Novel sperm storage and behavior of gametes in the fallopian tube of the white-toothed shrew,Crocidura russula monacha

Abstract

The gametes of an insectivore, the white‐toothed shrew, Crocidura russula monacha, present certain idiosyncratic features not seen in most other eutherian mammals. The spermatozoa display an acrosome of giant proportions, and are produced in relatively small numbers. In trans‐illuminated oviducts examined with DIC optics, spermatozoa were first sequestered in languid clutches within the isthmus in deep narrow crypts, with some eventually ingested by the crypt epithelium. Then, at ovulation (ca. 15 hr after hCG), many ascended to occupy “bubble‐like” ciliated crypts distributed randomly within the ampulla, as active groups of acrosome‐intact spermatozoa. However, eggs (3.95; range 2–6) were first retained for several hours and were fertilized in an upper crypt‐free infundibulum before moving down to the ampulla. At fertilization, individual spermatozoa penetrate an unusually compact matrix‐free cumulus oophorus which is stabilized by intercellular junctions, is insensitive to hyaluronidase, and persists for ∼13 hr around fertilized and for ∼24 hr around unfertilized eggs. In contrast to the free ampullary spermatozoa, active spermatozoa accumulating within the cumulus all had shed the acrosome, an observation consistent with evidence from other shrews suggesting that the cumulus may necessarily induce the acrosome reaction in this ancient line. Hypertrophy of the acrosome, isthmic sperm storage crypts, and stable cumulus oophorus that develops a peri‐zona space, all may prove to be typically crocidurine characteristics of use where the classification of a shrew is in doubt. J. Exp. Zool. 277:262–273, 1997. © 1997 Wiley‐Liss, Inc.

Spermatozoa of the Shrew, Suncus murinus, Undergo the Acrosome Reaction and Then Selectively Kill Cells in Penetrating the Cumulus Oophorus1

“…In another (crocidurine) shrew, Suncus murinus, the giant form of the acrosome made it possible to see that this fan-like organelle is lost in all spermatozoa present within the cumulus around unfertilized and fertilized eggs, whether motile or not, and in any spermatozoa binding to the zona surface of unfertilized eggs [5,7]. The same was true for Crocidura russula [8], another crocidurine shrew with a similarly large acrosome [9]. The evidence suggests, therefore, that the cumulus around the eggs of shrews has an essential role in fertilization-most likely as the inducer of the acrosome reaction.…”

“…In the perifertilization period in the crocidurine shrews, S. murinus and C. russula, acrosome-free spermatozoa within the cumulus typically congregate within the perizonal space-a cavity brought by withdrawal of the otherwise intact cumulus from around the zona pellucida [7,8]. However, in reaching that space, it is not clear how the spermatozoa penetrate a barrier of cumulus cells linked at multiple sites by specialized cell-cell junctions or at what point in its interaction with the cumulus the acrosome of Suncus begins to react; and finally, whether the reaction involves the point fusions between the plasma and outer acrosomal membranes seen in other mammals.…”

Achieving monospermy or preventing polyspermy?

“…71,75,[83][84][85] In human in vitro fertilization, it is the normal practice to inseminate cumulus intact oocytes with a concentration of at least 100,000 spermatozoa/mL. 86 The oocytes remain in this sperm bath for 18 hours until they are cleaned and transferred to fresh medium for a check on whether they have been fertilized correctly or not.…”

The 'hybrid' character of the gametes and reproductive tracts of the African shrew, Myosorex varius, supports its classification in the Crocidosoricinae

“…None the less, it is clear that various details of their reproductive tracts and the form and behaviour of their gametes differ quite obviously from one shrew to another, and 'diversity' already seems an appropriate first watchword for the reproductive system in shrews. So far, these differences have tended to distinguish the crocidurine subfamily, exemplified by Suncus and Crocidura (Bedford et al, 1994(Bedford et al, , 1997a Bedford, unpublished). Therefore, it was our expectation that Myosorex, as a putative member of the Crocidurinae, would help to substantiate as definitively 'croci¬ durine' some unusual reproductive characteristics manifested by Suncus and Crocidura, but not by indisputable soricines such as Sorex, Blarina and Cryptotis.…”

“…Scale bar represents 210 µ . (Bedford et al, 1994(Bedford et al, , 1997a. In addition, the glans penis in both Suncus and Crocidura is covered with spines.…”