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Tubal ovum in Ochotonidae (Lagomorpha).

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TUHAL OVUM I N OCHOTOXIDAE
(LAGOMORPHA)
ELMER ROSTWICK H A R V E Y
Jloiitana Agrzciiltiiral E . z p e r ~ m o z t Station, Noittuna S t a t e College
TITO FIGURES
Descriptions of tuba1 ova of laboratory and doniestic animals arc readily found in the literature ; however, few recent
papers deal with ova of wild Eutherian mammals. Tuba1 ova
of leporids liave been described extensively by Bischoff (1842),
Van Benedin (1880), Asslietoil (1894), Gregory ( ' 3 0 ) and
others. The dimemioils of eggs in a number of species of
rriamrnals a r e listed iii reviews by Hartman ('29) and Lewis
aiid T\-right ( '35).
Braden ct al. ( '54) describes sperm penetration clspcriments on ova of rats, mice, rabbits, sheep and dogs. The appendix of their paper presents a review of observations on
spermatozoa penetration of the zona pellucida in 32 species
of 9 different orders.
Mossman ( ' 3 7 , '53) discussed the use of fetal membranes
aiid egg-uterine relationship a s taxonomic criteria. I n his
inonograph, Mossman ('37) suggested that a comparison of
fetal membranes should be done on the most primitive faniilies in the Order Lagomorpha (Ochotonidae) and Rodentia
(Aplodontidae). Subsequently, Harvey ( '58) described fetal
membranes of these primitive families.
I n this paper is described a pronuclcus-stage ovum from
Ochotonn princeps (pika) the single genus of the family
Ochotonidae, Order Lagomorpha. This ovum is compared with
ova from rabbits and selected rodents, and some discussion
of egg-sperm relationship as a taxonomic criterion is included.
Contribution from Montana State College, Agricultural Experiment Station.
P:iper KO. 417 Journal Series.
113
114
ELM Eli IIOST\VlCK HARVEY‘
klA ‘1’E 11I A LS AK 1) 31ISTROI?S
Reproductive tracts \\ere collected from pikas (Ocliotoiztr
princeys) taken at Bodie, Moiio County, California, May 14,
1%5. The tracts and ovaries were fixed in Bouiii’s fluid containing 5% acetic acid and crnbcdded in paraffin. Oviducts
and ovaries were serially sectioned at 10 p and stained with
heniatoxylin
and cosin.
V it ell us
C oroii:~ Itndiata
Poloeytc (2nd)
Froiinclci
Perivitelliiie sp:icc
Outside diametc,r of
Zolla
82.8
11-18
124.2
16.5-27
14.4
21.6
14.4
41.6
10.9
16.2
100.8
151.2
93.6
140.4
7.2
10.8
Iiiside di;i~iictcruf
2011:1
Zonn Pellwida
16-165
11-19.0
-
-
96.8
87.8
12.5
25.2
-
Cnlciilntccl ~iiensurcmeiitis 50% grc;ttcr t1i;iii ocular niicroincter readings.
This v:rlue is included t o make nl1om:iiicc for 50% sliriiikagc that may occur in
1,rcparntion of the 5hde ( H:II tiiiaii, ’29 mid Hartin:iii :ind Imvis, ’31 ). This still
iri:ry not repicsent tlic living egg diniciisioiis.
Descriptioii of pronucleus ocum
Ova of pikas are typical of mammals in size, shape aid wit11
respect to the corona 1-adiata and zona pelluckla. Table 1
shows rrieasuremcnts of the various morphological features
of tlic pronuclcus-stage egg of the pika.
Tlic vitellus of the pronucleus zygotc has three distinct
areas. The outer compact “cortical” zone (exoplasm) is 7-9 p
TI‘ljAL O V U M
115
thick (10.5-13.5 p allowing for 50% shrinkage). There is little
vacuolation in this zone suggesting a sparsity of lipid material.
The middle zone is highly vacuolated alid is 18 p thick or
27 p allowing f o r shrinkage in preparation. The central zone
in which the pronuclei lie is compact (fig. 1). The pronuclei
are equal in all dimensions.
The noii-cellular zona pellucida is tightly applied over most
of the perimeter of the vitellus. According to Gregory (’30),
Braden et al. (’54), and others there is a pcrivitelline space
in living eggs of mammals at this stage. IJntil further work
is done the absence of a definite perivitelline space in the
pika ovum may he a n artifact of slide preparation (figs. 1, 2).
The corona radiata forms a dense layer of cells around the
zoiia pellucida. Some disorganization of corona cells i q evidenced since a number of these cells were f i w i n the ovitluct
a i d others adhere loosely to several areas of the corona (figs.
1, 2).
Fifty-four spermatozoa, many with recognizable tails, were
counted lying between the inner border of the zona pellucida
and vitellus of the egg. The position of the spcrrnatozoa suggest that a definite “vitelline” (fertilization) memhranc exists
in the pika egg. I n areas where the vitcllus is f i w of thc1
zona pellucida, the “ sub-zonal” spermatozoa appear to he
held to the inner border of the zona possibly hy some restricting sub-microscopic membrane. Spermatozoa were
clearly observed to follow a contour of a possible membrane
pushed out by extrusion of the second polocyte (fig. 2).
DISCUSSION
Mossman (’37, ’53) points out the value of fetal-mcmInranes, genital tracts, and other conservative sti*ucturcs to
taxonomy. If this thesis (that fetal structures ai-e conservative) is correct, comparison of any unique occurrence during
insemination of ova would he particularly useful in the evaluation of phylogenetic relationship. Rfossman ( ’53) proposes
that regardless of rate of genetic variation of a conservative
system divergence would be relatively slow and n a i ~ o \ v .Thus,
iiitcrgradatioii ~\-ouldbe tlic rule cveii though other organ
systems were diverging widely. Lack of divergence should
make it possible to detect coniinoii characteristics among
groups widely separatcd from oiie another in other characteristics. Conversely, dissimilarity in characters of a coilservativc organ system woultl be good evidence of remote
pliylogciietic relationship.
The vitellus of the pika approximates in size that of rwhhits but is one-half again as large as the typical rodent ova
(table 1). The blastocpst of Aplodontiu, a primitive rodent,
is considcrahly smaller than a blastocyst of a comparable stage
in the pika (Harvey, '%a, '58h). It usually f o l l o ~ sthat a
small ovum gives rise to a hlastocyst of comparable size.
Braden ct al. (',54) prcseiit evidence that entry of the first
spermatozoa iiito tlie zoiia pellucitln of many mammals initiates a reactioii which precludes tlie entry of further s p e r m tozoa into the zona. In Appendix I of the above paper all
known observations of spermatozoa present in the zoiia o r
perivitelline space of 32 species of 9 orders arc summai*ized.
H e points out that the rabhit appears to he unique arnoiig
mammals in that its ova commonly have as many ;is 50
spermatozoa in the peiivitelliiie space. Twenty spcimatozoa
liave 1)eeii observed in the pciivitclline space of mole eggs ;
several to numerous " sub-zonal " spermatozoa in ova of tlie
pocket gopher and up to ten in tlie rat, mouse, guinca pig, cat,
ferret aiid bats.
Attention is drawn to studies of " sub-zoiial" spcrriiatozoa
hecause 54 of these were counted in the perivitclliiic space of
the pronucleus-stage pika ovuni. No other spermatozoa were
observed in the reproductive tract, thus it is assumed that the
maximum numbers for conditions of this pregnancy had ciitered tlic zona of the pika egg. The presence of this characteristic in the only two living faniilies of the 01dci.
Lagomorpha makes it unique for this order.
Fetal rncmhrane studies by Harvey ( '%a, '381)) indicate
that leporids aiid ochotoriids may beloiig in the same family
and that rodents and lagomorphs a r e distiiictly cliff erent when
TUHAL O V U M
117
classificatioii is based on Mossman’s criteria ( ’37). Presence
~~
in both families
of as many as 50 “ s ~ b - z o n a lspermatozoa
(Leporidae and Ochotonidae) of the Order IJagornorpha support fetal membrane studies which demonstrate closeness of
relatioriship of pikas and rabbits. ‘‘ Sub-zonal Polyspermia’ ’
iii tlie Order Lagomorplia and not in Rodcntia clearly supports evidence of rcrriote relationship of lagornorphs and
rodents a s demonstrated by other taxonomic features (Simpson, ’45).
Rc~tc~ntion
of corona cells through a t least the pronucleus
stage and possibly later occurs in lagomorphs while in rodents the corona is lost or completely disorg:aiiizcd at an
earlier stage.
SUMMARY
A pronncleus-stage ovum of pika (Ochofovzn p r i w e p s ) is
described and found to he similar in size and shape to other
mammalian ova. It is unique (as in the ovum of rabbits) in
having as many as 50 spermatozoa in the perivitelline space.
“Sub-zoiial polyspermia ” is discussed a s a taxonomic characteristic wl1icl1 supports classical methods in scparating
roclcnts and lagomorphs.
LZTERATURE CI‘I‘ET)
ASSHETON, R.
1894 A re-invcstigntion into the w r l y stages of the dcvclopiiitiit
of t h e rabbit. Quxrt. Jour. Micr. Sci., 3 7 : 113-164.
BIscsorF, T. L. W. 1842 ~iitwicklungsgcsc,liiclitc~
dcs I<a~iinrhriiEics. R Y ~ U I I schweig.
RR~ZUEN,
A. W. H., C. R. AUSTI?: ASD H. A. I>.\vID 1954 The renckiou of thc
zona pelluciila t o sperm prnctrntion. Aust. Jour. R i d . Sci., 7 ( 3 ) :
39 1-409.
GRAVES,A. P. 1945 Tlic development of t,lie goldcn hnmstcr, C7-icc(7rs nuratus
W:tterlioiisc, (luring tlie first 9 (lays. Am. J . Aiint., 7 7 ( 2 ) : 219-251.
GKEGOKY, P. W.
1930 The rnrly enibrq.ology of thc rn1)bit. Coutr. I’h~l)r!.ol.
Cnriicgic Instn., “1: 141-168.
HARTMAN,
C. G. 1929 How lsrgc is thc mammn1i:nl cgg? A rrvicw. Quart.
Rev. Riol., 4 : 373-388.
TIAIITXAX,C. G., AND W. €1. I>ETVIS 1931 F i r s t filldings of tuba1 ovn i n tlir
cow, together with notes on orxtrus. Aiint. Ree., 4 8 ( 2 ) : 267-275.
IIARVEIT,
E. R. 1958 P1acciit:itioli in Ocliotoniclnc (111 Prcss). Am. J. A n n t .
1958 Placentation i n Aploclolltidnc. ( T n Press). Tbicl.
11s
ELMIS11 ROSTWICK HARJ’EY
LEWIS,TV. H., I X D E. S. WRIGHT 1935 On the early development of the niouse
egg. Cotitr. Eiiibryol. Cariiegie Instn., 25 : 113-143.
J ~ O S S M A N , H. W.
1937 Coiiip:rrativc morphogenesis of fetal iiienibraiies and
ncccssorp uterine structures. Ibid., 26 : 129-246.
1953 The geuit:il systein atid the fetal membranes a s critcrin for
innniiiialia. pliylogetiy and taxonomy. Jo u r . 1Llamm., 34 : 289-298.
S n r ~ s o s ,(3. G. 1945 The 1)rinciplw of classification atid a classification of
iiimiinials. Bull. Aiiier. Mus. Kat. Hist., 85.
SQUIER,
R. R. 1932 Tlic living egg and early stages of its developnlent in tllc
guiuea-pig. Contr. Ehbryol. Cariiegie Instn., 33 : 223-250.
V I N I 3 k SLDEN, E. 1880 Rrclirrchcs bur l’rmbryologie des mamrniferes: In
forinntioti des fcuillcts rlicz lc lapin. Arch. de hiol., 1 : 136-224.
A B B R E V I A T I O N S IJXED I N FIGUltEB
A , artifact
CR, corona rndintn
CZ, ‘ ‘cortical ’ ’ zoiic
MZ, middle zone
PN, proiiiicleiis
I’VS, perivitelliiie space
S, spermatozoa
2nd P, second polocyte
V, vitellus
ZP, zotia prllucidn
PLATE 1
E X P L A N A T I O N OF F I G U R E S
1
Cro\\ section of pika ovum s l i o ~ i i i gthe mxle aiid fetiiale pronuclei ancl
x 500.
"sub zonal” spermatozoa. 10 .u. H 6: E.
2
Sanic. ovum as figure 1, but tlirougli n u area with the 211d polocyte. Notc
spcrnintozoxii head hcld agaiiist the zoiia pellucida near the 2nd polocTtc1.
10 p. 11 6: E. x 500.
119
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