Mother-to-embryo vitellogenin transport in a viviparous teleost Xenotoca eiseni

Abstract

SignificanceViviparity is a type of reproductive system in which the embryo utilizes a maternal nutrient supply until birth. Viviparous species occur in many taxa including bony fish. The mother fish raises her offspring in the ovarian lumen or oviduct during gestation. Embryos of the viviparous bony fish Xenotoca eiseni (family Goodeidae) utilize nutrients secreted into the ovarian lumen. However, the source of the maternal nutrients and their mother-to-embryo transport have not been experimentally demonstrated. In this study, we focus on the yolk nutrient protein vitellogenin (Vtg) as a matrotrophic factor. Our results are of fundamental importance to the investigation of viviparous systems in teleosts and in other vertebrates and invertebrates.

Histological observation of the reproductive system in a viviparous teleost Xenotoca eiseni Rutter 1896 (Cyprinodontiformes: Goodeidae)

“…The trophotaenial epithelial cells absorb the maternal nutrients including vitellogenin via vesicle trafficking (Grosse-Wichtrup & Greven, 1985;Iida et al, 2019;Lombardi & Wourms, 1985). This endocytosis-mediated absorption is similar to that of the lysosome-rich enterocytes (LREs) in the gut of zebrafish embryos (Park et al, 2019).…”

“…The nutrient source for the embryonic development and growth changes from lecithotrophy to matrotrophy during gestation (Uribe, Grier, Avila‐Zúñiga, & García‐Alarcón, 2018). One of the maternal nutrients, vitellogenin, is secreted into the ovarian lumen via the septum and then absorbed into the embryo from the trophotaeniae (Iida et al., 2019). The functional tissues or cells for the nutrient transfer were clearly visible in the histological sections.…”

“…The functional tissues or cells for the nutrient transfer were clearly visible in the histological sections. Our previous immunohistochemistry‐based research focused on specific target molecules (Iida et al., 2015,2019). In addition to the molecular methods, we believe that the anatomical and histological methods employed in the current study are valuable tools to improve understanding of the physiology of the viviparous system.…”

“…The embryo of goodeid species possesses trophotaeniae that function as a pseudoplacenta to absorb the maternal nutrients during gestation. We have previously reported apoptotic regression of trophotaeniae and identification of vitellogenin as a maternal nutrient (Iida et al., 2019; Iida, Nishimaki, & Sehara‐Fujisawa, 2015). These findings are unique traits in the viviparity of the goodeid fish that have not been reported in mammals or other viviparous animals.…”

Nutritional status and fecundity are synchronised by muscular exopheresis

“…Neuronal exopher formation occurs in higher animals 3 . In addition, yolk protein can be synthesized in the muscles of oviparous animals like zebrafish 20 , and is supplemented from the mother to the intraovarian embryo in viviparous animals 21 . Hence, it is tempting to speculate that the role of muscular expheresis in supporting progeny development could be evolutionarily conserved.…”