolhaas et al, 2010;Sluyter et al, 1996;Tudorache et al, 2018;Veenema et al, 2004Veenema et al, , 2003, various neuropeptide and neurotransmitter systems (Thörnqvist et al, 2019;Veenema et al, 2004), and their associated receptors (Alfonso et al, 2019;Kabelik et al, 2021;Kanitz et al, 2019).…”

Social boldness correlates with brain gene expression in male green anoles

“…Such behavioral phenotypes, also referred to as behavioral syndromes, personalities, or coping styles (Koolhaas et al, 1999; Réale et al, 2010; Sih et al, 2004), often manifest as correlated suites of behavioral outputs, presumably due to regulation by shared neural underpinnings. The neural substrates that lead an individual toward exhibiting a bold or shy phenotype likely rely on brain regions involved in social decision-making (Newman, 1999; O’Connell and Hofmann, 2011, 2012), and neuroendocrine mediators of these circuits (Baugh et al, 2012; Félix et al, 2020; Ketterson and Nolan Val, 1999). Although numerous neural systems have been associated with social behavioral output, the bases of stable bold-shy behavioral phenotypes remain poorly understood.…”

“…Although a continuum of such behavioral propensity usually exists within a population, we can categorize individuals at each end of such a continuum as either behaviorally 'bold' or 'shy', with bold individuals exhibiting lower latency, higher frequency, and higher intensity of exhibited social behaviors across contexts than shy individuals. Such behavioral phenotypes, also referred to as behavioral syndromes, personalities, or coping styles 2012, 2011) and neuroendocrine mediators of these circuits (Baugh et al, 2012;Félix et al, 2020;Ketterson and Nolan Val, 1999). Although numerous neural systems have been associated with social behavioral output, the specific proximate variables that determine stable bold-shy behavioral phenotypes remain unknown.…”