Follicular placenta of the viviparous fish, Heterandria formosa: II. Ultrastructure and development of the follicular epithelium

Abstract

Embryos of the viviparous poeciliid fish, Heterandria formosa, develop to term in the ovarian follicle where they undergo a 3,900% increase in embryonic dry weight. Maternal-embryonic nutrient transfer occurs across a follicular placenta that is formed by close apposition of the embryonic surface (i.e., the entire body surface during early gestation and the pericardial amnionserosa during mid-late gestation) to the follicular epithelium. To complement our recent study of the embryonic component of the follicular placenta, we now describe the development and fine structure of the maternal component of the follicular placenta. Transmission electron microscopy reveals that the ultrastructure of the egg envelope and the follicular epithelium that invests vitellogenic oocytes is typical of that described for teleosts. The egg envelope is a dense matrix, penetrated by microvilli of the oocyte. The follicular epithelium consists of a single layer of cuboidal cells that lack apical microvilli, basal surface specializations, and junctional complexes. Follicle cells investing the youngest embryonic stage examined (Tavolga's and Rugh's stage 5-7 for Xiphophorus maculatus) also lack apical microvilli and basal specializations, but possess junctional complexes. In contrast, follicle cells that invest embryos at stage 10 and later display ultrastructural features characteristic of transporting epithelial cells. Apical microvilli and surface invaginations are present. The basal surface is extensively folded. Apical and basal coated pits are present. The cytoplasm contains a rough endoplasmic reticulum, Golgi complexes, and dense staining vesicles that appear to be lysosomes. The presence of numerous apically located electron-lucent vesicles that appear to be derived from the apical surface further suggests that these follicle cells may absorb and process follicular fluid. The egg envelope, which remains intact throughout gestation and lacks perforations, becomes progressively thinner and less dense as gestation proceeds. We postulate that these ultrastructural features, which are not present in the follicles of the lecithotrophic poeciliid, Poecilia reticulata, are specializations for maternal-embryonic nutrient transfer and that the egg envelope, follicular epithelium, and underlying capillary network form the maternal component of the follicular placenta. © 1994 Wiley-Liss, Inc.

Evidence of maternal copper and cadmium transfer in two live-bearing fish species

“…The finding of maternal metal transfer in H. formosa was not surprising, since it is considered a matrotrophic species (Grove and Wourms 1994;Uribe and Grier 2011). We would not expect differences in metal levels among first-brood offspring from exposed and control females if G. affinis were fully lecitotrophic (i.e.…”

“…Heterandria formosa is a species with specialized matrotrophy; a provisioning mode in which the female continues to transfer provisions to the embryo during development (Grove and Wourms 1994;Wourms et al 1988;Uribe and Grier 2011). Furthermore, this species exhibits superfetation, which is the simultaneous development of multiple broods at different developmental stages (Marsh-Matthews 2011;Pires et al 2011).…”

Placental structures and their association with matrotrophy and superfetation in poeciliid fishes

“…In the inner layer, we identified numerous vesicles, microvilli on the apical surface (zone closest to the embryonic tissue), cell junctions and extensive endoplasmic reticulum. An additional characteristic we noticed was the presence of a follicular ribbon or egg envelope (porous fertilization membrane), which was observed in some species of the genera Heterandria and Poeciliopsis (Heterandria formosa, Poeciliopsis gracilis, P. latidens, P. occidentalis, P. turrubarensis and P. viriosa; Grove & Wourms, 1994;Kwan et al, 2015). We can conclude that the inner follicular layer in all species has a high degree of metabolic activity and is responsible for the transfer of nutrients from the mother to the embryo.…”

“…To date, this is the only study that has examined the relationship between degree of matrotrophy and placental complexity, even though many studies have assumed that higher degrees of matrotrophy require more complex placentas (Ostrovsky et al, 2016;Pollux et al, 2014;Reznick, Mateos, & Springer, 2002). The hypothesis is that females that transfer more nutrients to their embryos during development (i.e., more matrotrophic species) require a more complex placenta (Grove & Wourms, 1994;Jollie & Jollie, 1964;Kwan et al, 2015;Turner, 1940). Therefore, one of the main objectives of this study was to analyse whether there is a relationship between degree of matrotrophy and several ultrastructural characteristics of the maternal follicular placenta.…”

Ultrastructural observations on sperm storage in the ovary of the platyfish, Xiphophorus maculatus (Teleostei: Poeciliidae): The role of the duct epithelium

“…This study demonstrated impressively that the embryo-allograft within the follicle was isolated from maternal immune rejection. Tight junctions have been described connecting cells of the follicular epithelium in Heterandria formosa (Grove and Wourms, 1994) and in Poecilia reticulata (Jollie and Jollie, 1964). Here, as in the luminal walls of the ovary, tight junctions are believed to produce an effective barrier preventing the movement of molecular and cellular agents of maternal immune rejection to the embryo.…”