Culture systems that support development and maturation of oocytes in vitro with a high efficiency would have great impact not only on research addressed at underlying mechanisms of oocyte development but also on preservation of fertility. Recently, attention has turned to using culture systems that preserve follicle integrity, in contrast to existing systems that do not maintain follicle integrity, with the hope of improving oocyte development. We report that an alginate-based follicle culture system supports both follicular and oocyte growth in vitro, with little effect on the oocyte transcriptome. Nevertheless, oocytes obtained from these follicles exhibit an increased incidence of defects in spindle formation and chromosome alignment as well as pronounced abnormalities in cortical granule biogenesis. Developmental competence is also highly compromised, because few matured oocytes develop into 1-cell embryos with pronuclei. This situation contrasts with a high incidence of pronuclear formation following development using an existing in vitro culture system that does not preserve follicle integrity.