Unusual ampullary sperm crypts, and behavior and role of the cumulus oophorus, in the oviduct of the least shrew, Cryptotis parva

The gametes of the least shrew, Cryptotis parva, were studied in regard to their maturation and structure, and with particular emphasis on their behavior in the fallopian tube, from the time of ovulation until the appearance of two-cell embryos beginning some 9 h after ovulation. Cryptotis spermatozoa are organized according to the conventional eutherian mold, with the exception of a barbed perforatorium and an unusual plasma membrane density lent by a bristly coat where it overlies the acrosome rim. In the epididymis they undergo a maturation of the capacity for motility and an -S-S-related stabilization of the nucleus and tail organelles, with the cauda housing only approximately 4-5 million spermatozoa. Mating involves penile locking and also the deposition of a modest vaginal plug that covers the cervix. The short (4-5 mm) fallopian tube has three regions-a simple isthmus, a relatively narrow ampulla populated throughout by ciliated crypts, and a crypt-free terminal infundibulum-the fertilization site. Unlike the situation in most mammals, the tubal isthmus was devoid of spermatozoa in mated females before and after ovulation, which occurred approximately 13 h post-hCG and produced a mean of 5.7 ova. However, the ampulla then housed similar to 1500 active cells in groups within the ciliated crypts, sometimes together with leukocytes but with few spermatozoa above in the infundibulum. Within about 1 h after their ovulation from approximately 400-mu m follicles, eggs were penetrated while in the infundibulum despite the nonexpanded hyaluronidase-resistant state of the cumulus oophorus. However, on moving down to the ampulla by 2-4 h after ovulation, the dense cumulus around fertilized eggs appeared to proliferate and began to disperse coincidentally with secretion of a hyaluronidase-sensitive matrix in which hundreds of motile spermatozoa often became enmeshed. This cumulus change also occurred around unfertilized eggs, though more slowly, but not around fertilized or unfertilized eggs cultured in vitro. Thus, cumulus matrix production appeared to be stimulated to an important degree by factors in the oviduct, not by preovulatory gonadotropins as in many mammals. Although cumulus-invested eggs were fertilized readily in vitro, cumulus-free eggs of the same age were never fertilized, and spermatozoa bound to the zona pellucida had intact acrosomes. This and related evidence from other shrews makes it seem likely that the soricid cumulus has an essential role in fertilization and may induce the acrosome reaction.