Modifications of the Testis in Response to Sperm Bundle Formation in the Mediterranean Painted Frog Discoglossus pictus Otth, 1837 (Amphibia: Anura: Discoglossidae)
Larval, juvenile, and adult testes of Discoglossus pictus were examined to investigate how the extremely elongated sperm of this species, up to 2,500 μm, can be accommodated within the testicular tubules of the gonad. Seminiferous tubules in D. pictus are modest in number, of large diameter, and run straight from the posterior to the anterior ends of the testis. The modified testis structure originates in its unique development. The anterior part of the testis is composed of short and straight tubules forming the rete testis. The lumen of the seminiferous tubules is filled with bundles composed of sperm embedded in a periodic acid-Schiff stain (PAS)-positive matrix secreted by Sertoli cells. The formation of such extremely elongated spermatozoa is possible because of anatomical modifications including simplification of testis structure, enlargement of the diameter of testicular tubules, reduction in their number, assembly of rete testis tubules in the anterior part of the testis, reduction of the collecting system to a single duct, and the occurrence of sperm bundles embedded in secretion. Additionally, the secretion of a PAS-positive substance by Sertoli cells during spermatogenesis was described. Thus the urogenital system in D. pictus deviates dramatically from the typical structure of male gonads in other anurans.Abstract
Structure of the testis in Discoglossus pictus. (A) A longitudinal section shows the forming straight testis cords at the metamorphosis. Arrows indicate the wall of the cords that contain the spermatogonia. Staining according to Debreuill. (B) The rete testis composed of short sterile tubules (arrow) that join seminiferous tubules with one common duct of the rete testis (d). Staining according to Debreuill. (C) A cross-section through the testis shows large seminiferous tubules filled with sperm bundles (arrow). In the periphery unfilled, small-diameter seminiferous tubules are discernable (asterisk). Periodic acid-Schiff stain (PAS). (D) A longitudinal section through a seminiferous tubule at an early stage of spermatogenesis. Drops of PAS-positive substance (arrow) are located within the Sertoli cells and later form the matrix in the tubule lumen (asterisk). PAS staining. (E) A cross-section through a seminiferous tubule containing a sperm bundle. The sperm bundle fills almost the entire space of the tubule (see [F]). Peripheral lacunae (pl) are located near the wall of the tubule (arrowhead); central lacunae (cl) are situated in the PAS-positive matrix of the bundle. PAS. (F) Peripheral lacunae are filled with the heads of sperm, whereas the center is filled with sperm tails embedded in secretion (asterisk). PAS.
Testis and sperm bundle structure in Discoglossus pictus. (A) Scanning electron microscopy (SEM) micrograph taken after removal of tunica albuginea of the testis shows large unanastomosing seminiferous tubules (st) that run from the posterior toward the anterior end of the testis where rete testis is localized (rt). (B) Diagram showing the exit route of sperm in the male urogenital system of D. pictus. Sperm bundles (sb) are formed within the seminiferous tubules (st), which coalesce into rete testis (rt). Sperm are directed into the Wolffian duct (Wd). Some kidney tubules (kt) join the secondary ureter (su).
(A) Longitudinal section shows aggregating sperm located within the lumen of the seminiferous tubule. Sperm acrosome region (a) is stained red, nucleus (n) violet, and sperm tail (t) brown. Staining according to Gomori. (B) An aggregation of sperm. Staining according to Gomori. (C) Longitudinal section through a sperm bundle showing central lacunae. Staining according to Gomori. (D) Scanning electron microscopy (SEM) examination of the tubule lumen content shows the surface of a sperm bundle. (E) Transmission electron microscopy (TEM) examination presents a cross-section through a peripheral lacuna in secretion (s) of the sperm bundle that is filled with sperm heads at acrosome (a) level. (F) A cross-section through a peripheral lacunae containing sperm heads at the level of the nucleus (n). (G) Section of sperm tails (t) embedded individually in secretion filling mainly the center of the sperm bundle.
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