Prolonged epididymal sperm storage in vespertilionid and rhinolophid bats, provides an interesting experimental model for the study of spermatozoa epididymal maturation. We examined the presence of the cytoplasmic droplet, and the sequential induction of capacitation and the acrosome reaction in spermatozoa obtained from different epididymal regions (caput, corpus, cauda) throughout the annual reproductive cycle of Corynorhinus mexicanus (C. mexicanus). This is a vespertilionid bat that stores spermatozoa in the epididymis for several months after testes regression. The number of sperm recovered from the different epididymal regions indicate that epididymal transit in C. mexicanus is rapid. The persistence of a high percentage of sperm cells with cytoplasmic droplet in cauda epididymis was observed in addition to a low index of capacitation and acrosome reaction in sperm cells obtained from the corpus epididymis. There was a significant increase in the percentage of capacitated and acrosome reacted spermatozoa during the storage of sperm cells in the cauda epididymis and the percentage of capacitated spermatozoa was consistently, and significantly, higher (p < 0.05) in cauda compared to the corpus epididymis at all studied dates. Tthe process of epididymal maturation in C. mexicanus is completed in the caudal region of this organ encompassing a significant period. Our results also indicate that in C. mexicanus, and in other vespertilionid and rhinolophid bats that show the same temporal asynchrony in the function of male reproductive organs, the final phases of epididymal maturation and storage are, apparently, independent of testicular function.
The bat Corynorhinus mexicanus provides an interesting experimental model for the study of epididymal sperm maturation because after spermatogenesis and the regression of the testes, this bat stores sperm in the epididymal cauda for several months. Earlier research conducted by our group suggested that sperm maturation in this species must be completed in the caudal region of the epididymis. One of the major signal transduction events during sperm maturation is the tyrosine phosphorylation of sperm proteins. The aim of the present study was to comparatively evaluate tyrosine phosphorylation in spermatozoa obtained from the caput, corpus and cauda of the epididymis during the sperm storage period. The maturation status of the sperm was determined by the percentage of capacitation and tyrosine phosphorylation in sperm obtained from the epididymis. The highest proportion of tyrosine phosphorylation was registered after the sperm had reached the cauda epididymis during the middle of the storage period. In conclusion, in Corynorhinus mexicanus and most likely in other chiropteran species with an asynchronous male reproductive pattern, epididymal sperm maturation ends in the caudal region of the epididymis and is related to the time that the sperm remains in the epididymis before mating activity.
The results of this work support the existence of sperm storage in Corynorhinus mexicanus, a vespertilionid bat endemic to Mexico, and evidence is presented that modulation of peroxidative toxicity plays a role in the mechanism of prolonged sperm storage in Chiroptera. Spermatozoa were obtained from C. mexicanus by retrograde perfusion of the cauda epididymis, and from genital washings from previously inseminated females captured during reproductive activity. Ejaculated pig spermatozoa were simultaneously studied as controls. Lipid peroxidation was determined in both the presence and absence of genital secretions obtained from previously inseminated female C. mexicanus by measuring malondialdehyde generated during aerobic incubation of spermatozoa suspensions. The number of spermatozoa recovered from the cauda epididymis decreased steadily from November through January. Corpora lutea were observed in January. None of the female bats captured between October and January were pregnant, but some females captured in mid-February were already pregnant. Spermatozoa of C. mexicanus showed substantial lipid peroxidation activity (0.64 ± 0.11 nmol malondialdehyde was produced by 108 spermatozoa per 22 h), about half of that observed in ejaculated pig spermatozoa. Incubation of pig and C. mexicanus spermatozoa in the presence of bat female genital tract washings induced highly significant concentration-dependent inhibition of lipid peroxidation.
It has been proposed that reduced glutathione (GSH) or other thiol reagents may participate in the basic mechanism by which sperm-decondensing activity is accomplished. However, in vitro, these reagents seem to be inactive and require the presence of other chemicals, usually detergents. Heparin binds specifically to the sperm membrane and provokes the decondensation of human sperm and the activation of DNA transcription and synthesis. However, the concentrations at which these effects occur seem to be higher than those expected under physiological conditions. In the present study, thiol reagents at 10 mM concentration, either alone or combined, were completely ineffective in inducing any significant nuclear decondensation after prolonged exposures (24 hr) of incubation. Heparin, 153.8 microM, was capable of inducing only a small increase in nuclear swelling. However, GSH at concentrations as low as 0.1 mM in combination with heparin induces decondensation of human sperm nuclei in vitro. When GSH concentration was kept constant at 5 mM, nuclear decondensation was induced with heparin at concentrations as low as 11.6 microM, and a maximal decondensation (90%) was obtained with only 21.6 microM of heparin. The latter is more than ten times less than the minimal active concentration of heparin used alone.
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