The crazy ovary 2: a tribute to Ken McNatty

In 2021, Ken McNatty, Danielle Monniaux, and I published a review essay illustrating how ovarian folliculogenesis can sometimes be bizarre, amazing, or even almost incomprehensible. Examples included the mechanisms underlying intra- and inter-species differences in ovulation rates; the possibility of awakening human primordial follicles in vitro, maturing and fertilizing them to produce viable offspring; and a model in which inactivation of a single oocyte gene results in sterile mice with follicular growth blocked at the primary stage but normal steroid cyclicity maintained. The aim of this second essay is to present further examples of the extraordinary diversity of ovarian function across animal species and, where possible, to propose hypotheses that may explain them. These concern: 1) the presence of oogonial stem cells in the ovaries of invertebrates and non-mammalian vertebrates, and their very probable absence in mammals; 2) the many and varied strategies of ovarian development and oogenesis in teleosts; 3)the metabolic dialog between cumulus cells and oocytes across mammalian species; 4) the presence of numerous germline genes, specifically or even exclusively expressed in the mammalian oocyte, whose invalidation has no phenotypic consequence on fertility in the mouse; 5) the unique features of ovarian function in the dog, particularly the frequent presence of polyovular follicles and the distinctive mode of post-ovulatory oocyte maturation; and 6) the absence of an intra-ovarian dominance factor in mono-ovulating species, disproving an old hypothesis: the selection of a single follicle is instead due to a succession of negative and then positive feedback between follicles and the hypothalamic-pituitary axis. This essay is also a final tribute to Ken McNatty, who liked to say that the ovary could be crazy.