Sexual Kidneys in a Plethodontid Salamander
Previous studies observed the synthesis of an abundant glycoprotein secretion in the collecting duct tubules of ambystomatid and salamandrid salamanders. The synthesis and release of this secretion occurred during times of mating activity; therefore, researchers concluded that collecting ducts of the pelvic kidneys functioned as secondary sexual structures. The purpose of this study was to determine if any male plethodontids possess kidneys with similar secondary sexual function. We captured male and female Eurycea longicauda longicauda (Common Name) from every month possible and removed their urogenital organs, along with known male secondary sexual glands, for histological examination. The heights of collecting duct and known secondary sexual gland epithelia were measured every month as a proxy for secretory activity. We compared known secondary sexual gland seasonal secretory activity with that of the seasonal secretory activity of the collecting ducts. We then qualitatively compared these data with the seasonal spermatogenic cycle of the testes, seasonal sperm transport through male genital ducts, and seasonal sperm transfer from males to females. Known secondary sexual structures and pelvic kidney collecting ducts increase epithelial height directly prior to and during autumn months, concordant with the later stages of sperm development, transport of sperm through the genital ducts, and transfer of sperm from males to females; i.e., the mating season.Abstract
General schematic of kidney morphology in salamanders. The “simple” condition was previously reported for proteids and sirenids whereas the “complex” condition was reported for all other salamander families. The dotted line delineates nephrons from the pelvic and genital kidney regions. Cd, pelvic kidney collecting ducts; Cl, cloaca; Gk, genital kidney; Pk, pelvic kidney; T, testis.
Mean seasonal gonad growth of male and female E. l. longicauda. Error bars represent standard deviation.
Histology of sperm transport of E. l. longicauda (H&E). (A) Wolffian duct devoid of sperm from a male specimen collected in April. (B) Wolffian duct full of sperm from a male specimen collected in October. (C) Cloacal orifice devoid of sperm from a female collected in August. (D) Spermatophore filling the cloacal orifice from a female collected in October. (E) Spermathecal tubules with a scant amount of sperm in a female collected in June. (F) Spermathecal tubules with an abundance of sperm in a female collected in September. Clo, cloacal orifice; Sp, sperm; Spo, spermatophore; Spt, spermathecal tubules; Wd, Wolffian duct.
Sperm production, transport, and storage of E. l. longicauda. Unbroken bars indicate months where both specimens possessed a particular sperm stage or sperm presence in the testes or genital ducts, respectively. Broken bars indicate months where one specimen possessed a particular sperm stage or sperm presence in the testes or genital ducts, respectively. Light grey bar represents few sperm in spermathecae and black bar represents abundant sperm (for a pictorial representation see Fig. 2E,F).
Histology of seasonal secretory cycle of known secondary sexual structures and the collecting ducts of male E. l. longicauda (H&E). (A) Mental gland epithelial atrophy from a male collected in March. (B) Mental gland hypertrophy from a male collected in November. (C) Cloacal vent gland epithelial atrophy from a male collected in May (D). Cloacal vent gland epithelial hypertrophy from a male collected in November. (E) Caudal courtship gland epithelial atrophy from a male collected in April. (F) Caudal courtship gland epithelial hypertrophy from a male collected in September. (G) Collecting duct epithelial atrophy from a male collected in April (H). Collecting duct epithelial hypertrophy from a male collected in October. CdEp, collecting duct epithelium; CcgEp, caudal courtship gland epithelium; Ep, epidermis; Gh, geniohyoid; Sc, stratum compactum; Sm, secretory material; VgEp, Cloacal vent gland epithelium.
Seasonal secretory cycle based on mean monthly epithelial heights of known secondary sexual structures and the collecting ducts of male E. l. longicauda. Error bars represent standard deviation.
Histochemistry of collecting ducts of male E. l. longicauda. (A) Negative brilliant blue stain of cytoplasmic contents of collecting ducts from a male collected in April. (B) Positive brilliant blue stain of cytoplasmic contents of collecting ducts from a male collected in September. (C) Negative periodic-acid Schiff's stain and alcian blue stain of collecting duct cytoplasmic contents from a male collected in March. (D) A positive periodic-acid Schiff's stain and negative alcian blue stain of collecting duct cytoplasmic contents from a male collected in September. AB−, alcian blue negative; Bb+, brilliant blue positive; CdEp, collecting duct epithelium; PAS+, periodic-acid Schiff's reagent positive.
(A–C) Correlation of secretory cycle of known secondary sexual structures and (D) seasonal size changes of a primary sexual structure to collecting duct seasonal secretory activity. (A) y = 0.9445x − 4.1884, P = 0.0036. (B) y = 1.3814x − 2.8498, P = 0.0020. (C) y = 0.8944x − 3.4235, P < 0.0001. (D) y = −1.948x + 36.952, P = 0.3024.
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