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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. Whole‐genome assembly and annotation for the little yellow croaker ( Larimichthys polyactis ) provide insights into the evolution of hermaphroditism and gonochorism

   https://doi.org/10.1111/1755-0998.13731  

   Xie, Qing‐Ping ; Zhan, Wei ; Shi, Jian‐Zhi ; Liu, Feng ; Niu, Bao‐Long ; He, Xue ; Liu, Meng ; Wang, Jing ; Liang, Qi‐Qi ; Xie, Yue ; et al ( November 2022 , Molecular Ecology Resources)

   The evolutionary direction of gonochorism and hermaphroditism is an intriguing mystery to be solved. The special transient hermaphroditic stage makes the little yellow croaker (Larimichthys polyactis) an appealing model for studying hermaphrodite formation. However, the origin and evolutionary relationship between ofL. polyactisandLarimichthys crocea, the most famous commercial fish species in East Asia, remain unclear. Here, we report the sequence of theL. polyactisgenome, which we found is ~706 Mb long (contig N50 = 1.21 Mb and scaffold N50 = 4.52 Mb) and contains 25,233 protein‐coding genes. Phylogenomic analysis suggested thatL. polyactisdiverged from the common ancestor,L. crocea, approximately 25.4 million years ago. Our high‐quality genome assembly enabled comparative genomic analysis, which revealed several within‐chromosome rearrangements and translocations, without major chromosome fission or fusion events between the two species. Thedmrt1gene was identified as the male‐specific gene inL. polyactis. Transcriptome analysis showed that the expression ofdmrt1and its upstream regulatory gene (rnf183) were both sexually dimorphic.Rnf183, unlike its two paraloguesrnf223andrnf225, is only present inLarimichthysandLatesbut not in other teleost species, suggesting that it originated from lineage‐specific duplication or was lost in other teleosts.Phylogenetic analysis shows that the hermaphrodite stage in maleL. polyactismay be explained by the sequence evolution ofdmrt1. Decoding theL. polyactisgenome not only provides insight into the genetic underpinnings of hermaphrodite evolution, but also provides valuable information for enhancing fish aquaculture.

    

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3. Gene expression differentiation in the reproductive tissues of Drosophila willistoni subspecies and their hybrids

   https://doi.org/10.1111/mec.16941  

   Ranz, José M. ; Go, Alwyn C. ; González, Pablo M. ; Clifton, Bryan D. ; Gomes, Suzanne ; Jaberyzadeh, Amirali ; Woodbury, Amanda ; Chan, Carolus ; Gandasetiawan, Kania A. ; Jayasekera, Suvini ; et al ( April 2023 , Molecular Ecology)

   Early lineage diversification is central to understand what mutational events drive species divergence. Particularly, gene misregulation in interspecific hybrids can inform about what genes and pathways underlie hybrid dysfunction. InDrosophilahybrids, how regulatory evolution impacts different reproductive tissues remains understudied. Here, we generate a new genome assembly and annotation inDrosophila willistoniand analyse the patterns of transcriptome divergence between two allopatrically evolvedD. willistonisubspecies, their male sterile and female fertile hybrid progeny across testis, male accessory gland, and ovary. Patterns of transcriptome divergence and modes of regulatory evolution were tissue‐specific. Despite no indication for cell‐type differences in hybrid testis, this tissue exhibited the largest magnitude of expression differentiation between subspecies and between parentals and hybrids. No evidence for anomalous dosage compensation in hybrid male tissues was detected nor was a differential role for the neo‐ and the ancestral arms of theD. willistoni Xchromosome. Compared to the autosomes, theXchromosome appeared enriched for transgressively expressed genes in testis despite being the least differentiated in expression between subspecies. Evidence for fine genome clustering of transgressively expressed genes suggests a role of chromatin structure on hybrid gene misregulation. Lastly, transgressively expressed genes in the testis of the sterile male progeny were enriched for GO terms not typically associated with sperm function, instead hinting at anomalous development of the reproductive tissue. Our thorough tissue‐level portrait of transcriptome differentiation between recently divergedD. willistonisubspecies and their hybrids provides a more nuanced view of early regulatory changes during speciation.

    

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4. Sex determination, sexual development, and sex change in slipper snails

   https://doi.org/10.1007/978-3-030-23459-1_7  

   Lesoway, MP and ( January 2019 , Results and problems in cell differentiation)

   Tworzydlo, W and (Ed.)

   Sex determination and sexual development are highly diverse and controlled by mechanisms that are extremely labile. While dioecy (separate male and female functions) is the norm for most animals, hermaphroditism (both male and female functions within a single body) is phylogenetically widespread. Much of our current understanding of sexual development comes from a small number of model systems, limiting our ability to make broader conclusions about the evolution of sexual diversity. We present the calyptraeid gastropods as a model for the study of the evolution of sex determination in a sequentially hermaphroditic system. Calyptraeid gastropods, a group of sedentary, filter-feeding marine snails, are sequential hermaphrodites that change sex from male to female during their life span (protandry). This transition includes resorption of the penis and the elaboration of female genitalia, in addition to shifting from production of spermatocytes to oocytes. This transition is typically under environmental control and frequently mediated by social interactions. Males in contact with females delay sex change to transition at larger sizes, while isolated males transition more rapidly and at smaller sizes. This phenomenon has been known for over a century; however, the mechanisms that control the switch from male to female are poorly understood. We review here our current understanding of sexual development and sex determination in the calyptraeid gastropods and other molluscs, highlighting our current understanding of factors implicated in the timing of sex change and the potential mechanisms. We also consider the embryonic origins and earliest expression of the germ line and the effects of environmental contaminants on sexual development. 

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5. miRNA analysis with Prost! reveals evolutionary conservation of organ-enriched expression and post-transcriptional modifications in three-spined stickleback and zebrafish

   https://doi.org/10.1038/s41598-019-40361-8  

   Desvignes, Thomas ; Batzel, Peter ; Sydes, Jason ; Eames, B. Frank ; Postlethwait, John H. ( March 2019 , Scientific Reports)

   MicroRNAs (miRNAs) can have organ-specific expression and functions; they can originate from dedicated miRNA genes, from non-canonical miRNA genes, or from mirror-miRNA genes and can also experience post-transcriptional variation. It remains unclear, however, which mechanisms of miRNA production or modification are organ-specific and the extent of their evolutionary conservation. To address these issues, we developed the softwareProst!(PRocessing Of Short Transcripts), which, among other features, helps quantify mature miRNAs, accounts for post-transcriptional processing, such as nucleotide editing, and identifies mirror-miRNAs. Here, we appliedProst!to annotate and analyze miRNAs in three-spined stickleback (Gasterosteus aculeatus), a model fish for evolutionary biology reported to have a miRNome larger than most teleost fish. Zebrafish (Danio rerio), a distantly related teleost with a well-known miRNome, served as comparator. Our results provided evidence for the existence of 286 miRNA genes and 382 unique mature miRNAs (excludingmir430gene duplicates and the vaultRNA-derivedmir733), which doesn’t represent a miRNAome larger than other teleost miRNomes. In addition, small RNA sequencing data from brain, heart, testis, and ovary in both stickleback and zebrafish identified suites of mature miRNAs that display organ-specific enrichment, many of which are evolutionarily-conserved in the brain and heart in both species. These data also supported the hypothesis that evolutionarily-conserved, organ-specific mechanisms may regulate post-transcriptional variations in miRNA sequence. In both stickleback and zebrafish, miR2188-5p was edited frequently with similar nucleotide changes in the seed sequence with organ specific editing rates, highest in the brain. In summary,Prost!is a new tool to identify and understand small RNAs, to help clarify a species’ miRNA biology as shown here for an important model for the evolution of developmental mechanisms, and to provide insight into organ-enriched expression and the evolutionary conservation of miRNA post-transcriptional modifications.

    

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