21
P
ostembr
y
onic Development
1
. Intr
oduc
t
ion
Durin
g
their postembr
y
onic
g
rowth period insects pass throu
g
h a series of sta
g
es (instars)
u
ntil the
y
become adult, the time interval (stadium) occupied b
y
each instar bein
g
terminate
d
by

a molt. Apter
yg
otes continue to
g
row and molt as adults, periods of
g
rowth alternat-
i
ng w
i
t
h
per
i
o
d
so
f
repro
d
uct
i
ve act
i
v
i
ty.Int
h
ese
i

nsects structura
l diff
erences
b
etwee
n
j
uven
il
ean
d
a
d
u
l
t
i
nstars are s
li
g
h
t, an
d
t
h
e
i
r met
h
o

d
o
fd
eve
l
opment
i
st
h
us
d
escr
ib
e
d
a
s
ameta
b
o
l
ous. Amon
g
t
h
e Pter
yg
ota, w
hi
c

h
w
i
t
h
rare except
i
ons
d
o not mo
l
t
i
nt
h
ea
d
u
lt
sta
g
e, two forms of development can be distin
g
uished. In almost all exopter
yg
otes the late
r
j
uvenile instars broadl
y

resemble the adult, except for their lack of win
g
s and incompletel
y
f
orme
d
gen
i
ta
li
a. Suc
hi
nsects,
i
nw
hi
c
h
t
h
ere
i
s some
d
egree o
f
c
h
ange

i
nt
h
emo
l
t
f
rom
j
uven
il
etoa
d
u
l
t, are sa
id
to un
d
ergo part
i
a
l
(
i
ncomp
l
ete) metamorp
h
os

i
s, an
d
t
h
e
i
r
d
e-
ve
l
opment
i
s
d
escr
ib
e
d
as
h
em
i
meta
b
o
l
ous. En
d

opter
yg
otes an
d
a
f
ew exopter
yg
otes
h
ave
larvae whose form and habits, b
y
and lar
g
e, are ver
y
different from those of the adults. As
a result, the
y
under
g
o strikin
g
chan
g
es (complete metamorphosis), spread over two molts
,
i
nt

h
e
f
ormat
i
on o
f
t
h
ea
d
u
l
t(
h
o
l
ometa
b
o
l
ous
d
eve
l
opment). T
h
e
fi
na

lj
uven
il
e
i
nstar
h
a
s
b
ecome spec
i
a
li
ze
d
to
f
ac
ili
tate t
h
ese c
h
anges an
di
s
k
nown as t
h

e pupa (see a
l
so C
h
apter 2,
Sect
i
on 3.3
).
I
n insect evolution increasin
g
functional separation has occurred between the larva
l
phase, which is concerned with
g
rowth and accumulation of reserves, and the adult sta
g
e
,
wh
ose
f
unct
i
ons are repro
d
uct
i
on an

ddi
spersa
l
. Assoc
i
ate
d
w
i
t
h
t
hi
s tren
di
s a ten
d
ency
f
or
an
i
nsect to spen
d
a greater part o
fi
ts
lif
easa
j

uven
il
e, w
hi
c
h
contrasts w
i
t
h
t
h
es
i
tuat
i
o
n
i
n man
y
ot
h
er an
i
ma
l
s. T
h
us,

i
n apter
yg
otes, t
h
ea
d
u
l
t sta
g
ema
yb
e cons
id
era
bly l
on
g
er
t
han the
j
uvenile sta
g
e. Furthermore, feedin
g
(in the adult) serves to provide raw material
s
b

oth for reproduction and for
g
rowth. In exopter
yg
otes and primitive endopter
yg
otes adults
may live for a reasonable period, but this is not usually as long as the larval phase. Feeding
i
nt
h
ea
d
u
l
t stage
i
spr
i
mar
il
y assoc
i
ate
d
w
i
t
h
repro

d
uct
i
ve requ
i
rements, t
h
oug
hi
n som
e
i
nsects
i
t prov
id
es nutr
i
ents
f
or an
i
n
i
t
i
a
l
,s
h

ort “somat
i
c growt
h
p
h
ase”
i
nw
hi
c
h
t
h
e
fli
g
h
t
muscles,
g
ut, and cuticle become full
y
developed. Man
y
endopter
yg
otes live for a relativel
y
short time as adults and ma

y
feed little or not at all because sufficient reserves have been
acquired during larval life to satisfy the needs of reproduction.
62
3
6
24
CHAPTER
21
2
. Growth
2.1. Ph
y
sical As
p
ects
Growt
hi
n
i
nsects an
d
ot
h
er art
h
ropo
d
s
diff

ers
f
rom t
h
at o
f
mamma
l
s
i
nvar
i
ous respects
.
In
i
nsects growt
hi
sa
l
most ent
i
re
l
y restr
i
cte
d
to t
h

e
l
arva
li
nstars, t
h
oug
hi
n some spec
i
e
s
there is a short period of somatic
g
rowth in newl
y
enclosed adults when additional cuticle
m
a
y
be deposited, and
g
rowth of fli
g
ht muscles and the alimentar
y
canal ma
y
occur. As
a

c
onsequence, the length of the juvenile stage is considerably longer than that of the adult. An
e
xtreme examp
l
eo
f
t
hi
s
i
s seen
i
n some may
fl
y spec
i
es w
h
ose aquat
i
c
j
uven
il
e stage may
requ
i
re 2 or 3 years
f

or comp
l
et
i
on, yet g
i
ve r
i
se to an a
d
u
l
tt
h
at
li
ves
f
or on
l
ya
f
ew
h
ours or
da
y
s. Growth in man
y
animals is discontinuous or c

y
clic; that is, periods of active
g
rowth ar
e
separated b
y
periods when littleor no
g
rowth occurs. Nowhereis discontinuous
g
rowth better
seen than in arthropods, which must periodically molt their generally inextensible cuticle in
o
r
d
er to s
i
gn
ifi
cant
l
y
i
ncrease t
h
e
i
rs
i

ze (vo
l
ume). It s
h
ou
ld b
e apprec
i
ate
d
,
h
owever, t
h
at,
t
h
oug
hi
ncreases
i
nvo
l
ume may
b
e
di
scont
i
nuous,

i
ncreases
i
nwe
i
g
h
t are not (F
i
gure 21.1).
A
s an insect feeds durin
g
each stadium, reserves are deposited in the fat bod
y
, whose wei
g
h
t
and volume increase. In a hard-bodied insect this increase in volume ma
y
be compensated
f
or by a decrease in the volume occupied by the tracheal system or by extension of the
a
bd
omen as a resu
l
to
f

t
h
eun
f
o
ldi
ng o
fi
ntersegmenta
l
mem
b
ranes. In many en
d
opterygote
l
arvae, o
f
course, t
h
e ent
i
re
b
o
d
y
i
s
l

arge
l
y covere
d
w
i
t
h
extens
ibl
e cut
i
c
l
e, an
db
o
d
ys
i
ze
i
ncreases almost continuousl
y
(but see below).
Fo
r
m
an
y

insects
g
rown under standard conditions the amount of
g
rowth that occurs is
predictable from one instar to the next; that is, it obeys certain “growth laws.” For example
,
D
yar’s
l
aw,
b
ase
d
on measurements o
f
t
h
ec
h
ange
i
nw
id
t
h
o
f
t
h

e
h
ea
d
capsu
l
ew
hi
c
h
occurs
at eac
h
mo
l
t, states t
h
at growt
hf
o
ll
ows a geometr
i
c progress
i
on; t
h
at
i
s, t

h
e proport
i
onate
i
ncrease in size for a
g
iven structure is constant from one instar to the next. Mathematicall
y
e
x
p
ressed, the law state
s
x
/
y
=
c
onstant (value usuall
y
1.2–1.4), wher
e
x
=
size in a
g
ive
n
i

n
sta
r
a
n
d
y
=
s
ize in previous instar (Fi
g
ure 21.1). Thus, when the size of a structure is
pl
otte
dl
ogar
i
t
h
m
i
ca
ll
y aga
i
nst
i
nstar num
b
er, a stra

i
g
h
t
li
ne
i
so
b
ta
i
ne
d
,w
h
ose gra
di
ent
is
c
onstant
f
orag
i
ven spec
i
es (F
i
gure 21.2). In t
h

ose
i
nsects w
h
ere
i
t app
li
es Dyar’s
l
aw can
b
e use
d
to
d
eterm
i
ne
h
ow man
yi
nstars t
h
ere are
i
nt
h
e
lif

e
hi
stor
y
.However,soman
yf
actors
FIGURE 21.1
.
Ch
an
g
e
i
n
h
ea
d
w
id
t
h
w
i
t
h
t
i
me to
ill

ustrate D
y
ar’s
l
aw
.
6
2
5
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
F
I
GU
RE 21.2
.
Hea
d
w
id
t
h

p
l
otte
dl
o
g
ar
i
t
h
m
i
ca
lly
a
g
ainst instar number in various species. [After V. B
.
W
igglesworth, 1965
,
T
h
e Princip
l
es of Insect P
h
ysio
l
ogy

,
6
th ed., Methuen and Co. B
y
permission of the author.]
a
ff
ect growt
h
rates an
d
t
h
e
f
requency o
f
ec
d
ys
i
st
h
at t
h
e
l
aw
i
s

f
requent
l
y
i
napp
li
ca
bl
e. I
n
an
y
event, the law requires that the interval between molts remains constant, but this i
s
rarel
y
the case
.
As winged insects grow, they change shape; that is, the relative proportions of differen
t
parts o
f
t
h
e
b
o
d
yc

h
ange. T
hi
s
di
sproport
i
onate growt
h
,w
hi
c
hi
s not un
i
que to
i
nsects,
i
s
d
escr
ib
e
d
as “a
ll
ometr
i
c” (

h
eterogon
i
c,
di
s
h
armon
i
c). In ot
h
er wor
d
s, eac
h
part
h
as
i
ts own
g
rowth rate, expressed b
y
the equation
y
=
bx
k
(
y

=
l
inear size of the part,
x
=
linea
r
size of the standard (e.
g
., bod
y
len
g
th),
b
=
i
nitial
g
rowth index (
y
interce
p
t), and
k
=
allometric coefficient). Normally, allometric growth is expressed as a log-log plot, whe
n
k
i

st
h
e gra
di
ent o
f
t
h
es
l
ope (F
i
gure 21.3).
G
rowt
hl
aws
d
o not app
l
y
i
ns
i
tuat
i
ons w
h
ere t
h

e num
b
er o
fi
nstars
i
svar
i
a
bl
e. T
hi
s
variabilit
y
ma
y
be a natural occurrence, especiall
y
in primitive insects such as ma
y
flie
s
t
hat have man
y
instars. In addition, females that are t
y
picall
y

lar
g
er than males ma
y
have
a
g
reater number of instars than males. Variabilit
y
ma
y
also be induced b
y
environmenta
l
c
on
di
t
i
ons. For examp
l
e, rear
i
ng
i
nsects at a
b
norma
ll

y
hi
g
h
temperature o
f
ten
i
ncreases t
h
e
n
um
b
er o
fi
nstars, as
d
oes sem
i
starvat
i
on. In contrast,
i
n some caterp
ill
ars crow
di
ng
l

ea
d
s
t
oa
d
ecrease
i
nt
h
e num
b
er o
f
mo
l
ts
.
C
aterpillars and probabl
y
other larvae whose c
y
lindrical bod
y
is covered with a thin
i
nte
g
ument rel

y
on h
y
drostatic (hemol
y
mph) pressure to maintain the ri
g
idit
y
necessar
y
f
or
l
ocomot
i
on. However, t
hi
s presents a pro
bl
em w
i
t
h
respect to t
h
e
i
r
b

o
d
y
f
orm
d
ur
i
n
g
growt
h
. Mec
h
an
i
ca
ll
y,
i
nacy
li
n
d
er un
d
er
i
nterna
l

pressure t
h
e
h
oop stress (aroun
d
t
h
e
b
o
dy
)
i
stw
i
ce t
h
eax
i
a
l
(
l
en
g
t
h
w
i

se) stress. T
h
us, a caterp
ill
ar t
h
eoret
i
ca
lly
s
h
ou
ld b
ecome
proportionatel
y
fatter as it
g
rows, much like a balloon when inflated. That it does not d
o
6
2
6
CHAPTER
21
FIGURE 21.3
.
A
ll

ometr
i
c growt
hin
Carausius
(Phasmida). [After V. B. Wi
gg
lesworth, 196
5,
T
h
e
P
rinciples o
f
Insect Physiology, 6th ed., Methuen
a
n
d
Co. By perm
i
ss
i
on o
f
t
h
e aut
h
or.

]
so is due to the occurrence of axial
p
leats (transverse cuticular folds) that reduce the axial
stress
b
yun
f
o
ldi
ng as t
h
e
i
nsect en
l
arges (Carter an
d
Loc
k
e, 1993).
2.2. B
i
ochem
i
cal
C
han
g
es dur

i
n
gG
rowt
h
L
ike the physical changes noted above, biochemical changes that occur during postem
-
b
ryon
i
c
d
eve
l
opment may a
l
so
b
e
d
escr
ib
e
d
as a
ll
ometr
i
c. T

h
at
i
s, t
h
ere
l
at
i
ve proport
i
ons
of
t
h
evar
i
ous
bi
oc
h
em
i
ca
l
components c
h
ange as growt
h
ta

k
es p
l
ace. T
h
ese c
h
anges ar
e
e
speciall
y
noticeable in endopter
yg
otes durin
g
the final larval and pupal sta
g
es. At hatchin
g
,
the fat content of a larva is t
y
picall
y
low (less than 1% in the caterpilla
r
M
alacosoma,fo
r

e
xample) and remains at about this level until the final larval stadium when fat is s
y
nthesize
d
an
d
store
di
n
l
arge quant
i
ty, reac
hi
ng a
b
out 30% o
f
t
h
e
d
ry
b
o
d
ywe
i
g

h
t. T
h
oug
hf
at
i
st
h
e
typ
i
ca
l
reserve su
b
stance
i
n most
i
nsects, mem
b
ers o
f
some spec
i
es store g
l
ycogen. Aga
i

n
,
t
hi
s usua
lly
occurs
i
n sma
ll
amounts
i
nnew
ly h
atc
h
e
di
nsects,
b
ut
i
ts proport
i
on
i
ncrease
s
steadil
y

throu
g
h larval development, and at pupation
g
l
y
co
g
en ma
y
beasi
g
nificant com
-
ponent of the dr
y
wei
g
ht (one-third in the hone
y
bee). Like fat,
g
l
y
co
g
en is stored in the fa
t
b
o

d
y.
In contrast, t
h
e proport
i
ons o
f
water, prote
i
n, an
d
nuc
l
e
i
cac
id
s genera
ll
y
d
ec
li
ne
d
ur
i
ng
l

arva
ld
eve
l
opment. However, t
hi
s
i
so
f
ten not t
h
es
i
tuat
i
on
i
n
l
arvae t
h
at requ
i
re
l
ar
ge
amounts of protein for specific purposes, for example, spinnin
g

a cocoon. In
B
omybyx
m
o
r
i
,
for example, the hemol
y
mph protein concentration increases sixfold in late larva
l
develo
p
ment, and about 50% of the total
p
rotein content of a mature larva is used in
c
ocoon
f
ormat
i
on. T
h
e great
i
ncrease
i
n concentrat
i

on o
fh
emo
l
ymp
h
prote
i
no
f
ten can
b
e
accounte
df
or a
l
most ent
i
re
l
y
b
y synt
h
es
i
s,
i
nt

h
e
f
at
b
o
d
y, o
f
a
f
ew spec
ifi
c prote
i
ns. In t
h
e
fl
y
Calliphora stygi
a
,
for example, the protein “calliphorin” makes up 7
5
% (about 7 m
g
)o
f
6

2
7
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
t
he hemol
y
mph protein b
y
the time a mature larva stops feedin
g
. The calliphorin is used in
t
he pupa as a ma
j
or source of nitro
g
en (in the form of amino acids) for formation of adul
t
t
issues and as a source of the ener
gy

required in bios
y
nthesis. Thus, at eclosion (emer
g
ence
o
f
t
h
ea
d
u
l
t), t
h
e
h
emo
l
ymp
h
ca
lli
p
h
or
i
n content
h
as

f
a
ll
en to 0.03 mg, an
d
, 1 wee
k
a
f
te
r
emergence, t
h
e prote
i
n
h
as ent
i
re
l
y
di
sappeare
d
.
Durin
g
metamorphosis some of the above trends ma
y

be reversed. The proportions of fat
and/or
g
l
y
co
g
en decline as these molecules are utilized in ener
gy
production. I
n
C
alli
p
hora
t
he fat content decreases from 7% to 3% of the dr
y
wei
g
ht throu
g
h the pupal period. In th
e
h
oney
b
ee, w
hi
c

h
ma
i
n
l
y uses g
l
ycogen as an energy source, t
h
eg
l
ycogen content
d
rops
t
o
l
ess t
h
an 10% o
fi
ts
i
n
i
t
i
a
l
va

l
ue as metamorp
h
os
i
s procee
d
s. For most
i
nsects t
h
ere
i
s
li
tt
l
ec
h
an
g
e
i
nt
h
e net prote
i
n content
d
ur

i
n
g
pupat
i
on, t
h
ou
gh
ma
j
or qua
li
tat
i
ve c
h
an
g
es
occur as adult tissues develop. In members of a few species a si
g
nificant decline in total
protein content occurs durin
g
metamorphosis as protein is used as an ener
gy
source. Th
e
m

oth
C
e
l
erio,
f
or examp
l
e, o
b
ta
i
ns on
l
y 20% o
fi
ts energy requ
i
rements
i
n metamorp
h
os
is
f
rom
f
at, t
h
e rema

i
n
i
ng 80% com
i
ng
l
arge
l
y
f
rom prote
i
n
.
S
uper
i
mpose
d
on t
h
e overa
ll bi
oc
h
em
i
ca
l

c
h
an
g
es
f
rom
h
atc
hi
n
g
to a
d
u
l
t
h
oo
d
are
chan
g
es that occur in each stadium, related to the c
y
clic nature of
g
rowth and moltin
g
.Fac

-
t
ors to be considered include the phasic pattern of feedin
g
activit
y
throu
g
hout the stadium
,
synt
h
es
i
so
f
new an
dd
egra
d
at
i
on o
f
o
ld
cut
i
c
l

e, an
d
net pro
d
uct
i
on o
f
new t
i
ssues (t
h
oug
h
some
hi
sto
l
ys
i
sa
l
so occurs
i
n eac
hi
nstar).
Measurement o
f
ox

yg
en consumpt
i
on s
h
ows t
h
at
i
t
f
o
ll
ows a U-s
h
ape
d
curve t
h
rou
gh
each stadium with maximum values bein
g
obtained at the time of moltin
g
. The maxima ar
e
correlated with the
g
reat increase in metabolic activit

y
at this time, associated especiall
y
wi
t
h
t
h
e synt
h
es
i
so
f
new cut
i
c
l
ean
df
ormat
i
on o
f
new t
i
ssues. I
n
L
ocusta

l
ar
v
ae t
h
ere are
s
i
gn
ifi
cant
d
ecreases
i
nt
h
e car
b
o
h
y
d
rate an
dli
p
id
contents o
f
t
h

e
f
at
b
o
d
yan
dh
emo
l
ymp
h
at ec
d
ys
i
s, pro
b
a
bl
y corre
l
ate
d
w
i
t
h
t
h

e use o
f
t
h
ese su
b
strates to supp
l
y energy (H
ill
an
d
G
oldsworth
y
,19
6
8). Conversel
y
, as feedin
g
restarts after a molt, these materials are a
g
ai
n
accumulated
.
C
hanges in the amount of protein in the fat body and hemolymph of
L

ocust
a
are
a
l
so cyc
li
ca
l
,w
i
t
h
max
i
mum va
l
ues occurr
i
ng
i
nt
h
e secon
dh
a
lf
o
f
eac

h
sta
di
um (H
ill
and Goldsworthy, 19
6
8). The early increase in protein content is related to renewed feedin
g
activit
y
after the molt. Feedin
g
activit
y
reaches a peak in the middle of the stadium, providin
g
materials for
g
rowth of muscles (and presumabl
y
other tissues, thou
g
h these were not studie
d
by
Hill and Goldsworth
y
) and for the s
y

nthesis of cuticle. Excess material is stored in th
e
fat
b
o
d
yan
dh
emo
l
ymp
h
.Int
h
e secon
dh
a
lf
o
f
t
h
e sta
di
um
f
ee
di
ng act
i

v
i
ty
d
ec
li
nes, an
d
thi
s
i
s
f
o
ll
owe
db
ya
d
ecrease
i
nt
h
e
l
eve
l
o
f
prote

i
n
i
nt
h
e
h
emo
l
ymp
h
an
df
at
b
o
d
y. H
ill
and Goldsworth
y
(19
6
8) su
gg
ested that the latter probabl
y
reflects the use of protein in th
e
s

y
nthesis of new cuticle. However, rec
y
cled protein from the old cuticle ma
y
account fo
r
most (about 80% in
L
ocusta
)
o
f the
p
rotein content of the new cuticle
.
3
. Forms o
f
Develo
p
men
t
Throu
g
h insect evolution there has been a trend toward increasin
g
functional and struc-
t
ura

ldi
vergence
b
etween
j
uven
il
ean
d
a
d
u
l
t stages. Juven
il
e
i
nsects
h
ave
b
ecome mor
e
concerne
d
w
i
t
hf
ee

di
ng an
d
growt
h
,w
h
ereas a
d
u
l
ts
f
orm t
h
e repro
d
uct
i
ve an
ddi
spersa
l
phase. This specialization of different sta
g
es in the life histor
y
became possible with the
introduction into the life histor
y

of a pupal instar, thou
g
h the latter’s ori
g
inal function was
6
2
8
CHAPTER
21
probabl
y
related specificall
y
to eva
g
ination of the win
g
s and development of the win
g
m
usculature (Cha
p
ter 2, Section 3.3).
In modern insects three basic forms of postembr
y
onic development can be reco
g
nized
,

d
escr
ib
e
d
as ameta
b
o
l
ous,
h
em
i
meta
b
o
l
ous, an
dh
o
l
ometa
b
o
l
ous, accor
di
ng to t
h
e extent

of
metamorp
h
os
i
s
f
rom
j
uven
il
etoa
d
u
l
t(F
i
gure 21.4).
3
.1. Ametabolous Develo
p
ment
In T
h
ysanura (an
d
ot
h
er pr
i

m
i
t
i
ve
h
exapo
d
s), w
hi
c
h
as a
d
u
l
ts rema
i
nw
i
ng
l
ess, t
he
d
egree o
f
c
h
ange

f
rom
j
uven
il
etoa
d
u
l
t
f
orm
i
ss
li
g
h
tan
di
s man
if
est pr
i
mar
il
y
i
n
i
ncrease

d
b
o
dy
s
i
ze an
dd
eve
l
opment o
ff
unct
i
ona
lg
en
i
ta
li
a. Juven
il
ean
d
a
d
u
l
t apter
yg

otes
i
n
h
a
bi
t
the same ecolo
g
ical niche, and the insects continue to
g
row and molt after reachin
g
sexua
l
m
aturit
y
. The number of molts throu
g
h which an insect passes is ver
y
hi
g
h and variable.
F
o
r
e
xam

p
le, in the firebrat, Thermobia domestica
,
bet
w
een 4
5
and
60
molts ha
v
e been
recor
d
e
d.
3
.2. Hem
i
metabolous Developmen
t
E
xopterygotes usually molt a fixed number of times, but, with the exception of
Ep
h
emeroptera, w
hi
c
h
pass t

h
roug
h
aw
i
nge
d
su
bi
mago stage, never as a
d
u
l
ts. In spec
i
es
wh
ere t
h
e
f
ema
l
e
i
s muc
hl
arger t
h
an t

h
ema
l
e, s
h
e may un
d
ergo an a
ddi
t
i
ona
ll
arva
l
mo
l
t
.
The number of molts is t
y
picall
y
4or
5
, thou
g
h in some Odonata and Ephemeroptera whose
l
arval life ma

y
last2or3
y
ears a much
g
reater and more variable number of molts occur
s
(
e.
g
., 10–15 in species of Odonata, 15–30 in most Ephemeroptera).
In a
l
most a
ll
exopterygotes t
h
e
l
ater
j
uven
il
e
i
nstars
b
roa
dl
y resem

bl
et
h
ea
d
u
l
t, excep
t
t
h
at t
h
e
i
rw
i
ngs an
d
externa
l
gen
i
ta
li
a are not
f
u
ll
y

d
eve
l
ope
d
. Ear
l
y
i
nstars s
h
ow no trace o
f
wi
n
g
s,
b
ut,
l
ater, externa
l
w
i
n
gb
u
d
sar
i

se as sc
l
erot
i
ze
d
, non-art
i
cu
l
ate
d
eva
gi
nat
i
ons o
f
t
h
e
ter
g
opleural area of the win
g
-bearin
g
se
g
ments. Win

g
s develop within the buds durin
g
the
final larval stadium and are expanded after the last molt. Other, less obvious, chan
g
es that
o
ccur
d
ur
i
ng t
h
e growt
h
o
f
exopterygotes
i
nc
l
u
d
et
h
ea
ddi
t
i

on o
f
neurons, Ma
l
p
i
g
hi
an
tu
b
u
l
es, ommat
idi
a, an
d
tarsa
l
segments, p
l
us t
h
e
diff
erent
i
at
i
on o

f
a
ddi
t
i
ona
l
sens
ill
a
i
n
t
h
e
i
ntegument. T
hi
smo
d
eo
fd
eve
l
opment
i
s
d
escr
ib

e
d
as
h
em
i
meta
b
o
l
ous an
di
nc
l
u
d
es a
partial (incomplete) metamorphosis from larva to adult
.
3
.
3
. Holometabolous Develo
p
men
t
Ho
l
ometa
b

o
l
ous
d
eve
l
opment,
i
nw
hi
c
h
t
h
ere
i
s a mar
k
e
d
c
h
ange o
ff
orm
f
rom
l
arv
a

to adult (complete metamorphosis), occurs in endopter
yg
otes and a few exopter
yg
otes, fo
r
e
xample, whiteflies (Aleurodidae: Hemiptera), thrips (Th
y
sanoptera), and male scale insect
s
(
Coccidae: Hemi
p
tera). Perha
p
s the most obvious structural difference between the larval
an
d
a
d
u
l
t stages o
f
en
d
opterygotes
i
st

h
ea
b
sence o
f
any externa
l
s
i
gn o
f
w
i
ng
d
eve
l
opment
i
nt
h
e
l
arva
l
stages. T
h
ew
i
ng ru

di
ments
d
eve
l
op
i
nterna
ll
y
f
rom
i
mag
i
na
ldi
scs t
h
at
i
n most
l
arvae lie at the base of the peripodial cavit
y
,aninva
g
ination of the epidermis beneath th
e
l

arval cuticle, and are eva
g
inated at the larval-pupal molt (see Section 4.2 and Fi
g
ure 21.11)
.
As noted above, the evolution of a pupal sta
g
e in the life histor
y
has mad
e
h
o
l
ometa
b
o
l
ous
d
eve
l
opment poss
ibl
e. T
h
e pupa
i
s pro

b
a
bl
ya
hi
g
hl
ymo
difi
e
dfi
na
lj
u
-
v
en
il
e
i
nstar (C
h
apter 2, Sect
i
on 3.3) w
hi
c
h
,t
h

roug
h
evo
l
ut
i
on,
b
ecame
l
ess concerne
d
wi
t
hf
ee
di
n
g
an
db
u
ildi
n
g
up reserves (t
hi
s
f
unct

i
on
b
e
i
n
gl
e
f
ttoear
li
er
i
nstars) an
d
mor
e
6
2
9
P
OS
TEMBRY
O
NI
C
DEVELOPMEN
T
FI
G

URE 21.4.
Bas
i
ct
y
pes o
fd
eve
l
opment
i
n
i
nsects. Bro
k
en arrow
i
n
di
cates severa
l
mo
l
ts.
630
CHAPTER
21
specialized for the breakdown of larval structures and construction of adult features. I
n
o

ther words, the pupa has become a non-feedin
g
sta
g
e; it is
g
enerall
y
immobile as a result
o
f histol
y
sis of larval muscles; it broadl
y
resembles the adult and thereb
y
serves as a mold
f
or t
h
e
f
ormat
i
on o
f
a
d
u
l

tt
i
ssues, espec
i
a
ll
y musc
l
es
.
3
.3.1. The Larval Stage
Amon
g
en
d
opter
yg
otes t
h
e extent to w
hi
c
h
t
h
e
l
arva
l

an
d
a
d
u
l
t
h
a
bi
ts an
d
structur
e
differ [and therefore the extent of metamorphosis (Section 4.2)] is varied. Broadl
y
speakin
g
,
i
n members of more
p
rimitive orders the extent of these differences is small, whereas the
o
pposite is true, for example, in the Hymenoptera and Diptera. Endopterygote larvae can
be arranged in a number of basic types (Figure 21.
5
). The most primitive larval form is
t
h

eo
li
gopo
d
. Larvae o
f
t
hi
s type
h
ave t
h
ree pa
i
rs o
f
t
h
orac
i
c
l
egs an
d
awe
ll
-
d
eve
l

ope
d
head with chewin
g
mouthparts and simple e
y
es. Oli
g
opod larvae can be further subdivide
d
i
nto (1) scarabaeiform larvae (Fi
g
ure 21.5A), which are round-bodied and have short le
gs
and a weakly sclerotized thorax and abdomen, features associated with the habit of bur-
rowing into the substrate, and (2) campodeiform larvae (Figure 21.
5
B), which are active,
pre
d
aceous sur
f
ace-
d
we
ll
ers w
i
t

h
a
d
orsoventra
ll
y
fl
attene
db
o
d
y,
l
ong
l
egs, strong
l
ysc
l
e
-
rotized thorax and abdomen, and pro
g
nathous mouthparts. Scarabaeiform larvae are t
y
pical
F
I
GU
RE 21.5

.
Larval t
y
pes. (A) Scarabaeiform (
P
opillia
j
aponica
,
Coleo
p
tera); (B) cam
p
odeiform
(
Hipp
o
-
damia conver
g
ens
,
Coleoptera); (C) eruciform (Danaus
p
lexi
pp
u
s
, Lepidoptera); (D) eucephalous (B
ibio

s
p.,
D
i
ptera); (E)
h
em
i
cep
h
a
l
ous (Tanyptera fronta
l
is
,
D
i
ptera); an
d
(F) acep
h
a
l
ous (Musca
d
omestica
,
D
i

ptera).
[A–E, from A. Peterson, 19
5
1
,
L
arvae o
f
Insects
.
B
y
permission of Mrs. Helen Peterson. F, from V. B.
Wigglesworth, 1959, Metamorphosis, polymorphism, differentiation
,
Scienti
fi
c American, February 1959. By
p
erm
i
ss
i
on o
f
Mr. Er
i
c Mose, Jr.
]
63

1
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
of the Scarabaeidae and other beetle families; campodeiform larvae occur in Neuroptera
,
Coleoptera-Adepha
g
a, and Trichoptera
.
Pol
y
pod (eruciform) larvae (Fi
g
ure 21.5C) have, in addition to thoracic le
g
s, a varie
d
num
b
er o
f
a

bd
om
i
na
l
pro
l
egs. T
h
e
l
arvae are genera
ll
yp
h
ytop
h
agous an
d
re
l
at
i
ve
l
y
i
nact
i
ve

,
rema
i
n
i
ng c
l
ose to or on t
h
e
i
r
f
oo
d
source. T
h
et
h
orax an
d
a
bd
omen are wea
kl
ysc
l
erot
i
ze

din
compar
i
son w
i
t
h
t
h
e
h
ea
d
,w
hi
c
hh
as we
ll
-
d
eve
l
ope
d
c
h
ew
i
n

g
mout
h
parts. Eruc
if
orm
l
arvae
are t
y
pical of Lepidoptera, Mecoptera, and some H
y
menoptera [sawflies (Tenthredinidae)].
Apodous larvae, which lack all trunk appenda
g
es, occur in various forms in man
y
en
d
opterygote or
d
ers
b
ut
i
n common are a
d
apte
df
or m

i
n
i
ng
i
nso
il
,mu
d
,oran
i
ma
l
o
r
p
l
ant t
i
ssues. T
h
evar
i
a
bili
ty o
ff
orm concerns t
h
e extent to w

hi
c
h
a
di
st
i
nct
h
ea
d
capsu
le
is developed. In eucephalous larvae (Figure 21.
5
D), characteristic of some Coleoptera
(Buprestidae and Ceramb
y
cidae), Strepsiptera, Siphonaptera, aculeate H
y
menoptera, and
more
p
rimitive Di
p
tera (suborder Nematocera), the head is well sclerotized and bears normal
appendages. The head and its appendages of hemicephalous larvae (Figure 21.5E) are
re
d
uce

d
an
d
part
i
a
ll
y retracte
di
nto t
h
et
h
orax. T
hi
s con
di
t
i
on
i
s seen
i
n crane
fl
y
l
arva
e
(T

i
pu
lid
ae: Nematocera) an
di
nt
h
e
l
arvae o
f
ort
h
orrap
h
ous D
i
ptera. Larvae o
f
D
i
ptera-
M
uscomorpha are acephalous (Fi
g
ure 21.
5
F); no si
g
n of the head and its appenda

g
es ca
n
b
e seen a
p
art from a
p
air of minute
p
a
p
illae (remnants of the antennae) and a
p
air of
sclerotized hooks belie
v
ed to be much modified maxillae.
Frequent
l
ya
l
arva
i
nt
h
e
fi
na
li

nstar ceases to
f
ee
d
an
db
ecomes
i
nact
i
ve a
f
ew
d
ay
s
b
e
f
ore t
h
e
l
arva
l
-pupa
l
mo
l
t. Suc

h
a stage
i
s
k
nown as a prepupa. In some spec
i
es, t
h
e
entire instar is a non-feedin
g
sta
g
e in which important chan
g
es related to pupation occur.
Fo
re
x
ample, in the prepupal instar of sawflies, the salivar
yg
lands become modified fo
r
secretin
g
the silk used in cocoon formation
.
3.3.2. Heteromorphos
i

s
I
n most endopter
yg
otes the larval instars are more or less alike. However, in some
species of Neuroptera, Coleoptera, Diptera, Hymenoptera, and in all Strepsiptera, a larv
a
u
n
d
ergoes c
h
aracter
i
st
i
cc
h
anges
i
n
h
a
bi
tan
d
morp
h
o
l

ogy as
i
t grows, a p
h
enomeno
n
k
nown as
h
eteromorp
h
os
i
s(
h
ypermetamorp
h
os
i
s). In suc
h
spec
i
es severa
l
o
f
t
h
e

l
arva
l
ty
pes described above ma
y
develop successivel
y
(Fi
g
ure 21.
6
). For example, blister beetles
(Meloidae) hatch as free-livin
g
campodeiform larvae (planidia, triun
g
ulins) that activel
y
search for food (grasshopper eggs and immature stages, or food reserves of bees or ants).
At t
hi
s stage t
h
e
l
arvae can surv
i
ve
f

or per
i
o
d
so
f
severa
l
wee
k
sw
i
t
h
out
f
oo
d
. Larvae t
h
at
l
ocate
f
oo
d
soon mo
l
ttot
h

e secon
d
stage, a caterp
ill
ar
lik
e (eruc
if
orm)
l
arva. T
h
e
i
nsect
th
en passes t
h
rou
gh
two or more a
ddi
t
i
ona
ll
arva
li
nstars, w
hi

c
h
ma
y
rema
i
n eruc
if
orm or
b
ecome scarabaeiform. Some s
p
ecies overwinter in a modified larval form known as the
p
seudo
p
u
p
a or coarctate larva, so-called because the larva remains within the cuticle of
th
e prev
i
ous
i
nstar. T
h
e pseu
d
opupa
l

stage
i
s
f
o
ll
owe
d
t
h
enextspr
i
ng
b
ya
f
urt
h
er
l
arva
l
f
ee
di
ng stage, w
hi
c
h
t

h
en mo
l
ts
i
nto a pupa.
3.3.3. The Pupal Sta
ge
T
h
e pupa
i
s a non-
f
ee
di
ng, genera
ll
yqu
i
escent
i
nstar t
h
at serves as a mo
ld i
nw
hi
c
h

a
d
u
l
t
f
eatures can
b
e
f
orme
d
. For many spec
i
es
i
t
i
sa
l
so t
h
e stage
i
nw
hi
c
h
an
i

nsect surv
i
ves
a
d
verse con
di
t
i
ons
by
means o
fdi
apause (C
h
apter 22, Sect
i
on 3.2.3). T
h
e terms “pupa”
and “pupal sta
g
e” are commonl
y
used to describe the entire preima
g
inal instar. This is,
632
CHAPTER
21

F
I
GU
RE 21.6. Heteromorphosis i
n
E
pi
caut
a
(
Coleoptera). (A) Triungulin; (B) caraboid second instar; (C) final
f
orm of second instar; (D) coarctate larva; (E) pupa; and (F) adult. [From J. W. Folsom, 190
6,
E
ntomo
l
ogy: Wit
h
S
pecia
l
Reference to Its Bio
l
ogica
l
an
d
Economic Aspect
s

,B
l
a
ki
ston.]
str
i
ct
l
y spea
ki
ng,
i
ncorrect
b
ecause
f
oravar
i
e
d
per
i
o
d
pr
i
or to ec
l
os

i
on, t
h
e
i
nsect
i
s
a
“
p
h
arate a
d
u
l
t,” t
h
at
i
s, an a
d
u
l
t enc
l
ose
d
w
i

t
hi
nt
h
e pupa
l
cut
i
c
l
e. T
h
e
i
nsect t
h
us
b
ecome
s
an a
d
u
l
t
i
mme
di
ate
ly

a
f
ter apo
ly
s
i
so
f
t
h
e pupa
l
cut
i
c
l
ean
df
ormat
i
on o
f
t
h
ea
d
u
l
tep
i

cut
i
c
l
e
(
Chapter 11, Section 3.1). The distinction between the true pupal sta
g
e and the pharate adult
c
ondition becomes important in consideration of so-called “pupal movements,” includin
g
l
ocomot
i
on an
d
man
dib
u
l
ar c
h
ew
i
ng movements (use
di
n escap
i
ng

f
rom t
h
e protect
i
ve
c
ocoon or ce
ll i
nw
hi
c
h
metamorp
h
os
i
s too
k
p
l
ace). In most
i
nstances t
h
ese movements
resu
l
t
f

rom t
h
e act
i
v
i
t
y
o
f
musc
l
es attac
h
e
d
to t
h
ea
d
u
l
t apo
d
emes t
h
at
fi
t snu
gly

aroun
d
t
h
e
remains of the pupal apodemes (Fi
g
ure 21.7).
FI
GU
RE 21.7.
S
ection throu
g
h mandible of a decticous
p
upa to show adult apodemes around remains of pupa
l
ap
odemes. [After H. E. Hinton, 194
6
, A new classificatio
n
of insect
p
u
p
ae, Proc. Zool.
S
oc. Lond.

1
1
6
:
282–328. B
y
p
ermission of the Zoological Society of London.]
633
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
F
I
GU
RE 21.8
.
Pupal types. (A) Decticous
(
C
hr
y
sop

a
s
p., Neuroptera); (B) exarate adecticous (Brach
y
rhinu
s
s
u
l
catus
,
Co
l
eoptera); an
d
(C) o
b
tect a
d
ect
i
cous
(
He
l
iot
h
is armigera
,
Lepidoptera). [From A. Peterson, 19

5
1,
Larvae o
f
Insects
.
B
y
permission of Mrs. Helen Peterson.
]
Pupae are cate
g
or
i
ze
d
accor
di
n
g
to w
h
et
h
er or not t
h
e man
dibl
es are
f

unct
i
ona
l
an
d
w
hether or not the remainin
g
appenda
g
es are sealed closel
y
a
g
ainst the bod
y
(Fi
g
ur
e
2
1.8). Decticous pupae, found in more primitive endopter
yg
otes [Neuroptera, Mecoptera,
T
richoptera, and Lepidoptera (Zeugloptera and Dacnonypha)], have well-developed, artic-
ul
ate
d

man
dibl
es (move
db
yt
h
ep
h
arate a
d
u
l
t’s musc
l
es) w
i
t
h
w
hi
c
h
an
i
nsect can cut
i
ts
w
ay out o
f

t
h
e cocoon or ce
ll
. Dect
i
cous pupae are a
l
ways exarate; t
h
at
i
s, t
h
e appen
d
ages
are not sealed a
g
ainst the bod
y
so that the
y
ma
y
be used in locomotion. Some neuroptera
n
p
u
p

ae, for exam
p
le, can crawl and some
p
u
p
ae of Tricho
p
tera swim to the water surface
p
rior to eclosion. Adecticous
p
u
p
ae, whose mandibles are non-functional and often re-
d
uce
d
, may
b
ee
i
t
h
er exarate or o
b
tect. In t
h
e
l

atter con
di
t
i
on t
h
e appen
d
ages are
fi
rm
l
y
sea
l
e
d
aga
i
nst t
h
e
b
o
d
yan
d
are usua
ll
ywe

ll
sc
l
erot
i
ze
d
.A
d
ect
i
cous exarate pupae are c
h
ar
-
acteristic of Siphonaptera, brach
y
cerous Diptera, most Coleoptera and H
y
menoptera, an
d
Stre
p
si
p
tera. In nematocerous Di
p
tera, Le
p
ido

p
tera (Heteroneura), and in a few Coleo
p
ter
a
and Hymenoptera, pupae are of the adecticous obtect type
.
I
n muscomorp
h
D
i
ptera at t
h
een
d
o
f
t
h
e
fi
na
ll
arva
l
sta
di
um t
h

e cut
i
c
l
e
b
ecome
s
thi
c
k
ene
d
an
d
tanne
d
.T
h
e tanne
d
cut
i
c
l
e
i
s not s
h
e

db
ut rema
i
ns as a r
i
g
id
coat (pupar
i
um)
around the insect. A few hours after pupariation the larval epidermis apol
y
ses so that
a
pharate pupal instar is formed within the puparium, servin
g
as in other endopter
yg
otes as
t
he mold for adult tissues
.
An
i
mmo
bil
e pupa
i
svu
l

nera
bl
e to attac
kb
y pre
d
ators or paras
i
tes an
d
to severe c
h
ange
s
i
nc
li
mat
i
c con
di
t
i
ons, part
i
cu
l
ar
l
yast

h
e pupa
l
sta
di
um may
l
ast
f
or a cons
id
era
bl
et
i
me.
T
o
ob
ta
i
n protect
i
on a
g
a
i
nst suc
h
a

d
vers
i
t
i
es t
h
e pupa t
y
p
i
ca
lly h
asat
hi
c
k
, tanne
d
cut
i
c
l
e
.
Also, in man
y
species it is enclosed within a cocoon or subterranean cell constructed b
y
th

e
previous larval instar. The cocoon ma
y
comprise various kinds of extraneous material, for
examp
l
e, so
il
part
i
c
l
es, sma
ll
stones,
l
eavesorot
h
er vegetat
i
on, or may
b
ema
d
eso
l
e
l
yo
f

s
ilk
. In some en
d
opterygotes t
h
e pupa
i
s expose
d
(not surroun
d
e
db
y a protect
i
ve cocoon)
b
u
t
o
b
ta
i
ns a
ddi
t
i
ona
l

protect
i
on
by
ta
ki
n
g
on t
h
eco
l
or o
fi
ts surroun
di
n
g
s. Man
y
paras
i
t
i
c
species remain within, and are thus protected b
y
, the host’s bod
y
in the pupal sta

g
e
.
63
4
CHAPTER
21
4
. Histolo
g
ical Chan
g
es Durin
g
Metamorphosi
s
Th
ou
gh
we
h
ave
di
st
i
n
g
u
i
s

h
e
d
,
i
nt
h
e prece
di
n
g
account,
b
etween
h
em
i
meta
b
o
l
ous
development (where partial metamorphosis occurs in the molt from larva to adult) an
d
holometabolous development (in which metamorphosis is strikin
g
and requires two molts,
l
arva
l

-pupa
l
an
d
pupa
l
-
i
mag
i
na
l
,
f
or comp
l
et
i
on), t
h
e
di
st
i
nct
i
on
i
spr
i

mar
il
y use
f
u
li
n
di
scuss
i
ons o
fi
nsect evo
l
ut
i
on. In a p
h
ys
i
o
l
og
i
ca
l
sense t
h
e
diff

erence
b
etween part
i
a
l
an
d
c
omp
l
ete metamorp
h
os
i
s
i
s a matter o
fd
egree rat
h
er t
h
an
ki
n
d
.In
d
ee

d
,as
i
s
d
escr
ib
e
d
i
n Section
6
.1, the endocrine basis of
g
rowth, includin
g
moltin
g
and chan
g
e of form, i
s
c
ommon to all insects
.
4
.1. Exopterygote Metamorphosis
In most exopterygotes t
h
e

l
arva
l
an
d
a
d
u
l
t
f
orms o
f
a spec
i
es occupy t
h
e same
h
a
bi
tat,
e
at the same kinds of food (thou
g
h specific preferences ma
y
chan
g
e with a

g
e), and ar
e
sub
j
ect to the same environmental conditions. Accordin
g
l
y
, most or
g
an s
y
stems of a
j
uvenil
e
e
xopterygote are smaller and/or less well-developed versions of those found in an adult and
s
i
mp
l
y grow progress
i
ve
l
y
d
ur

i
ng
l
arva
l lif
e to accommo
d
ate c
h
ang
i
ng nee
d
s. Even
l
arva
l
Od
onata an
d
Ep
h
emeroptera t
h
at are aquat
i
can
d
possess trans
i

ent a
d
apt
i
ve
f
eatures suc
h
as
g
ills or caudal lamellae broadl
y
resemble the adult sta
g
e. The s
y
stem that under
g
oes th
e
m
ost obvious chan
g
e at the final molt is the fli
g
ht mechanism. In the last larval instar win
gs
develop within the win
g
buds as much folded sheets of inte

g
ument, and, concurrentl
y
, the
art
i
cu
l
at
i
ng sc
l
er
i
tes
diff
erent
i
ate. D
i
rect
fli
g
h
t musc
l
eru
di
ments are present
i

n
l
arva
li
nstar
s
an
d
are attac
h
e
d
to t
h
e
i
ntegument at po
i
nts correspon
di
ng to t
h
e
f
uture
l
ocat
i
ons o
f

t
he
sc
l
er
i
tes. Some o
f
t
h
ese (
bif
unct
i
ona
l
musc
l
es) ma
yb
e
i
mportant
i
n
l
e
g
movements
d

ur
i
n
g
l
arval life (Chapter 14, Section 3.3.1). Like the direct fli
g
ht muscles, the indirect fli
g
h
t
m
uscles
g
row pro
g
ressivel
y
throu
g
h larval life but remain unstriated and non-functional
unt
il
t
h
ea
d
u
l
t stage.

4
.2. Endopterygote Metamorphos
is
In more primitive endopter
yg
otes such as Neuroptera and Coleoptera, as in exopter
y-
g
otes, a
g
ood deal of pro
g
ressive development of or
g
an s
y
stems occurs durin
g
larval lif
e
so t
h
at metamorp
h
os
i
s, re
l
at
i

ve
l
y spea
ki
ng,
i
ss
li
g
h
tan
d
concerns, aga
i
n, ma
i
n
l
yt
h
e
fli
g
ht
m
ec
h
an
i
sm. At t

h
e oppos
i
te extreme, seen
i
n many D
i
ptera an
d
Hymenoptera, most
l
arva
l
t
i
ssues are
hi
sto
ly
ze
d
,w
i
t
h
a
d
u
l
tt

i
ssues
b
e
i
n
gf
orme
d
anew, o
f
ten
f
rom spec
ifi
c
g
roups
o
f undifferentiated cells, the ima
g
inal discs and abdominal histoblasts. The ima
g
inal discs
o
ccur as thickened re
g
ions of epidermis whose cells remain embr
y
onic; that is, in the larva

l
i
nstars t
h
e
i
r
diff
erent
i
at
i
on
i
s suppresse
db
yt
h
e
h
ormona
l
m
ili
eu ex
i
st
i
ng
i

nt
h
e
i
nsect at t
hi
s
t
i
me. At metamorp
h
os
i
s str
iki
ng c
h
anges occur
i
nt
h
e concentrat
i
on o
f
certa
i
n
h
ormones

,
as a resu
l
to
f
w
hi
c
h
t
h
ece
ll
s can mu
l
t
i
p
l
yan
d diff
erent
i
ate
i
nto spec
ifi
ca
d
u

l
t organs an
d
tissues (Fi
g
ure 21.9). Experiments in which cells have been selectivel
y
destro
y
ed b
y
X-
i
rradiation have shown that formation of ima
g
inal discs occurs ver
y
earl
y
in embr
y
o
g
enesis
and at specific sites. Furthermore, each imaginal disc differentiates in a predetermined man-
n
er. Dur
i
ng
l

arva
ld
eve
l
opment, t
h
e
di
scs grow exponent
i
a
ll
y
i
nre
l
at
i
on to genera
lb
o
d
y
growt
h
an
d
, typ
i
ca

ll
y, come to
li
ew
i
t
hi
nan
i
nvag
i
nat
i
on, t
h
e per
i
po
di
a
l
cav
i
ty,
b
eneat
h
t
he
c

uticle (Fi
g
ure 21.11). In contrast to the ima
g
inal discs, the abdominal histoblasts, which
635
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
F
I
GU
RE 21.9.
I
ma
g
inal discs o
f
D
roso
p
hil
a

and their derivatives in the adult bod
y
. [From H. Wildermuth, 1970,
Determ
i
nat
i
on an
d
trans
d
eterm
i
nat
i
on
i
nce
ll
so
f
t
h
e
f
ru
i
t
fl
y,

S
ci. Prog.
(
O
xfor
d
)
58:329–358. By permission o
f
B
l
ac
k
we
ll
Sc
i
ent
ifi
cPu
bli
cat
i
ons.]
are groups o
fl
oose
l
y assoc
i

ate
d
ce
ll
s
i
nt
h
e
l
arva
li
ntegument,
d
o secrete
l
arva
l
cut
i
c
l
e
.
At metamorp
h
os
i
s, un
d

er
h
ormona
li
n
fl
uence, t
h
ey
di
v
id
ean
d diff
erent
i
ate
i
nto t
h
ea
d
u
lt
a
bd
om
i
na
l

ep
id
erm
i
s,
f
at
b
o
d
y, oenocytes, an
d
some musc
l
es.
W
ith the evolution of ima
g
inal discs the wa
y
was open for the development of a larv
a
w
hose form is hi
g
hl
y
different from that of the adult, and capable of existin
g
in a different

h
abitat from that of the adult, thus avoiding competition for food and space.
T
o
cl
ar
if
yt
h
e
hi
sto
l
og
i
ca
l
c
h
anges t
h
at occur
i
nen
d
opterygote metamorp
h
os
i
s, t

h
e
v
ar
i
ous organ systems w
ill b
e cons
id
ere
d
separate
ly
Epidermal cells carried over from the larval sta
g
e produce the cuticle of most adul
t
endopter
yg
otes. However, in H
y
menoptera-Apocrita and Diptera-Muscomorpha the larval
epidermis is more or less completel
y
histol
y
zed and replaced b
y
cells derived from ima
g

inal
di
scs an
dhi
sto
bl
asts. In Muscomorp
h
a,
hi
sto
l
ys
i
so
f
t
h
e
l
arva
l
ep
id
erm
i
s
d
oes not occur
u

nt
il
a
f
ter pupar
i
at
i
on.
Appen
d
a
g
e
f
ormat
i
on
i
sa
l
so var
i
e
d
.In
l
ower en
d
opter

yg
otes
f
ormat
i
on o
f
a
d
u
l
t mout
h
-
parts, antennae, and le
g
sbe
g
ins earl
y
in the final larval stadium from larval epidermis. Cer
-
t
ain
p
redetermined areas of the e
p
idermis thicken, then
p
roliferate and differentiate so that,

at pupat
i
on, t
h
e
b
as
i
c
f
orm o
f
t
h
ea
d
u
l
t appen
d
ages
i
sev
id
ent. Dur
i
ng t
h
e pupa
l

sta
di
um t
he
fi
na
lf
orm o
f
t
h
ea
d
u
l
t appen
d
ages
i
s expresse
d
(F
i
gure 21.10). In contrast, w
h
ere t
h
e
l
arva

l
appen
d
a
g
es are ver
y diff
erent
f
rom t
h
ose o
f
t
h
ea
d
u
l
t, or are a
b
sent, t
h
ea
d
u
l
t structures
d
evelop from ima

g
inal discs that under
g
o marked proliferation and differentiation in the last
larval instar and are eva
g
inated from the peripodial cavit
y
at the larval-pupal molt. Win
g
s
are formed in all endopterygotes from imaginal discs. In most species their early develop-
ment
i
ss
i
m
il
ar to t
h
e
d
eve
l
opment o
f
pa
i
re
d

segmenta
l
appen
d
ages out
li
ne
d
a
b
ove; t
h
at
i
s, t
h
ew
i
ng ru
di
ments
f
orm
i
n a per
i
po
di
a
l

cav
i
ty an
db
ecome everte
d
at t
h
e
l
arva
l
-pupa
l
molt (Fi
g
ure 21.11). The formin
g
win
g
bud in the peripodial cavit
y
is initiall
y
a hollow,
636
CHAPTER
21
F
IGURE 21.10. Sections through leg o

f
P
ieri
s
(
Lepidoptera) to show development of adult appendage. (A) Leg
of l
ast-
i
nstar
l
arva 3
h
ours a
f
ter ec
dy
s
i
s; (B) same as (A)
b
ut 1
d
a
y
a
f
ter ec
dy
s

i
s; (C) same as (A)
b
ut 3
d
a
y
sa
f
te
r
e
cd
y
sis; (D) le
g
at be
g
innin
g
of prepupal sta
g
e showin
g
presumptive areas of adult le
g
; and (E) le
g
of pupa. [After
C

W. Kim, 1959, The differentiation center inducing the development from larval to adult leg in
P
ieri
s
bra
ss
icae
(Le
pid
o
p
tera)
,
J
.Em
b
ryo
l
. Exp. Morp
h
o
l.
7
:5
72–
5
82. B
y
permission of Cambrid
g

e Universit
y
Press.]
F
IGURE 21.11. Sect
i
ons t
h
roug
hd
eve
l
op
i
ng w
i
ng
b
u
d
o
ffi
rst
f
our
l
arva
li
nstars o
f

P
ieris (Lep
id
optera). [A
f
te
r
J. H. Comstoc
k,
1918
,
Th
e Wings of Insect
s
, Comstoc
k
.
]
6
3
7
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN

T
F
I
GU
RE 21.12. Transverse sections of developing wing o
f
Droso
p
hil
a
.
(A, B) Successive stages in pharat
e
p
upa; (C–G) stages
i
n pupa; an
d
(H) p
h
arate a
d
u
l
t. [A
f
ter C. H. Wa
ddi
ngton, 1941, T
h

e genet
i
c contro
l
o
f
w
i
ng
d
eve
l
o
p
ment
in
D
rosop
h
i
la
,
J.
G
enet.
41
:7
5
–139. B
y

permission of Cambrid
g
e Universit
y
Press.
]
fi
n
g
erlike structure, but this becomes flattened so that the central cavit
y
is more or les
s
obliterated, leavin
g
onl
y
small lacunae (Fi
g
ure 21.12A, B). A nerve and trachea that hav
e
b
een associated with the imaginal disc now grow along each lacuna occasionally branching
i
n a pre
d
eterm
i
ne
d

pattern. At t
h
e
l
arva
l
-pupa
l
mo
l
t,
h
emo
l
ymp
h
pressure
f
orces t
h
es
id
es
o
f
aw
i
ng
b
u

d
apart so t
h
at t
h
ere
i
ssu
ffi
c
i
ent space w
i
t
hi
n
i
t
f
or t
h
e
d
eve
l
opment o
f
an a
d
u

lt
w
in
g
(Fi
g
ure 21.12C, D). Durin
g
the pupal stadium extensive proliferation of the epidermal
cells occurs within the win
g
bud, as a consequence of which the epidermis becomes folde
d
and closely apposed over most of the wing surface. The epidermal layers remain separate
a
dj
acent to t
h
e nerve an
d
trac
h
ea,
f
orm
i
ng t
h
e
d

e
fi
n
i
t
i
ve w
i
ng ve
i
ns (F
i
gure 21.12E–H)
.
T
h
e gut o
f
en
d
opterygotes typ
i
ca
ll
yc
h
anges
i
ts
f

orm mar
k
e
dl
y
d
ur
i
ng metamorp
h
os
i
s.
I
nCo
l
eoptera t
h
e
f
ore
g
ut an
dhi
n
dg
ut un
d
er
g

ore
l
at
i
ve
ly
s
ligh
tmo
difi
cat
i
on, t
hi
s
b
e
i
n
g
achieved b
y
the activit
y
of larval cells. In hi
g
her endopter
yg
otes these re
g

ions are partiall
y
or entirel
y
renewed from
g
roups of primordial cells located at the
j
unctions of the fore
g
u
t
an
d
m
id
gut an
d
m
id
gut an
dhi
n
d
gut, an
d
a
dj
acent to t
h

e mout
h
an
d
anus. T
h
e
l
arva
l
m
id
gut
o
f
a
ll
en
d
opterygotes
i
s
f
u
ll
y rep
l
ace
d
as a resu

l
to
f
t
h
e act
i
v
i
ty o
f
e
i
t
h
er regenerat
i
ve ce
ll
s
f
rom t
h
e
l
arva
l
m
idg
ut, or un

diff
erent
i
ate
d
ce
ll
satt
h
e
j
unct
i
on o
f
t
h
em
idg
ut an
dhi
n
dg
ut
,
or both. In either arran
g
ement, the histol
y
zed larval cells eventuall

y
are surrounded b
y
adult
t
issue. To protect the insect from potential patho
g
ens in the absence of a peritrophic matrix,
t
he differentiating pupal midgut epithelium releases a mixture of antibacterial peptides int
o
t
he gut lumen (Russell and Dunn, 1996).
Larva
l
Ma
l
p
i
g
hi
an tu
b
u
l
es may
b
e reta
i
ne

di
n some a
d
u
l
tD
i
ptera,
b
ut
i
not
h
er en-
d
opter
yg
otes the
y
are partiall
y
or completel
y
replaced at metamorphosis from special cells
located either alon
g
the len
g
th of each tubule or at the anterior end of the hind
g

ut
.
638
CHAPTER
21
Generall
y
, the larval tracheal s
y
stem is carried over to the adult with little modification
,
e
xcept as required b
y
the development of new tissues such as fli
g
ht muscles and reproductiv
e
o
r
g
ans. However, in Diptera, considerable replacement of the larval s
y
stem occurs fro
m
scattere
d
ce
ll
s

i
nt
h
e
l
ar
v
a
l
trac
h
eae.
Th
e centra
l
nervous system o
f
most en
d
opterygotes
b
ecomes more concentrate
d
at
m
etamorp
h
os
i
s

b
ecause o
f
s
h
orten
i
n
g
o
f
t
h
e
i
nter
g
an
gli
on
i
c connect
i
ves an
d
t
h
e
f
orwar

d
m
i
g
ration of
g
an
g
lia. It is likel
y
that the surroundin
gg
lial cells are responsible for thi
s
process as their ensheathin
g
c
y
toplasm is filled with microtubules oriented len
g
thwise alon
g
t
h
e connect
i
ves. W
i
t
hi

nagang
li
on, some neurons may en
l
arge w
hil
eot
h
ers
diff
erent
i
ate
f
rom neuroblasts. Many others are phagocytozed by glial cells so that only a few (
5
%to10%
in
Droso
ph
i
l
a
,f
or examp
l
e) are carr
i
e
d

overtot
h
ea
d
u
l
t. T
h
ese are nevert
h
e
l
ess
i
mportant
as the
y
serve as a scaffold on which adult sensor
y
neurons can reach and connect with the
c
entral nervous s
y
stem (Williams and Shepherd, 2002). In some moths clusters of immature
n
eurons, each surrounded by a giant glial cell, migrate along the interganglionic connective
s
to t
h
e next poster

i
or gang
li
on (Canter
a
et a
l.
, 199
5
). The giant glial cells, which span the
i
ntergang
li
on
i
c connect
i
ves, pro
b
a
bl
y
d
rag t
h
e neuron c
l
usters
b
etween gang

li
a. Brea
kd
ow
n
and rebuildin
g
of the perineurium and neural lamella are necessitated b
y
these chan
g
es. In
i
nsects that as adults make extensive use of associative learnin
g
(Chapter 13, Section 2.4) the
m
ushroom bodies undergo large-scale reorganization during metamorphosis, with extensiv
e
d
egra
d
at
i
on o
f
t
h
e
l

arva
l
structures an
d
esta
bli
s
h
ment o
f
t
h
ea
d
u
l
t
f
orm
f
rom neuro
bl
asts
c
arr
i
e
d
over
f

rom t
h
eem
b
ryo (Farr
is
et a
l.
,
1999
)
.
D
urin
g
metamorphosis the muscular s
y
stem under
g
oes considerable modification es-
peciall
y
in connection with fli
g
ht. T
y
picall
y
, man
y

larval muscles histol
y
ze, thou
g
h the poin
t
at which histol
y
sis be
g
ins is varied and somewhat dependent on their function. For man
y
m
usc
l
es
hi
sto
l
ys
i
s
b
eg
i
ns
i
nt
h
e

fi
na
ll
arva
li
nstar an
d
cont
i
nues
i
nt
h
e pupa. Ot
h
er musc
l
es,
h
owever,
h
ave part
i
cu
l
ar
f
unct
i
ons at t

h
e
l
arva
l
-pupa
l
mo
l
tan
db
eyon
d
an
dd
o not
hi
sto
l
yz
e
unt
il l
ater. As an extreme examp
l
e, spec
i
a
l
ec

l
os
i
on musc
l
es t
h
at
f
ac
ili
tate t
h
ea
d
u
l
t’s escape
f
rom the puparium differentiate durin
g
the pupal sta
g
e but disappear within a few hours
o
f emer
g
ence. The muscles of an adult insect arise in several wa
y
s: (1) from larval mus-

cl
es t
h
at rema
i
n unc
h
ange
d
, (2)
f
rom part
i
a
ll
y
hi
sto
l
yze
d
an
d
reconstructe
dl
arva
l
musc
l
es,

(
3)
f
rom prev
i
ous
l
y
i
nact
i
ve
i
mag
i
na
l
nuc
l
e
i
w
i
t
hi
nt
h
e
l
arva

l
musc
l
es, (4)
f
rom myo
bl
ast
s
that previously adhered loosely to the surface of the larval muscles, or (
5
) from rudimentary,
n
on-functional fibers present in the larva (Whitten, 1968). Methods 3–5 are increasin
g
l
y
i
mportant in hi
g
her endopter
yg
otes. Further, the presence of motor neurons is essential for
the proliferation and correct organization of the new muscles (Ken
t
et al.
,
1995)
.
Th

e extent o
fhi
sto
l
ys
i
so
f
t
h
e
f
at
b
o
d
y
i
squ
i
te var
i
e
d
an
dd
epen
d
sont
h

e extent
of
metamorp
h
os
i
s. In more pr
i
m
i
t
i
ve en
d
opterygotes w
h
ere metamorp
h
os
i
s
i
sre
l
at
i
ve
ly
sli
g

ht, much of the larval fat bod
y
is carried over unchan
g
ed into the adult sta
g
e. However,
i
n muscomorph Diptera, for example, the larval tissue is completel
y
broken down, and the
adult fat body is formed from mesenchyme cells associated with imaginal discs
.
Th
e
h
eart an
d
aorta are norma
ll
y not
hi
sto
l
yze
d
an
d
cont
i

nue to contract
i
nt
h
e pupa
.
H
owever,
i
n muscomorp
h
D
i
ptera, contract
i
on stops m
id
way t
h
roug
h
t
h
e pupa
l
sta
di
um,
t
h

e
l
arva
lh
eart musc
l
ece
ll
s
b
rea
kd
own
,
an
d
new contract
il
ee
l
ements
diff
erent
i
ate
f
rom
my
oblasts. The dorsal and ventral diaphra
g

ms to
g
ether with the accessor
y
hearts are formed
at metamorphosis, apparentl
y
from m
y
oblasts associated with existin
g
neurons
.
R
are
l
y,
b
ot
h
ecto
d
erma
l
an
d
meso
d
erma
l

ru
di
ments o
f
t
h
e repro
d
uct
i
ve system
b
ecome
di
st
i
ngu
i
s
h
a
bl
e
i
n
l
ate
l
arva
li

nstars. However,
i
nt
h
e great ma
j
or
i
ty o
f
en
d
opterygotes t
h
e
e
nt
i
re process o
f diff
erent
i
at
i
on o
f
t
h
e repro
d

uct
i
ve s
y
stem occurs at metamorp
h
os
i
s, e
i
t
h
er
6
3
9
P
OS
TEMBRY
O
NI
C
DEVELOPMEN
T
from
g
roups of undifferentiated cells or, in the case of the muscomorph Diptera and hi
g
her
H

y
menoptera, from
g
enital ima
g
inal discs.
5
.E
c
l
osio
n
Fo
re
xopter
yg
otes adult emer
g
ence (eclosion) consists solel
y
of escape from the cuticle
of the previous instar. Man
y
endopter
yg
otes must, in addition, force their wa
y
out of the
cocoon or ce
ll i

nw
hi
c
hp
u
p
at
i
on occurre
d
an
d
,
i
n some s
p
ec
i
es, to t
h
e sur
f
ace o
f
t
h
e
su
b
strate

i
nw
hi
c
h
t
h
ey
h
ave
b
een
b
ur
i
e
d
. Some aquat
i
c spec
i
es t
h
at pupate un
d
er water
h
ave spec
i
a

ld
ev
i
ces to ena
bl
et
h
ea
d
u
l
t to reac
h
t
h
e water sur
f
ace.
For
adults of man
y
species, emer
g
ence is tri
gg
ered b
y
environmental factors, especiall
y
t

emperature and photoperiod, or is entrained as a circadian rh
y
thm (M
y
ers, 2003) (see als
o
C
h
apter 22, Sect
i
ons 2.3 an
d
3.1.1). As a resu
l
t, emergence o
f
popu
l
at
i
ons o
f
a
d
u
l
ts
i
s
hi

g
hl
y
sync
h
ron
i
ze
d
,t
hi
s
b
e
i
ng o
f
part
i
cu
l
ar
i
mportance
i
n spec
i
es w
h
ose a

d
u
l
t
lif
e
i
ss
h
ort.
Ec
l
os
i
on
i
s accomp
li
s
h
e
di
n a manner s
i
m
il
ar to
l
arva
l

-
l
arva
l
mo
l
ts.Ap
h
arate a
d
u
lt
swallows air to increase its bod
y
volume and, b
y
contraction of abdominal muscles, forces
h
emol
y
mph anteriorl
y
. As the hemol
y
mph pressure increases, the pupal cuticle splits alon
g
an ec
d
ys
i

a
lli
ne on t
h
et
h
orax an
d
/or
h
ea
d
.Ino
b
tect pupae t
h
e pupa
l
mout
hi
s sea
l
e
d
over,
b
u
t
t
h

ea
d
u
l
tswa
ll
ows a
i
rt
h
at enters t
h
e pupa
l
case v
i
at
h
e trac
h
ea
l
system. Some a
d
u
l
t
sp
i
rac

l
es rema
i
n
i
n contact w
i
t
h
t
h
ose o
f
t
h
e pupa, w
h
ereas ot
h
ers
b
ecome separate
d
so t
h
at
a channel is open alon
g
which air can move into the pupal case.
Amon

g
more primitive endopter
yg
otes an insect escapes from its cocoon or cell a
s
ap
h
arate a
d
u
l
tus
i
ng t
h
e man
dibl
es o
f
t
h
e
d
ect
i
cous pupa to
f
orce an open
i
ng

i
nt
h
e
w
a
ll
.P
h
arate a
d
u
l
ts o
f
some spec
i
es a
l
so
h
ave
b
ac
k
war
dl
y
f
ac

i
ng sp
i
nes on t
h
e pupa
l
cut
i
c
l
e, w
hi
c
h
ena
bl
et
h
em to wr
iggl
e out o
f
t
h
ece
ll
an
d
t

h
rou
gh
t
h
esu
b
strate. Man
y
pr
i
m-
itive Lepidoptera and Diptera, whose pupae are adecticous, also escape as pharate adults,
frequentl
y
makin
g
use of special spines (cocoon cutters) on the pupal cuticle. In hi
g
her
L
epidoptera, adults may shed the pupal cuticle while still in the cocoon. In such specie
s
th
e cocoon may possess an “escape
h
atc
h
” or part o
fi

t may
b
eso
f
tene
db
y spec
i
a
l
sa
li
-
var
y
secret
i
ons. Furt
h
er,
f
or t
h
ose spec
i
es t
h
at pupate
i
nso

il
,t
h
ea
d
u
l
t cut
i
c
l
ema
yb
ecome
t
emporaril
y
plasticized to facilitate tunnelin
g
to the surface. In muscomorph Diptera a
n
ev
ersible membranous sac on the head, the ptilinum, can be expanded b
y
hemol
y
mph pres-
sure. This enables an adult to
p
ush off the ti

p
of the
p
u
p
arium and tunnel to the surface of the
su
b
strate
i
nw
hi
c
hi
t
h
as
b
een
b
ur
i
e
d
.A
d
u
l
tCo
l

eoptera, Hymenoptera, an
d
S
i
p
h
onaptera
l
eave t
h
e pupa
l
cut
i
c
l
ew
hil
e
i
nt
h
e cocoon or ce
ll
,t
h
en use t
h
e
i

r man
dibl
es or cocoon cutters
t
o cut their wa
y
out. In some species this is the sole function of the mandibles, which, like
cocoon cutters, are shed after emer
g
ence.
6
.
C
ontrol o
f
Develo
p
ment
Despite the apparentl
y
wide differences in the pattern of development seen in Insecta,
t
he ph
y
siolo
g
ical s
y
stem that re
g

ulates
g
rowth, moltin
g
, and metamorphosis is commo
n
t
oa
ll
mem
b
ers o
f
t
h
ec
l
ass, name
l
y, t
h
een
d
ocr
i
ne system. Var
i
at
i
ons

i
nt
h
ere
l
at
i
ve
l
eve
l
s
o
f diff
erent
h
ormones
i
nan
i
nsect’s
b
o
d
y
d
eterm
i
ne t
h

e nature an
d
extent o
f
t
i
ssue
diff
er-
entiation that is expressed at the next molt. In other words, it is the hormone balance that
d
etermines, in a holometabolous insect, for exam
p
le, whether the next molt is larval-larval
,
6
4
0
CHAPTER
21
l
arval-pupal, or pupal-adult. Hormones also coordinate the sequence of events in the
g
rowth
and moltin
g
c
y
cle and in some species ensure that an adult emer
g

es when environmenta
l
c
onditions are suitable. The hormones act b
y
re
g
ulatin
gg
enetic activit
y
. In a particular hor-
m
ona
l
m
ili
eu, t
h
e genes t
h
at are act
i
ve are respons
ibl
e
f
or express
i
on o

fl
arva
l
c
h
aracters;
un
d
er ot
h
er
h
ormona
l
con
di
t
i
ons genes
f
or pupa
l
or
i
mag
i
na
lf
eatures are act
i

vate
d
.
M
an
y
env
i
ronmenta
lf
actors can mo
dify d
eve
l
opmenta
l
patterns. Some o
f
t
h
ese
f
actors,
f
or example, temperature, ma
y
act directl
y
to affect development; most factors, however
,

ex
e
rt their effect indirectl
y
via the endocrine s
y
stem
.
6.1. Endocrine Re
g
ulation of Development
P
ostem
b
ryon
i
c
d
eve
l
opment
i
s contro
ll
e
db
yt
h
ree en
d

ocr
i
ne centers: t
h
e
b
ra
i
n-corpora
c
ar
di
aca comp
l
ex, corpora a
ll
ata, an
d
mo
l
tg
l
an
d
s (see C
h
apter 13, Sect
i
on 3,
f

or a
d
escr
i
p-
t
i
on o
f
t
h
e
i
r structure an
d
pro
d
ucts). A mo
l
tc
y
c
l
e
i
s
i
n
i
t

i
ate
d
w
h
en, as a resu
l
to
f
appropr
i
ate
si
g
nals (see Section
6
.2), the median neurosecretor
y
cells of the brain release ecd
y
siotropin
[
prothoracicotropic hormone (PTTH)], which stimulates moltin
g
hormone (ecd
y
sone) (MH
)
pro
d

uct
i
on
b
yt
h
emo
l
tg
l
an
d
s. In a
ll i
nsects stu
di
e
d
t
h
ere
i
sama
j
or pea
k
o
f
MH
i

nt
he
h
emo
l
ymp
hd
ur
i
ng t
h
e secon
dh
a
lf
o
f
eac
h
mo
l
tcyc
l
e, an
di
t
i
st
hi
s MH surge [

i
n rea
li
ty, t
h
e
MH
i
s
fi
rst converte
d
to t
h
e
bi
o
l
o
gi
ca
lly
act
i
ve
f
orm, 20-
hyd
rox
y

ec
dy
sone (20-HE), pro
b
a
-
bl
y
at its tar
g
et site] that initiates the various ph
y
siolo
g
ical events constitutin
g
a molt c
y
cl
e
(
Fi
g
ure 21.13). In addition, in the final larval instar of holometabolous species one or more
smaller hemolymph MH peaks precede the major peak and are thought to be responsible
f
or reprogramm
i
ng t
i

ssues
f
or pupa
l
rat
h
er t
h
an
l
arva
l
synt
h
eses.
Th
e corpora a
ll
ata pro
d
uce
j
uven
il
e
h
ormone (JH). T
h
eregu
l

at
i
on o
f
corpus a
ll
atum
activit
y
is complex (Tobe and Sta
y
, 198
5
). Both allatotropic (corpus allatum-stimulatin
g)
and allatostatic (corpus allatum-inhibitin
g
) neurosecretor
y
factors have been reported, while
i
n some insects the brain exerts direct neural control over the gland. It should also be noted
t
h
at t
h
e
h
emo
l

ymp
h
conta
i
ns
hi
g
hl
y act
i
ve esterases w
i
t
h
t
h
e potent
i
a
lf
or
d
egra
di
ng
f
re
e
J
H. T

h
us, t
h
e concentrat
i
on o
f
c
i
rcu
l
at
i
ng JH
i
s
d
eterm
i
ne
d
not on
l
y
b
yt
h
e secretory act
i
v

i
t
y
of
t
h
e corpora a
ll
ata
b
ut a
l
so
by
t
h
ese
h
emo
ly
mp
h
esterases.
JH can exert an influence on development onl
y
in the presence of MH, that is, after
a moltin
g
c
y

cle has be
g
un. It is the concentration of circulatin
g
JH durin
g
one or more
c
r
i
t
i
ca
l
per
i
o
d
so
f
t
h
e sta
di
um t
h
at
d
eterm
i

nes t
h
e nature o
f
t
h
e succee
di
ng mo
l
t. I
f
t
h
e
c
oncentrat
i
on o
fJ
H
i
sa
b
o
v
eat
h
res
h

o
ld v
a
l
u
e
∗
d
ur
i
n
g
t
h
ecr
i
t
i
ca
l
per
i
o
d
,t
h
enextmo
l
tw
ill

be larval-larval
(
for this reason, JH has been described as the “
st
a
t
us
q
uo” hormone
)
. Whe
n
there is little or no circulatin
g
JH, an adult will appear at the next molt (Fi
g
ure 21.13)
.
Thi
s scenar
i
o app
li
es to
h
em
i
meta
b
o

l
ous
i
nsects, w
hi
c
hh
aveas
i
ng
l
ecr
i
t
i
ca
l
per
i
o
d
d
ur
i
ng eac
h
sta
di
um an
d

,o
f
course,
l
ac
k
a pupa
li
nstar. In
h
o
l
ometa
b
o
l
ous
i
nsects t
h
ere
a
re two cr
i
t
i
ca
l
per
i

o
d
s
i
nt
h
e
l
ast
l
arva
l
sta
di
um. In t
h
e
fi
rst t
h
ea
b
sence o
f
JH pro
g
rams
the development of pupal characters. In the second, which is
j
ust before the larval-pupal

m
olt, a shar
p
increase in JH concentration occurs that
p
revents
p
remature differentiatio
n
o
f imaginal discs. In the pupal stadium the absence of JH in the critical period permits the
e
xpress
i
on o
f
a
d
u
l
tc
h
aracters. In spec
i
es t
h
at s
h
ow p
h

enotyp
i
cpo
l
ymorp
hi
sm (Sect
i
on 7
)
t
h
ere may
b
e severa
l
extra JH-sens
i
t
i
ve cr
i
t
i
ca
l
per
i
o
d

s
f
or express
i
on o
f
t
h
evar
i
ous
f
orms
(
Ni
j
hout, 1994)
.
∗
Th
ea
b
so
l
ute concentrat
i
on appears un
i
mportant, prov
id

e
d
t
h
at
i
t
i
sa
b
ove or
b
e
l
owat
h
res
h
o
ld
range. However
,
th
et
h
res
h
o
ld
ran

g
ew
ill
var
y
amon
g
spec
i
es
.
6
41
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
F
IGURE 21.13
.
Sc
h
emat
i

c compar
i
son o
f
en
d
ocr
i
ne contro
l
o
fd
eve
l
opment
i
n
h
em
i
meta
b
o
l
ous an
d
h
olometabolous insects. Pulses of prothoracicotropic hormone (PTTH) tri
gg
er s

y
nthesis and release of MH
.
L
evels of JH determine the nature of the molt: when JH is present during a critical period, a larval-larval mol
t
occurs;
if
no JH
i
s present, t
h
enextmo
l
tw
ill b
e
l
arva
l
-a
d
u
l
t (Hem
i
meta
b
o
l

a), or
l
arva
l
-pupa
l
or pupa
l
-a
d
u
l
t
(
Holometabola). In the final larval sta
g
e of Holometabola there are two critical periods: in the first (no JH present)
t
he switch to pupal development occurs; in the second, there is a pulse of JH that prevents premature differentiation
o
fi
ma
gi
na
ldi
scs. Just pr
i
or to, or
i
mme

di
ate
ly
a
f
ter, eac
h
mo
l
t, re
l
ease o
f
ec
l
os
i
on
h
ormone (EH) or
b
urs
i
co
n
(
B), respectivel
y
, occurs (see also Fi
g

ure 21.14). JH and MH levels are not drawn to the same scale. Numbers
on the horizontal axes indicate the percent duration of each stadium. Other abbreviations: F-1, penultimate larval
s
ta
di
um; F-2, antepenu
l
t
i
mate
l
arva
l
sta
di
um. [Or
igi
na
l
,
b
ase
d
on
d
ata
f
rom severa
l
sources.

]
Apart from permitting the expression of adult characters, the low concentration o
f
JH
d
ur
i
ng t
h
e
fi
na
l
sta
di
um
h
as anot
h
er ma
j
or e
ff
ect:
i
t
l
ea
d
sto

d
egenerat
i
on o
f
t
h
emo
l
t
g
l
an
d
s, w
hi
c
hdi
sappear w
i
t
hi
na
f
ew
d
ays o
f
ec
l

os
i
on
i
n most
i
nsects, except
i
ons
b
e
i
n
g
apter
yg
otes, which, as noted earlier, continue to
g
row and molt as adults and solitar
y
locusts
w
hose corpora allata apparentl
y
do not become completel
y
inactive at the final molt. Thou
gh
d
e

g
eneration of the molt
g
lands is of critical importance in the life histor
y
of an insect, when
v
i
ewe
di
nt
h
e perspect
i
ve o
f
metamorp
h
os
i
st
h
ep
h
enomenon
b
ecomes s
i
mp
l

y an examp
l
e
o
f
apoptos
i
s (programme
d
ce
ll d
eat
h
). In ot
h
er wor
d
s, t
h
emo
l
tg
l
an
d
s,
lik
e many ot
h
er

structures
i
n
j
uven
il
e
i
nsects, espec
i
a
lly
en
d
opter
yg
otes, are
l
arva
l
t
i
ssues w
h
ose structura
l
w
ell-bein
g
is dependent on JH. In the absence of JH, at metamorphosis, the

y
histol
y
ze. I
t
remains unclear how JH affects the molt
g
lands. However, a ver
y
earl
y
si
g
n of apoptosis
i
nt
h
eg
l
an
d
s
i
s nuc
l
ear DNA c
l
eavage; t
hi
s

i
s prevente
db
yt
h
e exper
i
menta
l
app
li
cat
i
on o
f
JH (Da
i
an
d
G
ilb
ert, 1998).
T
h
e prec
i
se mo
d
es o
f

act
i
on o
f
t
h
e
d
eve
l
opmenta
lh
ormones rema
i
n unc
l
ear. One o
f
t
he earliest observable effects of PTTH is renewed RNA s
y
nthesis in the molt
g
lands. This
6
4
2
CHAPTER
21
e

ffect appears to be achieved, as for other peptide hormones, throu
g
h a second messen
g
e
r
s
y
stem, namel
y
,c
y
clic AMP and calcium ions.
By
contrast, 20-HE and JH are lipophilic and thus able to move throu
g
h the cell
m
em
b
rane to t
h
e nuc
l
ear mem
b
rane w
h
ere t
h

ey
bi
n
d
to spec
ifi
c receptors. I
n
Drosop
h
i
l
a
an
d
Man
d
uc
a
th
e receptor
f
or 20-HE
h
as
b
een
id
ent
ifi

e
d
an
d
c
h
aracter
i
ze
d
as a prote
i
n
h
etero
di
mer
(
Ha
ll
, 1999; R
iddif
or
d
et al.
, 1999). Its two components are EcR (ec
dy
sone
rece
p

tor) and USP (ultras
p
iracle
∗
)
, both of which ma
y
exist in sli
g
htl
y
different forms
and concentrations. The 20-HE binds to the EcR
p
art of the dimer, and while the function
of
USP rema
i
ns unc
l
ear,
b
ot
h
components o
f
t
h
e
di

mer are necessary to transport t
he
h
ormone to t
h
ec
h
romosomes
f
or gene act
i
vat
i
on (Lezz
i
e
ta
l.
,
1999). Prec
i
se
l
y
h
ow 20
-
H
Ewor
k

s
i
s not
k
nown; t
h
e most w
id
e
ly
accepte
d
v
i
ew
i
st
h
at t
h
e
h
ormone,
lik
et
he
s
teroid hormones of vertebrates, induces a
g
ene-activation cascade. The 20-HE activates

s
o-called “earl
y
”
g
enes that encode re
g
ulator
y
proteins. The latter, in turn, modulate the
act
i
v
i
ty o
f
“m
iddl
e,” an
d
eventua
ll
y“
l
ate,” genes w
h
ose transcr
i
pt
i

ona
l
pro
d
ucts carr
y
o
ut the appropriate tissue-specific process (Riddiford, 198
5
; Doctor and Fristrom, 198
5
).
T
h
e pat
h
wa
y
so
fg
ene act
i
vat
i
on t
h
at are
f
o
ll

owe
dd
epen
d
on t
h
e 20-HE concentrat
i
on an
d
r
eceptor isoform; as well, the
y
will be species- and tissue-specific, resultin
g
in the numerous
e
ffects induced b
y
this hormone
.
Th
es
i
te an
d
mo
d
eo
f

act
i
on o
f
JH are
l
ess c
l
ear, a statement t
h
at
i
s
p
er
h
a
p
s not
s
urpr
i
s
i
ng g
i
ven
i
ts mu
l

t
if
unct
i
ona
l
ro
l
e
i
n
i
nsects. However, w
i
t
h
respect to postem
b
ryon
ic
d
eve
l
opment w
h
ere
i
t qua
li
tat

i
ve
ly
mo
difi
es t
h
ee
ff
ects o
f
20-HE, JH
i
s
g
enera
lly
assume
d
to act at the same level; that is, it influences
g
ene activation and messen
g
er RNA s
y
nthesis.
Elucidation of its mode of action has been hampered b
y
the inabilit
y

to characterize it
s
r
ece
p
tors. T
h
e
p
ro
p
osa
l
o
f
Jones an
d
S
h
ar
p
(1997) t
h
at USP
i
s a rece
p
tor
f
or JH

in
D
rosop
h
i
l
a
i
s
i
ntr
i
gu
i
ng
b
ut requ
i
res extens
i
on to ot
h
er
i
nsects. One suggest
i
on
f
or t
h

e manner
i
nw
hi
c
h
J
Hwor
k
s
i
st
h
at
i
tma
y
a
l
ter t
h
e con
f
ormat
i
on o
f
t
h
ec

h
romat
i
nsot
h
at 20-HE can act
i
vate
o
nl
y
larva-specific
g
enes
.
6
.2. Factors In
i
t
i
at
i
n
g
and Term
i
nat
i
n
g

Molt
C
ycles
Com
p
ared with the enormous volume of literature on the endocrine interactions that
r
egu
l
ate growt
h
an
d
mo
l
t
i
ng, re
l
at
i
ve
l
y
li
tt
l
e
i
s

k
nown a
b
out t
h
e externa
lf
actors t
h
at
i
n
i
t
i
at
e
o
r term
i
nate mo
l
t
i
ng cyc
l
es
.
A
num

b
er o
f
env
i
ronmenta
l
var
i
a
bl
es
h
ave
b
een s
h
owntoa
ff
ect
g
rowt
h
an
d
mo
l
t
i
n

g
,
and some of these clearl
y
exert their effect via the neurosecretor
y
s
y
stem, that is, the
y
s
timulate or depress the s
y
nthesis/release of hormones from the brain. Probabl
y
the best
s
tu
di
e
d
o
f
t
h
ese var
i
a
bl
es are

f
ee
di
ng an
d
p
h
otoper
i
o
d.
In t
h
e
bl
oo
df
ee
d
ers R
h
o
d
niu
s
an
d
C
ime
x

a
n
di
n some sap-
f
ee
di
ng Hem
i
ptera,
f
or exam-
p
l
e,
O
nco
p
e
l
tus,w
h
ose
f
oo
di
s
highly
cons
i

stent
i
n nature, en
g
or
g
ement causes
di
stens
i
on
o
f the abdominal wall and initiates a molt c
y
cle. Information from stretch receptors in th
e
w
all passes alon
g
the ventral nerve cord to the brain where neurosecretor
y
cells are acti-
v
ated to release PTTH. In insects that feed more or less continuously through the stadium,
a
l
so, t
h
e
i

nta
k
eo
ff
oo
di
s pro
b
a
bl
yan
i
mportant st
i
mu
l
us
f
or t
h
ere
l
ease o
f
neurosecret
i
on
.
L
ocusta mi

g
ratoria,
f
or examp
l
e,
h
as stretc
h
receptors
i
nt
h
ewa
ll
o
f
t
h
ep
h
arynx, w
hi
c
h
are
s
timulated as food passes throu
g
h the fore

g
ut. Information from the receptors reaches the
∗
Th
e name
d
er
i
ves
f
rom t
h
e
f
act t
h
at t
h
e gene
(
us
p) pro
d
uc
i
ng t
hi
s prote
i
na

l
so
h
as ot
h
er
d
eve
l
opmenta
l
ro
l
es
.
Wh
en
i
tma
lf
unct
i
ons
,in
D
rosop
h
i
la
,t

h
e
l
arva
d
eve
l
o
p
s an extra
p
a
i
ro
fp
oster
i
or s
pi
rac
l
es.
6
4
3
P
OS
TEMBRY
O
NI

C
DEVEL
O
PMEN
T
b
rain-corpora cardiaca complex via the stomato
g
astric nervous s
y
stem (Clarke and Lan
g
le
y,
19
6
3
).
I
n continuous feeders it is often necessar
y
for an insect to achieve a minimal nutritional
status or
b
o
d
ywe
i
g
h

t
b
e
f
ore a new mo
l
tcyc
l
e
i
s
i
n
i
t
i
ate
d
.T
hi
s may
b
e espec
i
a
ll
y
i
mportant
f

or spec
i
es w
h
ose
di
et
i
svar
i
a
bl
e. In ot
h
er wor
d
s,
d
ur
i
ng eac
h
sta
di
um t
h
ere
i
san
i

n
i
t
i
a
l
per
i
o
d
o
f
o
blig
ate
f
ee
di
n
g
,w
hi
c
h
resu
l
ts
i
n acqu
i

s
i
t
i
on o
f
t
h
em
i
n
i
ma
l
nutr
i
t
i
ve requ
i
rement
s
(and release of sufficient PTTH to tri
gg
er a molt c
y
cle), followed b
y
a phase of facultative
feedin

g
, the nutritive contribution from which
g
ives rise to lar
g
er larvae.
P
h
otoper
i
o
di
s anot
h
er
i
mportant env
i
ronmenta
lf
actor
i
nt
h
eregu
l
at
i
on o
f

growt
h
an
d
mo
l
t
i
ng, part
i
cu
l
ar
l
y
i
nre
l
at
i
on to
di
apause, a more or
l
ess pro
l
onge
d
con
di

t
i
on o
f
arreste
d
d
eve
l
opment, w
hi
c
h
ena
bl
es
i
nsects to surv
i
ve per
i
o
d
so
f
a
d
verse con
di
t

i
ons (C
h
apter 22,
Section 3.2). Members of most species studied enter diapause when the dail
y
amount of li
g
ht
t
o which the
y
are exposed falls below a certain value (usuall
y
14–16 hours). In diapause,
an insect is physiologically “turned-off”; generally, it does not feed or move actively, an
d
i
ts meta
b
o
li
c rate
i
sa
b
norma
ll
y
l

ow. T
h
ese e
ff
ects resu
l
t
f
rom
i
nact
i
v
i
ty o
f
t
h
een
d
ocr
i
ne
system. In a manner t
h
at
i
s not c
l
ear, s

h
ort
d
ay
l
engt
h
s
l
ea
d
to re
d
uce
d
neurosecretory
activit
y
that, in turn, results in inactivit
y
of molt
g
lands and corpora allata. Conversel
y,
d
iapause is terminated as the da
y
len
g
th increases be

y
ond a certain point in sprin
g
, because
of renewed endocrine activity. In members of some species, however, the neurosecretor
y
system must
b
e expose
d
to
l
ow temperatures
f
oracr
i
t
i
ca
ll
engt
h
o
f
t
i
me
d
ur
i

ng
di
apaus
e
b
e
f
ore
i
t can respon
d
to
i
ncreas
i
ng
d
ay
l
engt
h
(C
hi
ppen
d
a
l
e, 1977)
.
I

n some insects, the “feel” of the surroundin
g
s is important for continued norma
l
d
evelopment. For example, larvae of the wheatstem sawfl
y
,
C
e
p
hus cinctus
,
will not
p
u
p
at
e
if removed from the cavit
y
at the base of the stem. Larvae of the squash fl
y
, Zeugoducus
d
epressu
s
,l
iv
ei

nt
h
ecav
i
ty o
f
squas
h
w
h
ere t
h
e car
b
on
di
ox
id
e concentrat
i
on
i
s
i
n
i
t
i
a
lly

about 4% to
6
%. Pupation is delayed by this concentration of gas and will not occur until th
e
level falls to about 1%, some
6
months later. This dela
y
serves to s
y
nchronize the emer
g
enc
e
of adult flies with the openin
g
of the squash flowers (in which e
gg
s are laid) the followin
g
season.
S
t
ill
re
l
at
i
ve
l

y unexp
l
ore
d
are t
h
ec
h
anges o
f
en
d
ocr
i
ne act
i
v
i
ty an
d
ot
h
er events t
h
a
t
b
r
i
ngamo

l
t
i
ng cyc
l
etoac
l
ose w
i
t
h
t
h
es
h
e
ddi
ng o
f
t
h
eo
ld
cut
i
c
l
e. Certa
i
n

l
y negat
i
v
e
f
ee
db
ac
k
pat
h
ways ex
i
st so t
h
at w
h
en t
h
e concentrat
i
on o
f
c
i
rcu
l
at
i

ng
h
ormone reac
h
es a
critical level, the activit
y
of the
g
land producin
g
it is depressed. The pathwa
y
ma
y
be direct,
t
hat is, the hormone itself depresses
g
landular activit
y
. Alternativel
y
, circulatin
g
ecd
y
sone
and JH may inhibit the activity of the PTTH- and allatotropic hormone-producing cells,
respect

i
ve
l
y.At
hi
r
d
poss
ibili
ty
i
st
h
at
h
ormone
l
eve
l
s are mon
i
tore
db
yc
h
emoreceptors,
whi
c
h
sen

d
t
h
e
i
n
f
ormat
i
on v
i
a sensory neurons to t
h
e
b
ra
i
n. Re
d
uct
i
on
i
n act
i
v
i
ty o
f
t

he
molt
g
lands and/or corpora allata mi
g
ht then be brou
g
ht about via the nerves to the
g
lands.
The com
p
lex behaviors that enable an insect to esca
p
e from the old exuvium are
coordinated by the interplay of several hormones, including 20-HE, eclosion hormone (EH),
pre-ec
d
ys
i
s-tr
i
gger
i
ng
h
ormone (PETH), ec
d
ys
i

s-tr
i
gger
i
ng
h
ormone (ETH), crustacean
cardioactive peptide (CCAP), and bursicon (Truman, 198
5
, 1990, 1992; Reynolds, 1986;
Horod
y
ski, 199
6
;M
y
ers, 2003). Onl
y
when the 20-HE level falls below a threshold value ca
n
moltin
g
occur, for two reasons. First, the tar
g
et tissues for EH onl
y
acquire their competenc
e
t
o respond and, second, EH release onl

y
occurs at ver
y
low 20-HE concentrations. EH i
s
p
ro
d
uce
di
nt
h
eC
hi
nese oa
k
s
ilk
mot
h,
A
nt
h
eraea pern
yi
,an
d
ot
h
er saturn

iid
mot
h
s
b
y
neurosecretory ce
ll
s
i
nt
h
e ventra
l
part o
f
t
h
e
b
ra
i
n. In
l
arva
li
nstars t
h
ese ce
ll

sre
l
ease E
H
at neuro
h
ema
l
or
g
ans on t
h
e
hi
n
dg
ut;
h
owever,
i
nt
h
ep
h
arate a
d
u
l
tt
h

e neurosecretor
y
ce
lls
6
44
CHAPTER
21
F
IGURE 21.14. Sc
h
eme
f
or t
h
e
h
ormona
l
contro
l
o
f
mo
l
t
i
ng. A
bb
rev

i
at
i
ons: CCAP, crustacean car
di
oact
i
ve
pept
id
e; EH, ec
l
os
i
on
h
ormone; ETH, ec
dy
s
i
s-tr
igg
er
i
n
gh
ormone; PETH, pre-ec
dy
s
i

s-tr
igg
er
i
n
gh
ormone. [A
f
ter
R
. F. Chapman, 1998, The Insects:
S
tructure and Function (4th ed.). Reprinted with the permission of Cambridge
Un
i
vers
i
ty Press.
]
are restructured and terminate in the corpora cardiaca. For about 25 years after its discover
y
i
nt
h
e ear
l
y 1970s, EH was t
h
oug
h

tto
b
et
h
eon
l
y
h
ormone
i
nvo
l
ve
di
nt
h
e
i
n
i
t
i
at
i
on o
f
t
h
e
v

a
r
i
ous
b
e
h
av
i
ors an
d
p
h
ys
i
o
l
og
i
ca
l
events t
h
at encompass t
h
es
h
e
ddi
ng o

f
t
h
e exuv
i
um
.
H
owever, it is now apparent that release of EH is but one step in a complex hormona
l
c
ascade
(
ˇ
Z
i
t
ˇn
a
n
et al.
, 1996;
ˇ
Zitˇnan and Adams, 2000
).
ˇ
Zitˇnan and Adams (2000) have proposed the followin
g
model for the control of moltin
g

,
whi
c
hi
nc
l
u
d
es t
h
ree p
h
ases: pre-ec
d
ys
i
s I, pre-ec
d
ys
i
s II, an
d
ec
d
ys
i
s(F
i
gure 21.14). T
he

b
e
h
av
i
ora
l
sequence
i
s
i
n
i
t
i
ate
d
w
h
en
l
ow
l
eve
l
so
f
EH are re
l
ease

d
.T
h
eEH
i
n
d
uce
s
P
ETH an
d
ETH secret
i
on
f
rom t
h
eIn
k
ace
ll
s(C
h
apter 13, Sect
i
on 3.4). PETH acts on
the abdominal
g
an

g
lia to tri
gg
er pre-ecd
y
sis I; that is, it causes motor neurons to fire
,
b
rin
g
in
g
about stron
g
dorsoventral muscle contractions in the bod
y
wall. ETH has two
eff
ects. F
i
rst,
b
y pos
i
t
i
ve
f
ee
db

ac
ki
t causes
f
urt
h
er, mass
i
ve re
l
ease o
f
EH (an
d
,
i
n turn
,
m
ore ETH),
l
eve
l
so
f
w
hi
c
h
pea

k
a
b
out 1
h
our
b
e
f
ore mo
l
t
i
ng occurs. Secon
d
,
i
t
i
n
d
uces
(
a
l
so
by
act
i
n

g
on t
h
ea
bd
om
i
na
lg
an
gli
a) pre-ec
dy
s
i
s II (stron
g
poster
i
oventra
l
an
d
pro
l
e
g
m
uscle contractions). The hi
g

h level of EH has both direct and indirect effects related to
6
4
5
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
moltin
g
. First, EH released from the tips of neurosecretor
y
axons within the abdominal
g
an
g
lia stimulates other neurons to release CCAP, which controls the initiation of the thir
d
phase, ecd
y
sis. CCAP switches off pre-ecd
y
sis I and II, then activates motor neurons that
contro

l
t
h
eswa
ll
ow
i
ng o
f
a
i
r,
h
eart
b
eat, an
d
s
k
e
l
eta
l
musc
l
e
f
unct
i
ons. Toget

h
er, t
h
es
e
act
i
ons
l
ea
d
to t
h
esp
li
tt
i
ng o
f
t
h
eo
ld
cut
i
c
l
e, wr
i
gg

li
ng
f
ree, an
d
expans
i
on o
f
t
h
enew
cuticle and win
g
s. In addition, EH released into the hemol
y
mph causes parts of the cuticle
t
o plasticize, stimulates the cement-producin
g
(Verson’s)
g
lands to dischar
g
e, and is a si
g
nal
for release of bursicon. As described in Cha
p
ter 11 (Section 3.4), bursicon has im

p
ortant
ro
l
es
i
n tann
i
ng o
f
t
h
e cut
i
c
l
e. It a
l
so appears to
b
e
i
nvo
l
ve
di
n cut
i
c
l

ep
l
ast
i
c
i
zat
i
on an
d
th
e
d
egenerat
i
on o
f
spec
ifi
c musc
l
es an
d
neurons. Ot
h
er processes
i
nw
hi
c

hb
urs
i
con may
p
l
a
y
aro
l
e
i
nc
l
u
d
e postec
dy
s
i
a
l
cut
i
c
l
e
d
epos
i

t
i
on, postec
dy
s
i
a
ldi
ures
i
s, an
d
trac
h
ea
l
a
i
r-
fi
llin
g
(Re
y
nolds, 198
6
). In some insects that must wri
gg
le to the surface of the substrate i
n

w
hich the
y
pupated, proprioceptive stimuli are also important. These inhibit earl
y
release
o
fb
urs
i
con, so t
h
at premature tann
i
ng o
f
t
h
ea
d
u
l
t cut
i
c
l
e
i
s avo
id

e
d
.
T
h
ea
b
ove mo
d
e
li
s
b
ase
dl
arge
l
yon
d
ata
f
rom exper
i
ments w
i
t
h
Lep
id
optera, espec

i
a
ll
y
Man
d
uca
s
ext
a
.H
o
w
ev
e
r
,b
ot
h
EH an
d
ETH
h
ave
b
een s
h
own to occur
i
n

l
arvae
f
rom
a
w
ide ran
g
e of insect orders (Truman
et al.
, 1981;
ˇ
Zitˇna
n
et al.
, 2003), su
gg
estin
g
that thi
s
mechanism for hormonal control of ecd
y
sis has been conserved across the Class.
7. Pol
y
mor
p
h
i

sm
Pol
y
morphism, the existence of several distinct forms of the same life sta
g
eofanor
-
ganism, though not a common phenomenon in insects, occurs in representatives of sev
-
era
l
w
id
e
l
y
diff
erent or
d
ers. T
h
ep
h
ases o
fl
ocusts (Ort
h
optera) an
d
some caterp

ill
ars
(Lep
id
optera), castes o
f
soc
i
a
li
nsects (Isoptera an
d
H
y
menoptera), w
i
n
g
po
ly
morp
hi
sm
in crickets (Orthoptera), aphids and other Hemiptera, and color pol
y
morphism of mimetic
b
utterflies (Lepidoptera) are examples of insect pol
y
morphism. Thou

g
h these examples
refer only to difference of form, it should be appreciated that the physiology, behavior, an
d
eco
l
ogy o
f
t
h
ese
f
orms are a
l
so
diff
erent (App
l
e
b
aum an
d
He
if
etz, 1999)
.
Po
l
ymorp
hi

sm,
lik
e
diff
erent
i
at
i
on,
h
as a genet
i
c
b
as
i
s. In some examp
l
es o
f
po
l
ymor
-
phism, such as the color forms of butterflies and moths, the
g
enetic s
y
stem is relativel
y

little influenced b
y
short-term chan
g
es in environmental conditions. This so-called “
g
eneti
c
(obligate) polymorphism” includes transient polymorphism, the situation in which a trai
t
i
s sprea
di
ng t
h
roug
h
a popu
l
at
i
on (e.g., me
l
an
i
sm
i
nt
h
e peppere

d
mot
h
, Bi
s
ton
b
etu
l
ari
a
),
an
db
a
l
ance
d
po
l
ymorp
hi
sm w
h
ere a tra
i
t
i
sma
i

nta
i
ne
d
at a constant
f
requency
i
nt
h
e pop-
u
lation b
y
opposin
g
selection pressures [e.
g
., mimicr
y
b
y
the (edible) vicero
y
butterfl
y
of
t
he (distasteful) monarch butterfl
y

(Fi
g
ure 9.15)]. At the opposite extreme is “phenot
y
pic
(facultative) polymorphism” (now commonly referred to as “polyphenism”) in which th
e
d
eve
l
opment o
f
c
h
aracters
i
s great
l
y
i
n
fl
uence
db
yc
h
ang
i
ng env
i

ronmenta
l
con
di
t
i
ons an
d
i
s man
if
est w
i
t
hi
na
f
ew generat
i
ons (e.g., caste po
l
ymorp
hi
sm, p
h
ase po
l
ymorp
hi
sm, an

d
w
in
g
pol
y
morphism). The chan
g
in
g
environmental conditions exert their influence via th
e
neuroendocrine s
y
stem; in other words, it is chan
g
es in the hormonal milieu that lead to
polyphenism, particularly changes in the level of JH, as will be shown in the examples
d
escr
ib
e
db
e
l
ow (N
ijh
out an
d
W

h
ee
l
er, 1982).
Ap
hid
po
l
ymorp
hi
sm
i
s a comp
l
ex p
h
enomenon
f
or,
i
na
ddi
t
i
on to extens
i
ve structura
l
pol
y

morphism (some species include as man
y
as ei
g
ht distinct forms) (Fi
g
ure 21.1
5
) and the
ph
y
siolo
g
ical pol
y
morphism that accompanies it, there is also “temporal” or “successive
”
6
4
6
CHAPTER
21
F
IGURE 21.15
.
F
orms o
f
t
h

e vetc
h
a
phid
.
M
egoura v
i
c
i
ae.T
h
e
f
un
d
atr
i
x
(
A
),
a parthenogenetic female that emerge
s
f
rom t
h
e overw
i
nter

i
ng egg, pro
d
uce
s
th
e
f
un
d
atr
ig
en
i
ae (B)
f
rom w
hi
c
h
man
y
generations of wingless (C) or winged
(
D) v
i
rg
i
noparae
d

eve
l
op. In
l
ate summer,
wi
n
gl
ess e
gg
-
l
a
yi
n
g
ov
i
parae (E) an
d
ma
l
e
s
(
F) are formed. [From A. O. Lees, 1961,
C
l
ona
l

po
l
ymorp
hi
sm
i
nap
hid
s,
S
ymp. R
.
Entomo
l
.
S
oc
.
1
:
6
8–79. B
y
permission of
t
he Royal Entomological Society.
]
polyphenism in which these structural and physiological features gradually change fro
m
generation to generation (Lees, 1966; Hardie and Lees, 198

5
). Aphids reproduce partheno
-
genet
i
ca
ll
y (an
di
n some spec
i
es pae
d
ogenet
i
ca
ll
y)
f
or a
l
arge part o
f
t
h
e year, g
i
v
i
ng r

i
s
e
to lar
g
e numbers of win
g
less individuals that can exploit the rich food supplies available i
n
sprin
g
and summer. However, to avoid starvation caused b
y
overcrowdin
g
,tomovetonu
-
tritionall
y
more valuable food sources, and to reproduce sexuall
y
, it is necessar
y
for win
g
e
d
i
n
di

v
id
ua
l
s(a
l
ates) to
d
eve
l
o
p.
Th
e
d
eve
l
opment o
f
a
l
ates
i
s
i
n
fl
uence
db
y many env

i
ronmenta
lf
actors,
f
or examp
l
e,
p
h
otoper
i
o
d
, temperature, popu
l
at
i
on
d
ens
i
t
y
,an
d
water content o
ff
oo
d

p
l
ants, a
ll
o
f
w
hi
c
h
ultimatel
y
appear to brin
g
about chan
g
es in endocrine activit
y
. Thus, treatment of presump
-
tive gynoparae (a winged migrant form) of the bean aphid (
Aphis fabae
(
(
) with JH mimic
s
t
h
ee
ff

ects o
fl
ong-
d
ay con
di
t
i
ons, caus
i
ng t
h
em to mo
l
ttow
i
ng
l
ess a
d
u
l
ts an
d
to s
h
ow
a
pre
f

erence
f
or t
i
c
b
ean (
V
icia
f
a
b
ae
)
,
t
h
e
i
r norma
l
summer
h
ost. Converse
l
y, top
i
ca
l
app

li
-
c
at
i
on o
f
precocene (w
hi
c
hd
estro
y
st
h
e corpus a
ll
atum) to w
i
n
g
e
d
a
d
u
l
ts o
f
ot

h
er spec
i
e
s
stimulates production of win
g
ed pro
g
en
y
. In some species these environmental factors ac
t
6
4
7
P
OS
TEMBRY
O
NI
C
DEVEL
O
PMEN
T
d
irectl
y
on an individual to modif

y
its form, whereas in others the effect is not seen until the
followin
gg
eneration. For example, when first- or, to a lesser extent, second-instar larvae o
f
t
he
g
reen peach aphid (Myzus pers
i
cae
)
are kept under crowded conditions, the
y
develop
i
nto w
i
nge
df
orms. In contrast,
i
nt
h
e vetc
h
ap
hid (
M

e
g
oura v
i
c
i
ae) crow
di
ng young
l
arvae
d
oes not
i
n
d
uce w
i
ng
d
eve
l
opment e
i
t
h
er
i
nt
h

e
l
arvae or
i
nt
h
e
i
r progeny. In t
hi
s spec
i
es,
sens
i
t
i
v
i
t
y
to crow
di
n
gd
eve
l
ops
i
nt

h
e
f
ourt
h
(
fi
na
l
)
i
nstar an
di
s reta
i
ne
d
t
h
rou
gh
a
d
u
l
t
-
h
ood. Thus, when older larvae or win
g

less adults are crowded, their pro
g
en
y
are win
g
ed
.
E
x
p
eriments have indicated that the stimulus is not visual or chemical but due to re
p
eate
d
p
h
ys
i
ca
l
contact
b
etween
i
n
di
v
id
ua

l
s. Interest
i
ng
l
y, ants t
h
at ten
d
ap
hid
s
f
or t
h
e
i
r
h
oney
-
d
ew
h
ave a “tranqu
ili
z
i
ng” e
ff

ect on t
h
eap
hid
s. T
hi
se
ff
ect apparent
l
y
l
ea
d
store
d
uct
i
o
n
i
nt
h
e amount o
f
p
h
ys
i
ca

l
contact
b
etween t
h
eap
hid
s, w
hi
c
h
t
h
us rema
i
n apterous, to t
he
ants’ obvious advanta
g
e. It is presumed that the crowdin
g
stimulus operates via the brain,
w
hich somehow reduces corpus allatum activit
y
. The nature of the link between the brain
and corpus allatum is not known but is likely to be hormonal because in species such as
M.
vi
c

i
ae
th
e crow
di
ng st
i
mu
l
us
i
s rece
i
ve
db
yt
h
e materna
lb
ra
i
n,
b
ut
i
ts e
ff
ect
i
sma

d
e
apparent
i
nt
h
e progeny. In ot
h
er wor
d
s,
i
t
i
st
h
e corpora a
ll
ata o
f
t
h
e
d
eve
l
op
i
ng em
b

ryos
w
ithin the mother whose activit
y
is modified,
y
et there is no nervous connection betwee
n
t
hese
g
lands and the mother’s brain (Lees, 1966).
I
n colonies of social insects, individuals fall into a number of functionally and, usu
-
a
ll
y, structura
ll
y
di
st
i
nct castes. In
l
ower term
i
tes,
f
or examp

l
e, t
h
ere
i
sapa
i
ro
f
pr
i
mar
y
repro
d
uct
i
ves (
ki
ng an
d
queen) w
hi
c
hf
oun
d
t
h
eco

l
ony, supp
l
ementary (rep
l
acement) re
-
productives which develop as the colon
y
reaches a certain size and eventuall
y
take over
t
he reproductive function, soldiers, n
y
mphs (
j
uveniles with win
g
buds from which primar
y
reproductives develop), and larvae (
j
uveniles that lack win
g
buds). Each caste contain
s
mem
b
ers o

fb
ot
h
sexes. T
h
e num
b
er o
fi
n
di
v
id
ua
l
s
b
e
l
ong
i
ng to eac
h
caste
i
s norma
ll
y
ma
i

nta
i
ne
d
as a
fi
xe
d
proport
i
on o
f
t
h
e tota
l
num
b
er o
fi
nsects
i
nt
h
eco
l
ony
b
y means o
f

i
n
hibi
tor
y
p
h
eromones secrete
dby
a
l
rea
dy diff
erent
i
ate
di
n
di
v
id
ua
l
s(C
h
apter 13, Sect
i
ons
4
.1.1 and 4.1.2). When the concentration of a pheromone falls below a certain level, resultin

g
from, for example,
g
rowth of the colon
y
or death of the pheromone-producin
g
individuals,
i
n
hibi
t
i
on no
l
onger occurs, an
d diff
erent
i
at
i
on o
f
new
i
n
di
v
id
ua

l
s restores t
h
e correct pro-
port
i
on. T
h
ere
l
at
i
ons
hi
po
f
t
h
e castes an
d
t
h
e course o
fd
eve
l
opment
i
na
l

ower term
i
te,
Z
ootermopsis an
g
ustico
ll
i
s
,
are indicated in Figure 21.1
6
. Young larvae pass through sev-
eral pro
g
ressive molts (i.e.,
g
row and differentiate) until the
y
become pseuder
g
ates (fals
e
w
orkers) comparable with the true workers of hi
g
her termites. Pseuder
g
ates ma

y
under
go
additional progressive molts to form specific castes, or may molt without differentiation
(stationary molts) (Yin and Gillott, 197
5
).
T
h
e
i
n
hibi
tory p
h
eromones
i
n
fl
uence caste
diff
erent
i
at
i
on
b
ymo
dif
y

i
ng t
h
e act
i
v
i
ty o
f
t
he endocrine s
y
stem, especiall
y
the corpora allata. The extensive studies of L¨uscher and
h
is associates in the 1950s led to the development of an elaborate h
y
pothesis for hormona
l
control (see Hardie and Lees, 1985). This included the suggestion that the corpora al1ata
pro
d
uce
d
t
h
ree
di
st

i
nct
h
ormones: JH,
f
or contro
l
o
fj
uven
il
e
→
j
uven
il
ean
dj
uven
il
e
→
ad
u
l
t
diff
erent
i
at

i
on (as
i
n non-po1ymorp
hi
c
i
nsects); so
ldi
er-
i
n
d
uc
i
ng
h
ormone t
h
at pro
-
mote
d
so
ldi
er
f
ormat
i
on; an

dg
ona
d
otrop
i
c
h
ormone, w
hi
c
h
was pro
d
uce
di
na
d
u
l
t
f
ema
l
e
s
t
o control ooc
y
te development
.

A
s a result of subsequent work b
y
L¨uscher’s
g
roup and other authors, especiall
y
ex-
per
i
ments
i
nvo
l
v
i
ng app
li
cat
i
on o
f
JH ana
l
ogues,
i
t was rea
li
ze
d

t
h
at t
h
e corpora a
ll
ata
d
o
not pro
d
uce more t
h
an one
h
ormone. Rat
h
er, a
ll d
eve
l
opmenta
l
poss
ibili
t
i
es resu
l
t

f
rom
var
i
at
i
ons
i
nt
h
e concentrat
i
on o
f
c
i
rcu
l
at
i
n
g
JH at cr
i
t
i
ca
l
t
i

mes
d
ur
i
n
g
a sta
di
um. N
ijh
out