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. 2023 Nov 13;13(1):19746.
doi: 10.1038/s41598-023-46900-8.

Post-testicular sperm maturation in ancient holostean species

Viktoriya Dzyuba  1 , William L Shelton  2 , Ana E Hiott, Jacky Cosson  2 , Olga Bondarenko  2 , Vitaliy Kholodnyy  2 , Borys Dzyuba  2
Affiliations

Post-testicular sperm maturation in ancient holostean species

Viktoriya Dzyuba et al. Sci Rep. .

Abstract

Fish speciation was accompanied by changes in the urogenital system anatomy. In evolutionarily modern Teleostei, male reproductive tracts are fully separated from the excretory system, while in evolutionarily ancient Chondrostei and Holostei, the excretory and reproductive tracts are not separated. Sturgeon post-testicular sperm maturation (PTSM) occurring as a result of sperm/urine mixing is phenomenologically well described, while, in holosteans, functional intimacy of seminal ducts with kidney ducts and the existence of PTSM still need to be addressed. In Lepisosteus platostomus (Holostei), sperm samples were collected from testes (TS), efferent ducts (EDS), and Wolffian ducts (WDS). While WDS was motile, no motility was found in TS and EDS. The existence of PTSM was checked by in vitro PTSM procedure. After TS and EDS incubation in seminal fluid from WDS, no more than 5% motile spermatozoa were observed in TS, whereas in EDS the motility percentage was up to 75%. Experimental dyeing of urogenital ducts in gars and sturgeons revealed some differences in the interconnection between sperm ducts and kidneys. It is concluded that post-testicular sperm maturation occurs in gars and suggests that infraclass Holostei occupies an intermediate evolutionary position between Teleostei and Chondrostei in the anatomical arrangement of the urogenital system.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Schematic representation of actinopterygian fish groups differing in anatomical association of urinary and reproductive systems. In dashed rectangle, fish groups in which sperm maturation process is known or supposed to occur.
Figure 2
Figure 2
Sperm concentration and seminal fluid osmolality in different types of gar sperm samples. (a)—Sperm concentration, × 109 spz mL−1. (b)—seminal fluid osmolality, mOsm kg−1. TS—sperm collected from testes, EDS—sperm collected from efferent ducts, WDS—sperm collected from Wolffian ducts. Values with different letters are significantly different (One-way ANOVA, Tukey test, P < 0.05).
Figure 3
Figure 3
Sperm motility percent (%) in different types of gar sperm samples before and after in vitro maturation. TS—sperm collected from testes, EDS—sperm collected from efferent ducts, WDS—sperm collected from Wolffian ducts. Values marked with a small letter a are not different (Student t-test, P = 0.74).
Figure 4
Figure 4
Wafer plots of three principal components (PC1, PC2, PC3), obtained after sperm kinematic parameters analysis in samples of Wolffian duct sperm (WDS) and efferent duct sperm (EDS) after in vitro maturation at different post-activation times. Dots represent individual spermatozoon in PC1–PC2 coordinates. Black dots are centroids of corresponding datasets (precise coordinates are presented in Table 2).
Figure 5
Figure 5
Scatterplot of two principal components from k-means clustering analysis showing the existence of two distinct sperm subpopulations in efferent duct sperm (EDS) after in vitro maturation at 10 s post activation with little overlap. By red and blue colors, the cases of different clusters are marked. The ellipses of 95% confidence for clusters 1 and 2 are presented in red and blue, respectively. Black dots are centroids of corresponding clusters.
Figure 6
Figure 6
Motility parameters in sperm collected from Wolffian ducts and sperm collected from efferent ducts after in vitro maturation. (a)—Curvilinear velocity, µm s−1. (b)—linearity. EDS—sperm collected from efferent ducts, WDS—sperm collected from Wolffian ducts. Values with different letters are significantly different (Tukey test, P < 0.05, for details of the repeated measures ANOVA analysis see Table 4).
Figure 7
Figure 7
Staining of gar urogenital system. Nigrosin was injected through the urogenital opening. (a)—Location of testes (T) in the abdominal cavity. (b)—Dye is in horns (H) of the urinary bladder, which is formed by fusion of enlarged posterior portions of Wolffian ducts (WD). (c)—Dye is in WD. (d)—Dye is entering efferent ducts (ED), connecting WD with testis.
Figure 8
Figure 8
Schematic presentation of differences in the urogenital structure of gars and sturgeons.
See this image and copyright information in PMC

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