EFFECTS OF CAUTHERYZAT工ON OF TETRODONTOPHORA B工ELANENS1S (COLLEMBOLA)
EGGS FROM OV1POS1T10N T1LL PREMATURE BLASTODERM STAGE
咽1NSTRUCT工VE EVENTS 工N EARLY DEVELOPMENT

Czes主aw Jura
Sugadaira Mont在 ne Research Center，University of Tsukuba，Sanada，Nagano，386‑22 Japan(Perm
昌n
ent Address: Zoologic呂 l 工nstitute，Jagiellonian Uロiversity，ul. Karasia 6，30‑060 Krakow，poland)

The ability of the fertilized egg or ofthe deve10ping embryo toreadjust，following 日 xperimental intervention，toward norma1 dev巴 lopment
V昌 ries from speci邑 s to species even wi七hin order.

But generally speaking the

Pterygota may be divided into t官 o groups.
Considerab1e differences exist between species in re日pect to the extendof the territorywhichis occupiedbythegermanl呂 ge官 工 thinth邑 egg. The e雪gsof short germ anlage typ巴 hav巴 great regulativ巴 power，in opposition to thos巴of long germ an1age type which ar日 determined.

T~ese

two main groups a~ 巴characterized a1so at other levels，startinヲ from type of oviposition，throughegg cytoarchitecture，up to the length of time r巴 quired for hatching.

1ngeneral， 七 he eggs of short ger田 anl丑 ge ar控 produced in re8ult of panoistic
oogenesis，wh日n laid，are characterized by thin peripheral cytoplasmic

layer(peripla8m) and developmental period of these eg守 $ 工 8 long. Th日 巴 gg8 of the
8econd type are produced in result of meroistic oogenesi8，they h丑 ve thickperiplasm (Fig. 1) 品 nd short developmental period (for review se巴 Sander
1983)•

Th控 egg typ巴 s outlines 品 bove ar日 of course extremes with v台ry variants in
between，nevertheless，they remain in agreement with separation of Pterygot昌
into two main taxa: H哲 郎 imetabol丑 and Holometabola

1

2

c
. JuraFig. 1.

Two pterygotan egg types (drawn toscale). The eggs are seen from left hand side andthe region of periplasm spotted， the region ofgerm anlage spotted and stippled.

Represented

are: A‑ Achaeta domesticus (adapted from Mahr，
1960)， Drosophila melanogaster (adapted from Tur‑ner and Mahowald，1976).

p

p
b
c

dgycp
Fig. 2. Effects of cautheryzation of Tetrodontophora eggs: A‑ immediately
after oviposition，B‑ at 8‑blastomere stage，C‑ localization of coagulated egg
portions in relation to germ anlage in eggs cautherized at 8‑blastomere stage
and succeeded development. Details in text. b‑ blastoderm，c‑blastodermic
cuticle，d‑ dorsal organ，g‑ germ anlage，h‑ chorion，p‑ coagulated egg
portion，y‑ yolk，v‑ vitelline membrane.

3

Errects orCautheryzation orTetrodontophora Eggs

According to the regulativ睦 power of th告(Apterygota，Ametabola) very little is known.

eggs of wingless ins号 cts

工n 1975 Jura has shown that theeggs ofTetrodontophora，wh桂 n cautheryzed prior to 8ωblastomere stage，are notab1e to repair d昌 mage. During successiv
号
years further developmenta1 st昌 ges
were tested，from 8‑blastomere to premature blastoderm stage. Resu1t日 of both
series of 暗 xperiments are summarized in this essay.
Tetrondontophora is especi昌 11y intriqu邑

The eggs of this speci告 S 丑 reproduced in result of p01ytrophic oogenesis but they are characterized byextremely thin perip1asm， 10ng germ an1age (Jura， 1965) and very 10ng
deve10pmental p君 主 iod (about 7 months).
The eggs of :!:etrodontophor~ are very suitab1e for experimenta1
manipulation because they are comparative1y 1arge (0.5 mm in diamet日r
)
.

The

品n
sparent and the progress of d邑 velopm色 nt in living
chorion is sミlfficiently tr

egg may be obs巴 rved.
For testing the regu1ative capacity of the eggs of Tetrodontophora th日
thermocaut母E

as used.

In a11 cases on1y eggs peripheries were injured (formethod se日 Jura 1975).

Th日 smallest lesions，which could be obtained by th日官

m日thod used，measured about 150 um in diameter，embraced about 8 も of egg
surface and about 1.5 % of egg volume into the depth of about 20 um.

The egg話

were also cauthe、
工yzed above this 1imit，up to lesions invo1ving about 20 も ofegg volume.
Since the living eggs are spherical and nothing can be observed which
would indicate their polarity，for cautheryzation the egg poles were check巴dhaphazardly.

工n each particular experim自 nt no less than 300 eggs were

cautherysed，thus the possibi1ity of injuring of the same egg pole in given
S日 ries of experiment was e
xcluded.

The eggs of Tetrodontophor~ exhibit a phase of total c1控 avage pr告 1iminary
to the formation of blastoderm.
synchronous.

The first two nuc1ear divisions are

These two nuc1ear divisions are comp1eted within an undivided

yolk mass，each qu品 drant of which becomes nuc1eated and the egg then divides
directly into four equal blastomeres (Fig. 3 control).

The third c1eavage

division，perpendicular to the previous two，is again equa1 and in r日 sult of
this 8‑blastomere stage is produced.

From this last stage th告 furrows do not

inv01ve th控 wh01e yolk material of b1astomeres，and innermost parts of pyrami叩

dal blastomeres are cut off as anuc1eate y01k mass日 s，then the yo1k masses
fuse into a single mass fi11ing the interior of the embryo， 1桂 昌 ving the 1ayerof blastomeres at the surface.

At about 64‑ce11s， radia1 divisions ensue inthe pyramidal b1astomeres，cutting of y01ky cells invards which unite withcentral yo1k mass 畠 nd became yolk c控 11s or primary 9控 rm cells. The peripher呂 l

4C. Jura

EXPERIMENTS

∞

、
J

c
n

、

u

4
訟

w

M

司

mの 吋 刃m明uhy‑刃ZO ︾∞‑=吋︿明HO刃OmH
Fig. 3. Diagram summarizing results of cautheryzation of Tetrodontophora eggs
from oviposition till premature blastoderm stage (experiments 1‑4 after Jura，
1975).

Details in text.

Effects ofCautheryzation 口f Tetrodontophora Eggs

5cells continue to divide with tangential spindles and again at every division
the innermost yolky parts of blastom巴 res are cut off.
stage the peripheral blastomeres became free of yolk.

At about 2500‑cell

Now they are irregulary

spherical in shape，loosely dispersed at the egg surface and represent pr巴
mature blastoderm (Fig. 4). The blastomeres continue to divide and give rise
to uniform mature blastoderm.
The eggs were cautheryzed from oviposition till premature blastoderm
stage (compare Fig. 4).

The effect of cautheryzation was not visible

immediately (Fig. 5)，only after some time the coagulated egg content wasobservable as milky spot.

For observations only those eggs were selectedwhich showed clearly a coagulation of peripheral region.
Cautheryzation of eggs immediately after oviposition，at 2‑ or 4‑nucleus
stage gave same results.

About 50 宅 of embryos failed to develop shortly

after cautheryzation.

The abnormalities took unity of form.

developmental processes were limited to the nuclei mitotic divisions only.

TheIn

all survived eggs depolarization of cleavage spindles，in relation to eachother and in relation to egg surface，was observed (Fig. 2A; see also Jura
1975 Figs. 2 and 3).

In opposition to controls，the mitotic divisions did notshow synchronization.

Within no one of these eggs cytokinesis occurred. Inr巴 sult of described abnormalities all eggs of this series of experim巴 nts diedafter several nucl巴 i divisions (Fig. 3 experiments 1，2 and 3). Analysis ofsections rev巴 al巴 d that the embryos r巴 presented many nuclear masses with nosigns of morphological differentiations.
The eggs cautheryzed at 4‑blastomere stage (Fig. 3 experiment 4) nevercontinued development，all died shortly aft巴 r operation.
Beginning with 8‑blastomere stage the results were completely different).
from those describ巴 d above (Fig. 3 experiment 5，6，7 and 8

We have also to

stress out that beginning with 8‑blastomere stage the analysis of exper工mental
eggs was much more easier then in the pr巴 vious case.

Amongst both living aswell as fixed eggs the borderlines betwe巴 n damaged and unaffected parts wer巴
well observable.

When eggs were cautheriz巴d at more advanc巴d stages，then the

8‑blastomere stage， the moment of operation was especially easy to determine
since the killed blastomeres kept unchanged shapes during long time.
The eggs cautheryzed at 8‑blastomere stage， as the former ones，d工d notshow visibl巴

eff巴 cts

immediately after operation (Fig. 5). Only after

prolonged period of time a milky spots were observable marking the coagulate
areas.

The mortality of the eggs operated at this developmental stag巴 was

も of these 91 宅 di巴d immediately after op巴 ration
very high， reached about 97 ，or somewhat latter，about 3 も developed into germ anlage but did not passc
. Jura6

Fig. 4. Embryo of Tetrodontophora at premature blastoderm stage as seen underscanning electron microscope.
Fig. 5.

Living cautheryzed embryo at 6‑blastomere stage.

The effect of

cautheryzation is not visible immediately after operation (compare in thisrespect Figs.6‑9).
Fig. 6.

Same embryo as shown in Fig. 5 but two days older.

Arrows show

incissions forming between cautheryzed and uninjured egg portions.
Fig. 7.

Same embryo as shown in Fig. 5 but four days older.

Beginning ofseparation of coagulated portion from the rest of the embryo body (arrows).
Fig. 6.

Whole mounted experimental embryo of the same age as show in Fig. 7.

Note separation of coagulated region (arrow).
Fig. 9. Same embryo as shown in Fig. 5 but one month older. The coagulated
egg portion already separated (arrow).

7

Effects of Cautheryzation of Tetrodontophora Eggs

beyond invagination stage.

Only about 3も succeeded invagination (Fig. 3

experiment 5)，developed further and b巴 fore hatching.did not show externallymorphological abnormalities. However，the retardation of dev巴 lopment of theseembryos，when compared with controls，ranged about two months.
Analysis of living 巴ggs cautheryzed at 8‑blastomere stage，which survived
operation，revealed that the cleavage of injured blastomeres was temporalilyarrested，while uninjured ones cl巴争 ved further.

Meantime，between uninjured

and injured embryo portions incisions appeared，especially well observable on
As the development proceeded， the incisions

living material (Fig. 6).

deepened and in result of this the uninjur巴 d and injured portions became
separated from each other (Fig. 6‑9).

After separation the blastomeres being

temporarily arrested in development recovered lost time and the embryos passed
through successive developmental stages，comparabl巴 to those of controls(Figs. 2B，3 experiment 5).
Survived eggs of this series of experiments，analysed at germ anlage
stage， showed different localization of coagulated separated egg portions inrelation to embryo (Fig. 2C).
Cautheryzation of the eggs at 16‑blastomere stage or at more advanced
stages，up to premature blastoderm stage，born same effects as in case of
cautheryzation of8‑blastomere stage (Fig. 3 experiments 6，7 and 8). Also
the retardation of developmental processes was similar. Mark巴 d difference
concerned the percentage of operated eggs which succeeded in passing beyond
the germ anlage stage. The percentage strikingly increased accordingly to theage of the operated eggs (Tab. 1). Moreover，beginning with 400‑blastom巴 restage some eggs in which about 12 宅 of their volume was coagulated could
regulate further development and at prehatching stage did not show externallyabnormalities.

Thus the proportions of fragments，which could b巴 killed

raised accordingly to more advanced age of embryo.

Table1. Capacity of Tetrodontophor~ eggs for complete recovery fol‑lowing cautheryzation of about 1.5も of ooplasmic content.

Stage treated

8

18

36

100

400

2500

3

3

5

9

18

2
1

(blastomere no.)宅of embryos (of total300) which succeeded
development

8c. JuraThe first impression which on邑 may get when ana1ysing figure 3，beingsummary of obtained resu1ts，is that the egg of !etrodontophora up to 4‑
b1astomere stage is not ab1e to repair d昌 mage，but beginning with 8‑b1astomere
日 tage shows great r
日 gu1ative power.

Short1y speaking， th日 egg is first

determinative then regu1ative in type.

However， these resu1ts are open for

C日rtain criticism.

1事74) has centrifuged Tetrodontophora 桂 gg priorKsiazkiewicz‑I1ij控 va (c1eavage using 10w speed. This procedur
告 詰tr昌七 ified th号邑ヲヲ cytop1asm to gaveband of 1ipid drop1ets， solub1e cytoplasm and yolk granule日
p唱 rpendicular to the c母 ntrifuga1 direct工on.

arranged

The treatment has b思 en shown tohave no effect on the subsequent deve10pment of ferti1ized egg，the embryo
before hatching was normal. This implies that the regu1ative response may
ref1ect the experimenta1 technique uti1ized，but v邑 ry striking difference incapacity for regulation exhibited by the eggs of !etrodontophora fo110wing
cautheryzation and c母 ntrifugation must be 思 xplained.
Eggs cau七herized prior to c1e昌 V呂 ge did not 器ucceeded development becauseof:‑ desynchronization of nuc1ei mitos母 s，【depolarization of mitotic spind1es orientation，‑ formation of supernumerous nuc1ei descendants in resu1t ofarrest of cytokinesis.
Sinc
色by the method used on1y egg periphery was inju主 ed we may conc1ude thatsyngamy initiates developmen七 but in egg periphery there exists extracaryotic.
inform昌 tion， 官 hich r母 gulates the behaviour of nuc1ei undergo'ing 出 itos色 s
Extracaryo七ic information contro1s， or most probab1y， 丑 lso initi丑 tes ear1y$日qu母 stration of egg oop1asm into first four individua1 c日 11s.

conc1u日 ion does not contradict with th日
centrifugation.

Such

re日u1ts obtained by means of

It is w日 11 known that 10w 日 peed centrifugation does not

destroy egg cortex which is much more stiff than the i‑nner oop1asm. on theother hand，the conclusion is a1so in agr告 emen七 with recen七 findings th
呂t inmost insects species the genom邑 of zygote nucleus is not on1y
inform品 tionfor e母 rly

embryogenesis (s合 住 Sander，
1空83).

詰

tore of

Unfortun丑 te1y themethod used is not pos日 ib1e to reso1v
号
the prob1em in which component of egg
periphery the extracryotic information is 呂 ituated.
brane or under‑ lying perip1asm?

Within the p1asma mem‑

Since both components were injured by themethod used.
工n case of Tetrodontophoril we must p品 y sp
日ci昌 1 attention to 4叩

bl王
， stomere s
tages.

and 8‑The 4‑blastomere stage is the last being not able tor桂 adjust after cautheryzation，while 8 blastomere stage shows surprising叩

9Effects of Cautheryzation of Tetrodontophora Eggs

capacity for complet自 regulation，though both s、tages are morphologicallysimilar.

To give ans官 er for this question we mus七 七 urn ag品 in to norm呂 ldevelopment.
From 8‑blastomer日 stage begins transition from total to superficial
cleavage and thus this stage must be already equiped with information for
decissive developmental ev日nts.

It is reasonable to postulate that at 4ble
ミs
tomere stage，or during the 七ransition fro認 4ゃ 七 o 8‑blastoll
出 re stage，new
information is elaborated b巴 cau自 由 beginning with 8‑blastom日 r巴 stag巴 th日process of yolk system form呂 tion must be controled.
Jura (1966)， Jura and Krzysztofowicz (1ヲ77) have document巴 d that in
吐~etrodontophora

midgut origins exclusively from yolk cells.

日asing on thisfinding we m昌 y postulate that the tr昌 nsition from tota工 to sup邑 rficial
cleavage may be homologized with gastrulation.

It is well known fact that inev邑 ry 品 nimaエ group the pregastrula is a critical stage for further
development. This stage is extremely sensitive for any intervention.

In caseof Tetrodontophor~ most probably 4‑blastomere stage is such a sensitive phasein which important events occur leading to equip 8‑bl担 stomere stage withnecessary information for gastrulation. Question is what is the nature ofthis inform呈七 ion?
It is reasonable to postulate that new information is connect日 d with
rapid increase of gene expression. The gene products start at this time tointerplay with extracaryotic inform呂 tion，as it occurs in other animal groups
at the onset of gastrulation.

This postulation finds al日o support in results

1ヲ75).
obtained by G丑 nc丑 rzewicz (The last author， by m桂 昌 ns of histochemical

reactions， has shown at 日一 blastomere stage a particularly high RNA
concentration in the central area of egg，including th令 innermost p品 rts of
blastomeres destined for future yolk system (compare Gancarzewicz，1975; Fig.
8).

It has b日目 n clearly d巴 monstrat日d in diverse animal groups that synthesisof v呂 rious molecular speci告 s of RNA，by embryonic cells is not inェ
tiatedimmediately after fertilization，for ins日 cts in particular. There are evi
dences th昌七 in insect embryos mid‑cl邑 呂 vage st丑 ges may represen七 丑 n e呂 E工ier
synthesis of rRNA.

We may a日sum巴 自 在 me for Tetrodontophor!'!.，and becaus日 from

8 blastomere stage the nuclei are active 呂 nd interpl丑y between caryotic and勾extracaryotic information occurs，from th工s stage the embryo is able for repro
吋graming its development in cas巴 of damag色。
We may postulate such events because the egg of 'retrodontophora shows
another properties being similar between many groups of animals.

This is th告common abili七y of e丑 rly embryos to regulate their proportions following analternation in normal size. As w自 have seen in these studies the normally

10

C. Juraproportioned embryos can deve10p from 82 % 日 ized fragment日 of cautheryzed eggs
at 400‑b1astomere stage. In this 1ast case not on1y oop1asm was ki11ed but
a1so b1astomere nuc1ei.

Thus the embryo of Tetrodontophora exhibits the.
universa1ity conc告 rning the totipotentia1ity of b1astomer桂 nuc1ei
Another fact is of interest more from the evo1utionary than from deve10p‑
menta1 point of view. In Pterygota 10ca1ized cautheryzation of the surface
oop1asm，prior to c1eavage or at intralecita1 nuclei multiplication phase，
does not prevent formation of c邑 llu1ar blastoder訟 (See Counce， 1973).

1
.
怠
主
主Q‑

dontophora a1so sho時 s transitional intra1ecita1 nuc1ei mu1tip1ic
昌七 ion phase(fir日t and second nuclei division) but descendants of zygote nuc1eus are notable， in case of cortex damage，to form cellular blastoderm.

Apparently theegg of 1.etrodontophora at ear1y developmenta1 p邑 riod represents different
在m
ic system from that of pterygote egg cl告 aving pure1y superfici昌 lly.
dyn

The

egg of Tetrodontophor~ is at ear1y period comparab1e rather to those of amphi‑
bian or mo11uscan 日ggs，in which partia1 injury of cortex after fertilization
causes arrest of cytokinesis (Brachet and Hubert，1972).
The differ暗 nc告 between Tetrodontophor~ and Pterygota eggs is probab1yconnected 腎 ith different mechanis罷 which regu1ates form呂 tion of ce11u1丑 r
b1astoderm.

As we remember， in Tetrodontophora beginning with 8‑b1astomere

stag日 at every fo11owing cleavage th巴 innermost parts of blastomere are cut ofas yolk masses.

As the blastomeres became narrow，the nucleus and as日ociatedcytop1asmic ha10 within each blastomere moves outwards 七owards the 告 xposed
surface of the ce11.

Such process of formation of blastoderm is connectedwith repetitious synthesis and lossing of c日 11 plasma membranes.

This type of

b1astoderm formation is energy absorptive and in conseguence of it the dev巴 ‑叩

10pment is relatively sluwed and may be estimated as primitive.

In Pt白 rygota

the cleaving nuc1ei，with 七heir cytop1asmic ha1o，wander direct1y to peri‑
plasm. Synthesis of c告 11 plasma membranes is comp1etely ommited unti1 th色
nuclei invade the perip1asm.

Thus the eggs of 1
.etrodontophora make link

between the eggs c1eaving pure1y totally and those cl日 aving pur日 ly super‑
ficia11y ones.
The eggs of Tetrodontophor呂 習 君 主 e haphaz昌 rd1y injur百 d. Th号 killed egg
portions were 10c11Effects ofCauther日zationofTetrod
口，ntophoraEqqs

Gancarzewicz (1雪75) has shown by 怒 号 丑 ns of histoch告 mica1 m曹 thod器 that one
po1e of freshly 1aid egg of ぐretrodontophor丑 is especia11y rich in RNA.

Accor・M

ding to Klag (1982) 七his egg oop1昌 smic het邑 rogenity bears for form呂 tion ofprimary germ ce11s.

Th号
region畠1 h
ete主 ogenity m昌 y refer to 1nterna1 morpho叩

10gy，th1s is to form昌 tion of germ c告 11s on1y，but for fina1 conc1usionfurth
思r 器 tudie器 ar思
necessary
喰

て
rh
母

gene.ra1 findin
ヲS

昌吉

e th
昌七 T
etrodontophora do号 s not exhibit corr設工品時

七ions estab11shed for pterygot
品 虫 色gg types.

The oogenesis in case of 主
ゑ
主
ぶQ
ω

is po1ytrophic but eggs are char昌 cterized by extreme1y thin p桂 ri‑
p1丑 sm，10ng 9告 主 総 畠 n1age and very 10ng period of deve1opment.

工njuring ofouter egg portion，prior to zygote nuc1eus division or during first c1e呂 vage
divisions，is critica1 for subsequent deve10pm告 nt昌 l 色 V号 nts. From 8‑b1品 stomere
器

tage the same experimenta1 treatment gives different effect，the embryo isab1e to r告 a1ize conseguently further deve1opmenta1 program.

We hav日 postu叩

l品 t昭 d that early deve10pmental program is under inf1uenc巴 of oop1asmic infor叩m呂 tion，situated in outermost part of the egg. Beginning with 8‑b1astomere
盟七品

ge genetic information comes in七 o int君 主 p1品 Y 官 ith oop1王，smic inform
ミ
，t
ion.

However，nothing is known at th1s moment what 1s the n丑 tur日 of sign昌 ls andre日ponses which regu1ate deve1opmenta1 decisions.
1n case of Tetrodontophora experiments with cautheryzation have show段 d
fai1ure to understand exact1y what is meant by det色 rminationor r日 gulation.
These terms imply radica11y different mechanisms regulating developmenta1
events.
合We have s告 邑 n that the arrest of deve1opmenta1 proc合 部 思 es follo明 ing

xperimental interventェon does not necessary mean determination.

Distinction

between determinative and regulative insect embryos，estab1ished in e品 rly partof this c日ntury，is probably not as valid as being used.

Acknow1担 金 守 告 mG
没与さ Z工 腎 ishto thank Professorぉiroshi Ando for inviting m時 toSugadaira Montane Research Center，Uniマersity of Tsukub
昌 昌nd for his magnifi
町

cient hospitality and to other Japanese co1le丑ヲ ues for differ邑 nt kind of h控 lp
ゆReferences
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