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1. Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions

   https://doi.org/10.1186/s13293-023-00534-7  

   Dai, Xiangyan ; Pradhan, Ajay ; Liu, Jiao ; Liu, Ruolan ; Zhai, Gang ; Zhou, Linyan ; Dai, Jiyan ; Shao, Feng ; Yuan, Zhiyong ; Wang, Zhijian ; et al ( August 2023 , Biology of Sex Differences)

   Sexually dimorphic mating behaviors differ between sexes and involve gonadal hormones and possibly sexually dimorphic gene expression in the brain. However, the associations among the brain, gonad, and sexual behavior in teleosts are still unclear. Here, we utilized germ cells-freetdrd12knockout (KO) zebrafish, and steroid synthesis enzymecyp17a1-deficient zebrafish to investigate the differences and interplays in the brain–gonad–behavior axis, and the molecular control of brain dimorphism and male mating behaviors.

   Tdrd12^+/−;cyp17a1^+/−double heterozygous parents were crossed to obtaintdrd12^−/−;cyp17a1^+/+(tdrd12 KO),tdrd12^+/+;cyp17a1^−/−(cyp17a1 KO), andtdrd12^−/−;cyp17a1^−/−(double KO) homozygous progenies. Comparative analysis of mating behaviors were evaluated using Viewpoint zebrafish tracking software and sexual traits were thoroughly characterized based on anatomical and histological experiments in these KOs and wild types. The steroid hormone levels (testosterone, 11-ketotestosterone and 17β-estradiol) in the brains, gonads, and serum were measured using ELISA kits. To achieve a higher resolution view of the differences in region-specific expression patterns of the brain, the brains of these KOs, and control male and female fish were dissected into three regions: the forebrain, midbrain, and hindbrain for transcriptomic analysis.

   Qualitative analysis of mating behaviors demonstrated thattdrd12^−/−fish behaved in the same manner as wild-type males to trigger oviposition behavior, whilecyp17a1^−/−and double knockout (KO) fish did not exhibit these behaviors. Based on the observation of sex characteristics, mating behaviors and hormone levels in these mutants, we found that the maintenance of secondary sex characteristics and male mating behavior did not depend on the presence of germ cells; rather, they depended mainly on the 11-ketotestosterone and testosterone levels secreted into the brain–gonad regulatory axis. RNA-seq analysis of different brain regions revealed that the brain transcript profile oftdrd12^−/−fish was similar to that of wild-type males, especially in the forebrain and midbrain. However, the brain transcript profiles ofcyp17a1^−/−and double KO fish were distinct from those of wild-type males and were partially biased towards the expression pattern of the female brain. Our results revealed important candidate genes and signaling pathways, such as synaptic signaling/neurotransmission, MAPK signaling, and steroid hormone pathways, that shape brain dimorphism and modulate male mating behavior in zebrafish.

   Our results provide comprehensive analyses and new insights regarding the endogenous interactions in the brain–gonad–behavior axis. Moreover, this study revealed the crucial candidate genes and neural signaling pathways of different brain regions that are involved in modulating brain dimorphism and male mating behavior in zebrafish, which would significantly light up the understanding the neuroendocrine and molecular mechanisms modulating brain dimorphism and male mating behavior in zebrafish and other teleost fish.

    

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2. Hormonal Prostaglandin F2α Mediates Behavioral Responsiveness to a Species-Specific Multi-component Male Hormonal Sex Pheromone in a Female Fish

   https://doi.org/10.1093/icb/icab061  

   Sorensen, Peter W ; Levesque, Haude M ( May 2021 , Integrative and Comparative Biology)

   Synopsis Although hormonally-derived female sex pheromones have been well described in approximately a dozen species of teleost fish, only a few male sex pheromones have been characterized and the neuroendocrine underpinnings of behavioral responsiveness to them is not understood. Herein, we describe a study that addresses this question using the goldfish, Carassius auratus, an important model species of how hormones drive behavior in egg-laying teleost fishes. Our study had four components. First, we examined behavioral responsiveness of female goldfish and found that when injected with prostaglandin F2α (PGF2α), a treatment that drives female sexual receptivity, and found that they became strongly and uniquely attracted to the odor of conspecific mature males, while non-PGF2α-treated goldfish did not discern males from females. Next, we characterized the complexity and specificity of the male pheromone by examining the responsiveness of PGF2α-treated females to the odor of either mature male conspecifics or male common carp odor, as well as their nonpolar and polar fractions. We found that the odor of male goldfish was more attractive than that of male common carp, and that its activity was attributable to both its nonpolar and polar fractions with the later conveying information on species-identity. Third, we hypothesized that androstenedione (AD), a 19-carbon sex steroid produced by all male fish might be the nonpolar fraction and tested whether PGF2α-treated goldfish were attracted to either AD alone or as part of a mixture in conspecific water. We found that while AD was inactive on its own, it became highly attractive when added to previously unattractive female conspecific water. Lastly, in a test of whether nonhormonal conspecific odor might determine species-specificity, we added AD to water of three species of fish and found that while AD made goldfish water strongly attractive, its effects on other species holding water were small. We conclude that circulating PGF2α produced at the time of ovulation induces behavioral sensitivity to a male sex pheromone in female goldfish and that this male pheromone is comprised of AD and a mixture of body metabolites. Because PGF2α commonly mediates ovulation and female sexual behavior in egg-laying fishes, and AD is universally produced by male fishes as a precursor to testosterone, we suggest that these two hormones may have similar roles mediating male–female behavior and communication in many species of fish. 

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3. Temperature fluctuations and estrone sulfate affect gene expression via different mechanisms to promote female development in a species with temperature-dependent sex determination

   https://doi.org/10.1242/jeb.244211  

   Marroquín-Flores, Rosario A. ; Paitz, Ryan T. ; Bowden, Rachel M. ( August 2022 , Journal of Experimental Biology)

   ABSTRACT Variation in developmental conditions can affect a variety of embryonic processes and shape a number of phenotypic characteristics that can affect offspring throughout their lives. This is particularly true of oviparous species where development typically occurs outside of the female, and studies have shown that traits such as survival and behavior can be altered by both temperature and exposure to steroid hormones during development. In species with temperature-dependent sex determination (TSD), the fate of gonadal development can be affected by temperature and by maternal estrogens present in the egg at oviposition, and there is evidence that these factors can affect gene expression patterns. Here, we explored how thermal fluctuations and exposure to an estrogen metabolite, estrone sulfate, affect the expression of several genes known to be involved in sexual differentiation: Kdm6b, Dmrt1, Sox9, FoxL2 and Cyp19A1. We found that most of the genes responded to both temperature and estrone sulfate exposure, but that the responses to these factors were not identical, in that estrone sulfate effects occur downstream of temperature effects. Our findings demonstrate that conjugated hormones such as estrone sulfate are capable of influencing temperature-dependent pathways to potentially alter how embryos respond to temperature, and highlight the importance of studying the interaction of maternal hormone and temperature effects. 

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4. Validation and effects of drying and prey hair on fecal hormone concentrations in spotted hyenas

   https://doi.org/10.1093/jmammal/gyab168  

   Greenberg, Julia R. ; Montgomery, Tracy M. ; Holekamp, Kay E. ; Beehner, Jacinta C. ; Hopkins, ed., Jack ( January 2022 , Journal of Mammalogy)

   As fecal steroid methods increasingly are used by researchers to monitor the physiology of captive and wild populations, we need to expand our validation protocols to test the effects of procedural variation and to identify contamination by exogenous sources of steroid hormones. Mammalian carnivore feces often contain large amounts of hair from the prey they consume, which itself may contain high concentrations of hormones. In this study, we report first a validation of two steroid hormone antibodies, corticosterone and progesterone, to determine fecal concentrations of these hormones in wild spotted hyenas (Crocuta crocuta). Next, we expand on these standard validation protocols to test two additional metrics: (i) whether hair from consumed prey or (ii) the specific drying method (oven incubation vs. lyophilization) affect steroid hormone concentrations in feces. In the first biological validation for the progesterone antibody in this species, progesterone concentrations met our expectations: (i) concentrations of plasma and fecal progesterone were lowest in immature females, higher in lactating females, and highest in pregnant females; (ii) across pregnant females, fecal progesterone concentrations were highest during late pregnancy; and (iii) among lactating females, fecal progesterone concentrations were highest after parturition. Our additional validation experiments indicated that contamination with prey hair and drying method are hormone-specific. Although prey hair did not release hormones into samples during storage or extraction for either hormone, its presence appeared to “dilute” progesterone (but not corticosterone) measures indirectly by increasing the dry weight of samples. In addition, fecal progesterone, but not corticosterone, values were lower for lyophilized than for incubated samples. Therefore, in addition to the standard analytical and biological validation steps, additional methodological variables need to be tested whenever we measure fecal hormone concentrations, particularly from predatory mammals.

    

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5. Neurogenomic landscape associated with status‐dependent cooperative behaviour

   https://doi.org/10.1111/mec.17327  

   Bolton, Peri E. ; Ryder, T. Brandt ; Dakin, Roslyn ; Houtz, Jennifer L. ; Moore, Ignacio T. ; Balakrishnan, Christopher N. ; Horton, Brent M. ( March 2024 , Molecular Ecology)

   The neurogenomic mechanisms mediating male–male reproductive cooperative behaviours remain unknown. We leveraged extensive transcriptomic and behavioural data on a neotropical bird species (Pipra filicauda) that performs cooperative courtship displays to understand these mechanisms. In this species, the cooperative display is modulated by testosterone, which promotes cooperation in non‐territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of three related traits: social status, cooperative display behaviour and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision‐making network (SDMN), and two key endocrine tissues that regulate social behaviour. We associated gene expression with each bird's behavioural and endocrine profile derived from 3 years of repeated measures taken from free‐living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex‐steroid and neuropeptide signalling appeared to be important in mediating status‐specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviours. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN‐wide gene expression differences between territorial and floater males that could form the basis of ‘status‐specific’ neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems‐level insights into the mechanisms of cooperative behaviour and suggest that differences in neurogenomic state are the basis for individual differences in social behaviour.

    

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