< o o l o p d Journal Ofthe Iinnenn So&p (1989),95: 11 7-124. With I figure
Ovarian programming of gamete progression
and maturation in the female genital tract
R. H. F. H U N T E R
School of Agriculture, Universily o f Edinburgh, Wesl Mains Road,
Edinburgh EH9 3JG*
\Yhilst the t-atc or displaccmrrit and migration of sperm cells in the female reproductive tract of
rodcmts, Eirm auimals and humans has a t t r x t r d attention ti)^ at least 50 years, the overriding purposr
ofsperm transport has not always h w n kept in focus. 'l'his report is concerned with spcrniiitozoii t h a t
can pent-tratc the rgg invcstmcnts and promote formation of a zygote, judgements involving a
surgical approach and subsequent phasc-contrast microswpy. A minimum period of 6-8 hour5 was
required for such sprrmatozoa t o hc rstablishcd i n thc oviducts in sheep and cows mated at the onset
o f O C S t I U S . Sperm wcrc then arrested in the caudal 1 2 cm of the isthmrrs for 17-18 hours or more until
j u s t before t h e moment of ovulation, whcn they wcre activated and displaced onwards to the site of
fcrtilization at the ampullary-isthmic junction. 'l'hc timc-scale of thcsc cuts diiTcrs in pigs as a rcsult
of the intra-uterine site of ejaculation and the 40-hour interval between the onset of ocstrub and
ovulation. hut the pre-ovulatory scqurstcritlg ofviahle spermatozoa in the caudal tip of the oviduct is
conspicuous for 36 hours o r i~iorc.'l'his function or the oviduct appears to he under local control lrom
ovarian follicular hormones and, as judgcd by sperm motility a n d membranous changes, so does the
procrss of capacitation. Completion of capacitation is intcrpreted as a pcri-ovulatory evctit.
KLY \.\'OKDS: Gametes
oviduct physiology.
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sprrmatozoa
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capacitation
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ovaries
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hormones
hypcrartivation
CON'IEN'I'S
Introduction .
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Experimental proccdurcs .
Observations .
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Sheep
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P i g s . .
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'l'hc functiotlal sperm rcscrvoir
Capacitation of spermatozoa
Acknowlrdgctncnts
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Refereti(.cs
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I17
1 19
1 I9
119
120
I21
I22
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124
INTRODUCI'ION
A vital component of fertility is the process of fertilization itself. However, a
successful union of gametes represents the culmination of diverse physiological
events, amongst which a timely arrival of male gametes at the site of fertilization
in the oviducts cannot be taken for granted. This caution applies especially to
*Present address: Faculty of Veterinary Mrdicine ( C R R A ) , University of Montreal, C.P. 5000, Saint
Hyacinthc, Qur:bec, Canada.
0024-4082/89/020 1 1 7 +OX $03.00/0
117
((3 1989 'l'hc
Lintwan Socicty of London
118
R. H . F. HUNTER
domestic farm animals in which procedures of artificial insemination are widely
employed, but it is also relevant to our own species where psychosomatic
influences appear to play a significant r6le in gamete transport within the oviduct.
Concerning the female gamete, eggs are shed from Graafian follicles as
secondary oocytes, usually with some investment of granulosa cells, although the
extent of such follicular cells varies with species. For example, in primates and in
pigs, there is a rather dense cumulus plug whereas in cows and sheep, granulosa
cells are seldom detected around recently ovulated eggs. Because the fimbriated
extremity of the oviduct intimately embraces the ovary at the time of ovulation,
capture of the follicular contents is not a hazardous process in mammals (cJ
birds), and transport of eggs to the site of fertilization at the ampullary-isthmic
junction is rarely a problem. Factors contributing to this transport include waves
of peristaltic contraction in the myosalpinx, the ab-ovarian beat of cilia lining the
ampulla, and movements of the supporting mesentery-the mesosalpinx. The
time required for passage of eggs from the ovarian surface to the ampullaryisthmic junction may be of the order of 10-15 minutes in laboratory species (see
Harper, 1961) or 30-45 minutes in farm species such as pigs (Hunter, 1974).
There is tentative evidence for a final maturation of the secondary oocyte during
this phase of transport; indeed, some form of membranous change would be
anticipated, bearing in mind the contrast between follicular and tuba1
environments.
Before considering the process of sperm transport within the mammalian duct
system in detail, it is necessary to suggest why further studies are valuable at a
time when classical physiological approaches have given way to molecular
techniques. First and foremost, the rate of sperm transport to the site of
fertilization has long been a controversial issue, as perusal of the extensive
literature would quickly demonstrate. Reported values have ranged from small
numbers of minutes to large numbers of hours. Second, studies on sperm transport
have seldom considered the competence of the population of cells in question, and
yet the ability of spermatozoa to penetrate and activate secondary oocytes is
surely the critical aspect. Measurements on the rate of sperm transport should
therefore be concerned with viable or functional spermatozoa. Third, the rate of
transport may vary with the stage of oestrus, and studies in the large domestic
species with their relatively long pre-ovulatory intervals may reveal new facets of
sperm storage and capacitation on the one hand, and ofoviduct physiology on the
other.
Reviews on the topic of sperm transport in the female genital tract have been
numerous during the last thirty years, but many of the interpretations are
compromised by the shortcomings outlined above and/or by technical
considerations. Outstanding among the latter are ( 1) the artefacts imposed by
procedures of slaughter, with massive contraction of the smooth musculature and
a consequent displacement of unattached cells; and (2) the fact that spermatozoa
may remain in certain regions of the tract for prolonged periods of time-even for
the duration of pregnancy. Thus, the presence of sperm cells in the higher reaches
of the tract after an experimental mating does not necessarily infer that the
observed spermatozoa were derived from such a mating. A further caution
concerns the failure to distinguish rigorously between the results of natural mating
and artificial insemination. T h e latter approach may have introduced a
suspension ofsperm cells deeper into the tract than would occur at coitus. Notable
SPERM-OVIDUCT INTERACTIONS
119
among the recent essays on the topic of sperm transport are those ofYanagimachi
(1981), Harper (1982), Mortimer (1983), Overstreet (1983), Hawk (1987) and
Hunter (1987a, 1988). References to the earlier literature can be found in these
works.
EXPERIMENTAL PROCEDURES
We have examined the length of time after natural mating within which a
sufficient population of spermatozoa is established in the oviducts to ensure
subsequent fertilization of the egg(s). This differs from previous experiments
which simply recorded the number of spermatozoa in smears, flushings or sections
of the oviduct contents or tissues. Our approach involved mating during
spontaneous oestrous cycles, followed by abdominal surgery under general
anaesthesia at specific intervals after mating. During a rapid mid-ventral
exposure of the reproductive tract, the oviducts were transected from the uterus,
and any subsequent passage of spermatozoa prevented by double ligatures of fine
braided silk placed at the utero-tubal junction. The animals recovered promptly
from anaesthesia and were left to ovulate. Eggs were flushed from the oviducts at
autopsy one or two days later, fixed and stained, and then examined by phasecontrast microscopy. Observations were made on the incidence offertilization and
the number of accessory spermatozoa in or attached to the zona pellucida.
Fertilization would be expected only if viable spermatozoa were already present
in the oviducts at the time of transection, whilst the number of spermatozoa
associated with the egg membranes should give some estimate of t11e size of
oviduct sperm populations at different intervals after mating.
OBSERVATIONS
Sheep
Four experiments have been completed in sheep. The first indicated that in
ewes mated at the onset of oestrus, fertilized eggs were not found as a sequel to
transection four or six hours after mating, whereas 30% and 100% of the eggs
were fertilized after transection at eight and ten hours, respectively (Hunter,
Nichol & Crabtree, 1980). The mean number of spermatozoa associated with the
zona pellucida at these later times increased from 2.0 to 13.4. The results are
interpreted as indicating only a gradual progression of viable spermatozoa from
the vagina through the cervix and uterus to the oviducts, with a threshold value of
six to eight hours for adequate numbers of competent spermatozoa to pass the
utero-tubal junction early in oestrus.
A second experiment examined the transport of viable spermatozoa in relation
to the time of ovulation: one group of ewes was mated at the onset of oestrus and a
second group close to the time of ovulation some 24 h later. Based on the results of
the previous study, the oviducts were transected from the uterus eight hours after
mating. Statistically significant differences were found in the incidence of
fertilization in the two groups, 20% of the eggs being fertilized in the group mated
at the onset of oestrus compared with 94% after the peri-ovulatory mating
(Hunter, Barwise & King, 1982). The numbers of accessory spermatozoa
increased in a parallel manner. This experiment therefore indicated an ovarian
endocrine influence on the rate of sperm transport, with an accelerated phase of
transport close to the time of ovulation. Accelerated sperm transport near the time
I20
R H F HUNTER
of ovulation has also been reported in rabbits, hamsters and rats, and may
represent a ‘biological safety mechanism’ that strives to ensure fertilization in
situations ofdelayed mating. A related requirement might be an enhanced rate of
capacitation (see below).
The third study examined the pre-and peri-ovulatory distribution of viable
spermatozoa within the oviducts by placing the ligatures 1.5-2.0 cm along the
isthmus instead of at the utero-tuba1 junction. Since some competent spcrmatozoa
would have entered the oviducts within eight hours of mating, it was important to
study their subsequent ad-ovarian progression. All ewes were mated at the onset
of’oestrus and the transection performed 10-27 h later. A large series of results
indicated that viable spermatozoa were arrested in the caudal 1.5-2.0 cm of the
oviduct during most of the period of oestrus, and only released towards the site of
fertilization in the last hour before ovulation (Hunter & Nichol, 1983). Sperm
motility appears to be suppressed in the caudal portion of the oviduct during the
pre-ovulatory interval, and parallels have been drawn with sperm storagc in the
caudal portion of the epididymal duct. Sperm activation (i.e, hyperartivation
expresscd as whiplash motility) and release at the time of ovulation may depend
principally on endocrine programming from the mature Graafian follicle(s), with
an incisive control achieved by a local counter-current vascular and lymphatic
transfer of ovarian hormones (Hunter, Cook & Poyser, 1983).
A final experiment in this series has been to examine the ad-ovarian progression
of spermatozoa within the oviducts at and shortly after the time of ovulation.
Once again, post-coital ligatures have been placed along the isthmus
progressively closer to the site of fertilization. The results indicate a discrete
release ofspermatozoa in the first hour after ovulation (Hunter & Nichol, 1986a),
during which time the block to polyspermy would be established in the egg
membranes. In the hours thereafter, appreciable numbers of spermatozoa reach
the eggs and attach to the zona pellucida, but they arrive too late to penetrate into
the vitellus and disturb the chromosome constitution of the fertilized egg. A
further finding in this study was that widely-spaced episodes of multiple mating
apparently did not alter the pre-ovulatory distribution of viable spermatozoa
already resident in the caudal isthmus, since there was no detectable influence of
this procedure on fertilization o r on the number of accessory spermatozoa.
A1though these experiments describe the rate of progress of viable spermatozoa
into and within the oviducts of spontaneously-mating ewes, they do not indicate
the proportion of the time required for cervical as distinct from uterine transport.
Previous estimates suggest that some 30-60 minutes may be needed for the
establishment of a cervical sperm population (Dauzier, 1958). We are currently
examining this aspect of the transport process, and would concur that effective
colonization of the cervix with viable spermatozoa requires a substantial period in
minutes ( 1 2 0 minutes) in most ewes mated once early in the period of oestrus.
This phase ofsperm transport again stands in contrast to the findings in rabbits, in
which sperm colonization of the cervix leading to high levels offertility (93% eggs
fertilized) occurred within five minutes of a single mating (Bedford, 197 1 ) .
Pigs
The time scale of sperm transport in domestic pigs contrasts with that i n
ruminants. This is because of the large volume of semen introduced almost
SPERM-OVIDUCT INTERACTIONS
121
directly into the uterus at ejaculation, and the fact that the uterine extremity of
the oviducts is bathed with semen by the completion of mating. Cervical and
uterine transport therefore do not require specific discussion. In these
circumstances, it is not surprising to find that sufficient spermatozoa have entered
the oviducts within 15 minutes of mating to fertilize in due course at least a
proportion of the eggs. Throughout the pre-ovulatory phase of oestrus, sperm
motility appears essential for traversing the utero-tuba1 junction and gaining
access to the oviduct lumen. During this passage, sperm cells are largely divested
of seminal plasma and resuspended in female tract fluids. Two studies based on
examination of large numbers of eggs indicated that (a) sufficient boar
spermatozoa have entered the oviducts within one hour of mating to ensure
subsequent fertilization of morc than 90% of the eggs ovulated (Hunter, 1981),
and (b) in pigs mated at the onset ofoestrus, viable spermatozoa are arrested close
to the utero-tuba1 junction for some 36 h or more; different episodes of multiple
mating did not displace viable spermatozoa already established in the isthmus
(Hunter, 1984). Ad-ovarian release and displacement of such spermatozoa were
activated only shortly before ovulation. A means whereby ovarian endocrine
control of this release might be obtained has been described (Hunter, Cook &
Poyser, 1983).
T H E FUNCTIONAL SPERM RESERVOIR
Studies on the rate of sperm transport and the distribution of viable cells in
sheep, cows and pigs all indicate that the fertilizing population of spermatozoa
spends most of the pre-ovulatory interval sequestered in the caudal portion of the
oviduct, emphasizing the fact that this portion of the duct system acts as the
functional sperm reservoir. Apart from being responsive to local ovarian control
mechanisms referred to above, this site of pre-ovulatory storage would also enable
sperm cells to be maintained beyond the reach of the (post-coital) uterine
population of polymorphonuclear leucocytes, and beyond the stimulatory
influence of uterine fluids, and yet not too distant from the site of fertilization at
the ampullary-isthmic junction. The intervening portion of isthmus would permit
regulation of the number of ascending spermatozoa close to the time of ovulation,
thereby minimizing the risk of polyspermic penetration. Recent observations on
sperm storage and release in the isthmus of mice and hamsters, and the possible
involvement of intermittent phases of sperm adhesion to the endosalpinx, include
ihose of Smith, Koyanagi & Yanagimachi (1987) and Suarez (1987).
The physiology of the oviduct lumen in relation to gametes and embryos is
mown to be complex, in effect there being a series of microenvironments within
:he duct and sophisticated interactions of luminal factors with sperm cells
:Hunter, 1988). These microenvironments doubtless underlie the storage of
;permatozoa and their subsequent activation, and seemingly produce a close
Ioordination in the meeting of male and female gametes. Evidence exists for a
emperature gradient in the oviduct, with a reduced temperature in the caudal
sthmus during the phase of pre-ovulatory sperm arrest (Hunter & Nichol,
1986b). Whilst this could influence the physiology of sperm cells directly, it might
3e at least as significant as an indicator of regional differences in vascular and
ymphatic activity. Components of the pre-ovulatory microenvironment in the
umen of the isthmus also include specific chemical constituents and modified gas
ensions. Such features may be accentuated in the porcine oviduct by an influence
I22
R. H. F. HUNTER
of seminal plasma which bathes the utero-tuba1 junction. Parallels between the
storage function of the Miillerian duct and that of the Wolffian duct (cauda
epididymidis) have been emphasized.
CAPAGITATION OF SPERMATOZOA
The above considerations undoubtedly bear on the final maturation of sperm
cells before fertilization-the
so-called process of capacitation. However, an
understanding of the pre-ovulatory physiology of the oviduct suggests that
traditional views of capacitation may not be strictly correct. Rather than this
terminal maturation requiring a given period of time in the female tract after
mating (e.g. 1-5 h, according to species), capacitation appears dependent upon
peri-ovulatory events. The latter relationship becomes crucial in the large
domestic species, in which spermatozoa remain in the oviducts for 20-40 h before
ovulation-and even longer in equids. Clearly, there would be little value in
achieving capacitation within a few hours of ejaculation if such capacitated cells
(hyperactive, fragile and short-lived) were to be non-functional by the time of
ovulation. In fact, specific oviduct proteins may act to suppress the achievement
of capacitation and/or the ensuing processes of the acrosome reaction and
hyperactivation until shortly before ovulation (4. the Wolffian duct protein,
immobilin).
Classical studies of capacitation, both in vivo and in uitro, have invariably been
performed in a ‘post-ovulatory environment’, that is, in the presence of eggs
and/or their investments, and this may have contributed to a misinterpretation.
Previous explanations for a prolonged availability of capacitated spermatozoa in
the female tract based upon (a) the heterogeneous nature of the cell population in
the ejaculate, and (b) variable rates of sperm maturation should now be
questioned, at least for the large domestic species (Hunter, 1987b). Even so, the
precise means of obtaining ovarian follicular control of sperm release and
capacitation remains an enigma. Locally-transmitted hormonal influences from
the Graafian follicle seem most probable, and steroids, peptide hormones and
prostaglandins may all contribute. Although the rBle of a counter-current system
from the ovarian vein to the oviduct branch of the ovarian artery has been
stressed above, the contribution of the autonomic nervous system and
catecholamines to activation and redistribution of oviduct spermatozoa requires
further consideration. The nature of hormone receptors on the sperm surface
should provide guidance here.
I n seeking a broader significance for the process of capacitation in mammals,
Bedford (1983) has proposed that it and/or the ensuing hyperactivation
phenomenon may represent an evolutionary adaptation to the presence of cellular
investments around the newly-ovulated egg, that is the granulosa cells associated
with the surface of the zona pellucida. ‘This may well be so, but it does not offer an
explanation for the chronological aspects referred to above. A rather different
(though not exclusive) interpretation is proposed by Hunter (1987a). In this, the
endocrine activity of the pre-ovulatory Graafian follicle(s)-the structure that
releases the female gamete-is considered paramount for programming the
physiology of the female genital tract and thereby the final maturation of
spermatozoa. By mechanisms that are not clearly understood, although doubtless
involving extremely sensitive and critical thresholds, follicular secretion of diverse
SPERM-OVIDUCT INTERACTIONS
123
Figure 1. Model to illustrate the manner whereby the endocrine activity of the pre- or peri-ovulatory
Graafian foIlicle acts locally to programme the membrane configuration and motility of spermatozoa
in the lumen of the oviduct isthmus. Gonadal hormones (from the follicles) act on the oviduct
epithelium whose secretions in turn influence the nature of the luminal fluids. Expression of
capacitation is reasoned to be a peri-ovulatory event, at least in the large farm species with a
protracted interval between the gonadotrophin surge and ovulation. A, Intart, relatively quicsccnt
spermatozoon under the overall influence of one or more pre-ovulalory follicles. Membrane vesiculation
on the anterior part of the sperm head is suppressed, as is the development ofwhiplash activity in the
flagellum presumably due to local molecular control mechanisms. The lumen of the oviduct isthmus
is extremely narrow, and myosalpingeal contractions are reduced. B, An acrosome-reacted,
hyperactive spermatozoon under the influence of a Graafian follicle on the point of ovulation. The
patency of the oviduct isthmus has commenced to increase, enabling expression of thc whiplash
pattern of flagellar beat. Progression of such spermatozoa to the site of fertilization is also aided by
enhanced contractile artivity of the myosalpinx. This model accords with the observation that high
proportions of spermatozoa undergoing the acrosome reaction in ruminants are found only in the
ampulla adjoining the ovulatory ovary and only at or following ovulation.
hormones is thought to control capacitation of spermatozoa in the distal isthmus
of the oviduct and the ensuing hyperactivation (i.e. whiplash motility) and
acrosome reaction. A tentative model is presented in Fig. 1. Hence, the
significance of capacitation is seen not primarily as a n adaptation to the cellular
investments of the mammalian oocyte-which, as noted above, are sparse in
cattle and sheep by the time the egg reaches the site of fertilization-but rather as
a vital response to endocrine signalling by the pre-ovulatory follicle.
ACKNOWLEDGEMENTS
The author’s own studies were supported by grants from the Agricultural
Research Council (U.K.). Gratitude is also expressed to Robert Nichol for
124
R. H . F. H U N T E R
technical assistance, Drs Charlotte Chalmers and Lawrence Smith for
commenting on a draft of the manuscript, and Frances Anderson for preparing
the typescript.
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