Development and steroidogenic properties of the Bidder's organ of the tadpole of Rhinella arenarum (Amphibia, Anura)

Abstract

Several studies suggested that in anuran amphibians steroidogenic enzymes are critical for gonadal differentiation, proposing that the amount of sex steroids would adjust this differentiation. Among anurans, bufonids are important for the study of sex differentiation due to the presence of Bidder's organ (BO) that differentiates as a rudimentary ovary in the cephalic portion of the genital ridge. Considering that in adult males of Rhinella arenarum, the BO synthesizes estradiol, the main purpose of this work is to examine, in this species, the morphogenesis of BO and the steroidogenic capacity of this organ during larval development. BO and the proper gonads are distinguished from Gosner stage 26. During metamorphosis, BO primary oogonia develop in oogonia in nests, early previtellogenic oocytes and late previtellogenic oocytes in follicles while proper gonads remain undifferentiated. Aromatase was detected by immunohistochemistry in almost all the largest follicles of the BOs while the cytochrome P450 side-chain cleavage was observed in only few oocytes. The proper gonad was not immunoreactive in any stage. The determination of aromatase and 5α-reductase activities showed that the population of tadpoles between stages 36-41 is not homogeneous in terms of aromatase activity. In addition, from stage 26 to the end of metamorphosis, all the stages were able to produce estradiol from endogenous substrate but stages 40-41, corresponding to the end of pro-metamorphosis, produced the highest values. In conclusion, BO is able to synthesize estradiol from endogenous precursors and proper gonad remains undifferentiated at least until the end of the metamorphosis.

Sex Reversal in Amphibians

“…This structure differentiates as a rudimentary ovary in the anterior part of the genital ridge. It appears in both sexes early in larval life, prior to gonad differentiation [Sassone et al, 2015]. The Bidder's organs are maintained in adults of both sexes in species like Bufo bufo and Rhinella icterica, whereas they disappear in adult females of species like R. marina and R. arenarum.…”

Gonadal morphogenesis in the South American toad Rhinella Arenarum (Anura, Bufonidae) unveils an extremely delayed rate of sex differentiation

“…Thus, the early differentiation of follicles in the BO of R. arenarum contrasts with their late occurrence in the ovary, which reveals a remarkably wide variation of the developmental timing between both organs. Interestingly, Sassone et al (2015) reported that during larval development of R. arenarum , the BO was able to synthesize estradiol from endogenous precursors due to the aromatase enzymatic activity of Bidderian follicles, whereas the undifferentiated gonad did not express detectable amounts of aromatase. In spite of the extensive literature on BO development and structure, its function still remains unclear.…”

Evolution in the Genus Rhinella: A Total Evidence Phylogenetic Analysis of Neotropical True Toads (Anura: Bufonidae)

“…horribilis, and R . marina) have been employed extensively as model organisms for various biological disciplines, such as biochemistry (e.g., Abel and Macht, 1912;Cei et al, 1968;Rash et al, 2011), developmental biology (e.g., Markovich and Regeer, 1999;Barisone et al, 2002;Brown et al, 2002), ecotoxicology (e.g., Lajmanovich et al, 2011), molecular biology (e.g., Estoup et al, 2004Estoup et al, , 2010Rollins et al, 2015;Edwards et al, 2018;Ceschin et al, 2020), and especially physiology (e.g., Houssay and Giusti, 1929;Houssay, 1949;Penhos et al, 1967;Sassone et al, 2015). This genus also contains a highly invasive species, R .…”