The Evolution of the Sperm Transport Complex in Male Plethodontid Salamanders (Amphibia, Urodela, Plethodontidae)
Based on previous literature, male salamanders of the genus Eurycea possess sperm transport ducts that are homogenous (in terms of histology) along their entire length; i.e., a transverse tubule. Considering this structural homogeneity is unique among salamanders, this feature could potentially be a synapomorphy for Spelerpinae. We tested this hypothesis by re-evaluating the histology of the sperm transport ducts of multiple members of Spelerpinae (Eurycea longicauda, E. lucifuga, and E. multiplicata) and compared our results with representatives from all subfamilies of Plethodontidae (Bolitoglossinae, Hemidactylinae, and Plethodontinae). We reject the findings of previous work that spelerpine salamanders possess homogenous sperm transport ducts along their entire length. Discrete regions are present along the sperm transport ducts of Spelerpinae that include, from proximal to distal, a vas efferens, genital kidney proximal tubule, genital kidney distal tubule, and genital kidney collecting tubule. A distinct renal corpuscle often exists between the communication of the vas efferens and genital kidney proximal tubule. This regionality is not only stereotypical for the sperm transport ducts in all plethodontid salamanders, but also for salamanders in general. Similar to other lineages of salamanders (i.e., Rhyacotritonidae and Sirenidae), all plethodontid salamanders examined lack a longitudinal collecting duct and distinct neck and intermediate segments. We found no characteristic that could potentially serve as a non-ambiguous synapomorphy for Spelerpinae or Plethodontidae with use of sperm transport duct histology. However, it appears that the Bolitoglossinae, Hemidactylinae, and Spelerpinae often lack arteriole connection to their glomeruli within the genital kidney renal corpuscles, yet this trait is ambiguous within taxa of these subfamilies.
Schematic of genital kidney nephrons in Plethodontidae. Ctd, central testicular duct; Gct, genital kidney collecting tubule; Gdt, genital kidney distal tubule; Gpt, genital kidney proximal tubule; Grc, genital kidney renal corpuscle; Vep, example of a genital kidney vas efferens terminating at a genital kidney proximal tubule; Ver, example of a vas efferens terminating at a genital kidney renal corpuscle; Wd, Wolffian duct.
Representative micrographs from the sperm transport ducts of Hemidactylium scutatum (scale bar 100 µm) depicting the transition from the central testicular duct to the vas efferens. (A–D) A testicular canal branch (arrowheads) traveling away from the central testicular canal (Ctc). (E–F) The testicular canal branch (arrowheads) emptying into a vas efferens (Ve).
Representative micrographs from the sperm transport ducts of Eurycea longicauda (scale bar = 50 µm) depicting the transition from the vas efferens to a genital kidney renal corpuscle. (A–D) The vas efferens (arrowheads) traveling away from the testis (Ts). (E–F) The transition of the vas efferens to a genital kidney renal corpuscle (arrowheads). (F) Note the remnant glomerulus (Gl) in the lumen of the testicular duct.
Representative micrographs from the sperm transport ducts of Eurycea longicauda (scale bar = 50 µm) depicting the transition from the genital kidney renal corpuscle to the genital kidney proximal tubule. (A–D) The genital kidney renal corpuscle transforming into a duct with a columnar epithelium and cilia (Ci) projecting from the apical plasma membranes of the epithelial cells (arrowheads). Dark elongated nuclei (Nu) found basally in these ciliated cells are stereotypical of a genital kidney neck segment. (E–F) The transition from the genital kidney neck segment to the genital kidney proximal tubule (arrowheads). Note the eosinophilic cytoplasm and cilia (Ci) that are stereotypical of the genital kidney proximal tubule epithelium.
Representative micrographs from the sperm transport ducts of Bolitoglossa subpalmata (scale bar = 50 µm) depicting the transition from the genital kidney proximal tubule to the genital kidney distal tubule. (A–D) The genital kidney proximal tubule transforming into a narrower duct (arrowheads; C–D). Note that the epithelia of both ducts are lined by cells with cilia (Ci) projecting from the apical plasma membranes. This narrow duct is stereotypical of a genital kidney intermediate segment. (E–F) The genital kidney intermediate segment (arrowheads) emptying into the genital kidney distal tubule (Dt). Note that cilia do not line the apical plasma membrane of the genital kidney distal tubule and the presence of secretory material (Sm) in the lumen of the genital kidney distal tubule.
Representative micrographs from the sperm transport ducts of Plethodon albagula (scale bar = 50 µm) depicting the transition from the genital kidney distal tubule to the genital kidney collecting tubule. (A–D) The genital kidney distal tubule (arrowhead) as it approaches the genital kidney collecting tubule (CT). (B–D) A transitional region between the two genital kidney nephron regions (arrows) is apparent, and is identified by a cuboidal epithelium, but the lack of secretory material (Sm) in the lumen (stereotypical of the genital kidney distal tubule in this taxa). (E–F) Communication of the two genital kidney nephron tubules.
Representative micrographs from the sperm transport ducts of Eurycea multiplicata (scale bar = 50 µm) depicting the transition from the genital kidney collecting tubule to the Wolffian duct. (A–D) The genital kidney collecting tubule (arrowheads) decreasing in size and approaching the Wolffian duct (Wd). (E–F) The genital kidney collecting tubule emptying into the Wolffian duct.
Comparison of genital kidney renal corpuscles (arrowheads; 1–5, proximal to distal) with vascular poles (Plethodontinae, Plethodon albagula, A1–A5) and those without (Bolitoglossinae, Bolitogolossa subpalmata, B1–B5; Hemidactylinae, Hemidactylium scutatum, C1–C5; Spelerpinae, Eurycea lucifuga, D1–D5; scale bar = 50 µm). Note that in Plethodontinae a vascular pole (arrow) exists from the intrusion of arterioles into the glomerulus at the vascular pole of the renal corpuscle (A), while in Bolitoglossinae, Hemidactylinae, and Spelerpinae the glomerulus is “floating” and no vascular pole is present (B–D).
Contributor Notes
Associate Editor: C. Beachy.