Comparative Morphology of Mammalian Gametes

  • David M. Phillips
  • Gil L. Dryden


Among mammals there is a wide variation in gamete structure—particularly of male gametes. Interspecies differences exist on the gross level in the lengths and widths of spermatozoa and in the shapes of sperm heads. On the ultrastructural level the morphological characteristics of intracellular organelles vary widely. The degree of morphological variation in spermatozoa between different mammalian groups is so great that a number of workers have used sperm morphology as a phylogenetic trait (Harding et al., 1981, 1982; Vitullo et al., 1988, Breed and Inns, 1985; Friend, 1936; Hirth, 1960; Helm and Bowers, 1973; Linzey and Layne, 1974; Breed and Sarafis, 1979; Feito and Gallardo, 1982). What is the relevance of the wide range of sperm morphology to the fertilization process? Although the morphology of spermatozoa has been characterized in hundreds of mammalian species at the light microscopic level and in dozens of species at the EM level, fertilization has been studied in relatively few species, and even in these species the characterization is largely incomplete. It is easy to see why this is so when one considers the enormous technical problems involved in mating wild mammals and then catching the one fertilizing spermatozoon at the moment of contact with the egg in a thin section. In this chapter we compare the morphology of gametes among mammals. We consider why there is so much variation in sperm morphology and how it could relate to the fertilization process. We do not describe the surface of the mammalian spermatozoon or the sperm tail, because these are discussed in Chapter 3.


Zona Pellucida Cumulus Cell Sperm Head Sperm Morphology Cortical Granule 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson, W. A., Weissman, A., and Ellis, R. A., 1967, Cytodifferentiation during spermiogenesis in Lumbricus terrestris, J. Cell Biol. 32: 11–26.PubMedCrossRefGoogle Scholar
  2. Asa, C. S., and Phillips, D. M., 1988, Nuclear shaping in spermatids of the Thai leaf frog, Megophrys montana, Anat. Rec. 220: 287–290.PubMedCrossRefGoogle Scholar
  3. Baccetti, B., Bigliardi, E., and Burrini, A. G., 1980, The morphogenesis of vertebrate perforatorium, J. Ultrastruct. Res. 71: 272–287.PubMedCrossRefGoogle Scholar
  4. Beatty, R. A., and Sharma, K. N., 1959, Genetics of gametes III. Strain differences in spermatozoa from eight inbred strains of mice, Proc. R. Soc. Edinb. B 68: 25–51.Google Scholar
  5. Bedford, J. M., and Nicander, L., 1971, Ultrastructural changes in the acrosome and sperm membranes during maturation in the testis and epididymis of the rabbit and monkey, J. Anat. 108: 527–543.PubMedGoogle Scholar
  6. Bedford, J. M., Rodger, J. C., and Breed, W. G., 1984, Why so many mammalian spermatozoa—a clue from marsupials, Proc. R. Soc. Land. B 221: 221–233.CrossRefGoogle Scholar
  7. Braden, A. W H., 1958, Strain differences in the morphology of the gamete of the mouse, Aust. J. Biol. Sci. 12: 65–71.Google Scholar
  8. Breed, W. G., and Inns, R. W, 1985, Variations in sperm morphology of Australian Vespertilionidae and its possible phylogenetic significance, Mammalia 49: 105–108.Google Scholar
  9. Breed, W. G., and Leigh, C. M., 1988, Morphological observations on sperm—egg interactions during in vivo fertilization in the Dasyurid marsupial Sminthopsis crassicaudata, Gamete Res. 19: 131–149.PubMedCrossRefGoogle Scholar
  10. Breed, W. G., and Sarafis, V, 1979, On the phylogenetic significance of spermatozoal morphology and male reproductive tract anatomy in Australian rodents, Trans. R. Soc. S. Aust. 103: 127–135.Google Scholar
  11. Breed, W. G., Cox, G. A., Leigh, C. M., and Hawkins, P, 1988, Sperm head structure of a murid rodent from South Africa: The red veld rat, Aethomys chrysophilus, Gamete Res. 19: 191–202.PubMedCrossRefGoogle Scholar
  12. Cohen, J., 1969, Why so many sperms? An essay on the arithmetic of reproduction, Sci. Prog. Oxf. 57: 23–41.Google Scholar
  13. Cohen, J., 1983, Selection among spermatozoa, in: The Sperm Cell ( J. Andre, ed.), Martinus Nijhoff, The Hague, pp. 33–37.CrossRefGoogle Scholar
  14. Cooper, G. W, and Bedford, J. M., 1976, Asymmetry of spermiation and sperm surface charge patterns over the giant acrosome in the musk shrew, Suncus murinus, J. Cell Biol. 69: 415–428.PubMedCrossRefGoogle Scholar
  15. Cummins, J. M., 1983, Sperm size, body mass and reproduction in mammals, in: The Sperm Cell ( J. Andre, ed.), Martinus Nijhoff, The Hague, pp. 395–398.CrossRefGoogle Scholar
  16. Cummins, J. M., and Woodall, P F., 1985, On mammalian sperm dimensions, J. Reprod. Fertil. 75: 153–175.PubMedCrossRefGoogle Scholar
  17. Dekel, N., 1986, Hormonal control of ovulation, in: Biochemical Actions of Hormones, Academic Press, New York, pp. 57–99.Google Scholar
  18. Dekel, N., and Phillips, D. M., 1979, Maturation of rat cumulus oophorus—a scanning electron microscope study, Biol. Reprod. 21: 9–18.PubMedCrossRefGoogle Scholar
  19. Fawcett, D. W., 1965, The anatomy of the mammalian spermatozoa with particular reference to the guinea pig, Z. Zellforsch. Mikrosk. Anat. 67: 279–296.PubMedCrossRefGoogle Scholar
  20. Fawcett, D. W., 1970, A comparative view of sperm ultrastructure, Biol. Reprod. [Suppl.] 2:90–127. Fawcett, D. W, 1975, The mammalian spermatozoon, Dev. Biol. 44: 394–436.CrossRefGoogle Scholar
  21. Fawcett, D. W, and Hollenberg, R., 1963, Changes in the acrosome of the guinea pig spermatozoa during passage through the epididymis, Z. Zellforsch. Mikrosk. Anat. 60: 276–292.CrossRefGoogle Scholar
  22. Fawcett, D. W, and Phillips, D. M., 1970, Recent observations on the ultrastructure and development of the mammalian spermatozoon, in: Comparative Spermatology ( B. Baccetti, ed.), Academia de Linceri/Academic Press, Rome, pp. 13–29.Google Scholar
  23. Feito, R., and Gallardo, M., 1982, Sperm morphology of Chilean species of Ctenomys (Octodontidae), J. Mamm. 63: 658–661.CrossRefGoogle Scholar
  24. Flaherty, S. P., and Breed, W. G., 1983, The sperm head of the plains mouse, Pseudomys australis: Ultrastructure and effects of chemical treatments, Gamete Res. 8: 231–244.CrossRefGoogle Scholar
  25. Flaherty, S. P, and Breed, W. G., 1987, Formation of the ventral hooks on the sperm head of the plains mouse, Pseudomys australis, Gamete Res. 17: 115–129.PubMedCrossRefGoogle Scholar
  26. Forman, G. L., and Genoways, H. H., 1979, Biology of Bats of the New World, Phyllostomadtidae Part III Special Publication 16,The Museum of Texas Tech University Lubbock, pp. 177–204.Google Scholar
  27. Friend, G. F., 1936, The sperms of the British Muridae, Q. J. Microsc. Sci. 78: 419–443.Google Scholar
  28. Furieri, P, 1970, Sperm morphology in some reptiles: Squamata and Chelonia, in: Comparative Spermatology ( B. Bacetti, ed.), Academic Press, New York, pp. 115–132.Google Scholar
  29. Green, J. A., and Dryden, G. L., 1976, Ultrastructure of epididymal spermatozoa of the Asiatic musk shrew, Suncus murinus, Biol. Reprod. 14: 327–331.PubMedCrossRefGoogle Scholar
  30. Harcourt, A. H., Harvey, P. H., Larson, S. G., and Short, R. V, 1981, Testis weight, body weight and breeding system in primates, Nature 293: 55–57.PubMedCrossRefGoogle Scholar
  31. Harding, H. R., Carrick, F. N., and Shorey, C. D., 1977, Spermatozoa of Australian marsupials: Ultrastructure and epididymal development, in: Reproduction and Evolution, Fourth International Symposium on Comparative Biology of Reproduction ( C. H. Tyndale-Biscoe, ed.), Australian Academy of Science, Canberra, pp. 151–152.Google Scholar
  32. Harding, H. R., Carrick, F. N., and Shorey, C. D., 1979, Special features of sperm structure and function in marsupials, in: The Spermatazoon ( J. M. Bedford, ed.), Urban & Schwarzenberg, Baltimore, pp. 289–303.Google Scholar
  33. Harding, H. R., Carrick, F. N., and Shorey, D. C., 1981, Marsupial phylogeny: New indications from sperm ultrastructure and development in Tarsipes spenserae, Search 12: 45–47.Google Scholar
  34. Harding, H. R., Woolley, P. A., Shorey, C. D., and Carrick, E N., 1982, Sperm ultrastructure, spermiogenesis and epididymal sperm maturation in Dasyurid marsupials: Phylogenetic implications, in: Carnivorous Marsupials ( M. Archer, ed.), Royal Zoological Society of New South Wales, Sydney, pp. 659–673.Google Scholar
  35. Hartman, C. G., 1916, Studies in the development of the opossum: Didelphis virginiana I. History of early cleavage II. Formation of the blastocyst, J. Morphol. 27: 1–83.CrossRefGoogle Scholar
  36. Heath, E., Schaeffer, N., Merit, D. A., and Jeyendran, R. S., 1987, Rouleaux formation by spermatozoa in the naked-tail armadillo, Cabassous unicinctus, J. Reprod. Fertil. 79: 153–158.PubMedCrossRefGoogle Scholar
  37. Helm, J. D., and Bowers, J. R., 1973, Spermatozoa of Tylomys and Ototylomys, J. Mamm. 54: 769–772.CrossRefGoogle Scholar
  38. Hendelberg, J., 1965, On different types of spermatozoa in Polycladida turbellaria, Ark. Zool. 18: 267–304.Google Scholar
  39. Hill, J. P, 1910, The early development of the marsupials with special reference to the mature cat (Dasyurus viverrinus), G. J Microsc. Sci. 56: 1–134.Google Scholar
  40. Hirth, H. F., 1960, The spermatozoa of some North American bats and rodents, J. Morphol. 106: 77–83.PubMedCrossRefGoogle Scholar
  41. Holstein, A. F., and Roosen-Runge, E. C., 1981, Atlas of Human Spermatozoa, Grosse Verlag, Berlin.Google Scholar
  42. Illison, L., 1969, Spermatozoal head shape in two inbred strains of mice and their Fl and F2 progenies, Aust. J. Biol. Sci. 22: 947–963.Google Scholar
  43. Jamieson, B., 1987, The Ultrastructure and Phylogeny of Insect Spermatozoa, Cambridge University Press, Cambridge.Google Scholar
  44. Katz, D. F, and Overstreet, J. W, 1980, Mammalian sperm movement in the secretions of the male and female genital tracts, in: Testis Development, Structure and Function ( A. Steinberger, ed.), Raven Press, New York, pp. 481–489.Google Scholar
  45. King, B. F., and Tibbits, F. D., 1977, Ultrastructural observations on cytoplasmic lamellar inclusions in oocytes of the rodent Thomomys, Anat. Rec. 189: 263–272.PubMedCrossRefGoogle Scholar
  46. Koehler, J. K., 1966, Fine structure observations in frozen-etched bovine spermatozoa, J. Ultrastruct. Res. 16: 359–375.PubMedCrossRefGoogle Scholar
  47. Koehler, J. K., 1977, Fine structure of spermatozoa of the Asiatic musk shrew, Suncus murinus, Am. J. Anat. 149: 135–151.PubMedCrossRefGoogle Scholar
  48. Koehler, J. K., Clark, J. M., and Smith, D., 1985, Freeze-fracture observations on mammalian oocytes, Am. J. Anat. 174: 317–329.PubMedCrossRefGoogle Scholar
  49. Krause, W. J., and Cutts, J. H., 1979, Pairing of spermatozoa in the epididymis of the opossum (Didelphis virginiana): A scanning electron microscopic study, Arch Histol. Jpn. 42: 181–90.PubMedCrossRefGoogle Scholar
  50. Krzanowska, H., 1976, Types of sperm-head abnormalities in four inbred strains of mice, Acta. Biol. Cracow (Ser. Zool.) 19: 79–85.Google Scholar
  51. Linzey, A. V, and Layne, J. N., 1974, Comparative morphology of spermatozoa of the rodent genus Peromyscus (Muridae), Am. Mus. Novitates 2355: 1–20.Google Scholar
  52. Martan, J., and Hruban, Z., 1970, Unusual spermatozoan formations in the epididymis of the flying squirrel, Glaucomys volans, J. Reprod. Fertil. 21: 167–170.PubMedCrossRefGoogle Scholar
  53. Nicander, L., and Bane, A., 1966, Fine structure of the sperm head in some mammals with particular reference to the acrosome and the subacrosomal substance, Z. Zellforsch. 72: 496–515.PubMedCrossRefGoogle Scholar
  54. Nicosia, S. V, Wolf, D. P, and Inoue, M., 1977, Cortical granule distribution and cell surface characteristics in mouse eggs, Biol. of Reprod. 57: 56–74.Google Scholar
  55. Olson, G. E., 1980, Changes in intramembranous particle distribution in the plasma membrane of Didelphis virginiana spermatozoa during maturation in the epididymis, Anat. Rec. 197: 471–486.PubMedCrossRefGoogle Scholar
  56. Olson, G. E., and Winfrey, V. P, 1988, Characterization of the postacrosomal sheath of bovine spermatozoa, Gamete Res. 20: 329–342.PubMedCrossRefGoogle Scholar
  57. Olson, G. E., Noland, T. D., Winfrey, V. P., and Garbers, D. L., 1983, Substructure of the postacrosomal sheath of bovine spermatozoa, J. Ultrastruct. Res. 85: 204–218.PubMedCrossRefGoogle Scholar
  58. Parker, G. A., 1970, Sperm competition and its evolutionary consequences in the insects, Biol. Rev. 45: 525–567.CrossRefGoogle Scholar
  59. Parker, G. A., 1982, Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes, J. Theor. Biol. 96: 281–294.PubMedCrossRefGoogle Scholar
  60. Pedersen, H., 1972, The postacrosomal region of the spermatozoa of man and Macaca arctoides, J. Ultrastruct. Res. 40: 366–377.PubMedCrossRefGoogle Scholar
  61. Phillips, D. M., 1970, Insect sperm: Their structure and morphogenesis, J. Cell Biol. 44: 243–277.PubMedCrossRefGoogle Scholar
  62. Phillips, D. M., 1974, Spermiogenesis, Academic Press, New York.Google Scholar
  63. Phillips, D. M., 1975, Mammalian sperm structure, in: Handbook of Physiology ( R. Greep and E. Astwood, eds.), Waverly Press, Baltimore, pp. 405–419.Google Scholar
  64. Phillips, D. M., 1977, Surface of the equatorial segment of the mammalian acrosome, Biol. Reprod. 16: 128–137.PubMedCrossRefGoogle Scholar
  65. Phillips, D. M., and Bedford, J. M., 1985, Ultrastructure of spermatozoa of the musk shrew Suncus murinus, J. Exp. Zool. 235: 119–126.PubMedCrossRefGoogle Scholar
  66. Phillips, D. M., and Bedford, J. M., 1987, Sperm-sperm associations in the loris, Gamete Res. 18: 17–23.PubMedCrossRefGoogle Scholar
  67. Phillips, D. M., and Fadem, B. H., 1987, The oocytes of a new world marsupial, Monodelphis domestica: Structure, formation and function of the enveloping mucoid layers,.1. Exp. Zool. 242: 363–371.CrossRefGoogle Scholar
  68. Phillips, D. M., and Kalay, D., 1984, Observations on mechanisms of flagellar motility deduced from backwards swimming bull sperm, J. Exp. Zool. 231: 109–116.PubMedCrossRefGoogle Scholar
  69. Phillips, D. M., and Shalgi, R., 1980a, Surface properties of the mouse and hamster zona pellucida and oocyte, J. Ultrastruct. Res. 72: 172.Google Scholar
  70. Phillips, D. M., and Shalgi, R., 1980b, Surface properties of the zona pellucida, J. Exp. Zool. 213: 1–8.PubMedCrossRefGoogle Scholar
  71. Phillips, D. M., Shalgi, R., and Dekel, N., 1985, Mammalian fertilization as seen with the scanning electron microscope, Am. J. Anat. 174: 357–372.PubMedCrossRefGoogle Scholar
  72. Phillips, D. M., Asa, C., and Stover, J., 1987, Ultrastructure of spermatozoa of the white-naped crane, J. Submicrosc. Cytol. 19: 489–494.PubMedGoogle Scholar
  73. Ploen, L., Ekwall, H., and Afzelius, B. A., 1979, Spermiogenesis and the spermatozoa of the European common shrew, Sorex aruneusl, J. Ultrastruct. Res. 68: 149–159.PubMedCrossRefGoogle Scholar
  74. Rattner, J. B., 1972, Nuclear shaping in marsupial spermatids, J. Ultrastruct. Res. 40:498–512. Retzius, G., 1906, Spermatozoa of the Marsupialia, Biol. Unters. N.F. 13: 77–86.Google Scholar
  75. Retzius, G., 1909a, Spermatozoa of Didelphys, Biol. Unters. N.E 14: 123–126.Google Scholar
  76. Retzius, G., 1909b, Spermatozoa of mammals, Biol. Unters. N.E 14: 163–178.Google Scholar
  77. Retzius, G., 1910, General contribution to the knowledge of spermatozoa with special reference to nuclear material, Biol. Unters. N.F. 15: 63–82.Google Scholar
  78. Sato, M., Motow, O., and Sakoda, K., 1966, Electron microscopic study of spermatogenesis in the lung fluke (Paragonium miyasakii), Z. Zellforsch. 77: 232–243.CrossRefGoogle Scholar
  79. Shalgi, R., and Phillips, D. M., 1983, Role of cumulus in zona penetration, in: Proceedings of the 4th International Symposium on Spermatology-Seillac ( J. Andre, ed.), Martinus Nijhoff, The Hague, pp. 90–93.Google Scholar
  80. Suttle, J. M., Moore, H. D. M., Peirce, E. J., and Breed, W. G., 1988, Quantitative studies on variation in sperm head morphology of the hopping mouse, Notomys alexis, J. Exp. Zool. 247: 166–171.CrossRefGoogle Scholar
  81. Szollosi, D., 1967, Development of cortical granules and the cortical reaction in rat and hamster eggs, Anat. Rec. 159: 431–446.PubMedCrossRefGoogle Scholar
  82. Talbot, P., and Dicarlantonio, G., 1984, Ultrastructure of opossum oocyte investing coats and their sensitivity to trypsin and hyaluronidase, Dev. Biol. 103: 159–167.PubMedCrossRefGoogle Scholar
  83. Temple-Smith, P. D., and Bedford, J. M., 1980, Sperm maturation and the formation of sperm pairs in the epididymis of the opossum, Didelphis virginiana, J. Exp. Zool. 214: 161–171.PubMedCrossRefGoogle Scholar
  84. van Dujin, C., 1975, Bibliography (with review) on maturation of spermatozoa, Biol. Reprod. 25: 241–248.Google Scholar
  85. van Dujin, C., and van Voorst, C., 1971, Precision measurements of dimensions, refractive index and mass of bull spermatozoa in the living state, Mikroskopie 27: 142–167.Google Scholar
  86. Vitullo, A. D., Roldan, E. R. S., and Marani, M. S., 1988, On the morphology of spermatozoa of tuco-tucos, Ctenomys (Rodentia: Ctenomyidae): New data and its implications for the evolution of the genus, J. Zool. Lond. 215: 675–683.CrossRefGoogle Scholar
  87. Yanagamachi, R., and Teichman, R. J., 1972, Cytochemical demonstration of acrosomal proteinase in mammalian and avian spermatozoa by a silver proteinase method, Biol. Reprod. 6: 87–97.Google Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • David M. Phillips
    • 1
  • Gil L. Dryden
    • 2
  1. 1.The Population CouncilNew YorkUSA
  2. 2.Biology DepartmentSlippery Rock UniversitySlippery RockUSA

Personalised recommendations