Reproductive neuroendocrinology of the female South American plains vizcacha, Lagostomus maximus

Abstract

Female plains vizcachas have several peculiar reproductive characteristics as a true reactivation of the hypothalamic–pituitary–ovarian axis during pregnancy among others. This axis-reactivation is enabled by precise regulation of the hypothalamic gonadotropin-releasing hormone (GnRH) neurons allowing the pulsatile delivery of GnRH at mid-gestation. Such an event is followed by sequential secretion of estradiol (E2), follicle-stimulating hormone (FSH), and luteinizing hormone (LH), ultimately leading to a reboot of luteal steroidogenesis and a consequent boost of progesterone (P4) that enables the successful delivery of (at most) two well-developed newborns. The regulation of the hypothalamic GnRH neurons results from the combination of different endocrine pathways. GnRH neurons located in the preoptic area express progesterone and estrogens receptors, and aromatase, the estradiol-synthesizing enzyme. This local expression points to a mechanism of direct hormonal regulation of GnRH neurons that would synergize with the classic feedback pathways driven from the ovaries. Furthermore, the conspicuous organization of the kisspeptin system and the neuromodulators prolactin and dopamine observed in this area strongly suggests their involvement in the modulation of GnRH neurons. All these hormones, receptors, enzymes, and neurotransmitters coordinately regulate the functioning of this distinctive mechanism of which many details remain to be elucidated. In addition, photoperiod information transduced through melatonin hormone would coordinate plains vizcacha gestation with the most favorable moment for offspring surviving. To our knowledge, plains vizcacha is the unique rodent species that has a true reactivation of the reproductive axis during pregnancy. This trait is likely related to a reproductive strategy of plains vizcacha favoring offspring success.