massive-ovulation-mammals-techniques-for-analyzing-natural

Massive Ovulation in Mammals: Techniques for Analyzing Natural Spontaneous Polyovulation and Induced Polyovulation in <em>Lagostomus maximus</em>

The South American plains vizcacha, Lagostomus maximus, is recognized as the mammalian species with the highest ovulation rate, which can reach as many as ...

Universidad Maimónides

The South American hystricognathe Lagostomus maximus is a fossorial rodent whose females show unique reproductive characteristics. They have a 155-day long gestation, show massive polyovulation and a selective process of embryonic resorption in the first half of gestation. In order to explore and perform an in-situ characterization of the reproductive tract, we visualized internal structures through ultrasonography and video-endoscopy in pregnant and non-pregnant females. We describe the finding of protruding structures that lie on the yolk sac and their histological and ultrastructural characterization. The placenta was covered with whitish, small pearl-shaped structures. These structures were also seen on the extra-embryonic space, being the amnion and the umbilical cord free of them. Pearl-shaped structures were composed with loose connective tissue, lacked blood vessels, and showed collagen fibers organized in a spiral form. They were anchored by pedicles to the villous surface of the extraembryonic membrane. We discuss the biological and evolutionary meaning of the pearl-shaped structures that relate L. maximus to the African origin of the South American hystricognathe fauna.

Endoscopy, histology and electron microscopy analysis of foetal membranes in pregnant South American plains vizcacha reveal unusual excrescences on the yolk sac.

The South American plains vizcacha, Lagostomus maximus, is the only mammal described so far that shows expression of estrogen receptors (ERs) and progesterone receptors (PRs) in gonadotropin-releasing hormone (GnRH) neurons. This animal therefore constitutes an exceptional model for the study of the effect of steroid hormones on the modulation of the hypothalamic-pituitary-ovarian (HPO) axis. By using both in vivo and ex vivo approaches, we have found that pharmacological doses of progesterone (P4) and estradiol (E2) produced an inhibition in the expression of hypothalamic GnRH, while physiological doses produced a differential effect on the pulsatile release frequency or genomic expression of GnRH. Our ex vivo experiment indicates that a short-term effect of E2 modulates the frequency of GnRH release pattern that would be associated with membrane ERs. On the other hand, our in vivo approach suggests that a long-term effect of E2, acting through the classical nuclear ERs-PRs pathway, would produce the modification of GnRH mRNA expression during the GnRH pre-ovulatory surge. Particularly, P4 induced a rise in GnRH mRNA expression and protein release with a decrease in its release frequency. These results suggest different levels of action of steroid hormones on GnRH modulation. We conclude that the fine action of E2 and P4 constitute the key factor to enable the hypothalamic activity during the pregnancy of this mammal.

The key action of estradiol and progesterone enables GnRH delivery during gestation in the South American plains vizcacha, Lagostomus maximus.

Plains vizcacha females are able to ovulate up to 800 oocytes per estrus cycle. However, just 10-12 embryos are implanted and only two of them, those located nearest the cervix, are gestated to term. Between 26 and 70 days post-coitum, a constitutive resorption occurs from the embryos located proximal to the ovary, extending progressively toward those distally implanted. Our previous studies on the dynamics of gestation in L. maximus, led us to hypothesize some kind of placental and nutritional insufficiency as the basis for the resorption process. We analyzed histology and arterial architecture of the reproductive tract in pregnant and non-pregnant females. Uterine horns are irrigated through the uterine artery, a branch of the internal iliac artery, in an ascending way from the cervix; segmental arteries irrigating the embryo vesicles become thinner as they approach the ovary. Contrast solution administered during angiographies accumulated in the placenta of embryos closest to cervix. Thus, blood stream favors the embryos nearest the cervix, indicating a gradual nutritional deficiency of those closest to the ovary. Besides, placenta becomes calcified early, at mid-gestation, during the resorption process. Finally, the detection of specialized endothelial venules and inflammatory cells suggest the concurrent participation of immunological processes in embryo vesicles undergoing resorption.

Nutritional deficiency and placenta calcification underlie constitutive, selective embryo loss in pregnant South American plains vizcacha, Lagostomus maximus (Rodentia, Caviomorpha).

Oxygenated blood is required for the adequate metabolic activity of the brain. This is supplied by the circle of Willis (CoW) and the vertebrobasilar and carotid systems. The CoW ensures blood flow in case of arterial stenosis or occlusion. Different animal models have been explored for the CoW morphological and functional study. This work aims to characterize the vascular architecture of the CoW of the plains vizcacha, Lagostomus maximus (Suborder: Hystricomorpha), and to compare it with evolutionarily related species of Caviomorpha and Muroidea. The blood supply in adult plains vizcachas was studied using latex cerebrovascular casts and angiography. A caudo-rostral flow direction was determined, beginning in the spinal and vertebral arteries and converging in the basilar artery which bifurcates in the carotid-basilar communication in the caudal communicating arteries. In the first third of its course, the caudal cerebral arteries project laterally, and the middle and rostral cerebral arteries bifurcate from their rostral terminal segment, supplying the temporo-parietal and frontal cortex. The CoW architecture is mainly conserved between rodent species. Likewise, the small neurovascular variations observed could be considered phylogenetic morphological variations more than evolutionary adaptations. The absence of the rostral communicating artery that generates the rostral open architecture of the CoW in the vizcacha as in the other analyzed species, supports the need for a revision of the CoW classical function as a security system. Finally, this work supports the importance of expanding our understanding of brain anatomy among species, which may contribute to a better understanding of functional neuroanatomy.

Neurovascular description in the South American plains vizcacha, Lagostomus maximus (Chinchilloidea, Caviomorpha). A study involving evolutionarily related species of Caviomorpha and Muroidea.

The South American plains vizcacha, Lagostomus maximus, is recognized as the mammalian species with the highest ovulation rate which can reach as many as 800 ova. This remarkable polyovulation phenomenon was first reported in the 1970s and has remained unchanged in its findings ever since. We conducted an extensive re-evaluation of ovulation in L. maximus by examining natural ovulation, ovulation induced through the administration of exogenous hormones and autologous seminal plasma, while also categorizing the morphological characteristics and maturation stages of the released ova. Our results confirm L. maximus as the foremost polyovulatory mammalian species, albeit with a mean of 154 ± 87, ranging from 29 to 326 oocytes per oestrous cycle. We observed the concurrent presence of spontaneous ovulation, serving as a mechanism to eliminate defective oocytes, alongside induced ovulation, referred to as "euovulation," that promotes the release of cumulus-oocyte complexes suitable for fertilization. In addition, we provide evidence for the involvement of seminal plasma in the process of induced ovulation and show that the "pseudovulation" phenomenon occurring at mid-gestation, which contributes to the formation of secondary corpora lutea, does not entail the release of oocytes into the oviducts. Our analysis also revealed the presence of spontaneous parthenogenetic oocyte activation and subsequent development, which occurred both during oocyte release in the ovulatory phase and within unruptured follicles in the ovary.

Article	Year
Endoscopy, histology and electron microscopy analysis of foetal membranes in pregnant South American plains vizcacha reveal unusual excrescences on the yolk sac. Journal of molecular histology\| PubMed ID: 29468298	2018
The key action of estradiol and progesterone enables GnRH delivery during gestation in the South American plains vizcacha, Lagostomus maximus. The Journal of steroid biochemistry and molecular biology\| PubMed ID: 32070756	2020
Nutritional deficiency and placenta calcification underlie constitutive, selective embryo loss in pregnant South American plains vizcacha, Lagostomus maximus (Rodentia, Caviomorpha). Theriogenology\| PubMed ID: 32629338	2020
Neurovascular description in the South American plains vizcacha, Lagostomus maximus (Chinchilloidea, Caviomorpha). A study involving evolutionarily related species of Caviomorpha and Muroide... Anatomical record (Hoboken, N.J. : 2007)\| PubMed ID: 38328879	2024
Polyovulation in the South American Plains Vizcacha, Revisited: Coexistence of Spontaneous and Induced Ovulation. Journal of experimental zoology. Part A, Ecological and integrative physiology\| PubMed ID: 40165530	2025

Mariela Giacchino

Biography

JoVE Journal Publications

Other Publications