Skip to main content
NCBI home page
Journal of Anatomy logoLink to Journal of Anatomy
. 1997 Feb;190(Pt 2):275–288. doi: 10.1046/j.1469-7580.1997.19020275.x

Posttesticular development of spermatozoa of the tammar wallaby (Macropus eugenii)

DADI SETIADI 1 ,2 , MINJIE LIN 1 ,✉, JOHN C RODGER 1
PMCID: PMC1467605  PMID: 9061449

Abstract

Tammar wallaby spermatozoa undergo maturation during transit through the epididymis. This maturation differs from that seen in eutherian mammals because in addition to biochemical and functional maturation there are also major changes in morphology, in particular formation of the condensed acrosome and reorientation of the sperm head and tail. Of spermatozoa released from the testes, 83% had a large immature acrosome. By the time spermatozoa reached the proximal cauda epididymis 100% of sperm had condensed acrosomes. Similarly 86% of testicular spermatozoa had immature thumb tack or T shape head-tail orientation while only 2% retained this immature morphology in the corpus epididymis. This maturation is very similar to that reported for the common brush tail possum, Trichosurus vulpecula. However, morphological maturation occurred earlier in epididymal transit in the tammar wallaby. By the time spermatozoa had reached the proximal cauda epididymis no spermatozoa had an immature acrosome and thumbtack orientation. Associated with acrosomal maturation was an increase in acrosomal thiols and the formation of disulphides which presumably account for the unusual stability of the wallaby sperm acrosome. The development of motility and progressive motility of tammar wallaby spermatozoa is similar to that of other marsupials and eutherian mammals. Spermatozoa are immotile in the testes and the percentage of motile spermatozoa and the strength of their motility increases during epididymal transit. During passage through the caput and corpus epididymis, spermatozoa first became weakly motile in the proximal caput and then increasingly progressively motile through the corpus epididymis. Tammar wallaby spermatozoa collected from the proximal cauda epididymis had motility not different from ejaculated spermatozoa. Ultrastructural studies indicated that acrosomal condensation involved a complex infolding of the immature acrosome. At spermiation the acrosome of tammar wallaby spermatozoa was a relatively large flat or concave disc which projected laterally and anteriorly beyond the limits of the nucleus. During transit of the epididymal caput and proximal corpus the lateral projections folded inwards to form a cup like structure the sides of which eventually met and fused. The cavity produced by this fusion was lost as the acrosome condensed to its mature form as a small button-like structure contained within the depression on the anterior end of the nucleus. During this process the dorsal surface of the immature acrosome and its outer acrosomal membrane and overlying plasma membrane were engulfed into the acrosomal matrix. This means that the dorsal surface of the acrosomal region of the testicular tammar wallaby sperm head is a transient structure. The dorsal acrosomal surface of the mature spermatozoon appears ultrastructurally to be the relocated ventral surface of the acrosomal projections which previously extended out beyond the acrosomal depression on the dorsal surface of the nucleus of the immature spermatozoon.

Keywords: Sperm maturation, acrosome, epididymis, disulphides, mBBR fluorescence, marsupials

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bedford J. M., Calvin H. I. Changes in -S-S- linked structures of the sperm tail during epididymal maturation, with comparative observations in sub-mammalian species. J Exp Zool. 1974 Feb;187(2):181–204. doi: 10.1002/jez.1401870202. [DOI] [PubMed] [Google Scholar]
  2. Bedford J. M., Calvin H., Cooper G. W. The maturation of spermatozoa in the human epididymis. J Reprod Fertil Suppl. 1973 Jul;18:199–213. [PubMed] [Google Scholar]
  3. Bedford J. M., Nicander L. Ultrastructural changes in the acrosome and sperm membranes during maturation of spermatozoa in the testis and epididymis of the rabbit and monkey. J Anat. 1971 Apr;108(Pt 3):527–543. [PMC free article] [PubMed] [Google Scholar]
  4. Calvin H. I., Bedford J. M. Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. J Reprod Fertil Suppl. 1971 May;13(Suppl):65–75. [PubMed] [Google Scholar]
  5. Harding H. R., Carrick F. N., Shorey C. D. Spermiogenesis in the brush-tailed possum, Trichosurus vulpecula (Marsupialia). The development of the acrosome. Cell Tissue Res. 1976 Aug 16;171(1):75–90. doi: 10.1007/BF00219701. [DOI] [PubMed] [Google Scholar]
  6. Harding H. R., Carrick F. N., Shorey C. D. Ultrastructural changes in spermatozoa of the brush-tailed possum, Trichosurus vulpecula (Marsupialia), during epididymal transit. Part II: The acrosome. Cell Tissue Res. 1976 Aug 16;171(1):61–73. doi: 10.1007/BF00219700. [DOI] [PubMed] [Google Scholar]
  7. Jones R. C., Clulow J. Interactions of sperm and the reproductive ducts of the male tammar wallaby, Macropus eugenii (Macropodidae: Marsupialia). Reprod Fertil Dev. 1994;6(4):437–444. doi: 10.1071/rd9940437. [DOI] [PubMed] [Google Scholar]
  8. Jones R. C., Hinds L. A., Tyndale-Biscoe C. H. Ultrastructure of the epididymis of the tammar, Macropus eugenii, and its relationship to sperm maturation. Cell Tissue Res. 1984;237(3):525–535. doi: 10.1007/BF00228437. [DOI] [PubMed] [Google Scholar]
  9. Mate K. E., Kosower N. S., White I. G., Rodger J. C. Fluorescent localization of thiols and disulfides in marsupial spermatozoa by bromobimane labelling. Mol Reprod Dev. 1994 Mar;37(3):318–325. doi: 10.1002/mrd.1080370311. [DOI] [PubMed] [Google Scholar]
  10. Mate K. E., Rodger J. C. Stability of the acrosome of the brush-tailed possum (Trichosurus vulpecula) and tammar wallaby (Macropus eugenii) in vitro and after exposure to conditions and agents known to cause capacitation or acrosome reaction of eutherian spermatozoa. J Reprod Fertil. 1991 Jan;91(1):41–48. doi: 10.1530/jrf.0.0910041. [DOI] [PubMed] [Google Scholar]
  11. Mercado E., Carvajal G., Reyes A., Rosado A. Sulfhydryl groups on the spermatozoa membrane. A study with a new fluorescent probe for SH groups. Biol Reprod. 1976 Jun;14(5):632–640. doi: 10.1095/biolreprod14.5.632. [DOI] [PubMed] [Google Scholar]
  12. Olson G. E., Orgebin-Crist M. C. Sperm surface changes during epididymal maturation. Ann N Y Acad Sci. 1982;383:372–392. doi: 10.1111/j.1749-6632.1982.tb23179.x. [DOI] [PubMed] [Google Scholar]
  13. Phillips D. M. Ultrastructure of spermatozoa of the wooly opossum Caluromys philander. J Ultrastruct Res. 1970 Nov;33(3):381–397. doi: 10.1016/s0022-5320(70)90030-4. [DOI] [PubMed] [Google Scholar]
  14. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Reyes A., Mercado E., Goicoechea B., Rosado A. Participation of membrane sulfhydryl groups in the epididymal maturation of human and rabbit spermatozoa. Fertil Steril. 1976 Dec;27(12):1452–1458. doi: 10.1016/s0015-0282(16)42263-6. [DOI] [PubMed] [Google Scholar]
  16. Shalgi R., Seligman J., Kosower N. S. Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane. Biol Reprod. 1989 May;40(5):1037–1045. doi: 10.1095/biolreprod40.5.1037. [DOI] [PubMed] [Google Scholar]
  17. Sistina Y., Lin M., Mate K. E., Robinson E. S., Rodger J. C. The unique stability of the marsupial sperm acrosomal membranes examined by unprotected freeze-thawing and treatment with the detergent Triton X-100. Reprod Fertil Dev. 1993;5(1):1–14. doi: 10.1071/rd9930001. [DOI] [PubMed] [Google Scholar]
  18. Temple-Smith P. D., Bedford J. M. The features of sperm maturation in the epididymis of a marsupial, the brushtailed possum Trichosurus vulpecula. Am J Anat. 1976 Dec;147(4):471–499. doi: 10.1002/aja.1001470407. [DOI] [PubMed] [Google Scholar]
  19. Temple-Smith P. D. Comparative structure and function of marsupial spermatozoa. Reprod Fertil Dev. 1994;6(4):421–435. doi: 10.1071/rd9940421. [DOI] [PubMed] [Google Scholar]
  20. WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Zirkin B. R., Chang T. S., Heaps J. Involvement of an acrosinlike proteinase in the sulfhydryl-induced degradation of rabbit sperm nuclear protamine. J Cell Biol. 1980 Apr;85(1):116–121. doi: 10.1083/jcb.85.1.116. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES