Modification of genital kidney nephrons for sperm transport in a plethodontid salamander, Eurycea longicauda

Salamanders possess kidneys with two distinct regions: a caudal pelvic portion and cranial genital portion. Nephrons of the pelvic region are responsible for urine formation and transport. Nephrons of the genital region transport sperm from testes to Wolffian ducts; however, nephrons of the genital region possess all the same functional regions found in pelvic kidney nephrons that are involved with urine formation and transport (renal corpuscles, proximal tubules, distal tubules, and collecting ducts). Morphological similarities between pelvic and genital regions stimulated past researchers to hypothesize that nephrons of genital kidneys possess dual function; that is, sperm transport and urine formation/transport. Considering size of glomeruli is directly related to the total amount of blood plasma filtered into the Bowman's space, we tested the hypothesis that nephrons of genital kidneys have reduced urine formation function by comparing glomerular size between nephrons of pelvic and genital kidney regions in Eurycea longicauda with general histological techniques. Light microscopy analysis revealed that glomeruli of pelvic kidneys were significantly larger than those measured from genital kidneys. Transmission electron microscopy analysis also revealed modifications in genital kidney nephrons when compared to pelvic kidney nephrons that suggested a decrease in urine formation function in genital kidneys. Such modifications included a decrease in basal and lateral plasma membrane folding in genital kidney proximal and distal tubules compared to that of pelvic kidney proximal and distal tubules. Genital kidney proximal tubules were also ciliated, which was not observed in pelvic kidney proximal tubules. In conclusion, although structurally similar at the histological level, it appears that nephrons of genital kidneys have decreased urine formation function based on glomerular size comparison and nephron ultrastructure.

[1]  D. Siegel,et al.  Sexual Kidneys in a Plethodontid Salamander , 2017, Journal of Herpetology.

[2]  S. Trauth,et al.  “Sexual tears” in a salamander? , 2017, Zoomorphology.

[3]  D. Siegel,et al.  Genital and Pelvic Kidney Renal Corpuscles of the Red-spotted Newt, Notophthalmus viridescens (Amphibia, Urodela, Salamandridae) , 2016, Copeia.

[4]  S. Trauth,et al.  The Evolution of the Sperm Transport Complex in Male Plethodontid Salamanders (Amphibia, Urodela, Plethodontidae) , 2014, Copeia.

[5]  D. Siegel,et al.  Modifications of the genital kidney proximal and distal tubules for sperm transport in Notophthalmus viridescens (Amphibia, Urodela, Salamandridae) , 2014, Journal of morphology.

[6]  S. Trauth,et al.  Spermatogenic cycle of a plethodontid salamander, Eurycea longicauda (Amphibia, Urodela) , 2014, Spermatogenesis.

[7]  D. Siegel,et al.  The testicular sperm ducts and genital kidney of male Ambystoma maculatum (Amphibia, Urodela, Ambystomatidae) , 2013, Journal of morphology.

[8]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[9]  D. Siegel,et al.  Sexual Kidneys in the Red-spotted Newt (Notophthalmus viridescens) , 2012 .

[10]  D. Siegel,et al.  The pelvic kidney of male Ambystoma maculatum (Amphibia, urodela, ambystomatidae) with special reference to the sexual collecting ducts , 2010, Journal of morphology.

[11]  D. Sever.  Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). VI. Anterior testicular ducts and their nomenclature , 2009, Journal of morphology.

[12]  H. Sasaki,et al.  Comparative anatomical study of the kidney position in amniotes using the origin of the renal artery as a landmark. , 2005, Okajimas folia anatomica Japonica.

[13]  M. Nakai,et al.  Estrogens and epididymal function. , 2001, Reproduction, fertility, and development.

[14]  S. K. Saidapur,et al.  The Excurrent Duct System of Sperm Transport in Rana cyanophlyctis, Rana limnocharis, Polypedates maculatus, Microhyla rubra, Bufo melanostictus and Bufo fergusonii , 2000 .

[15]  M. Matsuda.  Difference of fertilizing capacity between testicular sperm and vas deferens sperm in Cynops pyrrhogaster , 1986 .

[16]  S. Benyajati,et al.  Comparative aspects of glomerular filtration in vertebrates. , 1985, Renal physiology.

[17]  A. A. Williams,et al.  Male genital ducts in the salamanders Eurycea lucifuga and Eurycea longicauda , 1984 .

[18]  L. Russell,et al.  Spermatophores of the salamander Ambystoma texanum. , 1981, Tissue & cell.

[19]  John A. Kiernan,et al.  Histological and Histochemical Methods: Theory and Practice , 1981 .

[20]  A. Humphries,et al.  The jelly envelopes and fertilization of eggs of the newt, Notophthalmus viridescens , 1978, Journal of morphology.

[21]  R. P. Forster.  The nature of the glucose reabsorptive process in the frog renal tubule. Evidence for intermittency of glomerular function in the intact animal , 1942 .

[22]  北海道帝國大學.  Journal of the Faculty of Agriculture, Hokkaido Imperial University = 北海道帝國大學農學部紀要 , 1927 .

[23]  S. W. Chase.  The mesonephros and urogenital ducts of Necturus maculosus, Rafinesque , 1923 .