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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. Individual variation in preference behavior in sailfin fish refines the neurotranscriptomic pathway for mate preference

   https://doi.org/10.1002/ece3.10323  

   Young, Rebecca L. ; Price, Sarah M. ; Schumer, Molly ; Wang, Silu ; Cummings, Molly E. ( July 2023 , Ecology and Evolution)

   Social interactions can drive distinct gene expression profiles which may vary by social context. Here we use female sailfin molly fish (Poecilia latipinna) to identify genomic profiles associated with preference behavior in distinct social contexts: male interactions (mate choice) versus female interactions (shoaling partner preference). We measured the behavior of 15 females interacting in a non‐contact environment with either two males or two females for 30 min followed by whole‐brain transcriptomic profiling by RNA sequencing. We profiled females that exhibited high levels of social affiliation and great variation in preference behavior to identify an order of magnitude more differentially expressed genes associated with behavioral variation than by differences in social context. Using a linear model (limma), we took advantage of the individual variation in preference behavior to identify unique gene sets that exhibited distinct correlational patterns of expression with preference behavior in each social context. By combining limma and weighted gene co‐expression network analyses (WGCNA) approaches we identified a refined set of 401 genes robustly associated with mate preference that is independent of shoaling partner preference or general social affiliation. While our refined gene set confirmed neural plasticity pathways involvement in moderating female preference behavior, we also identified a significant proportion of discovered that our preference‐associated genes were enriched for ‘immune system’ gene ontology categories. We hypothesize that the association between mate preference and transcriptomic immune function is driven by the less well‐known role of these genes in neural plasticity which is likely involved in higher‐order learning and processing during mate choice decisions.

    

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3. Neurogenomic insights into paternal care and its relation to territorial aggression

   https://doi.org/10.1038/s41467-019-12212-7  

   Bukhari, Syed Abbas ; Saul, Michael C. ; James, Noelle ; Bensky, Miles K. ; Stein, Laura R. ; Trapp, Rebecca ; Bell, Alison M. ( September 2019 , Nature Communications)

   Motherhood is characterized by dramatic changes in brain and behavior, but less is known about fatherhood. Here we report that male sticklebacks—a small fish in which fathers provide care—experience dramatic changes in neurogenomic state as they become fathers. Some genes are unique to different stages of paternal care, some genes are shared across stages, and some genes are added to the previously acquired neurogenomic state. Comparative genomic analysis suggests that some of these neurogenomic dynamics resemble changes associated with pregnancy and reproduction in mammalian mothers. Moreover, gene regulatory analysis identifies transcription factors that are regulated in opposite directions in response to a territorial challenge versus during paternal care. Altogether these results show that some of the molecular mechanisms of parental care might be deeply conserved and might not be sex-specific, and suggest that tradeoffs between opposing social behaviors are managed at the gene regulatory level.

    

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4. 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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5. Social network differences and phenotypic divergence between stickleback ecotypes

   https://doi.org/10.1093/beheco/arad009  

   Neumann, Kevin M. ; Bell, Alison M. ; Briffa, ed., Mark ( March 2023 , Behavioral Ecology)

   Elucidating the mechanisms underlying differentiation between populations is essential to our understanding of ecological and evolutionary processes. While social network analysis has yielded numerous insights in behavioral ecology in recent years, it has rarely been applied to questions about population differentiation. Here, we use social network analysis to assess the potential role of social behavior in the recent divergence between two three-spined stickleback ecotypes, “whites” and “commons”. These ecotypes differ significantly in their social behavior and mating systems as adults, but it is unknown when or how differences in social behavior develop. We found that as juveniles, the white ecotype was bolder and more active than the common ecotype. Furthermore, while there was no evidence for assortative shoaling preferences, the two ecotypes differed in social network structure. Specifically, groups of the white ecotype had a lower clustering coefficient than groups of the common ecotype, suggesting that groups of the white ecotype were characterized by the formation of smaller subgroups, or “cliques”. Interestingly, ecotypic differences in the clustering coefficient were not apparent in mixed groups composed of whites and commons. The formation of cliques could contribute to population divergence by restricting the social environment that individuals experience, potentially influencing future mating opportunities and preferences. These findings highlight the insights that social network analysis can offer into our understanding of population divergence and reproductive isolation.

    

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