bims-cebooc Biomed News
on Cell biology of oocytes
Issue of 2026–06–21
sixteen papers selected by
Gabriele Zaffagnini, Universität zu Köln
  1. Aging disrupts spatiotemporal coordination in the cycling murine ovary.
  2. NEDDylation maintains oocyte quality by stabilizing mitochondrial transcription.
  3. The oocyte-enriched metabolite serotonin alleviates cellular senescence and aging phenotypes in the mouse.
  4. Molecular evidence for early deuterostome origins of ovarian cell types and neuroendocrine control of reproduction.
  5. Ubiquitin-proteasome system regulates pro-crossover protein dynamics during meiosis in Caenorhabditis elegans.
  6. Mouse Oocyte In Vitro Maturation, Fertilization, and Culture of Preimplantation Embryos.
  7. An integrated transcriptional regulation from zygotic genome activation to the first lineage segregation.
  8. Discovery of a novel putative Cdc14b transcript in mouse oocytes.
  9. Alternative 3' UTRs and RNA-binding proteins Ewsr1b, HuR, and Syncrip organize sequential waves of translation to drive embryonic development.
  10. Meiotic pairing through barcode-like satellite DNA repeats.
  11. Reconstitution of germ cell and gonadal development for in vitro gamete production.
  12. An Asynchronous Production Line of Meiotic Prophase I in the Mouse Fetal Ovary.
  13. Common Principles Underlie Mitochondrial DNA Heteroplasmy Dynamics in the Germline and Soma.
  14. A mechanism of target mRNA selection and activity regulation in meiosis-related RBM46-MEIOC-YTHDC2 complex.
  15. DNA methylation reprogramming in marsupial embryos is restricted to the extraembryonic lineage.
  16. Basal cytoplasmic calcium levels regulate C. elegans germ stem cell proliferation.
  1. Nat Aging. 2026 Jun;6(6): 1244-1266
    Aging disrupts spatiotemporal coordination in the cycling murine ovary.
    Tammy C T Lan, Alison Kochersberger, Ruth Raichur, Sophia Szady, Hien Tran, Radiana Simeonova, Ashley Helmuth, Andrew Minagar, Maria José Orozco Fuentes, Vipin Kumar, Giovanni Marrero, Irving Barrera, Sarah Mangiameli, Alex K Shalek, Pardis C Sabeti, Fei Chen, David S Fischer, Jennifer L Garrison, Hattie Chung.
      Throughout the female reproductive lifespan, the ovary undergoes hundreds of cycles of follicle development, ovulation and tissue regeneration. How aging disrupts the coordination of such precise, multicellular interactions across time and space is not well understood. Using Slide-seq, a near-cellular spatial transcriptomics method, here we profile 22 mouse ovaries across the reproductive cycle and chronological ages, capturing 610,620 spots across 69 spatial profiles. We develop a novel segmentation pipeline to examine the multicellular dynamics of 358 oocytes, 668 follicles and 236 corpora lutea to find that aging impairs the spatial and temporal coordination required for folliculogenesis even before reproductive cycles cease. These disruptions are characterized by altered immune cell dynamics, inflammatory signaling and global tissue disorganization, which impair the cyclic remodeling required for ovarian function. Our findings reveal how multicellular niches orchestrate ovarian function and demonstrate that age-related breakdown in tissue organization precedes the end of fertility.
    DOI:  https://doi.org/10.1038/s43587-026-01140-z
  2. Sci Adv. 2026 Jun 19. 12(25): eaec3505
    NEDDylation maintains oocyte quality by stabilizing mitochondrial transcription.
    Avery A Ahmed, Tessa E Steenwinkel, Bethany K Patton, Peixin Jiang, Matthew D Meyer, Jaspreet K Rishi, Mei Leng, Alexander B Saltzman, Elizabeth S Anaya, Momal Sharif, Laurie J McKenzie, Laura Detti, Anna Malovannaya, Sean M Hartig, Stephanie A Pangas.
      Age-related decline in oocyte quality increases the risk of infertility, miscarriage, and birth defects. Mitochondrial dysfunction is a key contributor to this decline. Here, we report that oocyte-specific deletion of Uba3, which encodes the catalytic subunit of the E1 NEDDylation-activating complex, causes sterility in mice. Fully grown, germinal vesicle-stage Uba3 conditional knockout oocytes exhibit mitochondrial dysfunction, including elevated reactive oxygen species, impaired oxidative phosphorylation, and depletion of mitochondrially encoded RNA transcripts. Proteomic analysis identified alterations in mitochondrial-associated proteins, including enrichment of mitochondrial matrix and respiratory chain components and reduced abundance of electron transport chain complexes. These defects were associated with reduced levels of the mitochondrial RNA polymerase, POLRMT [polymerase (RNA) mitochondrial DNA directed]. We further show that POLRMT is directly modified by NEDDylation, which alters its stability by antagonizing ubiquitylation and degradation. Notably, NEDD8 levels decline with age in both mouse and human oocytes. Together, these findings identify NEDDylation as a regulator of oocyte quality and connect this pathway to mitochondrial transcription in oocytes.
    DOI:  https://doi.org/10.1126/sciadv.aec3505
  3. EMBO J. 2026 Jun 16.
    The oocyte-enriched metabolite serotonin alleviates cellular senescence and aging phenotypes in the mouse.
    Yuyan Xu, Ling Zhang, Xufeng Liao, Yuhang Fan, Rouyi Shao, Mengchen Wu, Li Zhang, Min Zhang, Gang Wang, Hailing Zhang, Enze Li, Qixin Wu, Jing Zhao, Jia Zhang, Wenjie Wang, Limeng Cai, Jinjie Zhong, Lidan Hu, Jingjing Wang, Jianhua Mao, Bing Yang, Jin Zhang.
      Whether metabolites enriched at early developmental stages affect cellular and organismal aging remains unclear. In this study, we comprehensively profiled the metabolic landscape of mouse oocytes in comparison to cleavage-stage embryos. Our analysis revealed that oocytes display accumulation of reductive metabolites that diminish following fertilization. Notably, we identified serotonin (5-hydroxytryptamine, 5-HT) as an oocyte-enriched metabolite with protective roles in aging. The underlying mechanisms operate through dual pathways: (i) in a canonical pathway serotonin acts via its receptor 5HTR1B to modulate mitochondrial function, and (ii) in a non-canonical pathway serotonin promotes serotonylation of HSP90β, which effectively reduces endoplasmic reticulum stress. Overall, our study demonstrates that oocyte-enriched metabolites including serotonin can alleviate aging-related cellular and systemic phenotypes, suggesting new avenues for anti-aging strategies.
    DOI:  https://doi.org/10.1038/s44318-026-00832-x
  4. Nat Commun. 2026 Jun 13.
    Molecular evidence for early deuterostome origins of ovarian cell types and neuroendocrine control of reproduction.
    Periklis Paganos, Beverly Naigles, Carsten Wolff, Danila Voronov, S Zachary Swartz.
      Oogenesis requires complex interactions between germline and somatic cell types in the ovary. How did these cell types and their signaling interactions evolve? Here we use the sea star Patiria miniata as a non-chordate deuterostome representative to define the ovarian cell type toolkit in echinoderms. Sea stars continuously produce millions of new oocytes throughout their lifespan, making them a practical system to understand the mechanisms that drive oogenesis from a biomedical and evolutionary perspective. We performed scRNA-seq combined with high-resolution 3D imaging to reveal the ovarian cell types and their spatial organization. Our data support the presence of putative oogonial stem cells, granulosa-like, and theca-like cells, which display similarities with their mammalian counterparts. We also describe possible signaling interactions between somatic and germ line cells. Lastly, our data may suggest an intrinsic ovarian neuroendocrine system which could potentially regulate oogenesis.
    DOI:  https://doi.org/10.1038/s41467-026-74401-5
  5. PLoS Biol. 2026 Jun 16. 24(6): e3003868
    Ubiquitin-proteasome system regulates pro-crossover protein dynamics during meiosis in Caenorhabditis elegans.
    Hongtao Zhang, Wenqing Liang, Meng Li, Yuejun Yang, Lei He, Wencong Nan, Guoteng Liu, Bin Wang, Ye Hong.
      Crossover (CO) formation ensures accurate segregation of homologous chromosomes during the first meiotic division. The pro-crossover proteins are essential for crossover formation and undergo dynamic changes during meiotic prophase I, although the underlying regulatory mechanism is largely unknown. Here, we found that the ubiquitin-proteasome system (UPS) plays a pivotal role in orchestrating pro-crossover protein dynamics and crossover patterning during meiosis in Caenorhabditis elegans. Knockdown of either the ubiquitin-activating enzyme E1 or the proteasome resulted in elevated pro-crossover protein levels and crossover designation. Impairing ubiquitination, but not proteasome activity, led to persistent association of pro-crossover proteins on meiotic chromosomes, a process mediated by the CDC-48UFD-1/NPL-4 segregase. Utilizing a hypomorphic allele of cosa-1, a well-characterized pro-crossover protein-encoding gene, we further demonstrate that the UPS restricts crossover formation. Collectively, our findings reveal a multilayered UPS-mediated regulatory network that maintains proper pro-crossover protein dynamics, thereby coordinating crossover formation with meiotic chromosome segregation.
    DOI:  https://doi.org/10.1371/journal.pbio.3003868
  6. J Vis Exp. 2026 May 29.
    Mouse Oocyte In Vitro Maturation, Fertilization, and Culture of Preimplantation Embryos.
    Debao Wang, Xueting Li, Haoran Sun, Yong Zhang, Jingcheng Zhang.
      Mouse oocyte in vitro maturation, combined with in vitro fertilization and subsequent embryo culture, enables the generation of preimplantation embryos under defined conditions. These procedures facilitate the investigation of the biological functions and molecular mechanisms underlying oocyte maturation, fertilization, and early embryo development. However, the successful application of this approach depends on careful handling of oocytes and sperm, appropriate culture conditions, and accurate assessment of developmental progression at each stage. Here, we describe methods for isolating immature cumulus-oocyte complexes (COCs) from mouse ovaries, in vitro maturation of oocytes, in vitro fertilization, and in vitro culture of embryos to the blastocyst stage. These procedures include preparing and equilibrating media and culture dishes, isolating and selecting COCs after ovarian dissection, collecting sperm and capacitating them, performing insemination under standardized conditions, and subsequently culturing embryos for developmental assessment. Developmental progression is evaluated using morphological criteria, including the formation of male and female pronuclei, cleavage to the two-cell stage, and blastocyst formation. This protocol can be integrated into studies of oocyte maturation and maternal factor function, providing a valuable tool for basic research in mammalian reproductive biology.
    DOI:  https://doi.org/10.3791/71053
  7. Curr Opin Genet Dev. 2026 Jun 15. pii: S0959-437X(26)00070-5. [Epub ahead of print]99 102503
    An integrated transcriptional regulation from zygotic genome activation to the first lineage segregation.
    Qixuan Shan, Hu Wang, Qi Wang, Junfeng Ji.
      Early embryogenesis is driven by precisely regulated transcriptional programs that guide the transition from a fertilized zygote to a multicellular organism. This process proceeds through sequential phases, beginning with zygotic genome activation and progressing toward lineage specification. Disruptions to these programs can result in developmental defects or even embryonic lethality. Recent advances in multiomic technologies have revealed how developmental genes are regulated at layers of transcription factors, histone modifications, three-dimensional (3D) genome, and transposable elements. Here, we review recent progress on the mechanistic understanding of transcriptional regulation in early embryos and discuss their implications for fundamental principles of embryogenesis.
    DOI:  https://doi.org/10.1016/j.gde.2026.102503
  8. Biol Reprod. 2026 Jun 17. pii: ioag130. [Epub ahead of print]
    Discovery of a novel putative Cdc14b transcript in mouse oocytes.
    Alex S Flynt, Neta Nnabuenyi, Cory Von Eiff, Turner Smith, Nicole J Camlin.
      
    Keywords:   Cdc14b ; Oocyte; isoform; transcript variant
    DOI:  https://doi.org/10.1093/biolre/ioag130
  9. Cell Rep. 2026 Jun 13. pii: S2211-1247(26)00635-2. [Epub ahead of print]45(6): 117557
    Alternative 3' UTRs and RNA-binding proteins Ewsr1b, HuR, and Syncrip organize sequential waves of translation to drive embryonic development.
    Keisuke Sato, Ludivine Fierro, Anyu Suginishi, Takahiro Sanada, Tomoya Kotani.
      Eggs of many species accumulate thousands of dormant mRNAs that are translated after fertilization at specific times and locations to direct development. However, how embryos coordinate translation of these mRNAs remains unclear. In this study, we identify sequential waves of translation critical for proper development progression. The first wave occurs within 1 h and includes translation of ewsr1b mRNA that harbors a short 3' untranslated region (UTR) comprising 16 nucleotides. The resulting Ewsr1b protein triggers the second translation wave through binding cytoplasmic mRNAs, including pou5f3, which encodes a transcription factor promoting zygotic genome activation. In contrast, HuR and Syncrip repress translation until the first and second waves, respectively. ewsr1b mRNA that has a long 3' UTR is translated in the second wave, and the 3' UTR's length determines protein localization and function. Overall, our findings reveal previously unknown molecular principles that coordinate translation timings and protein functions to drive long-term, multilayered processes.
    Keywords:  3′ UTR; CP: developmental biology; CP: molecular biology; Ewsr1b; HuR; RNA granule; RNA-binding protein; Syncrip; embryo; subcellular compartment; translation; vertebrate
    DOI:  https://doi.org/10.1016/j.celrep.2026.117557
  10. Nat Commun. 2026 Jun 16.
    Meiotic pairing through barcode-like satellite DNA repeats.
    Lena Skrutl, Ankita Chavan, Anna Sintsova, Ilaria Ceppi, Corin J Ropp, Shinichi Sunagawa, Petr Cejka, Madhav Jagannathan.
      During meiosis, chromosomes must find, pair, and synapse with their homologous partners in the crowded milieu of the nucleus. Although homology detection generally relies on recombination, pairing can occur in its absence, suggesting alternative mechanisms. Here, we show that the barcode-like arrangement of non-coding satellite DNA repeats facilitates homologue pairing during meiosis. Using satellite DNA deletion, duplication, and translocation strains, we demonstrate that repeat mismatches perturb meiotic pairing, particularly at centromeres and pericentromeres. Notably, pairing defects are also observed in the progeny of D. melanogaster natural populations that have diverged in their satellite DNA content. In the absence of satellite DNA homology, pairing is antagonised by the HORMAD protein, Mad2, while a Pachytene checkpoint 2 (Pch2)-dependent meiotic delay restores pairing. In addition, compromised meiotic pairing is strongly correlated with mid-oogenesis cell death, a quality control mechanism that likely culls defective oocytes to prevent chromosome mis-segregation and aneuploidy. Taken together, our findings reveal an important role for satellite DNA repeats during meiotic homology detection. We propose that this repeat-based pairing mechanism exerts an underappreciated selective pressure, constraining the divergence of rapidly evolving satellite DNA within interbreeding natural populations.
    DOI:  https://doi.org/10.1038/s41467-026-74398-x
  11. J Reprod Dev. 2026 ;72(3): 115-120
    Reconstitution of germ cell and gonadal development for in vitro gamete production.
    Katsuhiko Hayashi, Takashi Yosihno, Kenjiro Shirane.
      Germ cell formation involves a unique developmental trajectory in which diploid pluripotent cells are transformed into haploid gametes through a series of tightly regulated processes. This trajectory encompasses fundamental biological events, including extensive epigenetic remodeling, sexual fate determination, and meiotic division. Understanding the molecular and cellular mechanisms governing these processes is a fundamental challenge in reproductive biology and medicine, yet many aspects remain elusive. One long-standing strategy to overcome this limitation has been the establishment of in vitro gametogenesis that recapitulates germ cell development under defined culture conditions. In recent years, advances in stem cell biology have dramatically accelerated the development of such systems, opening new experimental platforms to dissect germ cell development. Beyond their value as research tools, these technologies also hold potential as alternative sources of gametes for animal reproduction and, perhaps, for human applications. In this review, we discuss the historical evolution of in vitro gametogenesis, highlight recent progress in the field, and outline the remaining technical and conceptual challenges.
    Keywords:  Gonadogenesis; In vitro gametogenesis; Sex determination
    DOI:  https://doi.org/10.1262/jrd.2026-009
  12. Exp Cell Res. 2026 Jun 15. pii: S0014-4827(26)00216-8. [Epub ahead of print] 115099
    An Asynchronous Production Line of Meiotic Prophase I in the Mouse Fetal Ovary.
    Ziyi Jin, Chang Liu, Gan Liu, Guofeng Feng, Jie Li, Yiwei Wu, Hao Jia, David L Keefe, Lin Liu.
      The initiation of meiosis in the female germline of mammals is a gradual process, but there is currently no clear quantitative framework for determining the precise timing of its onset. Here, we attempt to standardize the description of meiotic entry timing through a systematic, quantitative analysis of meiotic entry and progression in the mouse fetal ovary. Using dynamic expression profiling of key regulators Stra8, Sycp1, and Sycp3 alongside proliferation markers, we demonstrate that germ cells enter meiosis asynchronously and continuously between embryonic days E12.5 and E16.5. During this extended period, mitotic proliferation persists, indicating that germ cells are progressively recruited into the meiotic pathway rather than halting division simultaneously. Homologous chromosome synapsis, marked by Sycp1/Sycp3 co-localization, initiates at E14.5 and is completed prenatally by E18.5. Using stage-composition data, we constructed a continuous-time Markov chain model to infer a population-level meiotic stage clock. This model estimates approximately conserved population-level effective intervals from the modeled early-prophase L compartment to pachytene-stage synapsis (∼72 h) and to the late-prophase/dictyate-associated D-state transition (∼91 h) across modeled cohort-start times. Our findings refine the conventional view by quantitatively defining the extended window of meiotic entry and subsequent progression through prophase I.
    Keywords:  Stra8; Sycp1; Sycp3; meiotic initiation; synapsis
    DOI:  https://doi.org/10.1016/j.yexcr.2026.115099
  13. Annu Rev Genomics Hum Genet. 2026 Jun 15.
    Common Principles Underlie Mitochondrial DNA Heteroplasmy Dynamics in the Germline and Soma.
    Cameron Ryall, Patrick F Chinnery, Jelle van den Ameele.
      Heteroplasmy is the mixture of mutant and wild-type mitochondrial DNA (mtDNA) within each of our cells. Heteroplasmy levels in cells, tissues, and organisms change over time, thus contributing to mitochondrial disease, aging, and evolution. Germline and pedigree studies first revealed heteroplasmy shifts between generations and have long offered a window into the dynamics of mtDNA inheritance through single oocytes. Single-cell technologies are now uncovering similar mechanisms that operate in somatic tissues throughout life. Stochastic processes (relaxed replication and vegetative segregation, enhanced through genetic bottlenecks) generate cell-to-cell variation, while selection mechanisms such as intercellular competition, mitophagy, and preferential replication allow or drive directional shifts. Single-cell sequencing, mtDNA imaging, and genetic screening, combined with mtDNA-editing technology and heteroplasmic model systems, have transformed our ability to dissect these processes, revealing heteroplasmy dynamics at molecular resolution. These approaches are uncovering quantifiable principles governing heteroplasmy across cell types and life stages, transforming our understanding from descriptive observations to predictive mechanistic models and novel therapeutic avenues.
    DOI:  https://doi.org/10.1146/annurev-genom-120324-032239
  14. iScience. 2026 Jun 19. 29(6): 116234
    A mechanism of target mRNA selection and activity regulation in meiosis-related RBM46-MEIOC-YTHDC2 complex.
    Ruixin Liang, Qizi Chen, Jiawei Li, Han Liu, Yanqiu Ma, Shenglin Han, Yunxin Li, Jingyu Gao, Lan Ye, Jian Zhou.
      MEIOC and its two partners, RBM46 and YTHDC2, function as posttranscriptional regulators to promote mitotic-to-meiotic transition in mammalian germ cells. However, the molecular mechanism underlying target mRNA selection and degradation by MEIOC complex is largely unknown. Here, we demonstrate that exogenously expressed RBM46/MEIOC/YTHDC2 binds to Rad21 and Meioc 3'UTR and targets these transcripts for degradation in cultured somatic cells. YTHDC2 stabilizes MEIOC through inhibiting its ubiquitination, and the coiled-coil domain of MEIOC mediates its association with YTHDC2 and RBM46. The target mRNA is required for the interaction of RBM46 with YTHDC2. Moreover, MEIOC recruits XRN2 in the cytoplasm as the likely ribonuclease. We propose that MEIOC is a critical component that recruits RNA binding proteins for target mRNA selection and XRN2 for RNA degradation, and regulates the complex activity by modulating its mRNA and protein stability.
    Keywords:  Molecular mechanism of gene regulation; Molecular network
    DOI:  https://doi.org/10.1016/j.isci.2026.116234
  15. Nat Commun. 2026 Jun 15.
    DNA methylation reprogramming in marsupial embryos is restricted to the extraembryonic lineage.
    Allegra Angeloni, Jillian M Hammond, Timothy J Peters, Andre L M Reis, Leah Kemp, Timothy G Amos, Hasindu Gamaarachchi, Sam Humphries, Lynda A Wilmott, Suranjana Pal, V Pragathi Masamsetti, Megan Weatherstone, Chi Kin Ip, Karina Pazaky, Alice Steel, Ruth Lyons, Elly D Walters, Ning Liu, Patrick Tam, Jose M Polo, Paul D Waters, Susan J Clark, Linda J Richards, Andrew D Smith, Heather J Lee, Ira W Deveson, Oliver W Griffith, Ksenia Skvortsova.
      DNA methylation (5mC) is an epigenetic mark that plays a critical role in defining cell fate. Following fertilisation, DNA methylation inherited from gametes must be reprogrammed to establish totipotency and enable the parental-to-zygotic transition. To accomplish this, non-mammalian vertebrates such as zebrafish and medaka subtly reprogramme maternal 5mC profiles while maintaining high methylation levels throughout embryogenesis. In contrast, eutherian mammals such as mouse and human undergo global 5mC erasure in both embryonic and extraembryonic lineages. However, while embryonic 5mC is rapidly re-established to high levels upon implantation, the trophectoderm, which gives rise to the placenta, displays sustained and conserved DNA hypomethylation, suggesting that this drastic 5mC erasure may be functionally linked to complex placentation in mammals. To clarify whether extensive post-fertilisation 5mC erasure co-evolved with placentation, we explored embryonic methylation dynamics in marsupials, a lineage of therian mammals with a short-lived placenta. We produced a near complete telomere-to-telomere (T2T) genome and generated detailed epigenome maps of embryonic development for an Australian marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). We found the dunnart embryo exhibits genome wide DNA demethylation at the blastocyst stage, but these changes occur in the trophectoderm only, suggesting that 5mC erasure in the placenta is an ancestral state in therian mammals. Furthermore, the T2T-level dunnart genome assembly enabled identification of sex chromosomes, uncovering extensive hypomethylation of the paternally-inherited inactive X chromosome in females and revealing the previously unannotated master regulator of X chromosome inactivation, lncRNA RSX. Our data indicate that while the use of genome-wide 5mC erasure differs between eutherian and marsupial lineages, 5mC erasure in extraembryonic tissue is ancestral to therian mammals and may be necessary to support placental development.
    DOI:  https://doi.org/10.1038/s41467-026-73847-x
  16. Development. 2026 Jun 15. pii: dev.205301. [Epub ahead of print]
    Basal cytoplasmic calcium levels regulate C. elegans germ stem cell proliferation.
    Fariha J Khan, Parva M Vyas, Aahana N Shankaran, Alexandra C Wells, Corrissa J Velder, Rabia N Kaya, Anuj R Nagula, Edward T Kipreos.
      The C. elegans germline is one of the foremost models for the study of germ cell biology. We created an integrated ratiometric calcium reporter to assess calcium levels in the C. elegans germ line. The reporter reveals changes in basal cytoplasmic calcium levels during hermaphrodite sexual development. Oogenic cells have elevated calcium levels, while spermatogenic cells have significantly reduced levels of calcium. There are a small number of germ cells in the bend region of mid-to-late L4 hermaphrodite germ lines with elevated calcium levels that are correlated with the spermatogenesis-to-oogenesis transition. We identified GON-2 as a calcium channel that is required for the maintenance of normal calcium levels in the germline. Significantly, basal calcium levels correlate with germ cell proliferation. Starvation and inactivation of pro-proliferation signaling pathways reduce basal calcium levels, while proliferating germline tumor cells have elevated basal calcium levels. Experimentally altering calcium levels leads to a concomitant increase or decrease in the proliferation rate of germ stem cells. These results imply that basal cytoplasmic calcium acts as a rheostat to regulate germ stem cell proliferation.
    Keywords:  Basal calcium; Cell proliferation; Germ cells; Germline development; Sex determination
    DOI:  https://doi.org/10.1242/dev.205301
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