Cell division is crucial for the development of complex organisms, for the homeostasis of tissues, and for the reproductive capacity of individuals. While most somatic cells are diploid and proliferate through mitosis, multiplication of sexually reproducing species relies on haploid gametes that are generated through a specialized cell division process called meiosis. To achieve this reduction in ploidy, two rounds of chromosome segregation follow a single phase of genome replication. Inaccuracy in this process leads to gametes that carry an incorrect number of chromosomes and to aneuploid embryos after fertilization. In their vast majority, these are non-viable and lead to spontaneous abortion: defective meiotic division is therefore a major obstacle in achieving reproduction. However, the key principles that drive this process are still poorly understood, one main reason being the diversity of the molecular scenarios that have been adopted across evolution to regulate oocyte chromosome segregation. Unlike any other type of cell division, reductional meiosis I leads to the segregation of chromosomes and not sister chromatids. This requires sister kinetochores, the macromolecular assemblies that link each chromosome to spindle microtubules, to function as a single unit. How this meiotic adaptation, which is essential for successful gamete production and reproduction, is achieved remains unclear. To dissect the key components of successful oocyte meiotic chromosome segregation, we propose to carry out a multi-disciplinary approach, combining two powerful model organisms, the nematode Caenorhabditis elegans and mice, with the use of cutting edge high-resolution live and electron microscopy methods. C. elegans and mice both produce haploid oocytes, but display drastically different chromosomal and kinetochore architectures. Our common project should therefore also provide an evolutionary perspective on oocyte meiosis. For this, we will: (AIM1) analyse meiotic kinetochore assembly and composition by immunostaining, live cell imaging and super resolution microscopy. Microtubule attachment sites will be identified by 3D-electron tomography, and the site and amplitude of forces applied to meiotic kinetochores in meiosis I and II will be determined with FRET-based tension sensors. (AIM 2) we will then assess whether a structure physically fusing sister kinetochores can be detected by performing Serial Block Face-Scanning Electron Microscopy (SBF-SEM) on high pressure frozen oocytes to reconstruct the whole meiosis I kinetochore in 3D. We will ask whether co-orientation and fusion of sister kinetochores depend on centromere-localized cohesion, on recombination, and/or on a protein that was previously proposed to fuse kinetochores together in mouse oocyte meiosis I. (AIM 3) finally, we will determine whether the meiotic segregation pattern is determined intrinsically by the chromosomes and/or by the cell cycle stage of the oocyte. Functional data will be obtained by employing a large panel of mouse and C. elegans genetic tools that are already available in the two partner groups, and sophisticated multimodal and latest state of the art. The combined expertise of the two partners and the large panel of tools already generated by both teams should allow successful implementation of the project to generate results that will have important implications for our understanding of meiotic cell division in oocytes.