Elevated cortical tension triggers precocious ectopic polarization in mammalian oocytes, associated with lower developmental potential.

Abstract

Oocytes from many organisms polarize early during development, unlike mammalian oocytes. The significance of maintaining this homogeneous state in mammals remains unclear. We show that elevated cortical tension, via increased actomyosin contractility or disrupted cortical architecture, induces precocious cortical polarization mid-meiosis I, with an ectopic actomyosin-rich domain opposite the future division site. This polarization generates directional cytoplasmic flows that displace organelles and the spindle, accelerating its migration and disrupting its orientation. A hydrodynamic model coupling the polarized cortex to a viscous cytoplasm accounts for these rearrangements. Ectopic polarization persists in meiosis II and is associated with mislocalization of fertilization factors, increased fertilization rates and polyspermy, and reduced early embryonic development. A similar morphological signature arises spontaneously in subsets of mouse and human oocytes. These results reveal precocious cortical polarization as a previously unrecognized, mechanically accessible state largely absent from mammalian oocytes, which may contribute to variability in oocyte quality.