20
E
mbr
y
onic Development
1
. Intr
oduc
t
ion
E
mbr
y
onic development be
g
ins with the first mitotic division of the z
yg
ote nucleus an
d
t
erminates at hatchin
g
. Not surprisin
g
l
y
, in view of their diversit
y
of form, function, and life
h
istor

y
, insects exhibit a variet
y
of embr
y
onic developmental patterns, thou
g
h certain evolu
-
ti
onary tren
d
s are apparent. Eggs o
f
most spec
i
es conta
i
n a cons
id
era
bl
e amount o
f
yo
lk
.In
exopterygote eggs t
h
ere

i
s suc
h
a prepon
d
erance o
f
yo
lk
t
h
at t
h
e egg cytop
l
asm
i
s rea
dil
yo
b
-
v
i
ous on
ly
w
h
en
i

t
f
orms a sma
ll i
s
l
an
d
surroun
di
n
g
t
h
e nuc
l
eus. In e
gg
so
f
en
d
opter
yg
otes,
t
he
y
olk:c
y

toplasm ratio is much lower than that of exopter
yg
otes and the c
y
toplasm can be
seen as a conspicuous network connectin
g
the central island with a la
y
er of periplasm l
y
in
g
b
eneat
h
t
h
ev
i
te
lli
ne mem
b
rane. T
hi
s tren
d
towar
d

re
d
uct
i
on
i
nt
h
ere
l
at
i
ve amount o
f
yo
lk
i
nt
h
e egg, carr
i
e
d
to an extreme
i
n certa
i
n paras
i
t

i
c Hymenoptera an
d
v
i
v
i
parous D
i
ptera
(Cec
id
om
yiid
ae), w
h
ose e
gg
s are
y
o
lkl
ess an
d
rece
i
ve nutr
i
ents
f

rom t
h
e
i
r surroun
di
n
g
s,
h
a
s
some important consequences. Broadl
y
speakin
g
, the e
gg
s of endopter
yg
otes are smaller
(size measured in relation to the bod
y
size of the la
y
in
g
insect) and develop more rapidl
y
th

an t
h
ose o
f
exopterygotes. T
h
e
i
ncrease
d
quant
i
ty o
f
cytop
l
asm
l
ea
d
stot
h
e more rap
id
f
ormat
i
on o
f
more an

dl
arger ce
ll
satt
h
eyo
lk
sur
f
ace t
h
at
f
ac
ili
tates t
h
e
f
ormat
i
on o
f
a
l
arger
em
b
r
y

on
i
c area
f
rom w
hi
c
hd
eve
l
opment can ta
k
ep
l
ace. Compare
d
w
i
t
h
t
h
at o
f
exopter
y
-
g
otes, development of endopter
yg

otes is streamlined and simplified. There has been, as
Anderson (1972b,
p
. 229)
p
ut it, “reduction or elimination of ancestral irrelevancies,” which
wh
en ta
k
en to an extreme, seen
i
nt
h
e apocr
i
tan Hymenoptera an
d
cyc
l
orr
h
ap
h
D
i
ptera, re-
su
l
ts
i

nt
h
e
f
ormat
i
on o
f
a structura
ll
ys
i
mp
l
e
l
arva t
h
at
h
atc
h
es w
i
t
hi
nas
h
ort t
i

me o
f
egg
l
a
yi
n
g
. However, super
i
mpose
d
on t
hi
s process o
f
s
h
ort-c
i
rcu
i
t
i
n
g
ma
yb
e
d

eve
l
opmenta
l
specializations associated with an increasin
g
dissimilarit
y
of
j
uvenile and adult habits.
2.
C
leavage and Blastoderm Format
i
o
n
As it moves toward the center of an e
gg
after fusion, the z
yg
ote nucleus be
-
g
i
ns to
di
v
id
em

i
tot
i
ca
ll
y. T
h
e
fi
rst
di
v
i
s
i
on occurs at a pre
d
eterm
i
ne
d
s
i
te, t
h
ec
l
eav
-
age center (F

i
gure 20.1),
l
ocate
di
nt
h
e
f
uture
h
ea
d
reg
i
on, w
hi
c
h
cannot
b
e recogn
i
ze
d
morpholo
g
icall
y
but which appears to become activated either when sperm enter an e

gg
o
r
w
hen an e
gg
is laid. Earl
y
divisions are s
y
nchronous, and as nuclei are formed and mi
g
rate
597
5
98
CHAPTER
20
FI
GU
RE 20.1. Positions of cleava
g
e center, activation center, and differen
-
t
i
at
i
on center
i

n eggs o
f
Pl
atycnemis (Odonata). [After D. Bodenstein, 1953
,
Em
b
r
y
on
i
c
d
eve
l
opment,
i
n
:
Insect P
h
ysio
l
og
y
(
K. D. Roe
d
er, e
d

.). Cop
y-
r
ight @ 1953, John Wiley and Sons, Inc. Reprinted by permission of John
Wil
ey an
d
Sons, Inc.]
throu
g
h the
y
olk toward the periplasm, each becomes surrounded b
y
an island of c
y
toplas
m
(
Fi
g
ure 20.2A). Each nucleus and its surroundin
g
c
y
toplasm are known as a cleava
g
e en-
e
rgid. In eggs of endopterygotes and possibly exopterygotes, but not those of apterygotes,

t
h
e energ
id
s rema
i
n
i
nterconnecte
db
y means o
ffi
ne cytop
l
asm
i
c
b
r
id
ges.
Th
e rate at w
hi
c
h
nuc
l
e
i

m
i
grate to t
h
eyo
lk
sur
f
ace an
d
t
h
e met
h
o
d
o
f
co
l
on
i
zat
i
on ar
e
v
aried. In e
gg
s of some species nuclei appear in the periplasm as earl

y
as the
6
4-ener
g
i
d
state (after six divisions); in others, nuclei are not seen in the
p
eri
p
lasm until the 1024
-
e
ner
g
id sta
g
e. In e
gg
s of most endopter
yg
otes and in those of paleopteran and hemipteroi
d
e
xopterygotes, t
h
e per
i
p

l
asm
i
s
i
nva
d
e
d
un
if
orm
l
y
b
yt
h
e energ
id
s. However,
i
n eggs o
f
o
rt
h
optero
id i
nsects t
h

e per
i
p
l
asm at t
h
e poster
i
or po
l
eo
f
t
h
e egg rece
i
ves energ
id
s
fi
rst
,
after which there is pro
g
ressive colonization of the more anterior re
g
ions.
In e
gg
s of most insects not all cleava

g
e ener
g
ids mi
g
rate to the peripher
y
but continue
to divide within the
y
olk to form primar
y
vitellopha
g
es, so-called because in most species
t
h
ey
b
ecome p
h
agocyt
i
cce
ll
sw
h
ose
f
unct

i
on
i
sto
di
gest t
h
eyo
lk
(F
i
gure 20.2B). In eggs o
f
Lep
id
optera, D
i
ptera, an
d
some ort
h
optero
id i
nsects,
h
owever, a
ll
o
f
t

h
e energ
id
sm
i
grate t
o
t
h
e per
i
p
l
asm an
d
on
ly l
ater
d
o some o
f
t
h
e
i
r pro
g
en
y
move

b
ac
ki
nto t
h
e
y
o
lk
as secon
d
ar
y
v
itellopha
g
es (Fi
g
ure 20.2F). Secondar
y
vitellopha
g
es are also produced in e
gg
s of other
i
nsects to supplement the number of primar
y
vitellopha
g

es. So-called tertiar
y
vitellopha
g
es
are pro
d
uce
di
n eggs o
f
some cyc
l
orr
h
ap
h
D
i
ptera an
d
apocr
i
tan Hymenoptera
f
rom t
h
e
anter
i

or an
d
poster
i
or m
id
gut ru
di
ments.
A
f
ter t
h
e
i
r arr
i
va
l
at t
h
e per
i
p
l
asm, t
h
e ener
gid
s cont

i
nue to
di
v
id
e, o
f
ten s
y
nc
h
ronous
ly,
until the nuclei become closel
y
packed (the s
y
nc
y
tial blastoderm sta
g
e), after which cell
m
embranes form b
y
radial infoldin
g
, then tan
g
ential expansion of the ori

g
inal e
gg
plas-
m
a
l
emma (t
h
eun
if
orm
bl
asto
d
erm stage) (F
i
gure 20.2C–F). From t
h
e resu
l
t
i
ng mono
l
aye
r
of
ce
ll

s
d
eve
l
op a
ll
o
f
t
h
ece
ll
so
f
t
h
e
l
arva
lb
o
d
y, except
i
na
f
ew spec
i
es w
h

ere v
i
te
ll
op
h
ages
o
ryo
lk
ce
ll
s contr
ib
ute to t
h
e
f
ormat
i
on o
f
t
h
em
id
gut (Sect
i
on 7.4).
3. Format

i
on and
G
rowth o
fG
erm Band
T
he next sta
g
e is blastoderm differentiation,
g
ivin
g
rise to the embr
y
onic primordium
(
an area of closel
y
packed columnar cells from which the future embr
y
o forms) and th
e
599
E
MBRY
O
NI
C
DEVELOPMEN

T
F
I
GU
RE 20.2.
S
tages in cleavage and blastoderm formation in egg of
D
acus tr
y
on
i
(Diptera). (A) Frontal
s
ection through anterior end during
6
th division; (B) transverse section after 8th division; (C) transverse section
a
f
ter 12t
hdi
v
i
s
i
on; (D) transverse sect
i
on
d
ur

i
n
g
13t
hdi
v
i
s
i
on; (E) transverse sect
i
on at s
y
nc
y
t
i
a
lbl
asto
d
erm
s
tage; and (F) frontal section through posterior end after formation of uniform cellular blastoderm. [After D. T
.
A
n
d
erson, 1972
b

,T
h
e
d
eve
l
opment o
fh
o
l
ometa
b
o
l
ous
i
nsects,
i
n: Deve
l
opmenta
l
Systems: Insects
,V
ol. I (S. J.
VV
Counce and C. H. Waddin
g
ton, eds.). B
y

permission of Academic Press Ltd., and the author.]
extra-embryonic ectoderm from which the extra-embryonic membranes later differentiat
e
(F
i
gure 20.3). For more t
h
an a century, attempts
h
ave
b
een ma
d
etoexp
l
a
i
n
h
ow t
h
e
b
o
d
y
pattern o
f
an
i

nsect
i
s
d
eterm
i
ne
d
.Fo
ll
ow
i
ng t
h
ec
l
ass
i
c exper
i
ments o
f
t
h
e German em
b
ry-
olo
g
ist Seidel in the late 1920s, it was widel

y
believed that differentiation was controlled
by
two centers (Counce, 1973; Hemin
g
, 2003). As ener
g
ids move toward the posterior end
of the e
gg
, the
y
interact with a so-called “activation center” (Fi
g
ure 20.1), and differen-
ti
at
i
on su
b
sequent
l
y occurs. Se
id
e
l
’s exper
i
ments s
h

owe
d
t
h
at ne
i
t
h
er an energ
id
nor t
he
act
i
vat
i
on center a
l
one cou
ld
st
i
mu
l
ate
diff
erent
i
at
i

on. It was presume
d
t
h
at t
h
e center
i
s
cause
d
to re
l
ease an un
id
ent
ifi
e
d
c
h
em
i
ca
l
t
h
at
diff
uses anter

i
or
ly
.T
hi
s
diff
us
i
on
i
s seen
morpholo
g
icall
y
as a clearin
g
and sli
g
ht contraction of the
y
olk. As the chemical reaches
600
CHAPTER
20
F
IGURE 20.3
.
D

i
a
g
rammat
i
c transverse (A) an
d
sa
gi
tta
l
(B) sect
i
ons o
f
e
gg
o
f
P
ontani
a
(
H
y
menoptera
)
t
o
s

how differentiation of blastoderm into embr
y
onic primordium and extra-embr
y
onic ectoderm. Note also th
e
g
erm (pole) cells at the posterior end. [After D. T. Anderson, 1972b, The development of holometabolous insects
,
i
n
:
D
eve
l
opmenta
l
Systems: Insects
,V
ol. I (S. J. Counce and C. H. Waddington, eds.). By permission of Academic
VV
P
ress Ltd., and the author.
]
the future prothoracic re
g
ion of the embr
y
o (the “differentiation center”) (Fi
g

ure 20.1), the
blastoderm in this re
g
ion
g
ives a sharp twitch and becomes sli
g
htl
y
inva
g
inated. Blastoderm
c
ells aggregate within this invagination and differentiate into the embryonic primordium
.
(
Later
i
nem
b
ryogenes
i
s, ot
h
er processes,
f
or examp
l
e, meso
d

erm
f
ormat
i
on an
d
segmen
-
tat
i
on,
b
eg
i
natt
h
e
diff
erent
i
at
i
on center an
d
sprea
d
anter
i
or
l

yan
d
poster
i
or
l
y
f
rom
i
t.
)
An alternate view for the cause of embr
y
onic differentiation is the “
g
radient h
y
pothesis,
”
w
hich had its ori
g
ins at the end of the 19th centur
y
but then fell out of favor after Seidel’s
pioneerin
g
work (Sander, 1984, 1997; Lawrence, 1992). Essentiall
y

, the h
y
pothesis propose
s
t
h
atac
h
em
i
ca
l
pro
d
uce
d
at eac
h
en
d
o
f
an egg
diff
uses t
h
roug
h
out t
h

e egg, pro
d
uc
i
ng tw
o
gra
di
ents o
f
concentrat
i
on (F
i
gure 20.4). Ce
ll
sw
i
t
hi
nt
h
e egg t
h
en “recogn
i
ze” t
h
e
i

r pos
i
t
i
o
n
wi
t
hi
nt
h
ee
gg by
t
h
ere
l
at
i
ve concentrat
i
ons o
f
t
h
ec
h
em
i
ca

l
an
d diff
erent
i
ate accor
di
n
gly.
Initial support for the existence of chemical
g
radients in e
gg
s came from experiments in
w
hich e
gg
s either were li
g
atured at various distances alon
g
their len
g
th and at varied time
s
a
f
ter em
b
ryon

i
c
d
eve
l
opment
b
egan or were centr
if
uge
d
,t
h
ere
b
y
di
srupt
i
ng t
h
e propose
d
gra
di
ent. Recent
l
y, t
h
e app

li
cat
i
on o
f
genet
i
can
d
mo
l
ecu
l
ar tec
h
n
i
ques to t
h
e stu
d
yo
f
pattern
d
eve
l
opment
in
D

roso
ph
i
la
h
as
gi
ven
f
urt
h
er support to t
h
e
id
ea o
fg
ra
di
ents. T
h
us
,
a modern interpretation of Seidel’s differentiation center is that it is a “commitment center”;
that is, it is the point at which blastoderm cells are committed to followin
g
a particular path
o
f differentiation by virtue of their position within the gradients (Heming, 2003).
F

I
G
URE 20.4
.
D
i
a
g
rammat
i
c representat
i
on o
f
t
h
e
g
ra
di
ent
hy
pot
h
es
i
s.Ac
h
em
i

ca
l
pro
d
uce
d
at eac
h
en
d
o
f
an e
gg
diffuses len
g
thwise, formin
g
two
g
radients of concentration. At an
y
point alon
g
the len
g
th of the e
gg
, the
relative concentration of the two chemicals provides positional information to cells.

60
1
E
MBRY
O
NI
C
DEVEL
O
PMEN
T
F
IGURE 20.5
.
F
orm an
d
pos
i
t
i
on o
f
em
b
ryon
i
cpr
i
mor

di
um
i
n exopterygotes. (A)
P
erip
l
anet
a
;(
B
)
P
l
atycnemi
s
;
(
C
)
Z
ootermops
is
;
an
d(
D
)
N
otonecta.[A

f
ter D. T. An
d
erson, 1972a, T
h
e
d
eve
l
o
p
ment o
fh
em
i
meta
b
o
l
ous
i
nsects,
in
:
Developmental S
y
stems: Insect
s
,
V

ol. I (S. J. Counce and C. H. Waddington, eds.). By permission of Academic
VV
P
ress Lt
d
., an
d
t
h
e aut
h
or.
]
As a result of the differin
g
amounts of
y
olk that exopter
yg
ote and endopter
yg
ote e
ggs
contain, important differences occur in the formation of the embr
y
onic primordium. I
n
exopterygote eggs where there is initially little cytoplasm, the embryonic primordium i
s
norma

ll
yre
l
at
i
ve
l
y sma
ll
,an
di
ts
f
ormat
i
on
d
epen
d
sont
h
e aggregat
i
on an
d
, to some extent
,
pro
lif
erat

i
on o
f
ce
ll
s. In t
h
ese eggs
i
t usua
ll
y occup
i
es a poster
i
or m
id
ventra
l
pos
i
t
i
on (F
i
gure
2
0.
5
A–D). In contrast, in endopter

yg
ote e
gg
s with their
g
reater quantit
y
of c
y
toplasm, the
primordium forms as a broad monola
y
er of columnar cells that occupies much of the ventral
surface of the yolk (Figure 20.6A,B). In other words, the primordium in endopterygote egg
s
d
oes not requ
i
re to un
d
ergo muc
hi
ncrease
i
ns
i
ze, as
i
s necessary
i

n eggs o
f
exopterygotes,
so t
h
at t
i
ssue
diff
erent
i
at
i
on can occur
di
rect
l
yan
d
em
b
ryon
i
c growt
h
more rap
idl
y. At
i
t

s
extreme, seen in e
gg
s of some Diptera and H
y
menoptera, the primordium occupies bot
h
ventral and lateral areas of the e
gg
, with the extra-embr
y
onic ectoderm coverin
g
onl
y
th
e
d
orsal surface (Fi
g
ure 20.6C)
.
T
h
es
h
ape o
f
t
h

epr
i
mor
di
um
i
svar
i
e
d
,t
h
oug
hi
n most
i
nsects t
h
e anter
i
or reg
i
on
i
s
expan
d
e
dl
atera

ll
yasapa
i
ro
fh
ea
dl
o
b
es
(
=
p
rotocep
h
a
l
on),
b
e
hi
n
d
w
hi
c
hi
sareg
i
on o

f
varied len
g
th, the protocorm (postantennal re
g
ion) (Fi
g
ure 20.
5
). In e
gg
s of Paleoptera
,
h
emipteroid insects, and some orthopteroid species, the protocorm is semilon
g
and at its
formation includes the mouthpart-bearin
g
se
g
ments, the thoracic se
g
ments, and a posterio
r
growt
h
reg
i
on

f
rom w
hi
c
h
t
h
ea
bd
om
i
na
l
segments ar
i
se. In eggs o
f
ot
h
er ort
h
optero
id
i
nsects t
h
e postantenna
l
reg
i

on cons
i
sts
i
n
i
t
i
a
ll
yo
f
on
l
yt
h
e growt
h
zone. T
h
oug
h
t
h
e proto
-
corm
i
n most en
d

opter
yg
ote em
b
r
y
os
i
s
l
on
g
,
i
ta
l
so
i
nc
l
u
d
es a poster
i
or
g
rowt
h
zone
f

ro
m
w
hich rudimentar
y
abdominal se
g
ments proliferate. As the embr
y
onic primordium elon-
g
ates and be
g
ins to differentiate, it becomes known as the
g
erm band. Durin
g
elon
g
atio
n
an
d diff
erent
i
at
i
on, t
h
ea

bd
omen grows aroun
d
t
h
e poster
i
or en
d
an
df
orwar
d
over t
h
e
d
orsa
l
sur
f
ace o
f
t
h
e egg (F
i
gure 20.7). In eggs o
f
some

hi
g
h
er en
d
opterygotes (Hymenoptera-
Apocr
i
ta an
d
D
i
ptera-Muscomorp
h
a), t
h
ere
i
s no poster
i
or growt
h
zone an
d
t
h
ea
bd
om
i

na
l
se
g
ments arise directl
y
from the primordium
.
602
CHAPTER
20
F
IGURE 20.6
.
F
orm and position of embryonic primordium in endopterygotes. (A) T
e
n
eb
r
io
;(
B
)
S
iali
s
;
and
(C)

P
imp
l
a.[A
f
ter D. T. An
d
erson, 1972a,
b
,T
h
e
d
eve
l
o
p
ment o
fh
em
i
meta
b
o
l
ous
i
nsects, an
d
T

h
e
d
eve
l
o
p
ment
o
f holometabolous insects
,
in
:
Developmental S
y
stems: Insects
,V
ol. I (S. J. Counce and C. H. Waddington, eds.).
V
V
B
y permission of Academic Press Ltd., and the author.
]
It
i
s
d
ur
i
n

g
t
h
e
diff
erent
i
at
i
on an
d
e
l
on
g
at
i
on o
f
t
h
e
g
erm
b
an
d
t
h
at t

h
epr
i
mor
di
a
l
g
erm cells first become noticeable in most endopter
yg
ote e
gg
s, thou
g
h in those of some
Coleoptera the
y
are distin
g
uishable even as the s
y
nc
y
tial blastoderm is formin
g
. The
y
ar
e
l

arg
i
s
h
, roun
d
e
d
ce
ll
s
i
na
di
st
i
nct group at t
h
e poster
i
or po
l
eo
f
t
h
eyo
lk
,an
d

accor
di
ng
l
y are
re
f
erre
d
to as po
l
ece
ll
s(F
i
gure 20.3). In eggs o
f
Dermaptera, Psocoptera, T
h
ysanoptera, an
d
h
omopterans a
l
so, t
h
e
g
erm ce
ll

s
diff
erent
i
ate ear
ly
at t
h
e poster
i
or en
d
o
f
t
h
epr
i
mor
di
um
.
In those of most exopter
yg
otes, however, the
y
are not apparent until
g
astrulation or somit
e

f
ormation has occurred
.
As the germ band elongates and becomes broader, segmentation and limb-bud formatio
n
appear externa
ll
yan
d
are accompan
i
e
di
nterna
ll
y
b
y meso
d
erm an
d
som
i
te
f
ormat
i
on.
Growt
h

o
f
t
h
e germ
b
an
d
may occur e
i
t
h
er on t
h
e sur
f
ace o
f
t
h
eyo
lk
(super
fi
c
i
a
l
growt
h

)a
s
seen in e
gg
s of Dict
y
optera, Dermaptera, Isoptera, some other orthopteroid insects, and al
l
e
ndopter
yg
otes (Fi
g
ure 20.7), or b
y
immersion into the
y
olk (immersed
g
rowth) as occurs
i
n eggs of Paleoptera, most Orthoptera, and hemipteroid insects (Figure 20.8). Immersion o
f
t
h
e germ
b
an
d
(anatreps

i
s)
f
orms t
h
e
fi
rst o
f
a ser
i
es o
f
em
b
ryon
i
c movements, co
ll
ect
i
ve
ly
k
nown as
bl
asto
ki
nes
i

s. T
h
e reverse movement (
k
atatreps
i
s), w
hi
c
hb
r
i
ngs t
h
eem
b
ryo
back to the surface of the
y
olk, occurs later (see Section
6
). Anatrepsis has developed
secondaril
y
(i.e., superficial
g
rowth is the more primitive method) and conver
g
entl
y

amon
g
those exopterygotes in which it occurs. Its functional significance is, however, not clea
r
(
An
d
erson, 1972a; Hem
i
ng, 2003)
.
4
. Gastrulation, Somite Formation, and Segmentatio
n
As the embr
y
onic primordium be
g
ins to increase in len
g
th, its midventral cells sink
i
nward to form a transient, lon
g
itudinal
g
astral
g
roove (Fi
g

ure 20.9A). The inva
g
inate
d
603
E
MBRY
O
NI
C
DEVEL
O
PMEN
T
F
I
GU
RE 20.7
.
S
ta
g
es in elon
g
ation and se
g
mentation of
g
erm band i
n

Zootermo
p
s
is
(Iso
p
tera) (A–C) an
d
Bruchi
d
iu
s
(Coleoptera) (D–F). [After D. T. Anderson, 1972a,b, The development of hemimetabolous insects
,
an
d
t
h
e
d
eve
l
o
p
ment o
fh
o
l
ometa
b

o
l
ous
i
nsects,
i
n
:
Deve
l
opmenta
l
Systems: Insect
s
,V
ol. I (S. J. Counce and
VV
C. H. Waddin
g
ton, eds.). B
y
permission of Academic Press Ltd., and the author.]
cells soon separate from the outer la
y
er, which closes to obliterate the
g
roove. It is fro
m
t
he anterior and posterior points of closure of the

g
astral
g
roove that the stomodeum an
d
proctodeum, respectivel
y
, develop. The outer la
y
er can now be distin
g
uished as the em-
b
ryon
i
c ecto
d
erm. T
h
e
i
nvag
i
nate
d
ce
ll
s, w
hi
c

h
pro
lif
erate an
d
sprea
dl
atera
ll
y,
f
orm t
h
e
meso
d
erm (F
i
gure 20.9B,C) except a
dj
acent to t
h
e
d
eve
l
op
i
ng stomo
d

eum an
d
procto
d
eum
wh
ere t
h
e
yb
ecome t
h
e anter
i
or an
d
poster
i
or m
idg
ut ru
di
ments, respect
i
ve
ly
.T
h
e meso-
d

ermal cells become concentrated into paired lon
g
itudinal tracts which soon separate int
o
60
4
CHAPTER
20
F
IGURE 20.8. Early embryonic development in Calopter
y
x to show anatrepsis andkatatrepsis. [A–E, after O. A.
Jo
h
annsen an
d
F. H. Butt
,
1941
,
Em
b
ryo
l
ogy of Insects an
d
Myriapo
d
s
.

By
perm
i
ss
i
on o
f
McGraw-H
ill
Boo
k
Co.,
Inc. F, After R. F. Cha
p
man, 1971
,
T
he Insects:
S
tructure and Function.
By
permission of Elsevier/North-Holland,
Inc., and the author.
]
se
g
mental blocks, leavin
g
onl
y

a thin lon
g
itudinal strip, the median mesoderm, from which
hemoc
y
tes later differentiate. From these se
g
mental blocks, paired hollow somites usuall
y
ar
i
se (F
i
gure 20.9E). Som
i
te
f
ormat
i
on
i
s
i
n
i
t
i
ate
d
an

d
occurs more or
l
ess s
i
mu
l
taneous
l
y
i
nt
h
e gnat
h
a
l
an
d
t
h
orac
i
c segments, sprea
di
ng anter
i
or
l
yan

d
poster
i
or
l
ya
f
ter gastru
l
at
i
o
n
ta
k
es p
l
ace. Format
i
on o
f
t
h
e coe
l
om (t
h
ecav
i
t

y
w
i
t
hi
n a som
i
te) ma
y
occur
i
n one o
f
two
w
a
y
s, b
y
internal splittin
g
of a somite or b
y
median foldin
g
of the lateral part of each somite.
605
E
MBRY
O

NI
C
DEVEL
O
PMEN
T
F
I
GU
RE 20.9.
F
o
rmation of gastral groove, somites, and embryonic membranes. [After D. T. Anderson, 1972a
,
Th
e
d
eve
l
opment o
fh
em
i
meta
b
o
l
ous
i
nsects,

i
n
D
eve
l
opmenta
l
Systems: Insect
s
,
V
ol. I (S. J. Counce and C. H.
VV
W
a
ddi
n
g
ton, e
d
s.). B
y
perm
i
ss
i
on o
f
Aca
d

em
i
c Press Lt
d
., an
d
t
h
e aut
h
or.]
I
nem
b
ryos o
f
ag
i
ven spec
i
es, one or
b
ot
h
met
h
o
d
s may
b

e seen
i
n
diff
erent segments. For
example, internal splittin
g
of the somites occurs in all se
g
ments of embr
y
os of Phasmida,
most hemipteroid insects, and most endopter
yg
otes, and in the abdominal se
g
ments of
Locust
a
embryos. Median folding is the method used in all segments in embryos of Odonata,
D
i
ctyoptera, an
d
Ma
ll
op
h
aga, an
di

nt
h
e gnat
h
a
l
an
d
t
h
orac
i
c segments o
f
t
h
ose o
f
Locu
s
t
a
,
an
d
some Co
l
eoptera, Lep
id
optera, an

d
Mega
l
optera. In exopterygote em
b
ryos, a
ll
som
i
te
s
u
suall
y
develop a central cavit
y
, thou
g
h this ma
y
be onl
y
temporar
y
. Amon
g
endopter
yg
otes,
members of more primitive orders retain a full complement of somites in their embr

y
os and
t
he latter usually develop a coelom. In embryos of some species, however, cavities may no
t
f
orm, an
d
som
i
te
f
ormat
i
on may
b
e suppresse
di
nt
h
e
h
ea
d
segments. In em
b
ryos o
f
D
i

pter
a
an
d
Hymenoptera, no
di
st
i
nct
h
ea
d
som
i
tes appear, an
di
nt
h
ose o
f
some Muscomorp
h
a
and Apocrita, somite formation is entirel
y
suppressed, so that mesodermal derivatives ar
e
produced directl
y
from a sin

g
le midventral mass.
5
. Format
i
on o
f
Extra-Embr
y
on
i
c Membrane
s
S
imultaneousl
y
with
g
astrulation and somite formation, two extra-embr
y
onic mem
-
b
ranes, t
h
e amn
i
on an
d
serosa,

d
eve
l
op
f
rom t
h
e extra-em
b
ryon
i
c ecto
d
erm (F
i
gure 20.9).
Ce
ll
satt
h
ee
d
ge o
f
t
h
e germ
b
an
d

pro
lif
erate an
d
t
h
et
i
ssue
f
orme
d
on eac
h
s
id
e
f
o
lds
ventra
lly
to
gi
ve r
i
se to t
h
e amn
i

ot
i
c
f
o
ld
s. T
h
ese meet an
df
use
i
nt
h
e ventra
l
m
idli
ne to
form inner and outer membranes, the amnion and serosa, respectivel
y
, the former enclosin
g
a central fluid-filled amniotic cavit
y
. Man
y
authors have su
gg
ested that such a cavit

y
woul
d
606
CHAPTER
20
provide space in which an embr
y
o could
g
row and also prevent ph
y
sical dama
g
e. Ander
-
son (1972a) considered, however, that these functions are redundant and that the cavit
y
m
ust have an as
y
et unidentified function. Another possibilit
y
is that the amnion and it
s
c
av
i
ty are use
d

to store wastes, w
hi
c
h
are t
h
us
k
ept separate
f
rom t
h
eyo
lk
.T
h
e genera
l
m
et
h
o
d
o
f
amn
i
on an
d
serosa

f
ormat
i
on out
li
ne
d
a
b
ove
i
s
f
oun
di
na
ll i
nsect em
b
ryos (w
i
t
h
some modification where immersion of the
g
erm band into the
y
olk occurs) except those
o
f Muscomorpha and Apocrita, in which, it will be recalled, the embr

y
onic primordiu
m
c
overs most of the
y
olk surface. In these, embr
y
onic membranes are
g
reatl
y
reduced o
r
l
ost. In em
b
ryos o
f
Apocr
i
ta t
h
e extra-em
b
ryon
i
c ecto
d
erm separates

f
rom t
h
ee
d
ge o
f
t
h
e
pr
i
mor
di
um an
d
grows ventra
ll
yto
f
orm t
h
e serosa; t
h
at
i
s, amn
i
ot
i

c
f
o
ld
s are not
f
orme
d
.In
e
m
b
r
y
os o
f
Muscomorp
h
ane
i
t
h
er an amn
i
on nor a serosa
f
orms, an
d
t
h

e extra-em
b
r
y
on
ic
e
ctoderm covers the
y
olk until definitive dorsal closure occurs (see below)
.
After the embr
y
onic membranes form, the serosa in most insect e
gg
s secretes a cuticle
t
h
at
i
so
f
ten as t
hi
c
k
as t
h
ec
h

or
i
on. For severa
l
s
p
ec
i
es,
p
ro
d
uct
i
on o
f
t
h
e serosa
l
cut
i
c
l
e
i
s
cl
ose
l

y sync
h
ron
i
ze
d
w
i
t
h
a pea
k
o
f
mo
l
t
i
ng
h
ormone
i
nt
h
e egg (see Sect
i
on 9)
.
6. Dorsal Closure and Katatrepsis
W

h
en germ
b
an
d
e
l
ongat
i
on an
d
segmentat
i
on are comp
l
ete,
li
m
bb
u
d
s
d
eve
l
op, t
he
e
m
b

r
y
on
i
c ecto
d
erm
g
rows
d
orso
l
atera
lly
over t
h
e
y
o
lk
mass, an
di
nterna
lly
or
g
ano
g
enes
is

be
g
ins. This phase of
g
rowth is ended abruptl
y
as the extra-embr
y
onic membranes fuse
and rupture and the
g
erm band reverts to its ori
g
inal (pre-anatreptic) position (in most
e
xopterygotes) or s
h
ortens (en
d
opterygotes).
In em
b
ryos o
f
most
i
nsects, t
h
e amn
i

on an
d
serosa
f
use
i
nt
h
ev
i
c
i
n
i
ty o
f
t
h
e
h
ea
d
,an
d
t
h
e com
bi
ne
d

t
i
ssue t
h
en sp
li
ts to expose t
h
e
h
ea
d
an
d
ro
ll
s
b
ac
kd
orsa
ll
y over t
h
eyo
lk
(
Fi
g
ure 20.10A). As a result, the serosa is reduced to a small mass of cells, the secondar

y
dorsal or
g
an, and the amnion becomes stretched over the
y
olk, formin
g
the provisiona
l
dorsal closure (Figure 20.10B). In some endopterygote embryos, variations of this process
c
an
b
e seen. In t
h
ose o
f
Nematocera (D
i
ptera) an
d
Symp
h
yta (Hymenoptera),
f
or examp
l
e
,
i

t
i
st
h
e amn
i
on t
h
at ruptures an
di
sre
d
uce
d
,
l
eav
i
ng t
h
e serosa
i
ntact. As note
d
a
b
ove,
i
n
egg

s of Apocrita onl
y
a serosa is formed, and this persists until definitive dorsal closure
o
ccurs, and in those of Muscomorpha no extra-embr
y
onic membranes develop, and the
y
olk
remains covered by the extra-embryonic ectoderm until definitive dorsal closure.
E
xcept
i
n
di
ctyopteran em
b
ryos w
h
ere t
h
e germ
b
an
d
rema
i
ns super
fi
c

i
a
l
an
d
ventra
l
d
ur
i
ng e
l
ongat
i
on, extens
i
ve movement o
f
t
h
e germ
b
an
d
now occurs
i
n exopterygote egg
s
w
hich serves (1) to brin

g
an immersed
g
erm band back to the surface of the
y
olk and (2) to
restore the
g
erm band to its pre-anatreptic orientation, that is, on the ventral surface of the
yolk with the head end facing the anterior pole of the egg. This movement, the reverse of
anatreps
i
s,
i
s
k
nown as
k
atatreps
i
s(F
i
gure 20.8).
At t
h
e
b
eg
i
nn

i
ng o
f
prov
i
s
i
ona
ld
orsa
l
c
l
osure, t
h
e germ
b
an
d
o
f
most en
d
opterygotes
i
s quite lon
g
so that, althou
g
h its anterior end is ventral, its posterior component passes

round the posterior tip of the
y
olk and forward alon
g
the dorsal side (Fi
g
ure 20.7F). Durin
g
c
losure, the germ band shortens and broadens rapidly so that its posterior end now come
s
to
li
e near t
h
e poster
i
or en
d
o
f
t
h
e egg (F
i
gure 20.11A).
D
e
fi
n

i
t
i
ve
d
orsa
l
c
l
osure, t
h
at
i
s, t
h
e enc
l
os
i
ng o
f
t
h
eyo
lk
w
i
t
hi
nt

h
eem
b
ryo, t
h
e
n
o
ccurs. It is achieved in all insect embr
y
os b
y
a lateral
g
rowth of the embr
y
onic ectoderm
,
w
hich
g
raduall
y
replaces the amnion or, rarel
y
, the serosa (Fi
g
ures 20.10C and 20.11B).
6
0

7
E
MBRY
O
NI
C
DEVEL
O
PMEN
T
F
I
G
URE 20.10
.
Di
a
g
rammat
i
c representat
i
on o
fd
orsa
l
c
l
osure. (A) In
i

t
i
a
lf
us
i
on o
f
amn
i
on an
d
serosa an
d
b
e
g
innin
g
of rollin
g
back; (B) provisional dorsal closure with amnion coverin
gy
olk; and (C) definitive dorsa
l
closure with yolk enclosed within embryonic ectoderm
.
7. T
i
ssue and

O
rgan Development
7
.1.
A
ppendages
Pa
i
re
d
segmenta
l
evag
i
nat
i
ons o
f
t
h
eem
b
ryon
i
c ecto
d
erm appear on t
h
et
h

orac
i
c,
antennal, and
g
nathal se
g
ments while the abdominal part of the
g
erm band is still formin
g
(see Fi
g
ure 20.7). Their subsequent
g
rowth results from proliferation of the ectoderm
as a sin
g
le la
y
er of cells and of mesodermal cells within. The cephalic and thoracic
li
m
b
su
l
t
i
mate
l

y
diff
erent
i
ate
i
nto t
h
e
i
r spec
ifi
c
f
orm, except
i
n eggs o
f
secon
d
ar
il
y apo
d
ou
s
spec
i
es w
h

ere t
h
ey soon s
h
orten or
b
ecome re
d
uce
d
to ep
id
erma
l
t
hi
c
k
en
i
ngs. In em
b
ryos
of Muscomorpha, the thoracic appenda
g
es never develop be
y
ond the epidermal thickenin
g
s

t
a
g
e.
608
CHAPTER
20
F
IGURE 20.11.
(
A) F
i
ve-
d
ay em
b
ryo o
f
Bruc
h
i
d
iu
s
(Co
l
eoptera) a
f
ter s
h

orten
i
ng o
f
germ
b
an
d
. Compare t
hi
s
fig
ure w
i
t
h
F
ig
ure 20.7F; an
d
(B) em
b
r
y
oo
f
Bruc
h
i
d

iu
s
at
h
atc
hi
n
g
sta
g
e(9
d
a
y
s). [A
f
ter D. T. An
d
erson, 1972
b
,
T
he development of holometabolous insects in:
D
evelopmental S
y
stems: Insects
,V
ol. I (S. J. Counce and C. H.
VV

Wa
ddi
ngton, e
d
s.). By perm
i
ss
i
on o
f
Aca
d
em
i
c Press Lt
d
., an
d
t
h
e aut
h
or.
]
In Pa
l
eoptera an
d
ort
h

optero
id i
nsects, 11 pa
i
rs o
f
a
bd
om
i
na
l
appen
d
ages evag
i
nate
b
e-
f
ore prov
i
s
i
ona
ld
orsa
l
c
l

osure. In most
h
em
i
ptero
id
em
b
r
y
os, no s
ig
no
f
a
bd
om
i
na
lli
m
b
s
i
s evident, thou
g
h in those of Hemiptera and Th
y
sanoptera appenda
g

es develop on th
e
first and last abdominal se
g
ments. Ten pairs of abdominal eva
g
inations develop in most en-
d
opterygote em
b
ryos. T
h
e
f
ate o
f
t
h
ea
bd
om
i
na
l
appen
d
ages var
i
es, an
d

some or a
ll
o
f
t
h
em
m
ay
di
sappear
b
e
f
ore em
b
ryon
i
c
d
eve
l
opment
i
s comp
l
ete
d
.T
h

e
fi
rst (most anter
i
or) pa
ir
di
sappears a
f
ter
bl
asto
ki
nes
i
s
i
nem
b
r
y
os o
f
Pa
l
eoptera an
d
some ort
h
optero

id i
nsects,
b
ut
remains as
g
landular pleuropodia in those of Dict
y
optera, Phasmida, Orthoptera, Hemiptera,
and some Coleoptera and Lepidoptera. The function of the pleuropodia is uncertain, thou
g
h
some aut
h
ors
h
ave suggeste
d
t
h
at
i
n ort
h
opteran em
b
ryos t
h
ey secrete c
hi

t
i
nase t
h
at
b
r
i
ngs
a
b
out
di
sso
l
ut
i
on o
f
t
h
e serosa
l
cut
i
c
l
e. T
h
ep

l
europo
di
a are resor
b
e
d
or
di
scar
d
e
db
e
f
ore o
r
s
h
ort
l
ya
f
ter
h
atc
hi
ng. T
h
e appen

d
ages o
f
t
h
e secon
d
t
h
roug
h
sevent
h
a
bd
om
i
na
l
segment
s
are resorbed, except in some endopter
yg
otes where the
y
persist as larval prole
g
s. Pairs 8–10
m
a

y
differentiate into the external
g
enitalia or disappear, while the last pair either persist
s
as cerci or disa
pp
ears
.
7.2. Integument and Ectodermal Derivatives
Soon a
f
ter
d
e
fi
n
i
t
i
ve
d
orsa
l
c
l
osure, t
h
e outer em
b

ryon
i
c ecto
d
erm
diff
erent
i
ates
i
nt
o
e
pidermis, which in embr
y
os of most insects then secretes the first instar larval cuticle. In
some insects, however, one or more embr
y
onic cuticles are produced which ma
y
be shed
before or at hatchin
g
. As in larvae, production of the cuticles in embr
y
os appears to be
regu
l
ate
db

ymo
l
t
i
ng
h
ormone (Sect
i
on 9).
E
xterna
l
sens
ill
a genera
ll
y
d
eve
l
op
f
rom a
di
v
idi
ng precursor ep
id
erma
l

ce
ll
,w
h
ose
d
au
gh
ter ce
ll
st
h
en
diff
erent
i
ate to
f
orm t
h
e sensor
y
neuron an
d
accessor
y
ce
ll
s(C
h

apter 12).
The axon of the sensor
y
neuron finds the appropriate interneurons within the central nervous
6
0
9
E
MBRY
O
NI
C
DEVELOPMEN
T
s
y
stem b
yg
rowin
g
alon
g
the surface of pioneer neurons (Section 7.3) or neurons of previ-
ousl
y
formed sensilla (Hemin
g
, 2003). Similarl
y
, both compound and simple e

y
es develo
p
from
g
roups of epidermal cells, each of which divides and differentiates to form the pho-
t
orecept
i
ve an
d
accessory components o
f
t
h
e
li
g
h
t-sens
i
t
i
ve structures
.
I
mag
i
na
ldi

scs an
dhi
sto
bl
asts,
f
rom w
hi
c
h
many a
d
u
l
tt
i
ssues are
d
er
i
ve
d
at metamor-
p
h
os
i
s
i
n

high
er D
i
ptera an
d
H
y
menoptera (C
h
apter 21, Sect
i
on 4.2), can
b
e reco
g
n
i
ze
d
soon after
g
erm-band formation. The
y
are
g
roups of cells that separate from the ectoderm
in characteristic numbers, sizes and shapes, at specific sites in the bod
y
(Hemin
g

, 2003)
.
C
oncurrent
l
yw
i
t
h
t
h
e
f
ormat
i
on o
f
a
bd
om
i
na
l
appen
d
ages a num
b
er o
f
ecto

d
erma
l
i
nvag
i
nat
i
ons
d
eve
l
op,
f
rom w
hi
c
h diff
erent
i
ate en
d
os
k
e
l
eta
l
components, var
i

ous g
l
an
d
s,
th
e trac
h
ea
l
system, an
d
certa
i
n parts o
f
t
h
e repro
d
uct
i
ve tract (
f
or t
h
e
l
atter, see Sect
i

on
7.
6
). From ventrolateral inva
g
inations at the
j
unctions of the antennal/mandibular se
g
ments
and the mandibular/maxillar
y
se
g
ments are derived the anterior and posterior arms of the
t
entorium. Paired mandibular apodemes differentiate from invaginations near the bases o
f
th
e man
dibl
es. T
h
e apo
d
emes o
f
t
h
e trun

k
reg
i
on ar
i
se
f
rom
i
ntersegmenta
li
nvag
i
nat
i
ons
i
nt
h
et
h
orax an
d
a
bd
omen.
S
alivar
yg
lands develop from a pair of inva

g
inations near the bases of the labial ap-
penda
g
es. When the appenda
g
es fuse the inva
g
inations mer
g
e to form a common salivar
y
d
uct that opens midventrally on the hypopharynx
.
T
h
e corpora a
ll
ata
d
eve
l
op
f
romapa
i
ro
f
ventro

l
atera
li
nvag
i
nat
i
ons at t
h
e
j
unct
i
on
o
f
t
h
e man
dib
u
l
ar/max
ill
ary segments. In
i
t
i
a
ll

y, t
h
ey ex
i
st as
h
o
ll
ow ves
i
c
l
es, t
h
oug
h
t
h
es
e
fi
ll in as the
y
move dorsall
y
to their final position ad
j
acent to the stomodeum. The molt
g
lands also ori

g
inate as paired ventral ectodermal inva
g
inations, usuall
y
on the prothoracic
se
g
ment. Althou
g
h the endocrine
g
lands arise before katatrepsis, at this time the
y
are non-
secretory, an
d
materna
ll
y
d
er
i
ve
dh
ormones (espec
i
a
ll
yec

d
ystero
id
s) store
di
nt
h
e egg are
u
se
di
nem
b
ryon
i
cen
d
ocr
i
ne regu
l
at
i
on (Sect
i
on 9). Ot
h
er
i
nvag

i
nat
i
ons on t
h
e
h
ea
d
ma
y
gi
ve r
i
se to spec
i
a
li
ze
d
exocr
i
ne
gl
an
d
sont
h
e man
dibl

es or max
ill
ae.
Elements of the tracheal s
y
stem can be seen first as paired lateral inva
g
inations on
each se
g
ment from the second thoracic to the ei
g
hth (ninth in a few Th
y
sanura) abdominal
.
However, not a
ll
o
f
t
h
ese
i
nvag
i
nat
i
ons
d

eve
l
op comp
l
ete
l
y
i
nto trac
h
eae. T
h
ose t
h
at
d
o
,
bif
urcate an
d
anastomose w
i
t
hb
ranc
h
es
f
rom a

dj
acent segments an
df
rom t
h
e
i
r oppos
i
te
partner o
f
t
h
e same segment. T
h
ece
ll
s
diff
erent
i
ate as trac
h
ea
l
ep
i
t
h

e
li
um an
d
t
h
en secrete a
cuticular linin
g
. After cuticle secretion but before hatchin
g
,
g
as is secreted into the trachea
l
s
y
stem. Some of the inva
g
inated ectodermal cells differentiate into oenoc
y
tes. These ma
y
remain closely associated with the tracheal system, form definite clusters in specific body
reg
i
ons, or
b
ecome em
b

e
dd
e
d
as s
i
ng
l
ece
ll
s
i
nt
h
e
f
at
b
o
d
y
.
7
.3. Central Nervous
S
ystem
S
oon after somite formation has commenced, s
p
ecialized ectodermal cells on eac

h
s
id
eo
f
t
h
em
id
ventra
lli
ne, t
h
e neuro
bl
asts (F
i
gure 20.9E),
b
eg
i
ntopro
lif
erate, resu
l
t
i
ng
i
nt

h
e
f
ormat
i
on o
f
pa
i
re
dl
ong
i
tu
di
na
l
neura
l
r
id
ges separate
db
y a neura
l
groove. As
pro
lif
erat
i

on occurs, t
h
ece
ll
s move s
ligh
t
ly i
nwar
d
so t
h
at t
h
e
yb
ecome separate
df
rom
t
he ectoderm. The
y
then be
g
in to divide verticall
y
, unequall
y
and repeatedl
y

, the smal
l
d
au
g
hter cells eventuall
y
developin
g
into
g
an
g
lion cells from which both neurons and
g
lia
l
ce
ll
s
diff
erent
i
ate (F
i
gure 20.12). Remar
k
a
bl
y, t

h
e num
b
er an
d
arrangement o
f
neuro
bl
asts
i
s
hi
g
hl
y conserve
d
across t
h
e Insecta: eac
hh
a
lf
-gang
li
on
h
as 30 or 31 neuro
bl
asts

f
ro
m
whi
c
h
a
ll
neurons are pro
d
uce
d
(T
h
omas et a
l
., 1984
)
. However, t
h
e num
b
er o
f
neurons
i
n
6
1
0

CHAPTER
20
F
I
G
URE 20.12.
T
ransverse sect
i
ons to s
h
ow
d
eve
l
o
p
ment o
f
nervous t
i
ssue an
d
meso
d
erma
ld
er
i
vat

i
ves
i
n
prothoracic se
g
ment of
Tac
hy
cine
s
(
Orthoptera). In A–D, which are prekatatreptic sta
g
es, the serosa is omitted.
[After D. T. Anderson, 1972a, The development of hemimetabolous insects, in:
D
evelopmental S
y
stems: Insect
s
,
V
o
l
. I (S. J. Counce an
d
C. H. Wa
ddi
n

g
ton, e
d
s.). B
y
perm
i
ss
i
on o
f
Aca
d
em
i
c Press Lt
d
., an
d
t
h
e aut
h
or.]
a gang
li
on can
b
ew
id

e
l
yvar
i
e
d
;
f
or examp
l
e,
i
nat
h
orac
i
c gang
li
on o
f
an aptergygote t
h
er
e
are about 1
5
00 neurons, whereas in the thoracic ganglia of grasshoppers and flies there ar
e
about 3000 and 4000 neurons, respectivel
y

, reflectin
g
the increased demands on the nervou
s
s
y
stem associated with the evolution of fli
g
ht (Truman and Ball, 1998).
With the onset of se
g
mentation, neuroblasts in the interse
g
mental re
g
ions become less
act
i
ve,sot
h
at pa
i
re
d
segmenta
l
swe
lli
ngs, t
h

e
f
uture gang
li
a, now
b
ecome apparent. A
s
t
h
e neurons
f
orm, t
h
e
i
rce
ll b
o
di
es
b
ecome arrange
d
per
i
p
h
era
ll

y aroun
d
t
h
e centra
l
ax
is
(
neurop
il
e). Su
b
sequent
g
rowt
h
o
f
t
h
e axons
l
ea
d
sto
f
ormat
i
on o

fl
on
gi
tu
di
na
l
connect
i
ves,
transverse commissures, and to motor nerves innervatin
g
a variet
y
of effector or
g
ans. A
s
n
oted above, sensor
y
nerves form as a result of the inward
g
rowth of axons from peripheral
sense ce
ll
s.
An
i
mportant aspect o

f
t
h
e
d
eve
l
opment o
f
t
h
e nervous system
i
s
h
ow
d
eve
l
op
i
n
g
n
eurons
fi
n
d
ot
h

er neurons so t
h
at t
h
e correct connect
i
ons are ma
d
ew
i
t
hi
nt
h
e
i
nsect’s
b
o
dy
.
The first neurons to arise (from the central nervous s
y
stem) are the central pioneer neurons.
Their axons
g
row alon
g
predetermined paths when their tips reco
g

nize particular cues o
n
6
11
E
MBRY
O
NI
C
DEVEL
O
PMEN
T
cell surfaces within the embr
y
o. Thus, a scaffold of axonal pathwa
y
s is initiall
y
erected
,
w
hich later-developin
g
axons are then able to follow, bein
gg
uided b
y
specific reco
g

nitio
n
si
g
nals on the surfaces of the pioneer neurons (Goodman, 1984; Goodman and Bastiani
,
1984). Per
i
p
h
era
l
p
i
oneer neurons, or
i
g
i
nat
i
ng
f
rom ecto
d
erm at t
h
et
i
ps o
f

appen
d
ages,
h
ave a
l
so
b
een
id
ent
ifi
e
d
.T
h
ese grow towar
d
t
h
e centra
l
nervous system, serv
i
ng
l
ater a
s
g
u

id
es
f
or motor axons
i
nnervat
i
n
g
e
ff
ectors, espec
i
a
lly
musc
l
es, an
d
t
h
e sensor
y
axons
f
ro
m
inte
g
umental sensilla. The peripheral pioneer axons die when the necessar

y
connections
h
ave been established (Hemin
g
, 2003).
As em
b
ryogenes
i
s cont
i
nues,
f
us
i
on o
f
gang
li
a occurs
i
nt
h
e
h
ea
d
reg
i

on to
f
orm t
he
b
ra
i
nan
d
su
b
esop
h
agea
l
gang
li
on an
d
at t
h
e poster
i
or en
d
o
f
t
h
ea

bd
omen w
h
ere gang
lia
f
rom segments 8–11
f
orm a compos
i
te structure. In em
b
ryos o
f
spec
i
es
b
e
l
ong
i
ng to
diff
erent
orders of Insecta, var
y
in
g
de

g
rees of fusion of other
g
an
g
lia ma
y
subsequentl
y
occur
.
7
.4. Gut and Derivatives
As note
d
ear
li
er, t
h
e stomo
d
eum an
d
procto
d
eum ar
i
se at t
h
e anter

i
or an
d
poster
i
or en
d
s
of the
g
astral
g
roove, respectivel
y
. Both develop as hollow inva
g
inated tubes, the stomodeu
m
sli
g
htl
y
earlier than the proctodeum, and as the
y
differentiate into the subdivisions of the
foregut and hindgut, respectively, various associated structures arise.
On t
h
e roo
f

o
f
t
h
e stomo
d
eum, evag
i
nat
i
ons or t
hi
c
k
en
i
ngs g
i
ve r
i
se to t
h
e
f
ronta
l
gang
li
on,
h

ypocere
b
ra
l
gang
li
on,
i
ntr
i
ns
i
cce
ll
so
f
t
h
e corpora car
di
aca, an
di
ng
l
uv
i
a
l
gan
-

g
lia. At its anterior end, the proctodeum develops pouches, which are the rudiments of th
e
M
alpi
g
hian tubules. (In man
y
insects additional tubules develop durin
g
larval life.)
The anterior and posterior mid
g
ut rudiments that appeared at
g
astrulation be
g
in t
o
pro
lif
erate at a
b
out t
h
et
i
me o
f
prov

i
s
i
ona
ld
orsa
l
c
l
osure to
f
orm t
h
em
id
gut. Eac
h
ru
di
ment
pro
lif
erates a pa
i
ro
f
stran
d
st
h

at grow cau
d
a
d
or cep
h
a
l
a
d
, respect
i
ve
l
y,
b
etween t
h
e nerve
cor
d
an
dy
o
lk
.A
f
ter stran
d
s

f
rom eac
h
ru
di
ment meet
i
nt
h
em
iddl
eo
f
t
h
eem
b
r
y
o, t
h
e
yg
row
laterall
y
and dorsall
y
so as to eventuall
y

enclose the
y
olk mass. The cells then differentiat
e
as mid
g
ut epithelium. Prior to this, in embr
y
os of some species, the vitellopha
g
es form a
t
emporary “yo
lk
sac” aroun
d
t
h
eyo
lk
mass
.
7
.5. Circulatory
S
ystem, Muscle, and Fat Bod
y
The heart, aorta, musculature, fat bod
y
, linin

g
of the hemocoel, and some components
of the reproductive system are derived from the somites and median mesoderm formed after
gastru
l
at
i
on. As note
d
ear
li
er, t
h
eme
di
an meso
d
erm g
i
ves r
i
se to
h
emocytes. In most em
-
b
ryos, eac
h
som
i

te
b
ecomes
h
o
ll
ow an
df
orms t
h
ree
i
nterconnecte
d
c
h
am
b
ers, t
h
e anter
i
or,
posterior, and ventrolateral pouches. The latter
g
rows into the ad
j
acent ectodermal limb
bud
a

nd breaks up to form intrinsic limb muscles (Fi
g
ure 20.12). The splanchnic walls (i.e.,
t
hose facin
g
the
y
olk) of the two remainin
g
pouches spread round the
g
ut, formin
g
the
g
ut
musculature, some fat body, and part of the reproductive system (Section 7.6). The somati
c
w
a
ll
s(t
h
ose
f
ac
i
ng t
h

e ecto
d
erm) o
f
t
h
e anter
i
or an
d
poster
i
or pouc
h
es g
i
ve r
i
se to extr
i
ns
i
c
li
m
b
musc
l
es,
d

orsa
l
an
d
ventra
ll
on
gi
tu
di
na
l
musc
l
es, an
d
more
f
at
b
o
dy
. For eac
h
musc
l
e
in an insect there is a sin
g
le founder (pioneer) cell that serves as a base to which other

pro
g
enitor muscle cells (m
y
oblasts) become attached. As each muscle develops, it
g
rows
t
owar
d
as
p
ec
ifi
ce
pid
erma
li
nsert
i
on s
i
te (C
h
a
p
ter 14, Sect
i
on 2.1)
.

T
h
e
b
rea
ki
ng up o
f
t
h
e som
i
te wa
ll
s
i
nto
di
screte t
i
ssues means t
h
at
i
n
i
nsects a
s
i
not

h
er art
h
ropo
d
st
h
ere
i
s no true coe
l
om. Rat
h
er, t
h
e
l
atter mer
g
es w
i
t
h
t
h
eep
i
neura
l
sinus (the space between the dorsal surface of the embr

y
o and the
y
olk) and is correctl
y
6
1
2
CHAPTER
20
c
alled a mixocoel (hemocoel). From mesodermal cells at the dorsal
j
unction of the somatic
and s
p
lanchnic walls of the labial to the tenth abdominal somites, a sheet of cardioblasts
develops. As the mesoderm
g
rows around the
g
ut, the sheets on each side become appose
d
to
f
orm t
h
e
h
eart. Ot

h
er somat
i
c meso
d
erm ce
ll
sa
dj
acent to t
h
e car
di
o
bl
asts
diff
erent
i
ate
as a
l
ary musc
l
es, per
i
car
di
a
l

septum, an
d
per
i
car
di
a
l
ce
ll
s. T
h
e aorta
d
eve
l
ops
f
rom t
he
m
edian walls of the antennal somites, which become apposed and
g
row posteriorl
y
to meet
the heart
.
In embr
y

os of insects where the somites remain solid or are not formed as discret
e
segmenta
l
structures, t
h
e meso
d
erm st
ill
g
i
ves r
i
se to t
h
e same components.
7.6. Reproductive
S
yste
m
T
he reproductive s
y
stem includes both mesodermal and ectodermal components. In
f
ema
l
e exopterygotes, t
h

evag
i
na an
d
spermat
h
eca
d
eve
l
op a
f
ter
h
atc
hi
ng as m
id
ventra
l
ec
-
to
d
erma
li
nvag
i
nat
i

ons o
f
t
h
e sevent
h
or e
i
g
h
ta
bd
om
i
na
l
segment. In ma
l
es, t
h
ee
j
acu
l
ator
y
d
uct an
d
ecta

d
enes (ecto
d
erma
l
accessor
ygl
an
d
s) are
f
orme
df
romas
i
m
il
ar m
id
ventra
l
i
nva
g
ination of the ectoderm of the ninth or tenth abdominal se
g
ment.
T
he paired
g

enital ducts and mesadenes (mesodermal accessor
yg
lands) arise in ex-
o
pterygotes
f
rom meso
d
erm o
f
t
h
esp
l
anc
h
n
i
cwa
ll
so
f
certa
i
na
bd
om
i
na
l

som
i
tes w
hi
c
h
fi
rst t
hi
c
k
ens t
h
an
h
o
ll
ows out to
f
orm coe
l
omo
d
ucts. Some o
f
t
h
ese soon
di
sappear,

b
ut
t
h
ose o
f
t
h
e sevent
h
an
d
e
igh
t
h
som
i
tes (
i
n
f
ema
l
es) or n
i
nt
h
an
d

tent
h
som
i
tes (
i
nma
l
es)
e
nlar
g
e to form the ducts and/or accessor
yg
land components. In endopter
yg
otes, the
g
enita
l
ducts are formed durin
g
postembr
y
onic development. In
D
rosophila and other muscomor
ph
D
iptera the reproductive system (excluding the gonads) develops from a single or pair o

f
i
mag
i
na
ldi
scs
d
ur
i
ng metamorp
h
os
i
s(C
h
apter 21, Sect
i
on 4.2)
.
D
eve
l
opment o
f
t
h
e gona
d
svar

i
es, t
h
oug
h
two re
l
ate
d
tren
d
s can
b
e seen, name
l
y, ear
li
er
se
g
re
g
ation of the primordial
g
erm cells and restriction of these cells to fewer abdomina
l
se
g
ments. In the most primitive arran
g

ement, seen in some th
y
sanuran and orthoptera
n
e
mbryos, the germ cells do not become distinguishable until they appear in the splanchnic
w
a
ll
so
f
se
v
era
l
a
bd
om
i
na
l
som
i
tes. In
L
ocu
s
ta em
b
ryos,

f
or examp
l
e, t
h
ey are
f
oun
di
n
i
t
i
a
ll
y
i
n the somites of abdominal segments 2–10, though they remain only in segments 3–
6.
E
ventua
lly
t
h
e
yf
use
l
on
gi

tu
di
na
lly
to
f
orm a compact
g
ona
d
on eac
h
s
id
e. Suc
h
ase
g
menta
l
arran
g
ement is presumabl
y
primitive as it is seen also in adult Annelida, On
y
chophora,
My
riapoda, and non-insectan apter
yg

otes (Anderson, 1972a).
In em
b
ryos o
f
D
i
ctyoptera, P
h
asm
id
a, Em
bi
optera, an
d
Heteroptera t
h
e germ ce
ll
s
b
ecome apparent ear
l
y
i
n gastru
l
at
i
on. Nevert

h
e
l
ess, t
h
ey st
ill b
ecome assoc
i
ate
d
w
i
t
h
t
he
sp
l
anc
h
n
i
c meso
d
erm o
f
severa
l
anter

i
or a
bd
om
i
na
l
se
g
ments.
In embr
y
os of Dermaptera, Psocoptera, Th
y
sanoptera, homopterans, and endopter
y-
g
otes, the
g
erm cells differentiate as the blastoderm forms (see Fi
g
ure 20.3B). After somite
f
ormat
i
on, t
h
ey m
i
grate to a

bd
om
i
na
l
segments 3 an
d
4
i
n exopterygote em
b
ryos or a
b
-
dominal segments
5
and 6 in endopterygote embryos where they divide into left and right
h
a
l
ves an
db
ecome surroun
d
e
db
ysp
l
anc
h

n
i
c meso
d
erm.
8. S
p
ecial Forms of Embr
y
onic Develo
p
men
t
T
he
g
reat ma
j
orit
y
of insect species are bisexual and females la
y
e
gg
s that contain a
c
onsiderable amount of
y
olk. However, in some species, males ma
y

be rare and females
6
1
3
E
MBRY
O
NI
C
DEVEL
O
PMEN
T
ma
y
produce viable offsprin
g
from unfertilized e
gg
s (partheno
g
enesis). In another form of
asexual reproduction, pol
y
embr
y
on
y
, which is characteristic of some parasitic H
y

menopter
a
and Strepsiptera, several embr
y
os develop from one fertilized e
gg
. In other insects, fertilized
eggs may
b
e reta
i
ne
d
w
i
t
hi
nt
h
e
f
ema
l
e repro
d
uct
i
ve tract
f
or var

i
e
d
per
i
o
d
so
f
t
i
me so t
h
at
a young
i
nsect may
h
atc
hf
rom t
h
e egg a
l
most as soon as or even
b
e
f
ore t
h

e
l
atter
i
s
l
a
id
(v
i
v
i
par
i
t
y
). In a
f
ew spec
i
es pae
d
o
g
enes
i
sma
y
occur w
h

ere mature
l
arvae are a
bl
et
o
produce, partheno
g
eneticall
y
and usuall
y
viviparousl
y
, a further
g
eneration of
y
oun
g.
8.1. Parthenogenesi
s
T
h
ea
bili
t
y
o
f

un
f
ert
ili
ze
d
e
gg
sto
d
eve
l
op
i
s common to man
yi
nsect spec
i
es an
di
n
some is the normal mode of reproduction under certain conditions. In all insects except
L
epidoptera and Trichoptera, the female is the homo
g
ametic sex (i.e., havin
g
two X se
x
chromosomes) and the male, heterogametic (XY or XO). Unfertilized eggs, therefore, wil

l
conta
i
non
l
yXc
h
romosomes. However, w
h
et
h
er t
h
ey conta
i
n one or two suc
h
c
h
romo-
somes an
d
,t
h
ere
f
ore, t
h
esexo
f

part
h
enogenet
i
co
ff
spr
i
ng,
d
epen
d
sont
h
e
b
e
h
av
i
or o
f
t
he
chromosomes durin
g
meiosis in the ooc
y
te nucleus (Suomalainen, 19
6

2; White, 1973).
T
wo forms of female-producin
g
partheno
g
enesis (thel
y
tok
y
) are known. In som
e
species no meiotic division occurs during oogenesis. Therefore, offspring are diploid and
f
ema
l
e (ame
i
ot
i
c or apom
i
ct
i
c part
h
enogenes
i
s) an
d

w
ill h
ave t
h
e same genet
i
cma
k
eup a
s
th
e mot
h
er, un
l
ess mutat
i
on or
i
nsert
i
on o
f
transposa
bl
ee
l
ements occurs (Hem
i
ng, 2003). I

n
meiotic (automictic) partheno
g
enesis, the t
y
pical reduction division is followed b
y
nuclear
fusion so that a diploid chromosome complement is retained. A
g
ain, therefore, the offsprin
g
are female but they have a different genetic make up from their mother.
H
ap
l
o
id
part
h
enogenes
i
s (arr
h
enoto
k
y), w
h
ere t
h

e oocyte nuc
l
eus un
d
ergoes me
i
os
i
s
th
at
i
s not
f
o
ll
owe
db
y nuc
l
ear
f
us
i
on,
i
so
f
re
l

at
i
ve
l
y rare occurrence, t
h
oug
h
typ
i
ca
l
o
f
H
y
menoptera, T
hy
sanoptera, an
d
some
h
omopterans an
d
Co
l
eoptera. It resu
l
ts
i

nt
he
production of males. In H
y
menoptera, haploid partheno
g
enesis is facultative; that is,
a
female determines whether or not an e
gg
will be fertilized. In the hone
y
bee, for example,
a
queen norma
ll
y
l
ays
f
ert
ili
ze
d
eggs t
h
at
d
eve
l

op
i
nto wor
k
ers (
di
p
l
o
id f
ema
l
es). However,
u
n
d
er certa
i
n con
di
t
i
ons,
f
or examp
l
e, w
h
en t
h

e
hi
ve
i
s crow
d
e
d
,an
d
t
h
ewor
k
ers construc
t
l
ar
g
er t
h
an norma
ld
rone ce
ll
sont
h
e
h
one

y
com
b
,s
h
ew
ill l
a
y
un
f
ert
ili
ze
d
e
gg
s
f
rom w
hi
c
h
h
aploid males develop, as a preliminar
y
to swarmin
g
.
Partheno

g
enesis, producin
g
in most species female offsprin
g
,ma
y
confer two advan-
t
ages. In a species whose population density may be (temporarily) low, the ability of an
i
so
l
ate
df
ema
l
e to repro
d
uce part
h
enogenet
i
ca
ll
y may ensure surv
i
va
l
o

fh
er genotype un
-
til
t
h
e popu
l
at
i
on
d
ens
i
ty
i
ncreases an
d
ma
l
es are aga
i
n
lik
e
l
yto
b
e encountere
d

. Mor
e
often, however, partheno
g
enesis is emplo
y
ed as a mechanism that provides a rapid mod
e
of reproduction, to enable a species to take full advanta
g
e of temporaril
y
ideal conditions.
T
hus, a parthenogenetic female, who does not require to locate, or be located by, a male
can
d
evote
h
er t
i
me an
d
energy to egg pro
d
uct
i
on. Furt
h
er, a

ll h
er o
ff
spr
i
ng are
f
ema
l
e, so
th
at
h
er max
i
mum repro
d
uct
i
ve potent
i
a
l
can
b
e rea
li
ze
d
.T

h
e
di
sa
d
vantage o
f
part
h
eno
-
g
enesis is that the
g
enot
y
pe of successive
g
enerations remains more or less constant so tha
t
adaptation of a species to chan
g
in
g
environmental conditions is ver
y
slow. To counteract
t
his, man
y

species alternate one or more partheno
g
enetic
g
enerations with a normal sexua
l
generat
i
on. Ap
hid
s,
f
or examp
l
e, repro
d
uce
f
or most o
f
t
h
e year
b
y ame
i
ot
i
c part
h

enogene-
s
i
s(F
i
gure 8.8). However, towar
df
a
ll
(an
d
a
ff
ecte
db
yc
h
ang
i
ng env
i
ronmenta
l
con
di
t
i
ons)
th
ere occurs,

d
ur
i
n
g
maturat
i
on o
f
some ooc
y
tes, a separat
i
on o
f
t
h
etwoXc
h
romosomes,
6
14
CHAPTER
20
o
ne of which mi
g
rates to the polar bod
y
and is destro

y
ed. From such e
gg
s (with an XO
c
onstitution) males will develop. As spermato
g
enesis occurs in these individuals, sperma-
toc
y
tes containin
g
either one or no X chromosome are produced. However, the latter d
o
n
ot mature, so t
h
at on
l
y sperm w
i
t
h
anXc
h
romosome resu
l
t. T
h
ere

f
ore, t
h
e overw
i
nter
i
n
g
e
ggs pro
d
uce
d
as a resu
l
to
f
mat
i
ng w
ill h
aveanXXsexc
h
romosome comp
l
ement an
d
g
i

ve
r
i
se t
h
e
f
o
ll
ow
i
n
g
spr
i
n
g
on
ly
to
f
ema
l
es.
8
.
2
.Pol
y
embr

y
on
y
P
o
l
yem
b
ryony, t
h
e
d
eve
l
opment o
f
more t
h
an one em
b
ryo
f
rom one egg,
i
s
k
nown to
b
e a norma
l

occurrence
i
na
b
out 30 spec
i
es o
f
paras
i
t
i
cH
y
menoptera (most
ly
Enc
y
rt
id
ae,
P
lat
yg
asteridae, and Braconidae) and one species of Strepsiptera (Ivanova-Kasas, 1972)
.
In these insects it is alwa
y
s associated with either parasitism or viviparit
y

and is presumed
to have evolved in conjunction with the abundance of food offered by these two modes of
lif
e. C
h
aracter
i
st
i
ca
ll
y, t
h
e eggs o
f
po
l
yem
b
ryon
i
c spec
i
es are m
i
nute an
dd
evo
id
o

f
yo
lk
.
Because t
h
ey
d
epen
d
on an externa
l
(
h
ost or materna
l
) source o
f
nutr
i
ents t
h
ec
h
or
i
on
,
w
hich is initiall

y
thin and permeable, soon disappears. Further, in H
y
menoptera, the serosa
becomes modified for the u
p
take of nutrients and is known as a “tro
p
hamnion.”
B
oth the number of embryos formed and the point in development at which they becom
e
di
scern
ibl
evary.InP
l
at
yg
aster
h
iema
l
i
s
,a
paras
i
te o
f

Hess
i
an
fl
y
l
arvae,
f
or examp
l
e, at
t
h
e
f
our-ce
ll
stage, t
h
ece
ll
s may separate
i
nto two groups so t
h
at tw
i
nem
b
ryos are

f
orme
d.
In contrast
,
in the chalcidi
d
Litomastix truncatellu
s
, which parasitizes larvae of the mot
h
gen
u
s
Plusi
a
,
formation of embr
y
os does not be
g
in until the 220- to 225-blastomere sta
g
e.
A
t this stage, certain of the blastomeres become spindle-shaped and fuse to form a syncytia
l
s
h
eat

h
t
h
at
di
v
id
es t
h
e rema
i
n
i
ng
bl
astomeres
i
nto groups, t
h
epr
i
mary em
b
ryon
i
c masses.
In
d
ue course, secon
d

ary, tert
i
ary, etc., em
b
ryon
i
c masses
f
orm so t
h
at t
h
e
fi
na
l
num
b
er o
f
potent
i
a
l
em
b
r
y
os ma
y

excee
d
1000. T
h
e ear
ly d
eve
l
opment o
f
L
itoma
s
ti
x
i
s summar
i
ze
din
Fi
g
ure 20.13. Eventuall
y
the pol
yg
erm (the total embr
y
onic mass within the trophamnion)
disinte

g
rates, and each embr
y
o develops into a larva. The larvae feed within a host until all
t
h
e usa
bl
e parts are consume
d
an
d
t
h
en pupate. At t
hi
spo
i
nt t
h
e
h
ost
i
s not
hi
ng more t
h
an
a cut

i
cu
l
ar
b
ag
f
u
ll
o
f
paras
i
tes (F
i
gure 20.14)
.
8.3. V
i
v
i
par
i
t
y
Vi
viparity, the retention of developing offspring within the maternal genital tract, is
f
oun
di

n a range o
f
comp
l
ex
i
ty w
i
t
hi
nt
h
e Insecta. It
i
s seen
i
n
diff
erent
f
orms
i
n spec
i
es
f
rom severa
l
or
d

ers,
b
ut among D
i
ptera t
h
e ent
i
re range o
f
var
i
at
i
on may occur.
In its simplest form (ovoviviparit
y
) the e
gg
s retain their full complement of
y
olk for
n
ourishment of the embr
y
o. The e
gg
sma
y
be retained within the mother for a varied perio

d
o
f time but usually are laid just before they hatch. Such an arrangement is seen in many
Tachinidae (Figure 20.1
5
) where the first-instar larvae actually escape from the chorion
d
ur
i
ng ov
i
pos
i
t
i
on. Assoc
i
ate
d
w
i
t
h
retent
i
on o
f
t
h
e eggs, w

hi
c
h
presuma
bl
ya
ff
or
d
st
h
em
g
reater protection, is a trend toward production of fewer of them. As fewer e
gg
s are produce
d
e
ach can acquire more
y
olk so that larvae can hatch at more advanced sta
g
es of development.
Fo
re
x
ample, many Sarcophagidae (flesh flies) produce only 40–80 eggs but are larviparous;
t
h
at

i
s,
l
arvae
h
atc
hf
rom t
h
e eggs w
hil
et
h
e
l
atter are st
ill
w
i
t
hi
nt
h
e repro
d
uct
i
ve tract.
A
tt

h
e extreme, t
h
e num
b
er o
f
eggs t
h
at mature s
i
mu
l
taneous
l
y
i
sre
d
uce
d
to one, as,
f
or
e
xamp
l
e,
in
H

yl
em
y
a stri
g
osa (Ant
h
om
yiid
ae) an
d
Te
rm
itoxe
n
ia
sp. (P
h
or
id
ae). I
n
Hyl
em
y
a
6
1
5
E

MBRY
O
NI
C
DEVEL
O
PMEN
T
F
I
GU
RE 20.13
.
Ear
ly d
eve
l
opment o
f
L
i
tomast
i
x
(
H
y
menoptera). (A) Fert
ili
zat

i
on; (B)
fi
rst c
l
eava
g
e; (C) two
-
cell stage; (D–F) next stages; (G) formation of spindle cells; and (H) formation of secondary embryonic masses.
[
A
f
ter O. M. Ivanova-Kasas, 1972, Po
l
yem
b
ryony
i
n
i
nsects,
i
n
:
D
eve
l
opmenta
l

Systems: Insects
,V
ol. I (S. J.
V
V
Counce an
d
C. H. Wa
ddi
n
g
ton, e
d
s.). B
y
perm
i
ss
i
on o
f
Aca
d
em
i
c Press Lt
d
., an
d
t

h
e aut
h
or.]
t
he larva that emer
g
es from a newl
y
laid e
gg
molts immediatel
y
to the second instar; i
n
T
erm
i
toxen
ia
,
w
h
ose egg
i
sre
l
at
i
ve

l
y
l
arger,
i
t
i
sat
hi
r
d
-
i
nstar
l
arva t
h
at emerges
f
rom an
eg
g
an
di
t pupates w
i
t
hi
na
f

ew m
i
nutes.
I
n tru
ly
v
i
v
i
parous spec
i
es,
d
eve
l
op
i
n
g
o
ff
spr
i
n
g
o
b
ta
i

nt
h
e
i
r
f
oo
df
rom t
h
e mot
h
er.
Accordin
g
l
y
, the structures of the maternal reproductive s
y
stem and e
gg
are modified to
facilitate this exchan
g
e. As in ovoviviparit
y
, the trend is toward reduction of the number of
em
b
ryos

b
e
i
ng
d
eve
l
ope
d
s
i
mu
l
taneous
l
y.
S
ome ap
hid
s, Psocoptera, an
d
Dermaptera
(
H
emimeru
s
)s
h
ow pseu
d

op
l
acenta
l
v
i
v
i
par-
ity (Hagan, 19
5
1). Eggs of these insects contain little or no yolk and lack a chorion. The
y
d
evelop within the ovariole, where the follicle cells supposedl
y
suppl
y
at least some nourish-
ment to the embr
y
o. (In species with meroistic ovarioles, the nurse cells are also important)
.
In
Hem
i
meru
s
, for example, follicle cells adjacent to the anterior and posterior ends of a
n

oocyte pro
lif
erate an
db
ecome connecte
d
w
i
t
h
t
h
eem
b
ryon
i
c mem
b
ranes
f
orm
i
ng pseu-
d
op
l
acentae. Later, t
h
e
f

o
lli
c
l
ece
ll
s
d
egenerate
b
ecause,
i
t
i
s assume
d
,t
h
ey are supp
l
y
i
n
g
nutrients to the developin
g
embr
y
o (Fi
g

ure 20.1
6
)
.
F
IGURE 20.14
.
C
aterp
ill
ars paras
i
t
i
ze
d
by
Li
tomast
i
x.
[
From R. R. As
k
ew,
1971
,
P
ar
asitic Insects.

r
r
B
y permission o
f
He
i
nemann E
d
ucat
i
ona
l
Boo
k
sLt
d
.
]
6
1
6
CHAPTER
20
F
I
G
URE 20.15
.
F

ema
l
e repro
d
uct
i
ve s
y
stem o
f
t
h
e tac
hi
n
id
Pan
z
eri
a
(D
i
ptera). (A) New
ly
emer
g
e
dfly
;an
d

(B) mature female, with
g
reatl
y
enlar
g
ed va
g
ina formin
g
a brood chamber. An e
gg
containin
g
a full
y
forme
d
e
mbryo is being laid, [After V. B. Wigglesworth, 1965, The Principles o
f
Insect Physiolog
y
,
6th ed., Methuen and
C
o. B
y
perm
i

ss
i
on o
f
t
h
e aut
h
or.]
In
Gl
ossina
s
pp. an
d
pup
i
parous D
i
ptera a
d
enotrop
hi
cv
i
v
i
par
i
ty occurs. In t

hi
s arrange-
m
ent, an egg
i
s norma
l
,t
h
at
i
s, conta
i
ns yo
lk
an
d
possesses a c
h
or
i
on, yet
i
s reta
i
ne
d
w
i
t

hi
n
t
h
e expan
d
e
db
ursa, t
h
e so-ca
ll
e
d
uterus. Em
b
r
y
on
i
c
d
eve
l
opment
i
s, t
h
ere
f

ore, correct
ly
described as ovoviviparous. However, after hatchin
g
, the larva remains within the uterus and
f
eeds on secretions (uterine milk) of the enormous accessor
yg
lands that ramif
y
throu
g
h the
abdomen (Figure 20.17). One larva at a time develops and pupation occurs shortly after birth
.
In
h
emocoe
li
cv
i
v
i
par
i
ty, use
db
y Streps
i
ptera an

d
some pae
d
ogenet
i
c Cec
id
omy
iid
ae
(
D
i
ptera), oocytes are re
l
ease
df
rom t
h
eovar
i
o
l
es
i
nto t
h
e materna
lh
emocoe

l
. In Streps
i
ptera
f
ertilization occurs within the maternal bod
y
cavit
y
, and, durin
g
embr
y
onic development,
FIGURE 20.16.
L
ongitudinal section through ovarian follicle
o
f
H
emimerus (Derma
p
tera) to s
h
ow
p
seu
d
o
pl

acentae. (A
f
ter V.
B. Wi
gg
lesworth, 196
5,
T
he Principles o
f
Insect Physiology
,
6th
ed., Methuen and Co. By permission of the author.
]
6
1
7
E
MBRY
O
NI
C
DEVEL
O
PMEN
T
F
I
G

URE 20.17
.
Fema
l
e repro
d
uct
i
ve s
y
stem o
f
Gl
ossina
(
D
i
ptera) to s
h
ow en
l
ar
g
e
d
accessor
ygl
an
d
s. Not

e
also that onl
y
one e
gg
at a time is maturin
g
. [After V. B. Wi
gg
lesworth, 196
5
. The Principles o
f
Insect Physiology
,
6th ed., Methuen and Co. By permission of the author.]
nutr
i
ents are a
b
sor
b
e
ddi
rect
l
y
f
rom t
h

e
h
emo
l
ymp
h
.A
f
ter
h
atc
hi
ng, t
h
e
l
arvae escape
f
ro
m
th
e
f
ema
l
e’s
b
o
d
yv

i
at
h
e gen
i
ta
l
pores. In some cec
id
omy
iid
s, oocytes
d
eve
l
op part
h
eno-
g
eneticall
y
. Initiall
y
, development occurs within the ovarioles, but the larvae on hatchin
g
esca
p
e into the hemocoel. The larvae remain within the mother and feed on her tissues until
j
ust prior to pupation when they exit via the body wall

.
8.4. Paedo
g
enes
is
Though not actually a form of embryonic development, paedogenesis, that is, preco
-
c
i
ous sexua
l
maturat
i
on o
fj
uven
il
e stages,
i
s conven
i
ent
l
y ment
i
one
dh
ere. Pae
d
ogenes

i
s
i
s
u
sua
ll
y assoc
i
ate
d
w
i
t
hb
ot
h
part
h
enogenes
i
san
d
v
i
v
i
par
i
ty, an

d
, pro
b
a
bl
y,
i
s
b
est s
h
own
i
n
certain Cecidom
y
iidae, thou
g
h it is known to occur also in some Chironomidae (Diptera),
Coleoptera, and Hemiptera. In some cecidom
y
iids, the ooc
y
tes develop viviparousl
y
in the
h
emocoel of the last larval or pupal instar. In some chironomids, embryonic development
b
eg

i
ns
i
n
f
ema
l
e pupae. In t
h
ev
i
v
i
parous
h
em
i
pteran Hesperoctenes
f
ema
l
e
l
ar
v
ae t
h
a
t
h

ave
b
een
i
nsem
i
nate
dh
emocoe
li
ca
ll
y
d
eve
l
op em
b
ryos w
i
t
hi
nt
h
e
i
rovar
i
o
l

es. In an ex
-
t
reme situation seen in some aphids, development of
y
oun
g
ma
y
be
g
in in the mother whil
e
she herself is still in here own mother’s reproductive s
y
stem!
9
. Factors Affectin
g
Embryonic Developmen
t
Temperature
i
s pro
b
a
bl
yt
h
es

i
ng
l
e most
i
mportant env
i
ronmenta
l
var
i
a
bl
ea
ff
ect
i
n
g
em
b
ryon
i
c
d
eve
l
opment. For eggs o
f
most spec

i
es, t
h
ere are upper an
dl
ower tempera
-
t
ure
li
m
i
ts, outs
id
ew
hi
c
hd
eve
l
opment
i
s
g
reat
ly
retar
d
e
d

or comp
l
ete
ly i
n
hibi
te
d
.W
i
t
hin
t
hese limits, however, an inverse but linear relationshi
p
exists between tem
p
erature and
t
ime re
q
uired to com
p
lete develo
p
ment; that is, the total heat re
q
uirement (tem
p
erature

6
1
8
CHAPTER
20
above minimum required X duration of exposure to this temperature) is constant for a
g
iven species. This heat requirement is t
y
picall
y
measured in de
g
ree-da
y
s. Outside these
developmental limits,
y
et within the limits of viabilit
y
,ane
gg
ma
y
survive but does no
t
d
eve
l
op. Un

d
er t
h
ese con
di
t
i
ons,
i
t
i
ssa
id
to
b
equ
i
escent an
di
nt
hi
s state may surv
i
ve
f
o
r
a cons
id
era

bl
e
l
engt
h
o
f
t
i
me. In a qu
i
escent state, an egg
i
sa
l
ways rea
d
ytota
k
ea
d
van-
ta
g
eo
ff
avora
bl
e con
di

t
i
ons, even
if
on
ly
temporar
y
, to cont
i
nue
i
ts
d
eve
l
opment. However,
q
uiescence is a relativel
y
sensitive developmental state; that is, outside certain temperatur
e
l
imits, an e
gg
will be killed. For man
y
species, therefore, which exist in habitats exposed
to c
li

mat
i
c extremes, espec
i
a
ll
yo
f
temperature
b
ut a
l
so o
f
prec
i
p
i
tat
i
on, a more res
i
stan
t
state o
fd
eve
l
opmenta
l

arrest,
di
apause,
h
as evo
l
ve
d
to perm
i
tt
h
e
i
r surv
i
va
l
.D
i
apause
is
di
scusse
d
at greater
l
engt
hi
nC

h
apter 22 (Sect
i
on 3.2.3), t
h
oug
hi
nt
h
e present contex
t
i
t is worth notin
g
that diapause ma
y
occur at different sta
g
es of embr
y
onic development
and with varied stren
g
th in different species. In all instances, however, it is characterized
by a cessation of morphogenesis and a considerable lowering of the metabolic rate. Also
,
t
h
e water content o
f

an egg
i
so
f
ten
l
ow at t
hi
st
i
me. I
n
B
om
byx
,di
apause, w
hi
c
hb
eg
i
n
s
i
n overw
i
nter
i
ng eggs a

l
most as soon as t
h
ey are
l
a
id
,
i
s extreme
l
y strong; t
h
at
i
s, even
w
hen e
gg
s are experimentall
y
maintained at 1
5
◦
C
to
20
◦
C
from the time of la

y
in
g
the
y
will
n
ot develop. Development be
g
ins onl
y
after the
y
have been exposed to a temperature of
ab
out
0
◦
C
f
or severa
l
mont
h
s. In eggs o
f
t
h
e
d

amse
lfl
y
L
estes con
g
ene
r
,
di
a
p
ause
i
sa
l
so
s
trong
b
ut
d
oes not commence unt
il
a
f
ter anatreps
i
s. D
i

apause
i
n eggs o
f
t
h
e grass
h
oppe
r
M
e
l
anop
l
us
d
ifferentia
l
i
s
al
so occurs a
f
ter anatreps
i
s
b
ut
i

s wea
k
.S
h
ou
ld
t
h
e temperature
to which e
gg
s are exposed be maintained at summer levels (around 2
5
◦
C
), some of the e
ggs
will develop directl
y
, thou
g
h more slowl
y
than those that have under
g
one chillin
g
.Ine
gg
s

o
f some insects, for exam
p
le, certain mos
q
uitoe
s
(
Aedes
s
pp.) and the damselfly Leste
s
d
is
j
unctu
s
,
em
b
ryon
i
c
d
eve
l
opment
i
sa
l

most comp
l
ete
db
e
f
ore
di
apause
i
s
i
n
i
t
i
ate
d.
T
h
roug
h
an e
ff
ect on part
h
enogenes
i
s, temperature may a
l

so a
ff
ect t
h
e sex rat
i
oo
f
the offsprin
g
. For example, in H
y
menoptera hi
g
her temperatures often favor production o
f
haploid males. In some bisexual species, extreme hi
g
h or low temperatures ma
y
disrupt the
normal sex chromosome distribution that occurs during meiosis, so that a preponderance
of
ma
l
es or
f
ema
l
es resu

l
ts
.
Water
i
s anot
h
er
i
mportant requ
i
rement an
di
n eggs o
f
many spec
i
es must
b
e acqu
i
re
d
f
rom the external environment before embr
y
onic development can be
g
in. When it is avail-
a

ble to an e
gg
in insufficient quantit
y
, the embr
y
o becomes quiescent or remains in diapause
(
thou
g
h this was not induced b
y
the lack of moisture). Some species can obtain sufficient
water
f
rom mo
i
sture
i
nt
h
ea
i
r. For examp
l
e, eggs o
f
t
h
e

b
eet
l
e
S
itona,w
h
en
k
e
p
tat20
◦
C
a
nd 100% relative humidity, hatch in 10.
5
days; at the same temperature but only 62%
r
elative humidit
y
, development takes twice as lon
g
. In other species contact of the e
gg
with
l
iquid water is necessar
y
for continued development. Such is the case in the damselfl

y
e
ggs
mentioned above which
p
ass the winter in snow-covered, dried-out
S
cirpus
ste
m
sa
n
ddo
not cont
i
nue t
h
e
i
r
d
eve
l
opment unt
il
t
h
e stems
b
ecome water

l
ogge
df
o
ll
ow
i
ng t
h
e spr
i
n
g
t
h
a
w
.
T
h
ou
gh
t
h
e presence o
f
ec
dy
sone
lik

emo
l
ecu
l
es an
dj
uven
il
e
h
ormone was
fi
rst re-
p
orted some 40
y
ears a
g
o, their sources and roles in embr
y
onic development are onl
y
s
lowl
y
bein
g
clarified. As noted above, the source of these hormonal factors, at least until
af
ter

k
atatreps
i
s,
i
s materna
l
;t
h
at
i
st
h
e compoun
d
s are
d
epos
i
te
d
as con
j
ugates w
i
t
hi
nt
he
e

g
g
pr
i
or to ov
i
pos
i
t
i
on. For spec
i
es suc
h
as
l
ocusts an
d
grass
h
oppers t
h
at pro
d
uce severa
l
e
m
b
r

y
on
i
c cut
i
c
l
es, t
h
ere
i
sac
l
ear corre
l
at
i
on
b
etween pea
k
so
ff
ree ec
dy
sone an
db
out
s
o

f cuticle s
y
nthesis. In other species the onset and termination of embr
y
onic diapause is
6
1
9
E
MBRY
O
NI
C
DEVELOPMEN
T
associated with chan
g
es in free ecd
y
sone levels. Juvenile hormone seems to be involved
in embr
y
onic development in a manner similar to that in larvae, namel
y
, the qualitativ
e
expression of cuticle structure; however, little experimental evidence supports this con
j
ec-
t

ure. Some stu
di
es
h
ave
id
ent
ifi
e
dj
uven
il
e
h
ormone
i
nqu
i
te ear
l
y stages o
f
em
b
ryogenes
i
s
(
i
.e., we

ll b
e
f
ore cut
i
cu
l
ogenes
i
s) suggest
i
ng t
h
at
i
t
h
as ot
h
er ro
l
es. One suc
h
ro
l
e may
be
t
he re
g

ulation of ectodermal
g
rowth leadin
g
to dorsal closure. Thou
g
h neurosecretor
y
cells
and corpora cardiaca have been identified in descriptions of embr
y
onic development, and
specific products have been assa
y
ed in a few species, their roles in embr
y
o
g
enesis remai
n
u
n
k
no
w
n
.
1
0. Hatchin
g

T
o
escape
f
rom t
h
e egg, a
l
arva must
b
rea
k
t
h
roug
h
t
h
evar
i
ous mem
b
ranes t
h
at surroun
d
i
t. T
h
ese

i
nc
l
u
d
et
h
ec
h
or
i
on, v
i
te
lli
ne mem
b
rane, an
d
,
i
n eggs o
f
some spec
i
es, serosa
l
cut
i
c

l
e. Furt
h
er,
i
n man
y
exopter
yg
otes an
d
some en
d
opter
yg
otes a new
ly h
atc
h
e
dl
arva
i
s
surrounded b
y
embr
y
onic cuticle that also must be shed before the insect is trul
y

free
.
The
g
eneral mechanism of hatchin
g
is as follows. An insect first swallows amnioti
c
fl
u
id
,
∗
f
o
ll
owe
d
usua
ll
y
b
ya
i
r, or water, w
hi
c
h diff
uses
i

nto t
h
e egg. T
h
ea
bd
omen
i
st
h
en
contracte
d
to
f
orce
h
emo
l
ymp
hi
nto t
h
e
h
ea
d
an
d
t

h
orax, w
hi
c
h
en
l
arge an
d
cause t
h
eeg
g
mem
b
ranes to rupture. To
f
ac
ili
tate rupture t
h
ec
h
or
i
on ma
yh
ave pre
d
eterm

i
ne
dli
nes o
f
w
eakness that run lon
g
itudinall
y
or transversel
y
, the latter separatin
g
an anterior e
gg
cap
from the more posterior portion of the e
gg
.Inman
y
species, e
gg
bursters, in the form o
f
h
ar
d
cut
i

cu
l
ar sp
i
nes or p
l
ates, or t
hi
n evers
ibl
e
bl
a
dd
ers, may
d
eve
l
op on t
h
e
h
ea
d
,t
h
orax
,
or a
bd

omen. In Acr
idid
ae an
d
t
h
ose Hem
i
ptera
i
nw
hi
c
h
p
l
europo
di
a
d
eve
l
op,
i
t
i
s
b
e
li

eve
d
th
at t
h
ese
gl
an
d
s secrete c
hi
t
i
nase t
h
at
di
sso
l
ves t
h
e serosa
l
cut
i
c
l
easana
id
to

h
atc
hi
n
g.
L
arvae of Lepidoptera simpl
y
eat their wa
y
out of the e
gg
.
W
here an embr
y
onic cuticle is present, this ma
y
be shed concurrentl
y
with the other
enclosing membranes, or may ensheath a larva until it has completely escaped from th
e
egg, as
i
nO
d
onata, Ort
h
optera, an

d
some Hem
i
ptera. In t
h
ese
i
nsects t
h
eem
b
ryon
i
c cut
i
c
l
e
u
n
d
erwent apo
l
ys
i
s some t
i
me pr
i
or to

h
atc
hi
ng, an
d
t
h
e
fi
rst-
i
nstar
l
arva
l
cut
i
c
l
e
i
sa
l
rea
d
y
formed beneath. Thus, the insect hatches as a pharate first-instar larva. In Orthoptera an
d
endoph
y

tic Odonata, the embr
y
onic cuticle presumabl
y
protects a larva until it reaches th
e
surface of the substrate in which the egg was laid. In other species, however, its function is
u
nc
l
ear. It
i
ss
h
e
d
a
f
ew m
i
nutes a
f
ter a
l
arva
h
as reac
h
e
d

t
h
e sur
f
ace, a process ca
ll
e
d
t
he
i
nterme
di
ate mo
l
t.
1
1.
S
ummar
y
Most
i
nsects are ov
i
parous an
d
t
h
ere

f
ore
l
ay eggs t
h
at conta
i
n muc
h
yo
lk
. However,
th
ere
i
sanevo
l
ut
i
onar
y
tren
d
towar
d
re
d
uct
i
on o

f
t
h
e
y
o
lk
:c
y
top
l
asm rat
i
o to perm
i
t more
rapid embr
y
onic development
.
C
leava
g
ebe
g
ins at a predetermined site, the cleava
g
e center, and earl
y
divisions are s

y
n-
chronous. Most energids migrate through the yolk to the periplasm and form the blastoderm
;
∗
T
hi
s
fl
u
id i
sno
l
on
g
er
i
nt
h
e amn
i
ot
i
ccav
i
t
y
w
h
ose mem

b
ranes were
d
estro
y
e
dd
ur
i
n
gd
orsa
l
c
l
osure.
6
2
0
CHAPTER
20
some remain in the
y
olk as vitellopha
g
es that suppl
y
nutrients to the embr
y
o. Posteriorl

y
m
ovin
g
ener
g
ids receive a si
g
nal at the activation center, which stimulates differentiation
o
f part of the blastoderm into the embr
y
onic primordium. Differentiation be
g
ins at a pre
-
d
eterm
i
ne
d
s
i
te, t
h
e
diff
erent
i
at

i
on (comm
i
tment) center,
l
ocate
di
nt
h
ereg
i
on o
f
t
h
e
f
uture
prot
h
orax. T
h
eem
b
ryon
i
cpr
i
mor
di

um o
f
exopterygotes
i
s usua
ll
y sma
ll
an
d
grows
b
y
a
gg
re
g
at
i
on an
d
pro
lif
erat
i
on o
f
ce
ll
s, w

h
ereas t
h
at o
f
most en
d
opter
yg
otes
i
s
l
ar
g
etoper
-
m
it rapid tissue differentiation and embr
y
onic
g
rowth. Elon
g
ation and differentiation o
f
the primordium (now known as the
g
erm band) occur, and externall
y

se
g
mentation and
appen
d
age
f
ormat
i
on are o
b
v
i
ous;
i
nterna
ll
y som
i
tes
f
orm an
d
meso
d
erm
diff
erent
i
ates. S

i
-
m
u
l
taneous
l
y,
i
nem
b
ryos o
f
most spec
i
es t
h
e amn
i
on an
d
serosa
d
eve
l
op
f
rom pro
lif
erat

i
ng
e
xtra-em
b
ryon
i
cce
ll
satt
h
e marg
i
ns o
f
t
h
e germ
b
an
d
. Anatreps
i
s, movement o
f
t
h
e germ
band into the
y

olk core, occurs in e
gg
s of most exopter
yg
otes at this time
.
At the end of
g
erm band formation the amnion and serosa fuse, then break in the head
region, and the combination rolls back dorsally over the yolk which is left covered by onl
y
t
h
e amn
i
on (prov
i
s
i
ona
ld
orsa
l
c
l
osure). Katatreps
i
snowta
k
es p

l
ace
i
n eggs w
i
t
hi
mmerse
d
germ
b
an
d
s, so t
h
at t
h
eem
b
ryo
i
s returne
d
to t
h
eyo
lk
sur
f
ace w

i
t
hi
ts
h
ea
df
ac
i
ng t
h
e
anterior pole of the e
gg
. Embr
y
onic ectoderm now extends around the
y
olk to replace the
amnion
(
definitive dorsal closure
).
P
aired segmental appendages develop from evaginations of the embryonic ectoder
m
but
m
ay
b

ecome re
d
uce
d
or
di
sappear. S
h
ort
l
ya
f
ter
d
e
fi
n
i
t
i
ve
d
orsa
l
c
l
osure, t
h
eem
b

ry-
o
n
i
c ecto
d
erm
diff
erent
i
ates
i
nto ep
id
erm
i
san
d
secretes a cut
i
c
l
e. Spec
ifi
cep
id
erma
l
ce
ll

s
differentiate into external sensilla and e
y
es, and in some species form ima
g
inal discs and
histoblasts. Inva
g
inations of the ectoderm
g
ive rise to the endoskeleton, tracheal s
y
stem,
salivar
yg
lands, corpora allata, molt
g
lands, exocrine
g
lands, and, in females, the va
g
ina
an
d
spermat
h
eca,
i
nma
l

es, t
h
ee
j
acu
l
atory
d
uct an
d
ecta
d
enes. T
h
e
f
oregut an
dhi
n
d
gut
d
eve
l
op
f
rom ecto
d
erma
li

nvag
i
nat
i
ons at t
h
e anter
i
or an
d
poster
i
or en
d
s, respect
i
ve
l
y, o
f
t
h
e
g
astra
lg
roove. T
h
em
idg

ut
i
s
f
orme
df
rom anter
i
or an
d
poster
i
or m
idg
ut ru
di
ment
s
that
g
row toward each other and on meetin
g
extend dorsolaterall
y
to enclose the
y
olk. The
c
entral nervous s
y

stem arises from neuroblasts in the midventral line. The stomato
g
astri
c
n
ervous system
d
eve
l
ops
f
rom evag
i
nat
i
ons
i
nt
h
e roo
f
o
f
t
h
e stomo
d
eum.
Th
e

h
eart, aorta, septa, musc
l
e,
f
at
b
o
d
y, pa
i
re
d
gen
i
ta
ld
ucts, an
d
mesa
d
enes ar
e
m
eso
d
erma
ld
er
i

vat
i
ves. Gona
d
sar
i
se
f
rom pr
i
mor
di
a
l
germ ce
ll
st
h
at
b
ecome enc
l
ose
di
n
m
esoderm
.
P
artheno

g
enesis, the development of unfertilized e
gg
s, ma
y
be ameiotic (no meiosis
i
n oocyte nucleus) or meiotic (meiosis is followed by nuclear fusion), both of which result
i
n
di
p
l
o
id
(
f
ema
l
e) o
ff
spr
i
ng, or
h
ap
l
o
id
(me

i
os
i
s
i
s not
f
o
ll
owe
db
y nuc
l
ear
f
us
i
on)
f
ro
m
whi
c
h
ma
l
es ar
i
se
.

P
ol
y
embr
y
on
y
, the formation of more than one embr
y
oinasin
g
le, small,
y
olkless e
gg
,
i
s restricted to a few parasitic or viviparous H
y
menoptera and Strepsiptera.
Vi
viparity occurs in several forms. Ovoviviparity is retention of yolky eggs in the genita
l
tract. In true v
i
v
i
par
i
ty

d
eve
l
op
i
ng o
ff
spr
i
ng rece
i
ve t
h
e
i
r nour
i
s
h
ment
di
rect
l
y
f
rom t
he
m
ot
h

er. In pseu
d
op
l
acenta
l
v
i
v
i
par
i
ty t
h
e
f
o
lli
c
l
ece
ll
san
d
em
b
ryon
i
c mem
b

ranes
b
ecome
cl
ose
ly
appose
d
,an
d
nour
i
s
h
ment appears to
b
e
d
er
i
ve
dl
ar
g
e
ly f
rom t
h
e
d

e
g
enerat
i
on o
f
f
ollicle cells and from trophoc
y
tes. In adenotrophic viviparit
y
,e
gg
s are
y
olk
y
, but larvae ar
e
retained in the uterus and feed on secretions of the accessor
yg
lands. Hemocoelic viviparit
y
i
sw
h
ere em
b
ryos rece
i

ve nutr
i
ents
di
rect
l
y
f
rom t
h
e
h
emo
l
ymp
h.
P
ae
d
ogenes
i
s
i
s precoc
i
ous sexua
l
maturat
i
on o

fj
uven
il
e stages an
di
s norma
ll
y asso-
ci
ate
d
w
i
t
h
part
h
eno
g
enes
i
san
d
v
i
v
i
par
i
t

y
.
6
21
E
MBRY
O
NI
C
DEVEL
O
PMEN
T
W
ithin species-specific limits the rate of embr
y
onic development is inversel
y
relate
d
t
o temperature. Outside these limits, an embr
y
oma
y
survive but not develop; that is, it
is quiescent. Survival of an embr
y
o at extreme temperatures ma
y

be achieved throu
g
h
di
apause. Eggs o
f
many spec
i
es must ta
k
e up water
f
rom t
h
eenv
i
ronment
b
e
f
ore em
b
ryon
i
c
d
eve
l
opment can
b

eg
i
n. Ec
d
ysone an
dj
uven
il
e
h
ormone are
i
nvo
l
ve
di
nt
h
eregu
l
at
i
on o
f
embr
y
o
g
enesis thou
g

h their precise roles remain unknown. In respect of embr
y
onic cuticle
formation the
y
appear to work as the
y
do in postembr
y
onic development
.
At hatchin
g
, hemol
y
mph is forced into the head and thorax as a result of abdomina
l
musc
l
e contract
i
on. As t
h
e anter
i
or en
d
o
f
t

h
eem
b
ryo
i
ncreases
i
nvo
l
ume, t
h
ec
h
or
i
on
i
ssp
li
t. Hatc
hi
ng may
b
e
f
ac
ili
tate
db
y

li
nes o
f
wea
k
ness
i
nt
h
ec
h
or
i
on,
b
yegg
b
ursters
or evers
ibl
e
bl
a
dd
ers on t
h
e
h
ea
d

or t
h
orax, or
by
secret
i
on o
f
p
l
europo
di
a
l
c
hi
t
i
nase t
h
at
d
issolves the serosal cuticle
.
1
2. Lit
e
r
a
t

u
r
e
J
o
h
annsen an
d
Butt
(
1941
)
,An
d
erson
(
1972a,
b
, 1973
)
, Jura
(
1972
)
, Counce
(
1973
)
,
Sander

et al.
(
1985), and Hemin
g
(2003)
g
ive
g
eneral descriptions of insect embr
y
o-
g
enesis. Works dealin
g
with specific aspects of embr
y
onic development include thos
e
b
y Hagan (1951) and Retnakaran and Percy (1985) [viviparous insects], Ivanova-Kasa
s
(1972) and Retnakaran and Percy (198
5
) [polyembryony), White (1973) [parthenogenesis
and sex determination], Matsuda (197
6
) [embryogenesis of abdomen, gonads, and germ
cells], and Hoffmann and La
g
ueux (198

5
) [endocrine aspects]. Lawrence (1976, 1992) and
Sander (1984, 1997) review experimental embr
y
o
g
enesis, especiall
y
in relation to patter
n
formation.
A
n
d
erson, D. T., 1972a, T
h
e
d
eve
l
opment o
fh
em
i
meta
b
o
l
ous
i

nsects,
i
n:
D
eve
l
opmenta
l
Systems: Insect
s
,V
ol. 1
VV
(
S. J. Counce an
d
C. H. Wa
ddi
n
g
ton, e
d
s.), Aca
d
em
i
c Press, New Yor
k.
A
nderson, D. T., 1972b, The development of holometabolous insects, in:

D
evelopmental S
y
stems: Insects
,V
ol. 1
V
V
(
S. J. Counce an
d
C. H. Wa
ddi
ngton, e
d
s.), Aca
d
em
i
c Press, New Yor
k.
A
n
d
erson
,
D. T.
,
1973
,

E
m
b
ryo
l
ogy an
d
P
h
y
l
ogeny in Anne
l
i
d
san
d
Art
h
ropo
d
s
,
P
er
g
amon Press, E
l
ms
f

or
d
,NY
.
Counce, S. J., 1973, The causal analysis of insect embryogenesis, in:
D
evelopmental S
y
stems: Insect
s
,V
ol. 2
V
V
(S. J. Counce an
d
C. H. Wa
ddi
ngton, e
d
s.), Aca
d
em
i
c Press, New Yor
k.
Goo
d
man, C. S., 1984, Lan
d

mar
k
san
dl
a
b
e
l
st
h
at
h
e
l
p
d
eve
l
op
i
n
g
neurons
fi
n
d
t
h
e
i

rwa
y
, Bio
S
cienc
e
34
:
300–307.
Goodman, C. S., and Bastiani, M. J., 1984, How embryonic nerve cells recognize one another
,
S
ci.
A
m
.
25
1(June):58–66
.
H
a
g
an, H. R., 19
5
1,
E
m
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