A Stockpile of Ova in the Grass Frog Rana temporaria is Established Once for the Life Span. Do Ovaries in Amphibians and in Mammals Follow the Same Evolutionary Strategy?

Abstract

Most anuran amphibians produce high numbers of eggs during several consecutive breeding seasons. The question is still open whether oocytes are formed anew as a result of oogonial proliferation after each spawning or the definitive pool of oocytes is established during the juvenile period and is sufficient for the whole reproductive life span of a female. Our quantitative studies show that primary oogonia in adult female frogs can proliferate, but they fail to differentiate further and do not enter meiosis, and thereby there is no supplementation of new generations of oocytes after each spawning. Ovaries of one-year-old grass frogs contain (median) 53,447 diplotene oocytes, in two-years-old frogs this number decreased to 33,583 and eventually reached 25,679 in virgin mature females. More than 50% decrease in the total oocyte number was accompanied by massive degeneration (atresia) of oocytes. The final number of oocytes in a female forms a stock for 11-12 breeding seasons and exceeds the number of eggs produced during the potential reproductive life span of this species. The phylogenetic context of oocyte recruitment modes in the major clades of vertebrates is discussed in respect to their ability to replenish the stock (a renewable stock in ovaries named "open" vs. a non-renewable stock in ovaries named "closed"). Anat Rec,

Conserved form and function of the germinal epithelium through 500 million years of vertebrate evolution

“…The ovaries of amphibians are saccular structures, as in teleosts, but the germinal epithelium in amphibians is located at the periphery of the ovary, as in Ambystoma dumerilii (Uribe, 2009a), Rana temporaria (Ogielska et al, 2013), and Rana nigromaculata (Tanimura and Iwasawa, 1991), meanwhile in teleosts the germinal epithelium is located internally, surrounding the ovarian lumen. The previtellogenic ovaries of amphibian are thin; during the breeding season the ovaries grow to occupy much of the abdominal cavity and contain both previtellogenic and vitellogenic, yolked oocytes (Dodd, 1977;Lofts, 1984;Wallace and Selman, 1990;Uribe, 2009a,;Ogielska and Kotusz, 2004).…”

“…The germinal epithelium of the common frog Rana temporaria presents yet another variation on the theme: oogonia in the adult may proliferate but fail to enter meiosis, and there is no regeneration of new follicles after a spawning season. This anuran has functional lifetime determinate reproduction as represented by the pool of follicles established in the juvenile (Ogielska et al, ).…”

Biology of primordial germ cells in vertebrates with emphasis in urodeles amphibians

“…Therefore, the somatic context of the gonad determines the destination of the germinal cells (Evans et al, 1977). In anuran amphibians, a subpopulation of oogonia begins meiosis on every reproductive cycle, maintaining a niche of oogonia that serve as a reserve for the subsequent reproductive cycles (Bukovsky et al, 2005; Witschi, 1929); nevertheless, it has been reported at least an exception on R. temporaria , where a reservoir of oocytes establish in a single event (Ogielska et al, 2013). With the beginning of the meiosis, the ovarian morphology modifies due to the ovary grows because of the formation of the ovarian cavity and the thickening of the cortex, where some oogonia located at this ovarian cortex start meiosis increasing the number of oocytes at the diplotene stage in this region (Figure 2f) (Goldberg, 2015; Uribe, 2011).…”

The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus

“…The situation is different in females where meiosis starts early, so in developing ovaries we can observe both mitotically dividing gonocytes and meiocytes up to early diplotene that form a limited stockpile for the entire female’s life (for details see Ogielska et al . 60 ). Meiocytes (but not gonocytes) in amphibians form isogenic groups and are encapsulated inside cysts; only in females diplotene oocytes are individual cells (each inside its own ovarian follicle).…”