Entomology 3rd edition - C.Gillott - Chapter 2 ppt

2
Insect Diversit
y
1
. Intr
oduc
t
ion
I
n this chapter, we shall examine the evolutionar
y
development of the tremendous variet
y
of insects that we see toda
y
. From the limited fossil record it would appear that the earliest
insects were win
g
less, th
y
sanuranlike forms that abounded in the Silurian and Devonian pe
-
r
i
o
d
s. T
h
ema
j
or a

d
vance ma
d
e
b
yt
h
e
i
r
d
escen
d
ants was t
h
eevo
l
ut
i
on o
f
w
i
ngs,
f
ac
ili
tat
i
ng

di
spersa
l
an
d
,t
h
ere
f
ore, co
l
on
i
zat
i
on o
f
new
h
a
bi
tats. Dur
i
ng t
h
e Car
b
on
if
erous an

d
Per-
m
i
an per
i
o
d
st
h
ere was a mass
i
ve a
d
apt
i
ve ra
di
at
i
on o
f
w
i
n
g
e
df
orms, an
di

t was at t
hi
st
i
me
t
hat most of the modern orders had their be
g
innin
g
s. Althou
g
h members of man
y
of thes
e
orders retained a life histor
y
similar to that of their win
g
less ancestors, in which the chan
g
e
f
rom
j
uven
il
etoa
d

u
l
t
f
orm was gra
d
ua
l
(t
h
e
h
em
i
meta
b
o
l
ous or exopterygote or
d
ers),
i
n
ot
h
er or
d
ers a
lif
e

hi
story evo
l
ve
di
nw
hi
c
h
t
h
e
j
uven
il
ean
d
a
d
u
l
tp
h
ases are separate
db
y
a
pupa
l
sta

g
e(t
h
e
h
o
l
ometa
b
o
l
ous or en
d
opter
yg
ote or
d
ers). T
h
e
g
reat a
d
vanta
g
eo
fh
av
i
n

g
a
pupal sta
g
e (althou
g
h this is neither its ori
g
inal nor its onl
y
si
g
nificance) is that the
j
uvenile
and adult sta
g
es can become ver
y
different from each other in their habits, thereb
y
avoidin
g
compet
i
t
i
on
f
or t

h
e same resources. T
h
eevo
l
ut
i
on o
f
w
i
ngs an
dd
eve
l
opment o
f
a pupa
l
stage
h
ave
h
a
d
suc
h
a pro
f
oun

d
e
ff
ect on t
h
e success o
fi
nsects t
h
at t
h
ey w
ill b
e
di
scusse
d
as separate top
i
cs
i
n some
d
eta
il b
e
l
ow .
2. Pr
i

m
i
t
i
ve W
i
ngless Insect
s
The earliest win
g
less insects to appear in the fossil record are Microcor
y
phia
(Archeognatha) (bristletails) from the Lower Devonian of Quebec (Labandeir
a
et al.
, 1988)
an
d
M
iddl
eDevon
i
an o
f
New Yor
k
(S
h
ea

r
et a
l.
,
1984). T
h
ese, toget
h
er w
i
t
hf
oss
il
Monura
(F
i
gure 2.1A) an
d
Zygentoma (s
il
ver
fi
s
h
)(F
i
gure 2.1B)
f
rom t

h
e Upper Car
b
on
if
erous an
d
Permian periods, constitute a few remnants of an ori
g
inall
y
extensive apter
yg
ote fauna that
existed in the Silurian and Devonian periods. Primitive features of the microcor
y
phians
include the monocondylous mandibles which exhibit segmental sutures, fully segmented
(
i
.e.,
l
eg
lik
e) max
ill
ary pa
l
ps w
i

t
h
two term
i
na
l
c
l
aws, a
di
st
i
nct r
i
ng
lik
esu
b
coxa
l
segment
on t
h
e meso- an
d
metat
h
orax (
i
na

ll
rema
i
n
i
ng Insecta t
hi
s
b
ecomes
fl
attene
d
an
df
orms
part of the pleural wall), undivided cercal bases, and an ovipositor that has no
g
onan
g
ulum.
2
5
26
CHAPTER
2
m
s-
a
r-

t
h
e
7
–
o
r.]
The earl
y
bristletails, like their modern relatives, perhaps fed on al
g
ae, lichens, and debris
.
The
y
escaped from predators b
y
runnin
g
and
j
umpin
g
, the latter achieved b
y
abrupt flexin
g
o
f the abdomen
.

M
onura are un
i
que among Insecta
i
nt
h
at t
h
ey reta
i
n cerca
ll
egs (Ku
k
a
l
ov´a-Pec
k
,
1
98
5
). Other primitive features of this group are the segmented head, fully segmente
d
m
ax
ill
ar
y

an
dl
a
bi
a
l
pa
l
ps,
l
ac
k
o
f diff
erent
i
at
i
on o
f
t
h
et
h
orac
i
cse
g
ments, se
g

mente
d
abdominal le
g
lets, the lon
g
caudal filament, and the coatin
g
of sensor
y
bristles over the bod
y
(
Kukalov´a-Peck, 1991). Features the
y
share with the Z
yg
entoma and Pter
yg
ota are dicond
y-
l
ous man
dibl
es, we
ll
-sc
l
erot
i

ze
d
t
h
orac
i
cp
l
eura, an
d
t
h
e gonangu
l
um,
l
ea
di
ng Ku
k
a
l
ov´a-
P
ec
k
(1987) to suggest t
h
at t
h

e Monura are t
h
es
i
ster group o
f
t
h
e Zygentoma
+
P
terygota
.
Carpenter (1992),
h
owever,
i
nc
l
u
d
e
d
t
h
e Monura as a su
b
or
d
er o

f
t
h
eM
i
crocor
y
p
hi
a. S
h
ea
r
and Kukalov´a-Peck (1990) su
gg
ested, on the basis of their morpholo
gy
, that monurans
probabl
y
lived in swamps, climbin
g
on emer
g
ent ve
g
etation, and feedin
g
on soft mat-
ter. Escape

f
rom pre
d
ators may
h
ave occurre
d
,as
i
nt
h
eM
i
crocoryp
hi
a,
b
y runn
i
ng an
d
j
ump
i
ng
.
In contrast to t
h
e
i

r rap
idl
y runn
i
ng, mo
d
ern re
l
at
i
ves, t
h
e ear
l
ys
il
ver
fi
s
h
,
f
or examp
l
e
,
the
6
-cm-lon
g.

Ramsdele
p
idion schuster
i
(
Fi
g
ure 2.1B), with their weak le
g
s, probabl
y
av
oided predators b
yg
enerall
y
remainin
g
concealed. When exposed, however, the numer
-
o
us long bristles that covered the abdominal leglets, cerci, and median filament may hav
e
prov
id
e
d
a
hi
g

hl
y sens
i
t
i
ve, ear
l
y warn
i
ng system. O
f
part
i
cu
l
ar
i
nterest
i
nany
di
scuss
i
on
of
apterygote re
l
at
i
ons

hi
ps
i
st
h
e extant s
il
ver
fi
s
h
Tric
h
o
l
epi
d
ion
g
ertsc
hi
,di
scovere
di
n
California in 19
6
1. The species is sufficientl
y
different from other recent Z

yg
entoma that
i
t is placed in a separate famil
y
Lepidotrichidae, to which some Oli
g
ocene fossils als
o
belon
g
. Indeed, Tricholepidion
p
ossesses a number of features common to both Microco
-
ryphia and Monura (see Chapter
5
, Section 6), leading Sharov (1966) to suggest that the
f
amily to which it belongs is closer than any other to the thysanuranlike ancestor of the
f
f
P
ter
yg
ota
.
27
IN
S

E
C
TDI
V
ER
S
IT
Y
3
. Evolution of Win
g
ed Insects
3.1. Ori
g
in and Evolution of Win
g
s
T
h
eor
i
g
i
no
fi
nsect w
i
ngs
h
as

b
een one o
f
t
h
e most
d
e
b
ate
d
su
bj
ects
i
n entomo
l
ogy
f
or
c
l
ose to two centur
i
es, an
d
even to
d
ay t
h

e quest
i
on rema
i
ns
f
ar
f
rom
b
e
i
ng answere
d
. Most
authors a
g
ree, in view of the basic similarit
y
of structure of the win
g
s of insects, both fossil
and extant, that win
g
s are of monoph
y
letic ori
g
in; that is, win
g

s arose in a sin
g
le
g
roup o
f
ancestral apterygotes. Where disagreement occurs is with respect to (1) whether the win
g
precursors (pro-w
i
ngs) were
f
use
d
to t
h
e
b
o
d
y or were art
i
cu
l
ate
d
; (2) t
h
e pos
i

t
i
on(s) o
n
th
e
b
o
d
yatw
hi
c
h
pro-w
i
ngs
d
eve
l
ope
d
(an
d
,re
l
ate
d
to t
hi
s,

h
ow many pa
i
rs o
f
pro-w
i
ng
s
ori
g
inall
y
existed); (3) the ori
g
inal functions of pro-win
g
s; (4) the selection pressures that
led to the formation of win
g
s from pro-win
g
s; and (5) the nature of the ancestral insects;
t
hat is, were they terrestrial or aquatic, were they larval or adult, and what was their size
(Wootton, 1986, 2001; Brodsky, 1994; Kingsolver and Koehl, 1994).
At t
h
e core o
f

a
ll
t
h
eor
i
es on t
h
eor
i
g
i
no
f
w
i
ngs
i
st
h
e matter o
f
w
h
et
h
er t
h
e pro
-

w
in
g
s initiall
y
were out
g
rowths of the bod
y
wall (i.e., non-articulated structures) or were
h
in
g
ed flaps. Althou
g
h there have been several proposals for win
g
ori
g
in based on non-
articulated pro-wings (see Kukalov´a-Peck, 1978), undoubtedly the most popular of these
is the Paranotal Theory, suggested by Woodward (1876, cited in Hamilton, 1971), and sup-
ported by Sharov (19
66
), Hamilton (1971), Wootton (197
6
), Rasnitsyn (1981), and others.
T
he theor
y

is based on three pieces of evidence: (1) the occurrence of ri
g
id ter
g
al out
g
rowth
s
(win
g
pads) on modern larval exopter
yg
otes (onto
g
en
y
recapitulatin
g
ph
y
lo
g
en
y
); (2) th
e
occurrence in fossil insects, both winged (Figure 2.5) and wingless (Figure 2.1B), of large
paranota
ll
o

b
es w
i
t
h
a venat
i
on s
i
m
il
ar to t
h
at o
f
mo
d
ern w
i
ngs; an
d
(3) t
h
e assume
dh
omo
l
-
ogy o
f

w
i
ng pa
d
san
dl
atera
l
a
bd
om
i
na
l
expans
i
ons,
b
ot
h
o
f
w
hi
c
hh
ave r
i
g
id

connect
i
on
s
w
ith the ter
g
a and, internall
y
, are in direct communication with the hemol
y
mph
.
Essentiall
y
the theor
y
states that win
g
s arose from ri
g
id, lateral out
g
rowths (paranota)
of the thoracic ter
g
a that became enlar
g
ed and, eventuall
y

, articulated with the thorax. I
t
p
resumes t
h
at, w
h
ereas t
h
ree
p
a
i
rs o
fp
aranota
ll
o
b
es were
id
ea
lf
or att
i
tu
di
na
l
contro

l
(se
e
b
e
l
ow), on
l
ytwopa
i
rs o
ffl
app
i
ng w
i
ngs were necessary to prov
id
e a mec
h
an
i
ca
ll
ye
ffi
c
i
en
t

s
y
stem
f
or
fligh
t. (In
d
ee
d
,as
i
nsects
h
ave e vo
l
ve
d
t
h
ere
h
as
b
een a tren
d
towar
d
t
h

ere
d
uct
i
o
n
of the number of functional win
g
s to one pair [see Chapter 3, Section 4.3.2]). This free
d
t
he prothorax for other functions such as protection of the membranous neck and servin
g
as a
b
ase
f
or attac
h
ment o
f
t
h
e musc
l
es t
h
at contro
lh
ea

d
mo
v
ement.
Var
i
ous suggest
i
ons
h
ave
b
een ma
d
e to account
f
or
d
eve
l
opment o
f
t
h
e paranota. For
example, Alexander and Brown (19
6
3) proposed that the lobes functioned ori
g
inall

y
as
or
g
ans of epi
g
amic displa
y
or as covers for pheromone-producin
gg
lands. Whalle
y
(1979
)
and Dou
g
las (1981) su
gg
ested a role in thermore
g
ulation for the paranota, an idea that
h
as received support from the experiments of Kingsolver and Koehl (1985) using models
.
M
ost aut
h
ors,
h
owever,

h
ave tra
di
t
i
ona
ll
y
b
e
li
eve
d
t
h
at t
h
e paranota arose to protect t
h
e
i
n-
sect, espec
i
a
ll
y, per
h
aps,
i

ts
l
egsorsp
i
rac
l
es. En
l
argement an
d
art
i
cu
l
at
i
on o
f
t
h
e paranota
l
lobes were associated with movement of the insect throu
g
h the air. Packard (1898, cited i
n
Wi
gg
lesworth, 1973) su
gg

ested that win
g
s arose in surface-dwellin
g
,
j
umpin
g
insects and
served as gliding planes that would increase the length of the jump. However, the almost
sync
h
ronous evo
l
ut
i
on o
fi
nsect w
i
ngs an
d
ta
ll
p
l
ants supports t
h
e
id

ea t
h
at w
i
ngs evo
l
ve
d
in insects living on plant foliage. Wigglesworth (19
6
3a,b) proposed that wings arose in
small aerial insects where li
g
ht cuticular expansions would facilitate takeoff and dispersal.
28
CHAPTER
2
The appearance later of muscles for movin
g
these structures would help the insect to lan
d
the ri
g
ht wa
y
up. Hinton (19
6
3a), on the other hand, ar
g
ued that the

y
evolved in somewha
t
l
ar
g
er insects and the ori
g
inal function of the paranota was to provide attitudinal control i
n
f
a
lli
ng
i
nsects. T
h
ere
i
sano
b
v
i
ous se
l
ect
i
ve a
d
vantage

f
or
i
nsects t
h
at can
l
an
d
“on t
h
e
i
r
f
eet,” over t
h
ose t
h
at cannot,
i
nt
h
e escape
f
rom pre
d
ators. As t
h
e paranota

i
ncrease
di
n
s
i
ze, t
h
e
y
wou
ld b
ecome secon
d
ar
ily i
mportant
i
n ena
bli
n
g
t
h
e
i
nsect to
glid
e
f

or a
g
reater
distance. Flower’s (19
6
4) theoretical stud
y
examined the h
y
potheses of both Wi
gg
leswort
h
and Hinton. Flower’s calculations showed that small pro
j
ections (rudimentar
y
paranotal
l
o
b
es) wou
ld h
avenos
i
gn
ifi
cant a
d
vantage

f
or very sma
ll i
nsects
i
n terms o
f
aer
i
a
ldi
s-
persa
l
. However, suc
h
structures wou
ld
con
f
er great a
d
vantages
i
n att
i
tu
di
na
l

contro
l
an
d
,
l
ater, g
lid
e per
f
ormance
f
or
i
nsects 1–2 cm
i
n
l
engt
h
.F
l
ower’s proposa
l
s
h
ave
b
een ex-
amined experimentall

y
throu
g
h the use of models (Kin
g
solver and Koehl, 1985; Wootto
n
and Ellin
g
ton, 1991; Ellin
g
ton, 1991; Hasenfuss, 2002). These studies have served to em
-
phasize the importance of the ancestral insect’s body size, as well as confirming that even
q
u
i
te sma
ll
pro
j
ect
i
ons cou
ld
contr
ib
ute to sta
bili
ty (a poss

ibl
ero
l
e
f
or appen
d
ages suc
h
as antennae,
l
egs, an
d
cerc
i
s
h
ou
ld
not
b
e
i
gnore
d
,
h
owever). Anot
h
er cons

id
erat
i
on
i
st
he
i
nsect’s speed on landin
g
(and whether the insect mi
g
ht be dama
g
ed). Ellin
g
ton’s (1991
)
anal
y
sis su
gg
ested that the win
g
lets mi
g
ht have been important in reducin
g
this termina
l

v
elocity, and there would be strong selection pressure to increase their size as a means o
f
f
urt
h
er re
d
uc
i
ng
l
an
di
ng spee
d.
In t
h
e Paranota
l
T
h
eory a cr
i
t
i
ca
l
step
i

nt
h
e trans
i
t
i
on
f
rom g
lidi
ng to
fl
app
i
ng
fli
g
ht
w
ould be the development of a hin
g
e so that the win
g
lets became articulated with the bod
y.
Most supporters would su
gg
est that this would occur simpl
y
to improve the insect’s control

o
f attitude or landin
g
speed, thou
g
h various non-aerod
y
namic functions ma
y
also have been
i
mprove
d
t
h
roug
h
t
h
e
d
eve
l
opment o
f
art
i
cu
l
ate

d
w
i
ng
l
ets. For examp
l
e, K
i
ngso
l
ver an
d
K
oehl (198
5
) noted the potential for more efficient thermoregulation that would arise fro
m
h
av
i
n
g
mova
bl
ew
i
n
gl
ets. Ot

h
er aut
h
ors
h
ave su
gg
este
d
t
h
at t
h
e
hi
n
g
eevo
l
ve
di
n
i
t
i
a
lly in
o
rder that the pro
j

ections could be folded alon
g
the side of the bod
y
, thereb
y
enablin
g
the
i
nsect to crawl into narrow spaces and thus avoid capture. Onl
y
later would the movement
s
b
ecome su
ffi
c
i
ent
l
y strong as to ma
k
et
h
e
i
nsect more or
l
ess

i
n
d
epen
d
ent o
f
a
i
r current
s
f
or
i
ts
di
str
ib
ut
i
on. In t
hi
s
h
ypot
h
es
i
st
h

e ear
li
est
fl
y
i
ng
i
nsects wou
ld
rest w
i
t
h
t
h
e
i
rw
i
ng
s
sprea
d
at r
i
g
h
t ang
l

es to t
h
e
b
o
d
y, as
d
omo
d
ern
d
ragon
fli
es an
d
may
fli
es. T
h
e
fi
na
l
ma
j
or
step in win
g
evolution was the development of win

g
foldin
g
, that is, the abilit
y
to draw
the win
g
s when at rest over the back. This abilit
y
would be stron
g
l
y
selected for, as it
w
ould confer considerable advantage on insects that possessed it, enabling them to hide i
n
ve
getat
i
on,
i
n crev
i
ces, un
d
er stones, etc., t
h
ere

b
y avo
idi
ng pre
d
ators an
dd
es
i
ccat
i
on. An
i
mp
li
c
i
t part o
f
t
h
e Paranota
l
T
h
eory
i
st
h
at t

hi
sa
bili
ty evo
l
ve
di
nt
h
ea
d
u
l
t stage.
It was Oken (1811, cited in Wi
gg
lesworth, 1973) who made the first su
gg
estion that
w
in
g
s evolved from an alread
y
articulated structure, namel
yg
ills. Woodworth (1906, cite
d
i
n Wigglesworth, 1973), having noted that gills are soft, flexible structures perhaps not

e
as
il
y converte
d
(
i
nanevo
l
ut
i
onary sense)
i
nto r
i
g
id
w
i
ngs, mo
difi
e
d
t
h
eG
ill
T
h
eory

by
suggest
i
ng t
h
at w
i
ngs were more
lik
e
l
y
f
orme
df
rom accessory g
ill
structures, t
h
emova
ble
gill
p
l
ates w
hi
c
h
protect t
h

e
gill
san
d
cause water to c
i
rcu
l
ate aroun
d
t
h
em. T
h
e
gill
p
l
ates,
b
y
their ver
y
functions, would alread
y
possess the necessar
y
ri
g
idit

y
and stren
g
th. Thi
s
proposal receives support from embr
y
olo
gy
, which has shown abdominal se
g
mental
g
ills
of l
arva
l
Ep
h
emeroptera to
b
e
h
omo
l
ogous w
i
t
hl
egs, not w

i
ngs. W
i
gg
l
eswort
h
(1973
,
1
97
6
) resurrected, and attempted to extend, the Gill Theory by proposing that in terrestrial
apter
yg
otes t
h
e
h
omo
l
o
g
ues o
f
t
h
e
gill
p

l
ates are t
h
e coxa
l
st
yli
,an
di
twas
f
rom t
h
et
h
orac
ic
29
IN
S
E
C
TDI
V
ER
S
IT
Y
coxal st
y

li that win
g
s evolved. Kukalov´a-Peck (1978) stated that the homolo
gy
of the win
gs
and st
y
li as proposed b
y
Wi
gg
lesworth was not acceptable and pointed out that win
gs
are alwa
y
s located above the thoracic spiracles, whereas le
g
s alwa
y
s articulate with the
th
orax
b
e
l
ow t
h
esp
i

rac
l
es. In support o
f
W
i
gg
l
eswort
h
’s proposa
l
,
i
ts
h
ou
ld b
e note
d
t
h
at
pr
i
m
i
t
i
ve

l
yw
i
ngs are move
db
y musc
l
es attac
h
e
d
to t
h
e coxae (see C
h
apter 14, Sect
i
o
n
3.3.3) an
d
are trac
h
eate
dbyb
ranc
h
es o
f
t

h
e
l
e
g
trac
h
eae
.
G
raduall
y
, the “articulated pro-win
g
s” proposal has
g
ained support, drawin
g
on ev
-
idence from paleontolo
gy
, developmental biolo
gy
, neurobiolo
gy
,
g
enetics, comparativ
e

anatomy, an
d
transp
l
ant exper
i
ments. Among
i
ts
l
ea
di
ng proponents
i
sKu
k
a
l
ov´a-Pec
k
(1978, 1983, 1987) w
h
o not on
l
y presente
d
a strong case
f
oraw
i

ng or
i
g
i
n
f
rom art
i
cu
l
ate
d
pro-w
i
ngs,
b
ut s
i
mu
l
taneous
l
y cast ma
j
or
d
ou
b
tont
h

e paranota
l
t
h
eory an
d
t
h
eev
id
ence
f
o
r
it. She ar
g
ued that the fossil record supports none of this evidence. Rather, it indicates
j
ust
t
he opposite sequence of events, namel
y
, that the primitive arran
g
ement was one of freel
y
movable pro-wings on all thoracic and abdominal segments of juvenile insects, and it wa
s
f
rom t

hi
s arrangement t
h
at t
h
e
fi
xe
d
w
i
ng-pa
d
con
di
t
i
on o
f
mo
d
ern
j
uven
il
e exopterygotes
ev
ol
ve
d

. Accor
di
ng to Ku
k
a
l
ov´a-Pec
k
, numerous
f
oss
ili
ze
dj
uven
il
e
i
nsects
h
ave
b
een
f
oun
d
w
ith articulated thoracic pro-win
g
s. However, with few exceptions even in the earliest fossi

l
insects, both
j
uvenile and adult, the abdominal pro-win
g
s are alread
y
fused with the ter
ga
and frequently reduced in size. Some juvenile Protorthoptera with articulated abdomina
l
pro-w
i
ngs
h
ave
b
een
d
escr
ib
e
d
,an
di
n extant Ep
h
emeroptera t
h
ea

bd
om
i
na
l
pro-w
i
ngs are
reta
i
ne
d
as mova
bl
eg
ill
p
l
ates
.
I
n proposin
g
her ideas for the ori
g
in and evolution of win
g
s, Kukalov´a-Peck emphasized
t
hat these events probabl

y
occurred in “semiaquatic” insects livin
g
in swamp
y
areas and
feedin
g
on primitive terrestrial plants, al
g
ae, rottin
g
ve
g
etation, or, in some instances, othe
r
sma
ll
an
i
ma
l
s. It was
i
n suc
hi
nsects t
h
at pro-w
i

ngs
d
eve
l
ope
d
.T
h
e pro-w
i
ngs
d
eve
l
ope
d
on
a
ll
t
h
orac
i
can
d
a
bd
om
i
na

l
segments (spec
ifi
ca
ll
y
f
rom t
h
eep
i
coxa
l
ex
i
te at t
h
e
b
ase o
f
eac
h
l
e
g
), were present
i
na
ll i

nstars, an
d
at t
h
e outset were
hi
n
g
e
d
to t
h
ep
l
eura (not t
h
e ter
g
a)
.
W
ith regard to the selection pressures that led to the origin of pro-wings, Kukalov´
WW
a-Peck
´
u
sed ideas expressed b
y
earlier authors. She su
gg

ested that pro-win
g
sma
y
have functioned
i
n
i
t
i
a
ll
yassp
i
racu
l
ar
fl
aps to prevent entry o
f
water
i
nto t
h
e trac
h
ea
l
system w
h

en t
h
e
i
nsect
s
b
ecame su
b
merge
d
or to prevent
l
oss o
f
water v
i
at
h
e trac
h
ea
l
system as t
h
e
i
nsects c
li
m

b
e
d
vegetat
i
on
i
n searc
h
o
ff
oo
d
.A
l
ternat
i
ve
l
y, t
h
ey may
h
ave
b
een p
l
ates t
h
at protecte

d
t
h
e
g
ills and/or created respirator
y
currents over them, or tactile or
g
ans comparable to (but no
t
h
omolo
g
ous with) the coxal st
y
li of th
y
sanurans. Initiall
y
, the pro-win
g
s were saclike an
d
internally confluent with the hemocoel. Improved mechanical strength and efficiency would
b
ega
i
ne
d

,
h
owever,
b
y
fl
atten
i
ng an
db
y restr
i
ct
i
ng
h
emo
l
ymp
hfl
ow to spec
ifi
cc
h
anne
ls
(ve
i
n
f

ormat
i
on). Ku
k
a
l
ov´a-Pec
k
specu
l
ate
d
t
h
at eventua
ll
yt
h
e pro-w
i
ngs o
f
t
h
et
h
ora
x
and abdomen became structurall
y

and functionall
y
distinct, with the former
g
rowin
g
lar
ge
enou
g
h to assist in forward motion, probabl
y
in water. This new function of underwater
rowing would create selection pressure leading to increased size and strength of pro-wings,
i
mprove
d
muscu
l
ar coor
di
nat
i
on, an
db
etter art
i
cu
l
at

i
on o
f
t
h
e pro-w
i
ngs, ma
ki
ng rotat
i
on
poss
ibl
e. T
h
ese
i
mprovements wou
ld
a
l
so
i
mprove att
i
tu
di
na
l

contro
l
,g
lidi
ng a
bili
ty, an
d
th
ere
f
ore surv
i
va
l
an
ddi
spersa
lf
or t
h
e
i
nsects
if
t
h
e
yj
umpe

d
or
f
e
ll
o
ff
ve
g
etat
i
on w
h
en on
land. The final phase would be the development of pro-win
g
s of sufficient size and mobilit
y
t
hat fli
g
ht became possible.
Ama
j
or
diffi
cu
l
ty
i

nt
h
et
h
eory t
h
at w
i
ngs arose
f
rom art
i
cu
l
ate
d
pro-w
i
ngs
i
n aquat
i
c
or amp
hibi
ous ancestors
i
stoexp
l
a

i
n sat
i
s
f
actor
il
yt
h
e nature o
f
t
h
e
i
nterme
di
ate stages.
Th
at
i
s,
h
ow cou
ld fli
ers evo
l
ve
f
rom sw

i
mmers? Mar
d
en an
d
Kramer
(
1994
)
ma
d
et
h
e
30
CHAPTER
2
f
ascinatin
g
su
gg
estion that surface skimmin
g
, as seen in some livin
g
stoneflies (Plecoptera)
and the subadult sta
g
e of some ma

y
flies (Ephemeroptera), ma
y
represent this intermediat
e
phase. Essentiall
y
, surface skimmin
g
is runnin
g
on the water surface, usin
g
the weak flappin
g
m
ovements o
f
t
h
ew
i
ngs to generate propu
l
s
i
on. Because t
h
e water supports t
h

ewe
i
g
h
to
f
t
h
e
i
nsect’s
b
o
d
y, t
h
e muscu
l
ar
d
eman
d
so
f
s
ki
mm
i
ng are
f

ar
l
ess t
h
an t
h
ose requ
i
re
din
a
f
u
lly
a
i
r
b
orne
i
nsect. T
h
us, stone
fli
es w
i
t
h
qu
i

te sma
ll
w
i
n
g
san
d
wea
k fligh
t musc
l
e
s
c
an surface skim
.
Thomas
et al.
(2000) combined a molecular ph
y
lo
g
enetic anal
y
sis of th
e
P
lecoptera with an examination of locomotor behavior and win
g

structure in representatives
of f
am
ili
es across t
h
eor
d
er. T
h
e
i
r stu
d
ys
h
owe
d
t
h
at sur
f
ace s
ki
mm
i
ng, a
l
ong w
i

t
h
wea
k
fli
g
h
t,
i
s a reta
i
ne
d
ancestra
l
tra
i
t
i
n stone
fli
es, support
i
ng t
h
e
h
ypot
h
es

i
st
h
at t
h
e
fi
rs
t
wi
nge
di
nsects were sur
f
ace s
ki
mmers. Mar
d
en an
d
T
h
omas (2003)
h
ave prov
id
e
df
urt
h

er
support for Kukalov´a-Peck’s proposals b
y
stud
y
in
g
the Chilean stonefl
y
Diam
p
hi
p
no
p
sis
s
amali. The weakl
y
fl
y
in
g
adults o
f
D. samali use their forewin
g
s as oars to row across th
e
w

ater surface. Further, they retain abdominal gills. The larval stage is amphibious, living
b
y
d
ay
i
n
f
ast-mov
i
ng streams,
b
ut
f
orag
i
ng at t
h
e water’s e
d
ge
b
yn
i
g
h
t. T
h
us, D.
s

ama
l
i
m
ay represent a very ear
l
y stage on t
h
e roa
d
to true
fli
g
h
t: an amp
hibi
ous
lif
esty
l
e, t
he
c
o-occurrence of win
g
s and
g
ills, and the abilit
y
to row on the water surface.

In addition to her views on win
g
ori
g
in, Kukalov´a-Peck has also speculated on th
e
ev
olution of fused wing pads in juveniles and wing folding. Noting that the earliest flying
i
nsects
h
a
d
w
i
ngs t
h
at stuc
k
out at r
i
g
h
t ang
l
es to t
h
e
b
o

d
y, Ku
k
a
l
ov´a-Pec
k
po
i
nte
d
out t
h
at
,
as t
h
ey
d
eve
l
ope
d
(
i
n an ontogenet
i
c sense), t
h
e

i
nsects wou
ld b
esu
bj
ecte
d
to two se
l
ect
i
o
n
pressures. One, exerted in the adult sta
g
e, would be toward improvement of fl
y
in
g
abilit
y
; the
o
ther, which acted on
j
uvenile instars, would promote chan
g
es that enabled them to escape
o
r hide more easil

y
under ve
g
etation, etc. In other words, it would lead to a streamlinin
g
of b
o
d
ys
h
ape
i
n
j
uven
il
es. In most Pa
l
eoptera stream
li
n
i
ng was ac
hi
eve
d
t
h
roug
h

t
h
e
ev
o
l
ut
i
on o
f
w
i
ngs t
h
at
i
n ear
l
y
i
nstars were curve
d
so t
h
at t
h
et
i
ps were
di

recte
db
ac
k
war
d
.
A
t eac
h
mo
l
t, t
h
e curvature o
f
t
h
ew
i
n
g
s
b
ecame
l
ess unt
il
t
h

e “stra
igh
t-out” pos
i
t
i
on o
f
the full
y
developed win
g
s was achieved. Two other
g
roups of paleopteran insects became
m
ore streamlined as
j
uveniles throu
g
h the evolution of a win
g
-foldin
g
mechanism, a feature
t
h
at was a
l
so a

d
vantageous to, an
d
was t
h
ere
f
ore reta
i
ne
di
n, t
h
ea
d
u
l
t stage. T
h
e
fi
rst o
f
t
h
ese groups, t
h
e
f
oss

il
or
d
er D
i
ap
h
anoptero
d
ea, rema
i
ne
d
pr
i
m
i
t
i
ve
i
not
h
er respects an
dis
i
ncluded therefore in the infraclass Paleoptera (Table 2.1 and Figure 2.
6
). The second group
,

w
hose win
g
-foldin
g
mechanism was different from that of Diaphanopterodea, containe
d
the ancestors of the Neoptera. The
g
reatest selection pressure would be exerted on the older
juvenile instars, which could neither fly nor hide easily. In Kukalov´a-Peck’s scheme, the
old
er
j
uven
il
e
i
nstars were eventua
ll
y rep
l
ace
db
yas
i
ng
l
e metamorp
hi

c
i
nstar
i
nw
hi
c
h
t
h
e
i
ncreas
i
ng c
h
ange o
ff
orm
b
etween
j
uven
il
ean
d
a
d
u
l

t cou
ld b
e accomp
li
s
h
e
d
.To
f
urt
h
er
aid streamlinin
g
and, in the final
j
uvenile instar, to protect the increasin
g
l
y
more delicat
e
w
in
g
s developin
g
within, the win
g

sof
j
uveniles became firml
y
fused with the ter
g
aan
d
m
ore sclerotized, that is, wing pads. This state is comparable to that in modern exopterygote
(h
em
i
meta
b
o
l
ous)
i
nsects. Furt
h
er re
d
uct
i
on o
f
a
d
u

l
t structures to t
h
epo
i
nt at w
hi
c
h
t
h
e
y
e
x
i
st unt
il
metamorp
h
os
i
sasun
diff
erent
i
ate
d
em
b

ryon
i
ct
i
ssues (
i
mag
i
na
ldi
scs)
b
eneat
h
t
h
e
j
uven
il
e
i
nte
g
ument
l
e
d
to t
h

een
d
opter
yg
ote (
h
o
l
ometa
b
o
l
ous) con
di
t
i
on, t
h
at
i
s, t
h
e
ev
olution of the pupal sta
g
e (Section 3.3).
R
e
g

ardless of their ori
g
in, the win
g
s of the earliest fl
y
in
g
insects were presumabl
y
w
e
ll
-sc
l
erot
i
ze
d
,
h
eavy structures w
i
t
h
numerous
ill
-
d
e

fi
ne
d
ve
i
ns. S
li
g
h
t traces o
ffl
ut
i
n
g
(
t
h
e
f
ormat
i
on o
f
a
l
ternat
i
ng concave an
d

convex
l
ong
i
tu
di
na
l
ve
i
ns
f
or a
dd
e
d
strengt
h
)
m
a
yh
ave
b
een apparent (Ham
il
ton, 1971). T
h
ew
i

n
g
s (an
d fligh
te
ffi
c
i
enc
y
) were
i
mprove
d
31
IN
S
E
C
TDI
V
ER
S
IT
Y
T
ABLE 2
.
1
.

The Major Groups of Pterygota
D
ivisions within Neopter
a
I
nfraclass
O
rder
s
Mart
y
nov’s scheme Hamilton’s scheme
Paleodictyoptera
a
Megasecopter
a
a
D
i
a
ph
ano
p
tero
d
ea
a
P
aleo
p

tera
⎧
⎪
⎧
⎧
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎨
⎪
⎪
⎪
⎨
⎨
⎪
⎪⎪
⎪
⎪

⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎩
⎪
⎪
P
e
rm
ot
h
e
mi
st
i
da
a
Pr
otodo

n
ata
a
Od
onata (
d
ra
g
on
fli
es,
d
amse
lfli
es)
Ep
h
emeroptera (ma
yfli
es
)
Protort
h
optera
a
D
i
ct
y
optera (coc

k
roac
h
es, mant
id
s
)
Iso
p
tera (termites)
O
rthoptera (grasshoppers, locusts, crickets
)
M
i
omopter
a
a
P
li
coneo
p
teraProte
ly
troptera
a
⎫
⎪
⎫⎫
⎪

⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪

⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎬
⎪⎪
⎪
⎬
⎬
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪

⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎭
⎪
⎪
Dermaptera (earwigs
)
G
ry
ll
o
bl

atto
d
ea (gry
ll
o
bl
att
id
s)
⎫
⎪
⎫
⎫
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪

⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪

⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎬
⎪
⎪
⎪
⎬
⎬
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪

⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪

⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪

⎪⎪
⎭
⎪
⎪
P
o
l
yneoptera
Manto
p
hasmatodea
Phasmida (stick and leaf insects)
Em
bi
optera (we
b
sp
i
nners
)
Para
p
leco
p
tera
a
C
aloneurode
a
a

Protoper
l
ar
i
a
a
P
l
eco
p
tera (stone
fli
es)
Z
ora
p
tera (zora
p
terans)
N
eoptera
⎧
⎪
⎧⎧
⎪
⎪
⎪
⎪
⎪
⎪

⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪

⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪

⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪

⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪

⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪

⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎨
⎪⎪
⎪
⎨⎨
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪

⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪

⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪

⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪

⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪

⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎩
⎪
⎪
G
lossel
y
trode
a
a
Psoco
p
tera (
b

oo
kli
ce
)
Phthiraptera (biting and sucking lice)
⎫
⎪
⎫⎫
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎬
⎪
⎪
⎪
⎬⎬
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪

⎭
⎪
⎪
P
araneo
p
tera
Hemiptera (bugs
)
T
hy
sanoptera (t
h
r
i
ps
)
Megaloptera (dobsonflies, aIderflies
)
⎫
⎪
⎫⎫
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪

⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪

⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪

⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪

⎪
⎪⎪
⎪
⎪⎪
⎬
⎪⎪
⎪
⎬⎬
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪

⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪

⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪

⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎭
⎪
⎪
P
l
anoneoptera
Ra
phidi
o
p
tera (sna
k
e
fli
es
)
Neuroptera (lacewin
g
s, mantispids)
⎫
⎪

⎫⎫
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪

⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎬
⎪
⎪
⎪
⎬⎬
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪

⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪
⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎪
⎪⎪
⎭
⎪
⎪
Mecoptera (scorp
i
on
fli
es)
Le
pid
o

p
tera (
b
utter
fli
es, mot
h
s)
Tricho
p
tera (caddis flies
)
O
ligoneoptera
Diptera (true flies
)
Si
p
h
onaptera (
fl
eas)
H
y
menoptera (
b
ees, wasps, ants,
i
chneumons
)

Coleoptera (beetles
)
S
treps
i
ptera (sty
l
opo
id
s)
a
Entirel
y
fossil orders
.
b
y
a reduction in sclerotization, as seen in Paleoptera. Onl
y
the articulatin
g
sclerites at the
base of the wing and the integument adjacent to the tracheae remained sclerotized, the latter
g
i
v
i
ng r
i
se to t

h
eve
i
ns. F
l
ut
i
ng was accentuate
di
nt
h
ePa
l
eoptera, an
d
t
h
e
di
sta
l
area o
f
t
h
e
w
in
g
was additionall

y
stren
g
thened b
y
the formation of non-tracheated intercalar
y
veins
and numerous crossveins (Hamilton, 1971, 1972).
32
CHAPTER
2
F
I
GU
RE 2.2
.
A proposed
g
round plan of win
g
articulation and win
g
venation. Abbreviations: A, anterior;
A
n, anal; C, costa; Cu, cubitus; J, jugal; M, media; P, posterior; PC, precosta; R, radius; Sc, subcosta. [After J
.
Ku
k
a

l
ov´a-Pec
k
, 1983, Or
igi
no
f
t
h
e
i
nsect w
i
n
g
an
d
w
i
n
g
art
i
cu
l
at
i
on
f
rom t

h
e art
h
ropo
d
an
l
e
g,
C
an. J. Zoo
l.
61
:
1618–1669. B
y
permission of the National Research Council of Canada and the author.
]
K
u
k
a
l
ov´a-Pec
k
(1983) ar
g
ue
d
t

h
at t
h
e
g
roun
d
p
l
an o
f
w
i
n
g
art
i
cu
l
at
i
on
i
nc
l
u
d
e
d
e

igh
t
rows of four articulatin
g
sclerites (Fi
g
ure 2.2). These sclerites were derived, in her view,
f
rom the epicoxa of the primitive le
g
and, as a result, were moved b
y
ancestral le
g
muscles
.
O
riginating on the outer edge of each row was a wing vein. This articular arrangement, seen
o
n
l
y
i
nD
i
ap
h
anoptero
d
ea, a

ll
owe
d
t
h
esc
l
er
i
tes to
b
e crow
d
e
d
an
d
s
l
ante
db
y contract
i
on o
f
t
h
ese musc
l
es, so t

h
atapr
i
m
i
t
i
ve
f
orm o
f
w
i
ng
f
o
ldi
ng cou
ld
occur. In a
ll
ot
h
er Pa
l
eoptera,
f
ossil and extant, fusion of sclerites occurred to form axillar
y
plates that, in turn, became

united with some veins. Thou
g
h the details of this process varied amon
g
the paleopteran
groups, the end result was that, while it undoubtedly strengthened the wing attachment, i
t
prevente
d
w
i
ng
f
o
ldi
ng. Essent
i
a
ll
y,
i
nmo
d
ern Pa
l
eoptera t
h
e
b
ase o

f
eac
h
w
i
ng art
i
cu
l
ate
s
at t
h
ree po
i
nts w
i
t
h
t
h
e tergum, t
h
et
h
ree ax
ill
ary sc
l
er

i
tes runn
i
ng
i
n a stra
i
g
h
t
li
ne a
l
on
g
the bod
y
. In the evolution of Neoptera the axillar
y
sclerites altered their ali
g
nment so that
e
ach win
g
articulated with the ter
g
um at onl
y
two points. This alteration of ali

g
nment made
w
ing folding possible
.
A secon
di
mportant consequence o
f
t
h
ea
l
tere
d
art
i
cu
l
at
i
on o
f
t
h
ew
i
ng was a
f
urt

h
e
r
i
mprovement
i
n
fli
g
h
te
ffi
c
i
ency. In Ep
h
emeroptera an
d
, presuma
bl
y, most or a
ll f
oss
il
P
aleoptera the win
g
beat is essentiall
y
a simple up-and-down motion; in Neoptera eac

h
w
in
g
twists as it flaps and its tip traces a fi
g
ure-ei
g
ht path. In other words, the win
g
“rows
”
throu
g
h the air, pushin
g
a
g
ainst the air with its undersurface durin
g
the downstroke
y
e
t
c
utt
i
ng t
h
roug

h
t
h
ea
i
rw
i
t
hi
ts
l
ea
di
ng e
d
ge on t
h
e upstro
k
e. To carry out t
hi
srow
i
n
g
m
ot
i
on e
ff

ect
i
ve
l
y necess
i
tate
d
t
h
e
l
oss o
f
most o
f
t
h
ew
i
ng
fl
ut
i
ng. On
l
yt
h
e costa
l

are
a
(
F
ig
ure 3.27) nee
d
sto
b
er
igid
as t
hi
s
l
ea
d
st
h
ew
i
n
gi
n
i
ts stro
k
e, an
dfl
ut

i
n
gi
s reta
i
ne
d
here
(
Hamilton, 1971
).
Another evolutionar
y
trend, a
g
ain leadin
g
to improved fli
g
ht, was a reduction in win
g
w
e
i
g
h
t, perm
i
tt
i

ng
b
ot
h
eas
i
er w
i
ng tw
i
st
i
ng an
d
an
i
ncrease
d
rate o
f
w
i
ng
b
eat
i
ng (see a
l
s
o

C
h
apter 14, Sect
i
on 3.3.4). Concom
i
tant w
i
t
h
t
hi
sre
d
uct
i
on
i
nwe
i
g
h
t was a
f
us
i
on or
l
oss
of

some ma
j
or ve
i
ns an
d
t
h
e
l
oss o
f
crossve
i
ns. T
h
e extent an
d
nature o
ff
us
i
on or
l
oss o
f
v
eins followed certain patterns that, to
g
ether with other structural features, for example,

33
IN
S
E
C
TDI
V
ER
S
IT
Y
lines of flexion and lines of foldin
g
, are potentiall
y
important characters on which conclu-
sions about the evolutionar
y
relationships of neopteran insects can be based. Unfortunatel
y
,
complicatin
g
this important tool has been a tendenc
y
for authors to use different terminolo-
g
i
es w
h

en
d
escr
ibi
ng t
h
eve
i
ns an
d
w
i
ng areas o
f diff
erent groups o
fi
nsects, an aspect t
h
at
i
s
d
ea
l
tw
i
t
h
more
f

u
ll
y
i
nC
h
apter 3 (Sect
i
on 4.3.2)
.
3.2. Phylo
g
enetic Relationships of the Ptery
g
ota
There are some 2
5
–30 orders of living pterygote insects and about 10 containing only
f
oss
il f
orms, t
h
e num
b
er vary
i
ng accor
di
ng to t

h
e aut
h
or
i
ty consu
l
te
d
.C
l
ar
ifi
cat
i
on o
f
t
he
relationships of these
g
roups ma
y
utilize fossil evidence, comparisons of extant forms, or a
combination of both. Increasin
g
l
y
, morpholo
g

ical data and molecular information are bein
g
combined in massive cladistical anal
y
ses in an effort to resolve some lon
g
-standin
g
ar
g
u-
ments. For exam
pl
e, W
h
ee
l
e
r
et a
l.
(
2001) employed 27
5
morphological variables and 18
S
and 28S rDNA sequences from more than 120 species of hexapods, plus
6
outgroup repre-
sentat

i
ves, to o
b
ta
i
na“
b
est-
fi
t” ana
ly
s
i
so
f
t
h
ere
l
at
i
ons
hi
ps o
f
t
h
e
i
nsect or

d
ers. Even so
,
none of these approaches is entirel
y
satisfactor
y
. For example, in extant species secondar
y
modifications ma
y
mask the ancestral apomorphic characters. Equall
y
, molecular studies
may g
i
ve spur
i
ous resu
l
ts
if
t
h
e samp
l
es
i
ze
i

s too sma
ll
. Foss
il
s, on t
h
eot
h
er
h
an
d
, are re
l
a-
ti
ve
l
y scarce an
d
o
f
ten poor
l
yor
i
ncomp
l
ete
l

y preserve
d,
*
espec
i
a
ll
y
f
rom t
h
eDevon
i
an an
d
L
ower Carboniferous periods durin
g
which a
g
reat adaptive radiation of insects occurred.
By
the Permian period, from which man
y
more fossils are available, almost all of the modern
orders had been established. Misidentification of fossils and misinter
p
retation of structures
b
y ear

l
ypa
l
eonto
l
og
i
sts
l
e
d
to
i
ncorrect conc
l
us
i
ons a
b
out t
h
ep
h
y
l
ogeny o
f
certa
i
n group

s
an
d
t
h
e
d
eve
l
opment o
f
con
f
us
i
ng nomenc
l
ature. For examp
l
e
,
E
u
g
ereo
n
,
aLo
w
er Perm

i
a
n
f
oss
il
w
i
t
h
suc
ki
n
g
mout
h
parts, was p
l
ace
di
nt
h
eor
d
er Proto
h
em
i
ptera. It
i

s now rea
li
se
d
t
hat this insect is a member of the order Paleodict
y
optera and is not related to the modern
order Hemiptera as was ori
g
inall
y
concluded. Likewise the Protoh
y
menoptera, whose win
g
venat
i
on super
fi
c
i
a
ll
y resem
bl
es t
h
at o
f

Hymenoptera, were t
h
oug
h
tor
i
g
i
na
ll
yto
b
e ances
-
t
ra
l
to t
h
e Hymenoptera. It
i
s now apprec
i
ate
d
t
h
at t
h
ese

f
oss
il
s are pa
l
eopteran
i
nsects, mos
t
o
f
w
hi
c
hb
e
l
on
g
to t
h
eor
d
er Me
g
asecoptera (Ham
il
ton, 1972). Carpenter (1992) pu
bli
s

h
e
d
an authoritative account of the fossil Insecta in which he reco
g
nized nine orders of fossil
pter
yg
otes. With further work, some of these will undoubtedl
y
require splittin
g
(i.e., the
y
are polyphyletic groups), for example, the Protorthoptera [described by Kukalov´
a-Peck and
´
B
rauc
k
mann (1992) as t
h
e “waste
b
as
k
et taxon”!], an
d
spec
i

es now c
l
ass
ifi
e
d
i
ncertae
s
e
d
i
s
(
o
f
un
k
nown a
ffi
n
i
ty) w
ill b
ep
l
ace
di
nt
h

e
i
r correct taxon (Wootton, 1981).
T
o aid subsequent discussion of the evolutionar
y
relationships within the Pter
yg
ota,
t
he various orders referred to in the text are listed in Table 2.1
.
I
t has generally been assumed that the Paleoptera and Neoptera had a common ancestor
[in the hypothetical order Protoptera (Sharov, 1966)] in the Middle Devonian, although ther
e
i
sno
f
oss
il
recor
d
o
f
suc
h
an ancestor. Remar
k
a

bl
y, a recent re-exam
i
nat
i
on o
f
apa
i
ro
f
m
an
dibl
es
fi
rst
d
escr
ib
e
di
n1
9
28 as
Rhy
nio
g
nat
h

a
h
irsti
,f
rom t
h
e same Lower Devon
i
a
n
d
e
p
osits as the collembolan Rhyniella praecursor (Chapter 5, Section 2), su
gg
ests that
w
in
g
ed insects ma
y
have had a much earlier ori
g
in than previousl
y
thou
g
ht (En
g
el an

d
*
Many fossil orders were established on the basis of limited fossil evidence (e.g., a single wing). Carpenter (1977)
r
ecommen
d
e
d
t
h
at at
l
east t
h
e
f
ore an
dhi
n
d
w
i
ngs,
h
ea
d
,an
d
mout
h

parts s
h
ou
ld b
e
k
nown
b
e
f
ore a spec
i
men
i
s ass
ig
ne
d
to an or
d
er.
34
CHAPTER
2
Grimaldi, 2004). The mandibles are not onl
y
dicond
y
lic (Chapter 3, Section 3.2.2) but
have other features that are characteristic of mandibles of Pter

yg
ota. In other words, fl
y
in
g
i
nsects were alread
y
well established b
y
the Lower Devonian, some 80 million
y
ears earlie
r
t
h
an prev
i
ous
l
y assume
d
.T
hi
s conc
l
us
i
on agrees w
i

t
h
amo
l
ecu
l
ar c
l
oc
k
stu
d
y
i
n
di
cat
i
ng
t
h
at
i
nsects arose
i
nt
h
e Ear
l
yS

il
ur
i
an (a
b
out 430 m
illi
on years ago), w
i
t
h
neopteran
f
orms
present
by
a
b
out 390 m
illi
on
y
ears a
g
o (Gaunt an
d
M
il
es, 2002).
By

the Upper Carboniferous period, when conditions became suitable for fossilization
,
almost a dozen paleopteran and neopteran orders had evolved. Most authors, especiall
y
pa
l
eonto
l
og
i
sts, cons
id
er t
h
ePa
l
eoptera to
b
e monop
h
y
l
et
i
can
d
t
h
es
i

ster group to t
he
Neoptera, an
dli
st a num
b
er o
f
apomorp
hi
es
i
n support o
f
t
hi
sv
i
ew (Ku
k
a
l
ov´a-Pec
k
, 1991,
1
998). Furt
h
er, a recent stu
d

yo
f
18S an
d
28S rDNA sequences
f
rom a
l
most 30 spec
i
es o
f
O
donata, Ephemeroptera, and neopterans has provided stron
g
support for the monoph
y
l
y
o
f the Paleo
p
tera (Hovm¨olle
r
et al.
, 2002). However, there are those, notabl
y
Boudreaux
(
1979), Kristensen (1981, 1989,1995) and Willmann (1998), who, having undertaken cladis

-
t
i
c ana
l
yses o
f
t
h
e extant Ep
h
emeroptera (may
fli
es) an
d
O
d
onata (
d
amse
lfli
es an
dd
ragon-
fli
es),
b
e
li
eve t

h
ePa
l
eoptera to
b
e parap
h
y
l
et
i
c. In Bou
d
reaux’s v
i
ew t
h
eEp
h
emeropter
a
+
N
eoptera form the sister
g
roup to the Odonata, while accordin
g
to Kristensen the best
scenario has the Ephemeroptera as the sister
g

roup of the Odonat
a
+
N
eo
p
tera. Thi
s
v
iew is supported by Wheele
r
et al.
’s
(
2001) analysis, though these authors examined onl
y
t
h
ree spec
i
es eac
h
o
f
O
d
onata an
d
Ep
h

emeroptera. Accor
di
ng to Ku
k
a
l
ov´a-Pec
k
(1991),
wi
t
hi
nt
h
ePa
l
eoptera, two ma
j
or evo
l
ut
i
onary
li
nes appeare
d
, one
l
ea
di

ng to t
h
epa
l
eo
di
cty
-
o
pteroids (Paleodict
y
optera, Diaphanopterodea, Me
g
asecoptera, and Permothemistida), th
e
ot
h
e
r
to t
h
e odo
n
ato
i
ds
+
Ephemeroptera. All paleodict
y
opteroids (Upper Carboniferous-

P
ermian) had a h
y
po
g
nathous head with piercin
g
-suckin
g
mouthparts (Fi
g
ure 2.3). Adult
s
an
dl
arge
j
uven
il
es use
d
t
h
ese to suc
k
t
h
e contents o
f
cones w

hil
e younger
i
nstars pro
b
-
a
bl
y
i
ngeste
d
on
l
y
fl
u
id
s(S
h
ear an
d
Ku
k
a
l
ov´a-Pec
k
, 1990). Prot
h

orac
i
c extens
i
ons wer
e
FIGURE 2.3.
P
a
l
eo
di
ct
y
optero
id
s.
(A)
S
teno
di
ct
y
a
s
p.
(P
a
l
eo

di
ct
y
optera
)
;an
d (B)
P
ermot
h
em
is
sp. (Permoth-
e
mistida). [A, from J. Kukalov´a, 1970, Revisional study of the order Paleodictyoptera in the Upper Carboniferous
s
h
a
l
es o
f
Commentr
y
, France. Part III, Psyc
he
77
:1–44. B,
f
rom A. P. Rasn
i

ts
y
nan
d
D. L. J. Qu
i
c
k
e(e
d
s.),
2
002
,
H
istory o
f
Insect
s
.

c
K
luwer Academic Publishers, Dordrecht. With kind
p
ermission of Kluwer Academic
P
ublishers and the authors.
]
35

IN
S
E
C
TDI
V
ER
S
IT
Y
prominent in some paleodict
y
opteroids (Fi
g
ure 2.3A) and Kukalov´a-Peck (1983, 198
5)
su
gg
ested that these were articulated. There was no metamorphic final instar as in moder
n
exopter
yg
otes; that is, win
g
development was
g
radual and older
j
uveniles could probabl
y

fl
y. T
h
e
i
rext
i
nct
i
on at t
h
een
d
o
f
t
h
e Perm
i
an may
b
e corre
l
ate
d
w
i
t
h
t

h
e
d
em
i
se o
f
t
h
ePa
l
eo
-
z
o
i
c
fl
ora (see Sect
i
on 4.2). Pa
l
eo
di
ctyoptera
f
orme
d
t
h

e
l
argest or
d
er o
f
pa
l
eo
di
ctyoptero
id
s
and included some ver
y
lar
g
e species with win
g
spans up to
5
6 cm. As noted earlier, the
Diaphanopterodea, which ma
y
be the sister
g
roup of Paleodict
y
optera, were unique amon
g

Paleoptera in that the
y
were able to fold their win
g
s. Thou
g
h most diaphanopterodeans were
p
l
ant-
j
u
i
ce
f
ee
d
ers, Ku
k
a
l
ov´a-Pec
k
an
d
Brauc
k
mann (1990) o
b
serve

d
t
h
at some Perm
i
an
spec
i
es were remar
k
a
bl
y mosqu
i
to
lik
ean
d
specu
l
ate
d
t
h
at t
h
ese may
h
ave
f

e
d
on
bl
oo
d
.
M
egasecoptera
h
a
d
severa
lf
eatures
i
n common w
i
t
h
D
i
ap
h
anoptero
d
ea, t
h
oug
h

t
h
ese wer
e
likel
y
the result of conver
g
ence. Contrar
y
to earlier opinions, the Me
g
asecoptera were no
t
carnivores but sucked plant material; a few ma
y
have cau
g
ht other insects and sucked their
b
ody fluids. The Permothemistida [formerly the Archodonata and included in the Paleodic
-
t
yoptera
b
y Carpenter (1992)] were a sma
ll
group, c
h
aracter

i
ze
db
y
h
av
i
ng great
l
yre
d
uce
d
or no metat
h
orac
i
cw
i
ngs, s
h
ort mout
h
parts, an
d
un
i
que w
i
ng venat

i
on (F
i
gure 2.3B).
Earl
y
members of the Ephemeroptera
+
o
donatoid
g
roup had bitin
g
mouthparts an
d
aquatic
j
uveniles with nine pairs of abdominal
g
ill plates and le
g
lets. Adults of earl
y
E
phemeroptera (Upper Carboniferous-Recent) (including the Protoephemeroptera, for-
mer
l
y separate
db
ecause o

f
t
h
e
i
rtwopa
i
rs o
fid
ent
i
ca
l
w
i
ngs)
diff
ere
df
rom extant
f
orms
i
n
h
av
i
ng
f
unct

i
ona
l
mout
h
parts. Some very
l
arge
f
orms evo
l
ve
d
,
f
or examp
l
e,
B
ojop
hl
e
b
i
a
p
roko
pi
w
ith a win

g
span of 4
5
cm. The nature of their mouthparts su
gg
ests that n
y
mphs
w
ere probabl
y
predators, some perhaps feedin
g
on amphibian tadpoles (Kukalov´a-Peck,
1985) (Fi
g
ure 2.4A). The earl
y
odonatoids differed from Ephemeroptera in features of thei
r
venat
i
on an
di
n
h
av
i
ng nymp
h

st
h
at
l
ac
k
e
d
a
bd
om
i
na
l
g
ill
p
l
ates, us
i
ng
i
nstea
d
t
h
e rec
-
t
al branchial chamber for gas exchange (Chapter 1

5
, Section 4.1). The group includes tw
o
or
d
ers Proto
d
onata (Me
g
an
i
soptera) (Upper Car
b
on
if
erous-Tr
i
ass
i
c) an
d
O
d
onata (Tr
i
ass
i
c
-
R

ecent) that are evidentl
y
closel
y
related, some authorities even includin
g
the former i
n
t
he latter order. However, Kukalov´a-Peck (1991) presented five win
g
features, and feature
s
o
f
t
h
e gen
i
ta
li
aan
d
cerc
i
t
h
at
j
ust

if
yt
h
e
i
r separat
i
on. T
h
e Proto
d
onata were super
b
aer
i
a
l
pre
d
ators, catc
hi
ng prey
i
n
fli
g
h
tor
f
rom

i
ts perc
h
us
i
ng t
h
e
i
r
l
ong, strong
l
egs (F
i
gure 2.4B).
I
nt
hi
s
di
verse an
d
a
b
un
d
ant group were t
h
e

l
argest
k
nown
i
nsects (Meganeur
id
ae),
i
nc
l
u
di
n
g
F
IGURE 2.4. Early Paleoptera. (A) Juvenile of the Early Permian mayfly
,
K
ukalo
v
´
a americana
´
;(
B
)
A
rctot
y

pu
s
s
p., a
l
ate Perm
i
an proto
d
onatan; an
d
(C) Ear
ly
Jurass
i
c
d
ra
g
on
fly
n
y
mp
h,
Samamura gigante
a
.
T
h

ou
gh
t
he
ny
mph had lar
g
e anal flaps, reminiscent of the caudal lamellae of damselflies, it used a branchial chamber for
gas exchange. [From A. P. Rasnitsyn and D. L. J. Quicke (eds.), 2002
,
History o
f
Insect
s
.

c
K
lu
w
er Academic
P
u
bli
s
h
ers
,
Dor
d

rec
ht
.
W
i
t
hki
n
dp
erm
i
ss
i
on o
f
K
l
uwer Aca
d
em
i
cPu
bli
s
h
ers an
d
t
h
e aut

h
ors.]
36
CHAPTER
2
Meganeuropsis permiana
w
ith a 71-cm win
g
span. Onl
y
recentl
y
have protodonate
j
uve-
n
iles been discovered
(
Kukalov´a-Peck, 1991
)
; these had a mask similar to that of odonate
l
arvae (see Fi
g
ures 2.4C and 6.8). Some also had prominent win
g
s, leadin
g
to the possibilit

y
t
h
at t
h
ey cou
ld fl
y. A num
b
er o
f
Perm
i
an
f
oss
il
sor
i
g
i
na
ll
y
d
escr
ib
e
d
as O

d
onata, spec
ifi
-
c
a
ll
y
i
nt
h
esu
b
or
d
ers Arc
hi
zygoptera an
d
Protan
i
soptera,
h
ave now
b
een reass
i
gne
d
to t

h
e
P
roto
d
onata
(
Ku
k
a
l
ov´a-Pec
k
, 1991
)
so t
h
at true O
d
onata are not
k
nown
b
e
f
ore t
h
eTr
i
ass

i
c.
These
g
enerall
y
small predators alread
y
bore a stron
g
resemblance to the extant Z
yg
opter
a
and Anisoptera both in form and habits (Fi
g
ure 2.4C).
In contrast to t
h
ePa
l
eo
p
tera, w
hi
c
h
were
i
n

h
a
bi
tants o
f
o
p
en s
p
aces, t
h
e Neo
p
tera
ev
o
l
ve
d
towar
d
a
lif
e among overgrown vegetat
i
on w
h
ere t
h
ea

bili
ty to
f
o
ld
t
h
ew
i
ngs ove
r
t
h
e
b
ac
k
w
h
en not
i
n use wou
ld b
e great
l
ya
d
vantageous. T
h
e ear

l
y
f
oss
il
recor
df
or Neoptera
i
s poor, but from the
g
reat diversit
y
of fossil forms discovered in Permian strata it appear
s
that the ma
j
or evolutionar
y
lines had become established b
y
the Upper Carboniferous period.
Two
m
ajor schools of thought exist with regard to the origin and relationships of thes
e
ev
o
l
ut

i
onary
li
nes. T
h
e tra
di
t
i
ona
l
v
i
ew, propose
db
y Martynov (1938),
i
st
h
at, s
h
ort
l
ya
f-
ter t
h
e separat
i
on o

f
ancestra
l
Neoptera
f
rom Pa
l
eoptera, t
h
ree
li
nes o
f
Neoptera
b
ecam
e
distinct from each other (Table 2.1 and Fi
g
ure 2.
5
A). Based on his studies of fossil win
g
v
enation Mart
y
nov arran
g
ed the Neoptera in three
g

roups, Pol
y
neoptera (plecopteroid, or-
thopteroid, and blattoid orders), Paraneoptera (hemipteroid orders), and Oligoneoptera (en-
dopterygotes). In a modification of this view Sharov (1966) proposed that the Neoptera and
P
a
l
eoptera
h
a
d
a common ancestor (
i
.e., t
h
e
f
ormer
did
not ar
i
se
f
rom t
h
e
l
atter) an
d

, more
i
mportantl
y
, that the Neoptera ma
y
be a pol
y
ph
y
letic
g
roup. In his scheme (Fi
g
ure 2.
5
B
)
e
ach of the three
g
roups arose independentl
y
, a consequence of which must be the assump
-
tion that win
g
foldin
g
arose on three separate occasions.

R
oss (1955), from studies of body structure, and Hamilton (1972), who examined the
wi
ng venat
i
on o
f
aw
id
e range o
f
extant spec
i
es as we
ll
as t
h
at o
ff
oss
il f
orms, conc
l
u
d
e
d
t
h
at t

h
ere are two pr
i
mar
y
evo
l
ut
i
onar
yli
nes w
i
t
hi
nt
h
e Neoptera, t
h
eP
li
coneoptera an
d
F
I
GU
RE 2.5
.
Sc
h

emes
f
or t
h
eor
igi
nan
d
re
l
at
i
ons
hi
ps o
f
t
h
ema
j
or
g
roups o
f
Neoptera. (A) Mart
y
nov’s sc
h
eme;
(

B
)
Sharov’s scheme;
(
C
)
Hamilton’s scheme; and
(
D
)
Kukalova-Peck’s scheme.
37
IN
S
E
C
TDI
V
ER
S
IT
Y
F
IGURE 2.6.
A
poss
ibl
ep
h
y

l
ogeny o
f
t
h
e
i
nsect or
d
ers. Num
b
ers
i
n
di
cate ma
j
or evo
l
ut
i
onary
li
nes: (1) Pa
l
e
-
optera; (2) Neoptera; (3) Plecopteroids; (4) Orthopteroids; (
5
) Blattoids; (6) Hemipteroids; (7) Endopter

yg
otes;
(
8) Neuropteroids-Coleoptera; (9) Panorpoids-Hymenoptera; (10) Panorpoids; (11) Antliophora; (12) Amphies-
m
enoptera
.
t
he Planoneoptera (Fi
g
ures 2.5C and 2.6). The Pliconeoptera corresponds approximatel
y
t
o the Pol
y
neoptera of Mart
y
nov but excludes the plecopteroids and the Zoraptera, and
af
ew
f
f
f
oss
il
or
d
ers cons
id
ere

d
p
l
anoneopteran
b
y Ham
il
ton. T
h
eP
l
anoneoptera
i
nc
l
u
d
es
th
e Paraneoptera an
d
O
li
goneoptera o
f
Martynov’s sc
h
eme, p
l
us t

h
ep
l
ecoptero
id
san
d
Z
oraptera. In ot
h
er wor
d
s,
b
ot
h
sc
h
oo
l
sa
g
ree t
h
at t
h
ere are t
h
ree ma
j

or
g
roups w
i
t
hi
nt
h
e
N
eoptera but differ with re
g
ard to the relationships amon
g
these
g
roups
.
38
CHAPTER
2
T
he monoph
y
letic nature of the Planoneoptera is now widel
y
supported [e.
g
., se
e

Boudreaux (1979), Henni
g
(1981), Kristensen (1981,1989), Kukalov´a-Peck (1991), and
K
ukalov´a-Peck and Brauckmann (1992)]. However, there is still some ar
g
ument as t
o
wh
et
h
er t
h
eP
li
coneoptera const
i
tutes
i
ts s
i
ster group (
i
.e.,
i
s monop
h
y
l
et

i
c) or
i
s
a
po
l
yp
h
y
l
et
i
c assem
bl
age. In Martynov’s v
i
ew t
h
e
f
eatures un
i
t
i
ng t
h
ep
li
coneopteran or

d
er
s
i
nc
l
u
d
e
d
c
h
ew
i
n
g
mout
h
parts, a
l
ar
g
e ana
ll
o
b
e
i
nt
h

e
hi
n
d
w
i
n
g
t
h
at
f
o
ld
s
lik
ea
f
an a
l
on
g
n
umerous anal veins, complex win
g
venation (t
y
picall
y
includin

g
man
y
crossveins) tha
t
differs between fore and hind win
g
s, presence of cerci, numerous Malpi
g
hian tubules, and
separate gang
li
a
i
nt
h
e nerve cor
d
. However, except
f
or t
h
e
fi
rst two, t
h
ese
f
eatures ar
e

n
o
l
onger cons
id
ere
d
to
b
e synapomorp
hi
c. T
h
e propose
d
s
i
ster-group re
l
at
i
ons
hi
po
f
t
he
P
araneoptera an
d

O
li
goneoptera (
i
.e., t
h
eun
i
ty o
f
t
h
eP
li
coneoptera)
h
as
b
een g
i
ven stron
g
support b
y
the extensive anal
y
sis of Wheele
r
et al.
(

2001
)
. Kukalov´a-Peck
(
1991
)
an
d
K
ukalov´a-Peck and Brauckmann (1992) presented a new scheme for relationships amon
g
the Neoptera (Figure 2.5D), claiming several potential synapomorphic features of wing
v
enat
i
on
b
etween p
l
ecoptero
id
san
d
ort
h
optero
id
s(
i
mp

l
y
i
ngas
i
ster-group re
l
at
i
ons
hi
p)
.
Yet, t
h
ey
f
oun
d
no apomorp
hi
es s
h
are
db
y ort
h
optero
id
san

dbl
atto
id
s. Rat
h
er, t
h
e
l
atte
r
have possible s
y
napomorphies with the Paraneoptera; that is, the two ma
y
be sister
g
roups.
Generall
y
included in the plecopteroids are the fossil orders Protoperlaria (Upper
Carboniferous-Permian) and Para
p
leco
p
tera (U
pp
er Carboniferous-Jurassic) [both of which
are cons
id

ere
d
to
b
e Protort
h
optera
b
y Carpenter (1992)], an
d
t
h
e extant or
d
er P
l
ecopter
a
(
Perm
i
an-Recent
)
. However, mem
b
ers o
f
t
h
etwo

f
oss
il
or
d
ers are
i
nc
l
u
d
e
di
nt
he
Gr
y
lloblattodea b
y
Storozhenko (1997) (and see below). The Protoperlaria ma
y
have been
the ancestors of the P1ecoptera. Earl
y
plecopteroids had well formed prothoracic win
g
lets,
c
hewin
g

mouthparts, and lon
g
cerci. In some species there was no metamorphic final
j
uve-
nil
e
i
nstar. In some spec
i
es t
h
e young nymp
h
s were sem
i
aquat
i
c, w
i
t
h
art
i
cu
l
ate
d
t
h

orac
i
c
wi
ng
l
ets an
d
n
i
ne pa
i
rs o
f
a
bd
om
i
na
l
g
ill
s(F
i
gure 2.7A). O
ld
er
j
uven
il

es may
h
ave
b
een
terrestr
i
a
l
an
d
a
bl
eto
fly
.T
h
eP
l
ecoptera (stone
fli
es) appear to
h
ave separate
df
rom t
h
e
F
IGURE 2.7. (A) Ear

ly
Perm
i
an p
l
ecoptero
id
n
y
mp
h,
G
urianovae
ll
asi
l
p
h
i
d
oi
d
es;an
d
(B) T
h
e most pr
i
m
i

t
i
v
e
hemipteran, a member of the Archesc
y
tinidae, feedin
g
on a cone of an Earl
y
Permian
gy
mnosperm. [From A. P.
R
asnitsyn and D. L. J. Quicke (eds.), 2002
,
History o
f
Insects
.

c
Kluwer Academic Publishers, Dordrecht. Wit
h
ki
n
dp
erm
i
ss

i
on o
f
K
l
uwer Aca
d
em
i
cPu
bli
s
h
ers an
d
t
h
e aut
h
ors.
]
39
IN
S
E
C
TDI
V
ER
S

IT
Y
remainin
g
plecopteroids earl
y
and even b
y
the time at which fossil stoneflies appear, some
of these are assi
g
nable to extant families (Wootton, 1981).
As noted earlier, the Protorthoptera (Upper Carboniferous-Permian) is a “mixed ba
g
”of
f
oss
il
s, a
l
most certa
i
n
l
yapo
l
yp
h
y
l

et
i
c group. Not surpr
i
s
i
ng
l
y,
i
t
h
as o
f
ten
b
een suggeste
d
as t
h
e group
f
rom w
hi
c
h
t
h
e rema
i

n
i
ng ort
h
optero
id
or
d
ers evo
l
ve
d
.T
h
ema
j
or
diffi
cu
l
ty
i
n
c
l
ar
ifyi
n
g
re

l
at
i
ons
hi
ps w
i
t
hi
nt
h
e
g
roup
i
st
h
at some 80% o
f
Car
b
on
if
erous protort
h
opter
-
ans are known onl
y
from fore win

g
sorwin
g
fra
g
ments. Permian forms are
g
enerall
y
more
completel
y
preserved and superficiall
y
ma
y
resemble other
g
roups (e.
g
., Plecoptera and
D
i
ctyoptera), t
h
oug
h
are o
b
v

i
ous
l
y “too
l
ate” to
b
et
h
e
i
r ancestors (Wootton, 1981). A
recent re-exam
i
nat
i
on o
f
t
h
e Protort
h
optera
b
yKu
k
a
l
ov´a-Pec
k

an
d
Brauc
k
mann (1992)
i
n-
di
cate
d
t
h
at t
h
ema
j
or
i
ty o
f
protort
h
opterans are pr
i
m
i
t
i
ve
h

em
i
ptero
id
s, t
h
oug
h
t
h
e group
also includes plecopteroids, orthopteroids, blattoids, and even endopter
yg
otes! The orde
r
M
iomoptera (Upper Carboniferous-Permian) was erected to include a
g
roup of small, chew-
ing insects with homonomous wings, simple venation, and short, distinct cerci, that were
or
i
g
i
na
ll
y
i
nc
l

u
d
e
di
nt
h
e Protort
h
optera. T
h
e pos
i
t
i
on o
f
t
hi
sor
d
er rema
i
ns
d
e
b
ata
bl
e;
some aut

h
ors (e.g., Carpenter, 1992) suggeste
d
t
h
at m
i
omopterans may
b
e
h
em
i
ptero
id,
perhaps close to the Psocoptera, while others (e.
g
., Kukalov´a-Peck, 1991) believe that
t
he
y
ma
y
be endopter
yg
otes, possibl
y
close to the panorpoid-H
y
menoptera stem

g
roup.
Unfortunately, the immature stages are unknown. Another Upper Carboniferous-Permian
group, t
h
eCa
l
oneuro
d
ea,
i
sa
l
so pro
bl
emat
i
ca
l
.T
h
ec
h
ew
i
ng mout
h
parts seen
i
n some

f
oss
il
s, s
h
ort cerc
i
,an
d
w
i
ng venat
i
on
l
e
d
Carpenter (1977, 1992) to p
l
ace t
h
em c
l
ose to
t
he Protorthoptera. Shear and Kukalov´a-Peck (1990) and Kukalov´a-Peck (1991), on th
e
b
asis of the inflated cl
y

peus (housin
g
the suckin
g
apparatus) and the chisellike laciniae,
consider them hemipteroids, while some Russian paleontolo
g
ists have su
gg
ested the
y
are
p
l
ecoptero
id
sorevenen
d
opterygotes, per
h
aps c
l
ose to t
h
e
b
ase o
f
t
h

e neuroptero
id
san
d
Co
l
eoptera (Storoz
h
en
k
o, 1997).
T
h
e ort
h
optero
id
or
d
ers
i
nc
l
u
d
et
h
e Ort
h
optera, P

h
asm
id
a, Dermaptera, Gr
yll
-
oblattodea, probabl
y
the Mantophasmatodea, and possibl
y
the Embioptera and Zoraptera.
Orthoptera were widespread b
y
the Upper Carboniferous, bein
g
easil
y
reco
g
nizable b
y
th
e
i
rmo
difi
e
dhi
n
dl

egs an
d
part
i
cu
l
ar w
i
ng venat
i
on. Ear
l
y
i
nt
h
eevo
l
ut
i
on o
f
t
hi
sor
d
er
a
sp
li

t occurre
d
, one
li
ne
l
ea
di
ng to t
h
e Ens
if
era (
l
ong-
h
orne
d
grass
h
oppers an
d
cr
i
c
k
ets), t
h
e
ot

h
er to t
h
e Cae
lif
era (s
h
ort-
h
orne
d
grass
h
oppers an
dl
ocusts). In
d
ee
d
, Keva
n
(
198
6)
an
d
others have stron
g
l
y

ur
g
ed that the two
g
roups each be
g
iven ordinal status, an arran
g
emen
t
supported b
y
those who claim, on the basis of dubious paleontolo
g
ical evidence, that the
Caelifera and Phasmida (stick insects) may be sister groups. However, in addition to the
t
wo
f
eatures a
l
rea
d
y note
d
,t
h
e
l
atera

ll
y exten
d
e
d
pronotum cover
i
ng t
h
ep
l
euron, t
h
e
h
or
i
-
z
onta
ll
y
di
v
id
e
d
prot
h
orac

i
csp
i
rac
l
e, an
d
t
h
e
hi
n
d
t
ibi
aw
i
t
h
tworowso
f
teet
h
appear to
b
e
s
y
napomorphies confirmin
g

the unit
y
of the Orthoptera. The fossil record of the Phasmid
a
is poor, thou
g
h specimens are known from the Upper Permian onward. Kamp’s (1973)
phenetic analysis of extant forms indicated that the phasmids are closest to the Dermaptera
an
d
Gry
ll
o
bl
atto
d
ea, t
h
et
h
ree or
d
ers
f
orm
i
ng a natura
l
group. Bou
d

reaux (1979), on t
h
e
ot
h
er
h
an
d
,
li
ste
d
a num
b
er o
f
poss
ibl
e synapomorp
hi
es t
h
at wou
ld
ren
d
er t
h
eP

h
asm
id
aan
d
Ort
h
optera s
i
ster
g
roups, (a v
i
ew supporte
dby
W
h
ee
l
er
et al.
’
s (2001) stu
dy
). Aut
h
or
i
t
i

e
s
still disa
g
ree on the affinities of the Dermaptera (earwi
g
s), which do not appear in the fossil
record until the Lower Jurassic. Some have
p
laced them close to the Pleco
p
tera, Ortho
p
tera,
E
m
bi
optera, an
d
even t
h
een
d
opterygote Co
l
eoptera, w
hil
eot
h
ers cons

id
ere
d
t
h
em to
be
only distantly related to any of the extant orthopteroid groups. Giles’ (19
6
3) comparativ
e
morp
h
o
l
o
gi
ca
l
stu
dy
an
d
t
h
e com
bi
ne
d
morp

h
o
l
o
gi
ca
l
-mo
l
ecu
l
ar ana
ly
s
i
s
by
W
h
ee
l
er
et al.
40
CHAPTER
2
(
2001) su
gg
est that the

y
are the sister
g
roup to the Gr
y
lloblattodea. In contrast, Boudreaux
(
1979) and Kukalov´a-Peck (1991) included the order in the blattoid
g
roup, thou
g
h accord-
i
n
g
to Kristensen (1981) the presumed s
y
napomorphies are weak. Gr
y
lloblattodea (rock
c
raw
l
ers) s
h
ow an
i
nterest
i
ng m

i
xture o
f
ort
h
opteran, p
h
asm
id
,
d
ermapteran, an
ddi
cty-
o
pteran
f
eatures, w
hi
c
hl
e
d
to an ear
l
y suggest
i
on t
h
at t

h
ey are remnants o
f
apr
i
m
i
t
i
ve stoc
k
f
rom w
hi
c
hb
ot
h
ort
h
optero
id
san
dbl
atto
id
sevo
l
ve
d

. Accor
di
n
g
to Storoz
h
en
k
o (1997),
g
r
y
lloblattid fossils are known from the Middle Carboniferous onward, and these insects
w
ere amon
g
the most abundant insects in the Permian. He believes that the
g
roup included
t
h
e ancestors o
f
P
l
ecoptera, Em
bi
optera an
d
Dermaptera. As note

d
a
b
ove, Kamp’s ana
l
ys
i
s
s
h
owe
d
t
h
at cons
id
era
bl
es
i
m
il
ar
i
ty ex
i
sts
b
etween t
h

e gry
ll
o
bl
att
id
san
dd
ermapterans,
w
hich supports the conclusion reached by Giles (19
6
3) and Wheeler
e
ta
l.
(
2001
)
t
h
at t
h
e
two ma
y
be sister
g
roups.
T

he fossil record of the Embio
p
tera (web s
p
inners) extends back to the Lower Permian
,
though even by this stage the wing venation was reduced and the asymmetric genitalia
of
ma
l
es was ev
id
ent. We
b
sp
i
nners s
h
are
f
eatures w
i
t
h
t
h
eP
l
ecoptera, Dermaptera, an
d

Zoraptera], t
h
oug
hi
t
i
s unc
l
ear w
h
et
h
er t
h
ese are pr
i
m
i
t
i
ve or
d
er
i
ve
d
.W
h
ee
l

er et a
l.
(
2001) place them as the sister
g
roup to Plecoptera based on examination of two species
.
The ph
y
lo
g
enetic position of the Zoraptera (zorapterans) is also uncertain. The order i
s
n
ot encountered in the fossil record until the U
pp
er Eocene/Lower Miocene. As noted,
zorapterans s
h
are
f
eatures w
i
t
h
t
h
ewe
b
sp

i
nners, earw
i
gs, an
d
stone
fli
es;
h
owever, t
h
e
f
e
w
M
a
l
p
i
g
hi
an tu
b
u
l
es, compos
i
te a
bd

om
i
na
l
gang
li
a, an
d
two-segmente
d
tars
i
are
f
eature
s
that could ali
g
n them with the hemipteroids. Wheele
r
et al
.’s
(
2001) anal
y
sis su
gg
ests a
sister-
g

roup relationship with the Dict
y
opter
a
+
I
so
p
tera.
Included in the blattoid
g
roup of orders are the Protel
y
troptera (Permian-Lower Cre-
taceous), D
i
ctyoptera (Upper Car
b
on
if
erous-Recent), an
d
Isoptera (Lower Cretaceous-
Recent). Prote
l
ytropterans were apparent
l
yana
b
un

d
ant group
j
u
d
g
i
ng
b
yt
h
e amount o
f
f
oss
il
mater
i
a
ldi
scovere
d
,t
h
ou
gh
t
hi
sma
yb

e somew
h
at art
if
actua
lb
ecause t
h
e
i
r
highly
sclerotized, el
y
tralike fore win
g
s were readil
y
preserved. The latter are remarkabl
y
simila
r
to the el
y
tra of some earl
y
Coleoptera, and often it is onl
y
when other evidence is avail
-

a
bl
e (e.g., t
h
e
hi
n
d
w
i
ng) t
h
at t
h
e correct
id
ent
ifi
cat
i
on can
b
ema
d
e (Wootton, 1981). T
h
e
P
rote
l

ytroptera appear to
b
eanear
l
y
b
ranc
h
o
ff
t
h
e
li
ne
l
ea
di
ng to t
h
eD
i
ctyoptera, an
di
n
K
u
k
a
l

ov´a-Pec
k
’s (1991) v
i
ew were pro
b
a
bl
y ancestra
l
to t
h
e Dermaptera. T
h
eD
i
ctyoptera
(
cockroaches and mantids) and Isoptera (termites) are clearl
y
monoph
y
letic, and some au
-
thors (e.
g
., Kristensen, 1981, 1991) see little point in
g
ivin
g

each of these ordinal status
.
Cockroaches underwent a massive radiation in the U
pp
er Carboniferous (often referred to a
s
t
h
e Age o
f
Coc
k
roac
h
es
i
nv
i
ew o
f
t
h
e commonness o
f
t
h
e
i
r rema
i

ns) an
d
t
h
eor
d
er rema
i
n
s
e
xtens
i
ve to
d
ay. Fema
l
ePa
l
eozo
i
c coc
k
roac
h
es
h
a
d
a

l
ong, we
ll
-
d
eve
l
ope
d
ov
i
pos
i
tor, an
d
the evolution of the short, internal structure seen in modern forms apparentl
y
did not occur
until the end of the Mesozoic. Re
p
orts of fossilized oothecae from the U
pp
er Carbonifer-
o
us are, according to Carpenter (1992), “not very convincing.” Within the Dictyoptera tw
o
tren
d
s can
b

e seen. T
h
e coc
k
roac
h
es
b
ecame omn
i
vorous, saprop
h
agous, nocturna
l
,o
f
te
n
secon
d
ar
il
yw
i
ng
l
ess
i
nsects, w
h

ereas t
h
e mant
id
s (not
k
nown as
f
oss
il
s unt
il
t
h
e Eocene)
rema
i
ne
d
pre
d
aceous an
ddi
urna
l
.A
l
t
h
ou

gh
term
i
tes are
k
nown as
f
oss
il
son
ly f
rom t
he
Cretaceous onward, comparison of their structure and certain features of their biolo
gy
with
those of cockroaches (some of which are subsocial) indicates that the
y
are derived from
blattoidlike ancestors (Weesner, 1960). Indeed, certain venational features and the method
of
w
i
ng
f
o
ldi
ng
i
nt

h
epr
i
m
i
t
i
ve term
i
te Ma
s
toterme
s
r
esem
bl
et
h
ose o
ff
oss
il
rat
h
er t
h
a
n
e
xtant coc

k
roac
h
es
.
41
IN
S
E
C
TDI
V
ER
S
IT
Y
The relationships of the recentl
y
erected order Mantophasmatodea remain unclear.
T
hou
g
h unquestionabl
y
orthopteroid, members of this order possess a blend of features tha
t
su
gg
ests their closest relatives ma
y

be Gr
y
lloblattodea or Phasmida (Klass
et al.
, 2002)
.
T
h
e Paraneoptera (
h
em
i
ptero
id
or
d
ers) s
h
are a num
b
er o
ff
eatures. T
h
ey possess
suctor
i
a
l
mout

h
parts, an
d
t
h
ec
l
ypea
l
reg
i
on o
f
t
h
e
h
ea
di
sen
l
arge
d
to accommo
d
ate t
h
e
c
ib

ar
i
a1 suc
ki
n
g
pump (see F
ig
ure 3.17). T
h
e
i
r tars
ih
ave t
h
ree or
f
ewer se
g
ments, t
h
e
g
an
g
lia in the nerve cord are fused, there are six or fewer Malpi
g
hian tubules, and cerci ar
e

absent (at least in extant species). The anal lobe of the hind win
g
is reduced, never havin
g
more t
h
an
fi
ve ve
i
ns, an
d
w
h
en t
h
e
hi
n
d
w
i
ng
i
s
d
rawn over t
h
ea
bd

omen,
i
t
f
o
ld
s once
a
l
ong t
h
e ana
l
or
j
uga
lf
o
ld
, not
b
etween t
h
e ana
l
ve
i
ns as
i
nt

h
ep
li
coneopterans. T
h
ew
i
n
g
venat
i
on o
fh
em
i
ptero
id
s
i
s muc
h
re
d
uce
d
as a resu
l
to
ff
us

i
on o
f
pr
i
mary ve
i
ns an
d
a
l
most
complete loss of crossveins and, when both fore and hind win
g
s are present, is basicall
y
similar in each. Included in the hemipteroid assembla
g
e are four extant orders and a fe
w
entirely fossil groups, though the number of these will surely increase as the Protorthopter
a
are rewor
k
e
d
. As note
d
ear
li

er, t
h
eM
i
omoptera an
d
Ca
l
oneuro
d
ea are cons
id
ere
d
h
em
i
ptero
id b
y some aut
h
ors,
b
ut are
i
nc
l
u
d
e

di
nt
h
een
d
opterygote or p
li
coneopteran
g
roups b
y
others. The Glossel
y
trodea (Permian-Jurassic) are considered hemipteroi
d
by
Hamilton (1972) and Kukalov´a-Peck (1991) on the basis of limited win
g
-venational
features, though most authorities consider them endopterygotes close to the neuropteroids
(Carpenter, 1977, 1992),
b
ase
d
on
diff
erent
i
nterpretat
i

on o
f
t
h
e
h
omo
l
og
i
es o
f
t
h
ew
i
n
g
venat
i
on. Un
f
ortunate
l
y, t
h
e mout
h
parts an
di

mmature stages are not
k
nown. Hem
i
ptera
(true bu
g
s) (Fi
g
ure 2.7B), Psocoptera (psocids), and Th
y
sanoptera (thrips) are known fro
m
as earl
y
as the Lower Permian period. The rich fossil record of the hemipterans indicate
s
t
hat the three ma
j
or
g
roups (Sternorrh
y
ncha, Auchenorrh
y
ncha, and Heteroptera) wer
e
a
l

rea
d
y separate
di
nt
h
e Perm
i
an (Wootton, 1981; Ku
k
a
l
ov´a-Pec
k
, 1991). Psocopterans
may
b
et
h
ec
l
osest to t
h
e
h
em
i
ptero
id
stem group, t

h
oug
h
t
h
e
i
rs
i
mp
lifi
e
d
w
i
ng venat
i
on an
d
stu
bby
,tr
i
an
g
u
l
ar mout
h
parts are

d
er
i
ve
df
eatures. T
h
et
h
r
i
ps are poor
ly
represente
di
nt
he
Paleozoic fossil record, thou
g
h interestin
g
l
y
the earliest specimens still have s
y
mmetrica
l
mouthparts, unlike the extant forms in which the ri
g
ht mandible has been lost. Phthiraptera

(c
h
ew
i
ng an
d
suc
ki
ng
li
ce) are
b
are
l
y
k
nown as
f
oss
il
s
;
S
auro
d
ecte
s
,ac
h
ew

i
ng
l
ouse
f
rom
th
e Lower Cretaceous, may
h
ave paras
i
t
i
ze
d
pterosaurs. However, t
h
e many s
i
m
il
ar
i
t
i
es
b
etween t
h
em an

d
Psocoptera, nota
bl
yt
h
e spec
i
a
li
ze
d
preora
l
water-upta
k
e mec
h
an
i
sm,
o
v
ipositor structure, pol
y
trophic ovarioles, h
y
pophar
y
nx (in primitive chewin
g

lice), an
d
nuclear rDNA sequences, su
gg
est that the two are sister
g
roups (Wheele
r
et al.
,
2001).
I
ndeed, some authorities include them in a single order Psocodea.
T
h
ema
i
n
f
eature t
h
at un
i
tes mem
b
ers o
f
t
h
eO

li
goneoptera (en
d
opterygotes)
i
st
h
e pres-
ence o
f
t
h
e pupa
l
stage
b
etween t
h
e
l
arva
l
an
d
a
d
u
l
t stages
i

nt
h
e
lif
e
hi
story. Ot
h
er pro
b
a
bl
e
s
y
napomorphies include the absence of compound e
y
es in the immature sta
g
es (instead,
stemmata occur), development of the win
g
rudiments in pouches beneath the larval inte
g
u-
ment, and the absence of external genitalia in immature stages. Despite these features, early
i
nvest
i
gators exper

i
ence
d
some
diffi
cu
l
ty
i
n
d
ec
idi
ng w
h
et
h
er t
h
e group
h
a
d
a monop
h
y
l
et
ic
or po

l
yp
h
y
l
et
i
cor
i
g
i
n. T
h
e
diffi
cu
l
ty arose
b
ecause, w
h
ereas t
h
eor
d
ers Mecoptera, Lep
i-
d
optera, Tr
i

c
h
optera, D
i
ptera, an
d
S
i
p
h
onaptera s
h
ow o
b
v
i
ous a
ffi
n
i
t
i
es w
i
t
h
eac
h
ot
h

er an
d
form the so-called panorpoid complex (Hinton, 1958), the remainin
gg
roups (neuropteroids,
Coleoptera, H
y
menoptera, and Strepsiptera) appear quite distinct, each apparentl
y
bearin
g
li
tt
l
es
i
m
il
ar
i
ty to any ot
h
er en
d
opterygote group. T
h
emo
d
ern consensus, supporte
db

y
b
ot
h
morp
h
o
l
og
i
ca
l
an
d
mo
l
ecu
l
ar
d
ata,
i
st
h
at t
h
eO
li
goneoptera
i

s a monop
h
y
l
et
i
c taxon w
i
t
h
th
ema
j
or su
bg
roups
f
orm
i
n
g
ataver
y
ear
ly d
ate. However, op
i
n
i
ons

diff
er w
i
t
h
respect
42
CHAPTER
2
to the constituent sister
g
roups [see Boudreaux (1979), Kristensen (1981, 1989, 199
5
),
K
ukalov´a-Peck
(
1991, 1998
)
, Wheele
r
et al.
(
2001
)
, Kukalov´a-Peck and Lawrence
(
2004
)
]

.
Currentl
y
, the most favored view is that the two primar
y
sister
g
roups are the neuropteroid
s
+
Co
l
eo
p
tera an
d
t
h
e
p
anor
p
o
ids
+
Hymenoptera (temporar
il
y sett
i
ng as

id
et
h
e status o
f
t
h
e
S
treps
i
ptera),
b
ut
i
t must
b
e emp
h
as
i
ze
d
t
h
at t
h
e support
i
ng ev

id
ence
i
s not strong. Putat
i
ve
s
y
napomorp
hi
es o
f
t
h
e
f
ormer
g
roup
i
nc
l
u
d
et
h
ea
b
sence o
f

cruc
i
ate ventra
l
nec
k
mus
-
c
les, pro
g
nathous head with a
g
ula, female
g
enitalia, and campodeiform larva; those of the
p
anor
p
oids
+
Hy
menoptera are ortho
g
nathous head without a
g
ula, eruciform larva wit
h
s
i

ng
l
e-c
l
awe
dl
egs, an
d
a
bili
ty to pro
d
uce s
ilk f
rom
l
a
bi
a
l
g
l
an
d
s. T
h
ema
j
or
i

ty o
f
mo
l
ecu
l
ar
p
h
y
l
ogenet
i
c ana
l
yses support t
hi
s arrangement (see W
h
ee
l
er, 1989; W
h
ee
l
e
r
et a
l.
,

2001).
Th
e neuroptero
id
group
i
nc
l
u
d
es t
h
ree qu
i
te
h
omogeneous or
d
ers—Neuroptera
(
lacewin
g
s), Me
g
aloptera (alderflies and dobsonflies), and Raphidioptera (snakeflies)
—
w
hich are sometimes included in a sin
g
le order primaril

y
on the basis of their ver
y
similar
o
vipositor (and the difficulty in determining good apomorphic characters for each). Neu
-
roptera an
d
Mega
l
optera were a
l
rea
d
ywe
ll
esta
bli
s
h
e
di
nt
h
e Perm
i
an an
d
pro

b
a
bl
y reac
h
e
d
t
h
e
i
r pea
kdi
vers
i
ty
i
nt
h
eTr
i
ass
i
c/Jurass
i
c. Foss
il
Rap
hidi
optera are not

k
nown unt
il
t
h
e
J
urassic [reports su
gg
estin
g
their earlier existence are dubious accordin
g
to Kukalov´a-Peck
(
1991)] and never reached the abundance of the other neuro
p
teroids.
R
emains of genuine Coleoptera (beetles) are known from the Upper Permian period
.
Somew
h
at ear
li
er e
l
ytra
lik
e rema

i
ns, or
i
g
i
na
ll
yt
h
oug
h
tto
b
e
f
rom
b
eet
l
es, are now
k
nown
to
b
e
l
ong to t
h
e Prote
l

ytroptera (see a
b
ove). T
h
oug
h
some ear
l
ypa
l
eonto
l
og
i
sts suggeste
d
that the Coleoptera had protorthopteran ancestors, impl
y
in
g
at least a diph
y
letic ori
g
in fo
r
the endopter
yg
otes, Crowson (19
6

0, 1981) and Kukalov´a-Peck (1991), amon
g
others, made
a case for common ancestr
y
with the neuropteroids. Accordin
g
to Crowson, this proposal
i
ssu
b
stant
i
ate
db
yt
h
e Lower Perm
i
an
f
oss
il
T
sh
e
k
ar
d
oco

l
eu
s
,
w
hi
c
hi
s
i
nterme
di
ate
in
f
orm between Coleoptera and Megaloptera. Crowson (197
5
) include
d
Tsh
e
k
ar
d
oco
l
eu
s
in
t

h
esu
b
or
d
er Protoco
l
eoptera, w
i
t
hi
nt
h
eCo
l
eoptera. Ku
k
a
l
ov´a-Pec
k
(1991),
h
owever, pre-
f
erred to place it (and other beetlelike insects known from el
y
tra in the same period) in a
separate, probabl
y

paraph
y
letic order. The Coleoptera-neuropteroid sister-
g
roup relation
-
s
hi
p
i
s strong
l
y supporte
db
yt
h
e extens
i
ve ana
l
ys
i
so
f
W
h
ee
l
er
e

ta
l
. (2001)
.
Th
e pos
i
t
i
on o
f
t
h
e Streps
i
ptera (sty
l
opo
id
s),
hi
g
hl
ymo
difi
e
d
en
d
oparas

i
t
i
c
i
nsects,
rema
i
ns controvers
i
a
l
.T
h
e ear
li
est
f
oss
il
s,
f
rom t
h
e Lower Cretaceous, are ass
i
gna
bl
eto
the extant famil

y
Elenchidae, so that speculation on their ori
g
in is based on comparative
m
orpholo
gy
. Kristensen (1981, 1989, 1991) has repeatedl
y
noted that, based on the occur-
rence of instars with external wing buds and the carryover of larval eyes to the adult instar,
t
h
e sty
l
opo
id
s cou
ld b
e cons
id
ere
d
exopterygotes. However, on t
h
e
b
as
i
so

f
many ot
h
e
r
f
eatures, t
h
ey are unquest
i
ona
bl
yen
d
opterygotes an
d
on
diff
erent occas
i
ons t
h
ey
h
ave
b
een
allied with the panorpoids, H
y
menoptera, and Coleoptera. Man

y
authorities a
g
ree that the
l
atter is the most likel
y
arran
g
ement, thou
g
h opinions differ as to whether, for example
,
they are highly modified beetles [Crowson (1981) includes them as a family, Stylopidae, of
Co
l
eo
p
tera] or are t
h
es
i
ster or
d
er o
f
t
h
eCo
l

eo
p
tera (Bou
d
reaux, 1979; Kr
i
stensen, 1981;
K
u
k
a
l
ov´a-Pec
k
, 1991, 1998; Ku
k
a
l
ov´a-Pec
k
an
d
Lawrence, 1993, 2004). In support o
f
t
he
l
atter v
i
ew t

h
e use o
f
t
h
e
hi
n
d
w
i
n
g
son
ly i
n
fligh
tan
df
eatures o
f
t
h
e
hi
n
d
w
i
n

g
venat
i
on
are cited as s
y
napomorphies. Other features taken to indicate a close association between
the two
g
roups are the extensive sclerotization of the sternum (rather than the ter
g
um), th
e
resem
bl
ance
b
etween t
h
e
fi
rst
i
nstar
l
arva o
f
Streps
i
ptera an

d
t
h
etr
i
ungu
li
n
l
arva o
f
t
h
e
b
eet
l
e
f
am
ili
es Me
l
o
id
ae an
d
R
hi
p

i
p
h
or
id
ae, an
d
t
h
es
i
m
il
ar
i
ty
b
etween t
h
e
h
a
bi
ts o
f
en-
d
oparas
i
t

i
c
f
orms o
f
R
hi
p
i
p
h
or
id
ae an
d
t
h
ose o
f
Streps
i
ptera. B
y
contrast, a num
b
er o
f
43
IN
S

E
C
TDI
V
ER
S
IT
Y
molecular or combined morpholo
g
ical/molecular anal
y
ses have come out stron
g
l
y
in sup-
port of a Strepsiptera-Diptera sister-
g
roup relationship (see references in Whitin
g
, 1998 and
W
heeler
et al.
,
2001)
.
S
ynapomorp

hi
c
f
eatures o
f
t
h
eor
d
ers t
h
at ma
k
eupt
h
e panorpo
id
comp
l
ex ar
e
“a
d
m
i
tte
dl
y
i
nconsp

i
cuous” accor
di
ng to Kr
i
stensen (1991). T
h
ey
i
nc
l
u
d
et
h
e vest
i
g
i
a
l
or
l
ost ov
i
pos
i
tor,
i
nsert

i
on o
f
t
h
ep
l
eura
l
musc
l
eont
h
e
fi
rst ax
ill
ar
y
p
l
ate, transverse
ly di
-
vided larval sti
p
es, and loss or addition of various muscles in the larval labium and maxilla.
Within the panorpoid complex two well-substantiated sister
g
roups (sometimes desi

g
nated
su
p
eror
d
ers) Ant
li
o
ph
ora (Meco
p
tera, D
ip
tera, an
d
S
iph
ona
p
tera) an
d
Am
phi
esmeno
p
tera
(Tr
i
c

h
optera an
d
Lep
id
optera) are recogn
i
ze
d
.Ana
b
un
d
ance o
f
mecoptera
lik
e
f
oss
il
w
i
ngs
h
ave
b
een recovere
df
rom Pa

l
eozo
i
c strata,
b
ut
i
t
f
requent
l
y
h
as
b
een
diffi
cu
l
tto
d
eterm
i
n
e
w
hether these belon
g
to Mecoptera, Diptera, or the stem
g

roup ancestral to both of these
orders. Nevertheless,
g
enuine Mecoptera (scorpionflies) are known from Upper Permian
d
eposits and may have been the first endopterygotes to diversify widely. The close lin
k
b
etween D
i
ptera (true
fli
es) an
d
Mecoptera
i
mp
li
e
d
a
b
ove, t
h
at
i
s,
b
yt
h

e
i
na
bili
ty to
di
st
i
n-
gu
i
s
hb
etween
f
oss
il
w
i
ngs o
f
t
h
e two groups,
i
s supporte
db
yt
h
eex

i
stence o
ff
our-w
i
nge
d
fossil “flies”
(
P
ermotanyderu
s
a
n
d
C
horistotanyderus
)
in
t
he Upper Permian. These ma
y
not be true Diptera but
j
ust off the main evolutionar
y
line in a separate
g
roup Protodiptera.
I

nterestingly, the only direct evidence for the existence of Paleozoic Diptera (a single win
g
of
P
ermotipu
l
a patricia
,
c
o
ll
ecte
df
rom Upper Perm
i
an
d
epos
i
ts
i
n Austra
li
a
d
ur
i
ng t
h
e

1920s) was lost for more than
5
0 years, only to be rediscovered in the British Museu
m
(London) and redescribed in the late 1980s (Willmann, 1989). Thou
g
h the
y
ma
y
have ori
g
-
inated from the mecopteroid stem
g
roup durin
g
the Carboniferous (Kukalov´a-Peck, 1991),
t
he Si
p
hona
p
tera (fleas) do not a
pp
ear in the fossil record until the Lower Cretaceous. A
s
th
e
i

r names
i
n
di
cate, some o
f
t
h
ese
(
S
aurop
h
t
h
irus
a
n
d
S
aurop
h
t
h
iroi
d
es) are t
h
oug
h

tto
h
ave poss
ibl
y
b
een paras
i
tes o
ffl
y
i
ng rept
il
es. Because t
h
ey are so
hi
g
hl
ymo
difi
e
df
or t
h
e
i
r
ectoparas

i
t
i
cmo
d
eo
f lif
e, comparat
i
ve stu
di
es o
fli
v
i
n
gfl
eas must
b
e
i
nterprete
d
caut
i
ous
ly
.
With their apodous larvae and adecticous pupae, fleas resemble Diptera, su
gg

estin
g
the tw
o
ma
y
be sister
g
roups. However, most authors, notin
g
similarities in sperm ultrastructure,
th
orac
i
cs
k
e
l
eton, nervous system,
f
oregut, an
d
mo
l
ecu
l
ar genet
i
c sequences
b

e
li
eve t
h
at
th
ese
i
n
di
cate a s
i
ster-group re
l
at
i
ons
hi
p
b
etween t
h
e Mecoptera an
d
S
i
p
h
onaptera.
T

h
e monop
h
y
l
et
i
c nature o
f
t
h
e Amp
hi
esmenoptera
i
s unquest
i
one
d
w
i
t
h
more t
h
an 2
0
s
y
napomorphies common to the Trichoptera (caddisflies) and Lepidoptera (butterflies and

moths) (Kristensen, 1984). It is presumed that these orders had their ori
g
in in the Paleozoic
from mecopteralike ancestors, though there is little in the fossil record to substantiate thi
s
c
l
a
i
m. Micropt
y
sme
lla
an
d
re
l
ate
df
oss
il
s
f
rom t
h
e Lower Perm
i
an may
b
e mem

b
ers o
f
th
e stem group
f
rom w
hi
c
h
t
h
etwoor
d
ers are
d
er
i
ve
d
. From
hi
s compar
i
son o
f
pr
i
m
i

t
i
ve
members of both orders, Ross (19
6
7) su
gg
ested that the common ancestor was in the adul
t
sta
g
e trichopteran and in the larval sta
g
e lepidopteran in character. In the evolution o
f
T
richo
p
tera the larva became s
p
ecialized for an a
q
uatic existence, but the adult remaine
d
pr
i
m
i
t
i

ve. A
l
ong t
h
e
li
ne
l
ea
di
ng to Lep
id
optera t
h
e
l
arva reta
i
ne
di
ts pr
i
m
i
t
i
ve
f
eatures,
b

u
t
th
ea
d
u
l
t
b
ecame spec
i
a
li
ze
d
, espec
i
a
ll
y
i
nt
h
e
d
eve
l
opment o
f
t

h
e suctor
i
a
l
pro
b
osc
i
s. T
h
e
ear
li
est
g
enu
i
ne ca
ddi
s
fly f
oss
il
s are
f
rom t
h
eTr
i

ass
i
can
d
some o
f
t
h
ese are ass
ig
na
bl
e
t
o extant families. Most extant families probabl
y
ori
g
inated in the Jurassic (Henni
g
, 1981),
and caddis fl
y
cases have been found in Lower Cretaceous deposits. Fossil Lepidoptera ar
e
k
nown w
i
t
h

certa
i
nty on
l
y
f
rom t
h
e Lower Jurass
i
c onwar
d
, ear
li
er spec
i
mens
f
rom t
he
T
r
i
ass
i
c
b
e
i
ng more

lik
e
l
yTr
i
c
h
optera or Mecoptera. L
ik
et
h
ose o
f
extant M
i
cropter
i
g
id
ae,
a
d
u
l
ts o
f
t
h
e ear
li

est Lep
id
optera pro
b
a
bly h
a
d
c
h
ew
i
n
g
mout
h
parts an
d
were po
ll
en
f
ee
d
ers
;
44
CHAPTER
2
the larvae probabl

y
fed on liverworts and mosses. The
g
reat adaptive radiation of the orde
r
probabl
y
came at the end of the Cretaceous period and be
y
ond and was correlated with the
ev
olution of the flowerin
g
plants
.
Th
oug
h
genera
ll
ya
li
gne
d
w
i
t
h
t
h

e panorpo
id
s, t
h
e Hymenoptera (
b
ees, wasps, ants,
saw
fli
es) are qu
i
te
di
st
i
nct
f
rom a
ll
ot
h
er en
d
opterygotes. In
d
ee
d
,t
h
e recent stu

d
y
by
K
u
k
a
l
ov´a-Pec
k
an
d
Lawrence (2004)
h
as t
h
eH
y
menoptera as t
h
es
i
ster
g
roup to a
ll
ot
h
e
r

e
ndopter
yg
otes. Fossils are known from the Triassic period, but these were alread
y
quit
e
specialized, clearl
y
reco
g
nizable as belon
g
in
g
to the extant s
y
mph
y
tan famil
y
X
y
elidae
.
Mem
b
ers o
f
t

h
esu
b
or
d
er Apocr
i
ta, w
hi
c
h
conta
i
ns t
h
e paras
i
t
i
can
d
st
i
ng
i
ng
f
orms, are not
k
nown as

f
oss
il
s unt
il
t
h
e Jurass
i
can
d
Cretaceous per
i
o
d
s. T
h
e great a
d
apt
i
ve ra
di
at
i
on o
f
t
hi
ssu

b
or
d
er was,
lik
et
h
at o
f
t
h
e Lep
id
optera, c
l
ear
l
y assoc
i
ate
d
w
i
t
h
t
h
eevo
l
ut

i
on o
f
t
he
an
g
iosperms (see Section 4.1)
.
T
he fore
g
oin
g
discussion of the evolutionar
y
relationships within the Insecta is sum
-
m
arized in Figure 2.6.
3
.3. Origin and Functions of the Pup
a
As note
di
nt
h
e prev
i
ous sect

i
on t
h
eO
lig
oneoptera (en
d
opter
yg
ote or
d
ers) are c
h
arac-
terized b
y
the presence of a pupal sta
g
e between the
j
uvenile and adult phases in the lif
e
histor
y
. The development of this sta
g
e, which serves various functions, is a ma
j
or reason
f

or t
h
e success (
i
.e.,
di
vers
i
ty) o
f
en
d
opterygotes. G
i
ven t
h
e
i
mportance o
f
t
h
e pupa
l
stage
,
i
t
i
s not surpr

i
s
i
ng t
h
at severa
l
t
h
eor
i
es
h
ave
b
een propose
df
or
i
ts or
i
g
i
n(F
i
gure 2.8).
F
I
G
URE 2.8.

Th
eor
i
es
f
or t
h
eor
igi
no
f
t
h
e pupa
l
sta
g
e. A
bb
rev
i
at
i
ons: A, a
d
u
l
t; E, e
gg
;L,

l
arva; N, n
y
mp
h
;P,
pupa. [Partl
y
after H. E. Hinton, 1963b, The ori
g
in and function of the pupal sta
g
e,
P
roc. R. Entomol.
S
oc. Lond.
S
er.
A
38
:
77–85. By permission of the Royal Entomological Society.
]
45
IN
S
E
C
TDI

V
ER
S
IT
Y
Amon
g
the earliest proposals was that of Berlese (1913, cited in Hinton, 19
6
3b) wh
o
u
sed the principle of “onto
g
en
y
recapitulates ph
y
lo
g
en
y
” to develop his ideas. Durin
g
it
s
d
evelopment an insect embr
y
o passes throu

g
h three distinct sta
g
es. In the first (protopod)
stage no appen
d
ages are v
i
s
ibl
e; t
hi
s
i
s
f
o
ll
owe
db
yt
h
epo
l
ypo
d
stage (
i
nw
hi

c
h
appen
d
ages
are present on most segments); an
dfi
na
ll
yt
h
eo
li
gopo
d
stage (w
h
en t
h
e appen
d
ages on
th
ea
bd
omen
h
ave
b
een resor

b
e
d
) (see C
h
apter 20, Sect
i
on 7.1). Ber
l
ese su
gg
este
d
t
h
at
t
he e
gg
s of exopter
yg
otes, b
y
virtue of their
g
reater
y
olk reserves, hatch in a postoli
g
opod

sta
g
e of development, whereas the e
gg
s of endopter
yg
otes, which have less
y
olk, hatch
i
nt
h
epo
l
ypo
d
or o
li
gopo
d
stages. Accor
di
ng to Ber
l
ese, t
h
e
l
arvae o
f

en
d
opterygotes
correspon
d
to
f
ree-
li
v
i
ng em
b
ryon
i
c stages, w
hil
et
h
e pupa represents t
h
e compress
i
on
o
f
t
h
e exopterygote nymp
h

a
l
stages
i
ntoas
i
ng
l
e
i
nstar. T
h
ema
j
or
f
au
l
to
f
Ber
l
ese’s
id
ea
is the absence of evidence that the e
gg
s of exopter
yg
otes have a better suppl

y
of
y
olk
t
han those of endopter
yg
otes (Hinton 1963b). Further, the theor
y
implies that abdominal
prolegs (see Chapter 3, Section 5.2) are homologous with thoracic legs. Hinton (1963b
)
argue
d
t
h
at pro
l
egs are secon
d
ary
l
arva
l
structures, t
h
oug
h
t
hi

sc
l
a
i
m
i
s not
j
ust
ifi
e
d
g
i
ven
t
he multilegged nature of the ancestors of insects (Heslop-Harrison, 19
5
8; Kukalov´a-Peck,
1991). Truman and Riddiford (1999, 2002) have resurrected interest in Berlese’s proposal
followin
g
their detailed studies of the endocrine control of embr
y
onic development
.
T
ruman and Riddiford compared the subtle shifts in the timing of juvenile hormone activity
i
nem

b
ryos o
fh
em
i
meta
b
o
l
ous an
dh
o
l
ometa
b
o
l
ous
i
nsects. As we
ll
,t
h
ey exam
i
ne
d
t
h
e

e
ff
ects o
f
treat
i
ng em
b
ryos w
i
t
h
extra
j
uven
il
e
h
ormone or precocene (w
hi
c
hd
estroy
s
t
he corpora allata) at various sta
g
es of development. Truman and Riddiford ar
g
ued that

in ancestral hemimetabolous insects there were three postembr
y
onic sta
g
es: pron
y
mph,
n
y
mph and adult. These correspond to the larval, pupal, and adult sta
g
es, respectivel
y
,o
f
h
o
l
ometa
b
ous
f
orms. In mo
d
ern
h
em
i
meta
b

o
l
ous
f
orms t
h
e pronymp
hh
as
b
een reta
i
ne
d
asas
h
ort-
li
ve
d
, non-
f
ee
di
ng stage, w
hi
c
h
typ
i

ca
ll
y
i
s spent w
i
t
hi
nt
h
e egg. By contrast,
i
n
h
o
l
ometa
b
o
l
ous
i
nsects w
i
t
h
ear
li
er secret
i

on o
fj
uven
il
e
h
ormone t
h
e pron
y
mp
h
t
ook on increasin
g
importance, becomin
g
a lon
g
-lived, multi-instar feedin
g
sta
g
e while
t
he n
y
mphal instars, as proposed b
y
Berlese, would be reduced to the sin

g
le (pupal)
stage.
Poyarkoff’s (1914) theory (cited in Hinton, 1963b) offers a major advantage over
B
er
l
ese’s, name
l
y, t
h
at
i
t prov
id
es a causa
l
exp
l
anat
i
on
f
or t
h
eor
i
g
i
nan

df
unct
i
on o
f
t
h
e
pupal sta
g
e. Accordin
g
to this theor
y
, the e
gg
s of both endopter
yg
otes and exopter
yg
ote
s
h
atch at a similar sta
g
e of development. The adult sta
g
e in the exopter
yg
ote ancestors of

t
he endopterygotes became divided into two instars, the pupa and the imago. Poyarkof
f
suggested that the subimago of Ephemeroptera (see Chapter 6, Section 2) and the “pupal”
stage of some exopterygotes (see Chapter 8, Sections 4 and
5
) are equivalent to the en
-
d
opter
yg
ote pupal sta
g
e. Further, the pupa (especiall
y
that of primitive endopter
yg
otes such
as Neuroptera) resembles the adult rather than the larva. In his view the pupal sta
g
e evolve
d
in response to the need for a mold in which the adult systems, especially flight musculature,
cou
ld b
e constructe
d
.T
h
e secon

d
(pupa
l
-
i
mag
i
na
l
)mo
l
t was t
h
en necessary
i
nor
d
er t
h
at
th
e new musc
l
es cou
ld b
ecome attac
h
e
d
to t

h
e exos
k
e
l
eton. In Poyar
k
o
ff
’s t
h
eory t
h
ere
i
s
no
diff
erence
b
etween t
h
een
d
opter
yg
ote
l
arva an
d

t
h
e exopter
g
ote n
y
mp
h
.
∗
∗
Because t
h
e
y
were cons
id
ere
d
or
igi
na
lly
to
b
equ
i
te
di
st

i
nct, t
h
e
j
uven
il
e sta
g
es o
f
exopter
yg
otes an
d
en-
d
opterygotes were referred to as “nymph” and “larva,” respectively. The modern view (see Hinton’s theory) i
s
t
h
at nymp
h
a
l
an
dl
arva
l
stages are

h
omo
l
ogous, an
d
t
h
at pterygote
j
uven
il
e stages s
h
ou
ld b
eca
ll
e
dl
arvae. Fo
r
c
l
ar
i
t
y
o
fdi
scuss

i
on,
h
owever,
i
nt
hi
sc
h
apter on
ly
,t
h
e tra
di
t
i
ona
ldi
st
i
nct
i
on
h
as
b
een reta
i
ne

d
.
4
6
CHAPTER
2
T
hou
g
h it received support from some quarters, Po
y
arkoff’s theor
y
was stron
g
l
y
crit-
i
cized b
y
Heslop-Harrison (1958) and Hinton (1963b). Heslop-Harrison claimed that the
e
xplanation
g
iven for the ori
g
in of the pupal sta
g
e is teleolo

g
ical; in other words, Po
y
arkoff’s
e
xp
l
anat
i
on
i
st
h
at t
h
e pupa
l
stage arose
i
n
f
u
lfill
ment o
f
a “nee
d
.” H
i
nton state

d
t
h
at t
h
ere
i
s
di
rect ev
id
ence aga
i
nst Poyar
k
o
ff
’s
id
ea concern
i
ng t
h
e
f
unct
i
on o
f
t

h
e pupa
l
stage. F
i
rst
,
i
t
h
as
b
een s
h
own t
h
at tono
fib
r
ill
ae (m
i
crotu
b
u
l
es w
i
t
hi

nep
id
erma
l
ce
ll
sw
hi
c
h
attac
h
mus
-
c
les to the exoskeleton) (see Fi
g
ure 14.1) can be formed lon
g
after the pupal-adult mol
t
has occurred. Second, even in hi
g
hl
y
advanced endopter
yg
otes the fiber rudiments of the
wi
ng musc

l
es are present at t
h
et
i
me o
fh
atc
hi
ng. T
h
ese
d
eve
l
op
i
nt
h
e
l
arva
i
n prec
i
se
l
yt
h
e

same way as t
h
e
fli
g
h
t musc
l
es o
f
many pr
i
m
i
t
i
ve exopterygotes. In ot
h
er wor
d
s, no mo
l
t
i
s requ
i
re
d
.
Implicit in the theories of Berlese, Po

y
arkoff, and Hinton (19
6
3b) is the evolution o
f
e
ndopter
yg
otes from exopter
yg
ote ancestors. Heslop-Harrison (1958) su
gg
ested, however
,
that the earliest forms of both groups were present at the same time and evolved from
a common ancestor. T
hi
s ancestor
h
a
d
a
lif
e
hi
story s
i
m
il
ar to t

h
at o
f
mo
d
ern Isoptera
an
d
T
h
ysanoptera, name
l
y, EG
G
→
LARVAL INSTARS (s
h
ow
i
ng no s
i
gn o
f
w
i
ngs)
→
N
YMPHAL INSTARS (havin
g

external win
g
buds)
→
A
DULT (see Chapter 7, Section
5;
Chapter 8, Section 5; and Fi
g
ure 21.15). Heslop-Harrison proposed that in the evolution of
e
xopterygotes the larval instars were suppressed, and the modern free-living juvenile stage
s
c
orrespon
d
to t
h
e nymp
h
a
li
nstars o
f
t
h
e ancestors. In en
d
opterygote evo
l

ut
i
on t
h
e nymp
h
a
l
stages were compresse
di
nto t
h
e prepupa
l
an
d
pupa
l
stages o
f
mo
d
ern
f
orms. (T
h
e prepupa
l
sta
g

e is a period of quiescence in the last larval instar prior to the molt to the pupa. It is no
t
a distinct instar.) Thus, Berlese’s ori
g
inal concept that the pupa comprised the onto
g
eneti
c
c
ounterparts of n
y
mphal instars was supported b
y
Heslop-Harrison. The basis of Heslop
-
Harr
i
son’s t
h
eory was
hi
s comparat
i
ve stu
d
yo
f
t
h
e

lif
e
hi
story o
f
var
i
ous
h
omopterans
i
n
whi
c
h
t
h
e
l
ast nymp
h
a
li
nstar
i
s
di
v
id
e

di
nto two p
h
ases. In t
h
e most pr
i
m
i
t
i
ve con
di
t
i
on
t
h
e
fi
rst o
f
t
h
ese p
h
ases
i
sanact
i

ve one w
h
ere t
h
e
i
nsect
f
ee
d
san
d
/or prepares
i
ts “pupa
l
”
c
hamber. In the most advanced condition both
p
hases are inactive, and there are, for all
i
ntents and purposes, distinct prepupal and pupal sta
g
es, as in true endopter
yg
otes
.
Th
ema

i
n genera
l
cr
i
t
i
c
i
sm o
f
Hes
l
op-Harr
i
son’s t
h
eory
i
st
h
at
i
t
l
ac
k
s support
i
ng ev

i
-
d
ence. More spec
ifi
ccr
i
t
i
c
i
sms are t
h
at (1) t
h
ema
j
or
i
ty o
f
ear
l
y pterygote
f
oss
il
s(
i
.e.,

f
rom
t
h
e Car
b
on
if
erous per
i
o
d
)
b
e
l
ong to exopterygote groups, en
d
opterygotes most
l
y appear-
i
n
g
for the first time in the Permian, leadin
g
most authorities to believe that endopter
yg
ote
s

c
ame from exopter
yg
ote ancestors; (2) the Isoptera and Th
y
sanoptera on which Heslop
-
Harrison’s “primitive life history” was based are two highly specialized exopterygote orders
;
an
d
(3) t
h
e
i
mp
li
e
dh
omo
l
ogy o
f
t
h
een
d
opterygote pupa an
d
t

h
e
l
ast
j
uven
il
e
i
nstars o
f
t
h
e exopterygote
h
omopterans stu
di
e
db
y Hes
l
op-Harr
i
son
i
s not
j
ust
ifi
e

d
[see
di
scuss
i
o
n
i
n Hinton
(
19
6
3b
)
]
.
P
erhaps the attraction of Hinton’s (1963b) theor
y
is its simplicit
y
. It avoids the “sup
-
pression of larval,” “compression of nymphal,” and “expansion of imaginal” stages, found
i
nt
h
e ear
li
er t

h
eor
i
es an
dp
rov
id
esas
i
m
pl
e
f
unct
i
ona
l
ex
pl
anat
i
on
f
or t
h
eevo
l
ut
i
on o

fa
pupa
l
stage
.
In H
i
nton’s t
h
eor
y
t
h
e pupa
i
s
h
omo
l
o
g
ous w
i
t
h
t
h
e
fi
na

l
ny
mp
h
a
li
nstar o
f
exopter
y
-
g
otes, and the terms “larva” and “n
y
mph” are s
y
non
y
mous. Hinton proposed that, durin
g
the evolution of endopter
yg
otes, the last
j
uvenile sta
g
e (with external win
g
s) was retained
to comp

l
ete t
h
e
li
n
kb
etween t
h
e ear
li
er
j
uven
il
e stages (
l
arvae w
i
t
hi
nterna
l
w
i
ngs) an
d
t
h
e

a
d
u
l
t,
h
ence t
h
e genera
l
resem
bl
ance
b
etween t
h
e pupa an
d
a
d
u
l
t
i
nmo
d
ern en
d
opterygotes.
In

i
t
i
a
lly
,t
h
e pupa wou
ld
a
l
so resem
bl
et
h
e ear
li
er
i
nstars (
j
ust as t
h
e
fi
na
li
nstar n
y
mp

h
o
f
47
IN
S
E
C
TDI
V
ER
S
IT
Y
modern exopter
yg
otes resembles both the adult and the earlier n
y
mphal sta
g
es). Once this
intermediate sta
g
e had been established it is eas
y
to visualize how the earlier
j
uvenile sta
g
e

s
could have become more and more specialized (for feedin
g
and accumulatin
g
reserves) an
d
qu
i
te
diff
erent morp
h
o
l
og
i
ca
ll
y
f
rom
b
ot
h
t
h
e pupa an
d
t

h
ea
d
u
l
t(t
h
e repro
d
uct
i
ve an
d
di
spersa
l
stage). At t
h
e same t
i
me t
h
e pupa
i
tse
lf b
ecame more spec
i
a
li

ze
d
. It cease
df
ee
d
-
in
g
activel
y
, became less mobile, and was concerned solel
y
with metamorphosis from the
j
uvenile to the adult form.
C
oncernin
g
the functional si
g
nificance of the pupal sta
g
e, Hinton su
gg
ested that, as the
en
d
opterygote con
di

t
i
on evo
l
ve
d
,t
h
ere was
i
nsu
ffi
c
i
ent space
i
nt
h
et
h
orax to accommo
d
at
e
b
ot
h
t
h
e “norma

l
” contents (musc
l
es an
d
ot
h
er organ systems) an
d
t
h
ew
i
ng ru
di
ments. T
h
us
,
th
e
f
unct
i
on o
f
t
h
e
l

arva
l
-pupa
l
mo
l
t was to eva
gi
nate t
h
ew
i
n
g
s. T
hi
swou
ld
perm
i
t not
onl
y
considerable win
gg
rowth (as
g
reatl
y
folded structures within the pupal external win

g
cases) but also the enormous
g
rowth of the ima
g
inal win
g
muscles within the thorax. Th
e
l
atter
i
s
f
ac
ili
tate
d
,o
f
course,
b
y
hi
sto
l
ys
i
so
f

t
h
e
l
arva
l
musc
l
es (a process t
h
at
i
so
f
te
n
not comp
l
ete
df
or many
h
ours a
f
ter t
h
e pupa
l
-a
d

u
l
tmo
l
t). T
h
e
f
unct
i
on o
f
t
h
e pupa
l
-a
d
u
l
t
mo
l
t
i
ss
i
mp
ly
to e

ff
ect re
l
ease o
f
t
h
ew
i
n
g
s
f
rom t
h
e pupa
l
case. T
h
eor
igi
na
lf
unct
i
on
of the pupal sta
g
e was, then, to create space for win
g

and win
g
muscle development. But,
once a sta
g
e had been developed in the life histor
y
in which structural rearran
g
ement could
t
a
k
ep
l
ace, t
h
e way was open
f
or
i
ncreas
i
ng
di
vergence o
fj
uven
il
ean

d
a
d
u
l
t
h
a
bi
ts an
d
,
su
b
sequent
l
y, a
d
ecrease
i
nt
h
e compet
i
t
i
on
f
or
f

oo
d
, space, etc.
b
etween t
h
e two stages.
F
o
r
m
an
y
spec
i
es t
h
e pupa
h
as ta
k
en on a t
hi
r
df
unct
i
on, name
ly
as a sta

g
e
i
nw
hi
c
h
t
h
e
insect can pass throu
g
h adverse climatic conditions, especiall
y
freezin
g
temperatures.
4. The Success of Insect
s
The de
g
ree of success achieved b
y
a
g
roup of or
g
anisms can be measured either a
s
t

he total number of or
g
anisms within the
g
roup or, more commonl
y
, as the number o
f
d
ifferent species of organisms that comprise the group. On either account the insects mus
t
b
e cons
id
ere
dhi
g
hl
y success
f
u
l
. Success
i
s
d
epen
d
ent on two
i

nteract
i
ng
f
actors: (1) t
h
e
potent
i
a
l
o
f
t
h
e group
f
or a
d
apt
i
ng to new env
i
ronmenta
l
con
di
t
i
ons an

d
(2) t
h
e
d
egree t
o
w
hich the environmental conditions chan
g
e. As success measured as the number of different
species is a direct result of evolution, the environmental chan
g
es that must be considere
d
are the long-term climatic changes that have occurred in different parts of the world over
a
per
i
o
d
o
f
severa
lh
un
d
re
d
m

illi
on years
.
4.1. The Adaptab
i
l
i
ty o
f
Insects
The basic feature of insects to which their success can be attributed must surel
y
b
e
th
at t
h
ey are art
h
ropo
d
s. As suc
h
t
h
ey are en
d
owe
d
w

i
t
h
a
b
o
d
yp
l
an t
h
at
i
s super
i
or to
th
at o
f
any ot
h
er
i
nverte
b
rate group. O
f
t
h
evar

i
ous art
h
ropo
d
an
f
eatures t
h
e
i
ntegument
is
th
e most
i
mportant, as
i
t serves a var
i
et
y
o
ff
unct
i
ons. Its
ligh
tness an
d

stren
g
t
h
ma
k
e
i
tan
excellent skeleton for attachment of muscles as well as a “shell” within which the tissues
are protected. Its ph
y
sical structure (usuall
y
includin
g
an outermost wax la
y
er) makes i
t
espec
i
a
ll
y
i
mportant
i
nt
h

e water re
l
at
i
ons o
f
art
h
ropo
d
s. Because t
h
ey are genera
ll
y sma
ll
organ
i
sms, art
h
ropo
d
s
i
na
l
most any env
i
ronment
f

ace t
h
e pro
bl
em o
f
ma
i
nta
i
n
i
ngasu
i
ta
ble
sa
l
tan
d
water
b
a
l
ance w
i
t
hi
nt
h

e
i
r
b
o
di
es. T
h
ema
g
n
i
tu
d
eo
f
t
h
e pro
bl
em (an
d
,t
h
ere
f
ore, t
he
ener
gy

expended in solvin
g
it) is
g
reatl
y
reduced b
y
the impermeable cuticle (see Chapters
48
CHAPTER
2
1
1 and 18). Arthropods are se
g
mented animals and therefore have been able to exploit the
advanta
g
es of ta
g
mosis to the full extent. Directl
y
related to this is the adaptabilit
y
of th
e
basic
j
ointed limb, a feature used full
y

b
y
different
g
roups of arthropods (see Fi
g
ure 1.6
an
dd
escr
i
pt
i
ons o
f
segmenta
l
appen
d
ages
i
nC
h
apter 3).
As a
ll
art
h
ropo
d

s possess t
h
ese a
d
vantageous
f
eatures, t
h
eo
b
v
i
ous quest
i
on to as
k
i
s“W
hy h
ave
i
nsects
b
een espec
i
a
lly
success
f
u

l
?” or, put
diff
erent
ly
,“W
h
at
f
eatures
do
i
nsects have that other arthropods do not?” Answerin
g
this question will provide onl
ya
partial response for two reasons. First, as was stressed above, and is discussed more full
y
in
S
ect
i
on 4.2, t
h
eenv
i
ronmenta
l
c
h

anges t
h
at ta
k
ep
l
ace are a
l
so very
i
mportant
i
n
d
eterm
i
n
i
n
g
success. Cons
id
er,
f
or examp
l
e, t
h
e Crustacea. Compare
d

to ot
h
er
i
nverte
b
rate groups t
h
ey
m
ust
b
e regar
d
e
d
as success
f
u
l
(at
l
east 40,000 extant spec
i
es
h
ave
b
een
d

escr
ib
e
d
), yet
in
c
omparison to the Insecta the
y
come a ver
y
distant second. Althou
g
h this is related partl
y
to
their different features, it must also reflect the different habitats in which the
y
evolved. As
a predominantly marine group, crustaceans evolved under relatively stable environmental
c
on
di
t
i
ons. Furt
h
er,
i
t

i
s
lik
e
l
yt
h
at w
h
en t
h
ey were evo
l
v
i
ng t
h
e num
b
er o
f
n
i
c
h
es ava
il
a
ble
to t

h
em wou
ld b
equ
i
te
li
m
i
te
db
ecause most were occup
i
e
db
ya
l
rea
d
y esta
bli
s
h
e
d
groups.
Insects, on the other hand, evolved in a terrestrial environment sub
j
ect to
g

reat chan
g
es
i
nph
y
sical conditions. The
y
were one of the earliest animal
g
roups to “venture on land
”
and, therefore, had a vast number of niches available to them in this new ada
p
tive zone.
S
econ
d
,t
h
e success o
f
t
h
e Insecta as a w
h
o
l
e
i

spr
i
mar
il
yre
l
ate
d
to t
h
e extraor
di
nar
il
y
l
arge
n
um
b
er o
f
spec
i
es
i
na
h
an
df

u
l
o
f
or
d
ers, name
l
y, t
h
eCo
l
eoptera, Lep
id
optera, D
i
ptera, an
d
Hy
menoptera. Thus, the question ultimatel
y
becomes “What is it about these
g
roups that
allowed them to become so s
p
ecies-rich?” The answer to this is considered below
.
M
ost insects, modern and fossil, are small animals. A few earl

y
forms achieved a
l
arge s
i
ze
b
ut
b
ecame ext
i
nct presuma
bl
y
b
ecause o
f
c
li
mat
i
cc
h
anges an
d
t
h
e
i
r

i
na
bili
ty to
c
ompete success
f
u
ll
yw
i
t
h
ot
h
er groups. Sma
ll
s
i
ze con
f
ers severa
l
a
d
vantages on an an
i
ma
l
.

It
f
ac
ili
tates
di
spersa
l
,
i
t ena
bl
es t
h
ean
i
ma
l
to
hid
e
f
rom potent
i
a
l
pre
d
ators, an
di

ta
ll
ows
the animal to make use of food materials that are available in onl
y
ver
y
small amounts. The
g
reat disadvanta
g
e of small size in terrestrial or
g
anisms is the potentiall
y
hi
g
h rate of wate
r
l
oss
f
rom t
h
e
b
o
d
y. In
i

nsects t
hi
s
h
as
b
een success
f
u
ll
y overcome t
h
roug
h
t
h
e
d
eve
l
opment
of
an
i
mpermea
bl
e exos
k
e
l

eton
.
Th
ea
bili
ty to
fl
y was per
h
aps t
h
es
i
ng
l
e most
i
mportant evo
l
ut
i
onary
d
eve
l
opment
i
n
i
nsects. With this asset the possibilities for escape from predators and for dispersal were

g
reatl
y
enhanced. It led to colonization of new habitats,
g
eo
g
raphic isolation of populations,
and, ultimately, formation of new species. Wide dispersal is particularly important for thos
e
spec
i
es w
h
ose
f
oo
d
an
db
ree
di
ng s
i
tes are scattere
d
an
di
n
li

m
i
te
d
supp
l
y.
R
epro
d
uct
i
ve capac
i
ty an
d lif
e
hi
story are two re
l
ate
df
actors t
h
at
h
ave contr
ib
ute
d

t
o
the success of insects. Production of lar
g
e numbers of e
gg
s, combined with a short life
histor
y
, means a
g
reater amount of
g
enetic variation can occur and be tested out rapidl
y
w
ithin a population. This has two consequences. First, rapid adaptation to changes in envi
-
ronmenta
l
con
di
t
i
ons w
ill
occur. T
hi
s
i

s
b
est exemp
lifi
e
db
yt
h
e
d
eve
l
opment o
f
res
i
stanc
e
to pest
i
c
id
es (see C
h
apter 24, Sect
i
on 4.2). Secon
d
,t
h

ere w
ill b
e rap
id
atta
i
nment o
f
genet
ic
i
ncompat
ibili
t
yb
etween
i
so
l
ate
d
popu
l
at
i
ons an
df
ormat
i
on o

f
new spec
i
es. For examp
l
e,
the approximatel
y
10,000 species of native Hawaiian insects are thou
g
ht to have evolved
f
rom about 100 immi
g
rant species. The evolution of a pupal sta
g
e between the larval an
d
a
d
u
l
t stages
h
as
l
e
d
to a more spec
i

a
li
ze
d
(an
d
,
i
n a sense, a more “e
ffi
c
i
ent”)
lif
e
hi
story.
In some spec
i
es t
hi
s
h
as
l
e
d
to t
h
eexp

l
o
i
tat
i
on o
f diff
erent
f
oo
d
sources
b
yt
h
e
l
arva
e
an
d
a
d
u
l
ts (compare t
h
e
f
o

li
a
g
e-
f
ee
di
n
g
caterp
ill
ar w
i
t
h
t
h
e nectar-
d
r
i
n
ki
n
g
a
d
u
l
t mot

h
).
49
IN
S
E
C
TDI
V
ER
S
IT
Y
F
urther, it enables insects to use food sources that are available for onl
y
short periods of
t
ime. Eventuall
y
, the main function of the larva becomes the accumulation of metabolic
reserves, whereas the adult is primaril
y
concerned with reproduction and dispersal (and in
some spec
i
es
d
oes not
f

ee
d
). A
l
t
h
oug
h
t
h
e pupa
i
spr
i
mar
il
ytoa
ll
ow trans
f
ormat
i
on o
f
t
h
e
l
arvatot
h

ea
d
u
l
t,
i
n many spec
i
es
i
t
h
as
b
ecome a stage
i
nw
hi
c
hi
nsects can res
i
st un
f
a
-
vora
bl
e con
di

t
i
ons. T
hi
s
d
eve
l
opment an
d
t
h
e restr
i
ct
i
on o
ff
ee
di
n
g
act
i
v
i
t
y
to one p
h

ase
of the life histor
y
have facilitated the expansion of insects into some of the world’s mos
t
inhos
p
itable habitats.
Four or
d
ers o
fi
nsects
h
ave
b
ecome extreme
l
y
di
verse: Co
l
eoptera (300,000 spec
i
es)
L
ep
id
optera (200,000), Hymenoptera (130,000), an
d

D
i
ptera (110,000). C
l
ear
l
y, t
h
ese must
h
ave part
i
cu
l
ar
f
eatures t
h
at a
ll
owe
d
t
h
em to pre
f
erent
i
a
ll

yexp
l
o
i
tnewn
i
c
h
es as t
h
ese
b
ecame available throu
g
h evolutionar
y
time
.
For
C
oleoptera, the features were the development of el
y
tra that protect the hind win
gs
and cover the spiracles to reduce water loss, the “compact” body as a result of housing
th
e coxa
l
segments
i

ncav
i
t
i
es, an
d
t
h
e
i
ncrease
d
proport
i
on o
f
t
h
e
i
ntegument t
h
at was
sc
l
erot
i
ze
d
.T

h
ese a
ll
owe
d
t
hi
s group to occupy enc
l
ose
d
spaces an
d
crypt
i
c
h
a
bi
tats suc
h
as soil and litter, and to invade arid environments. Within the Coleoptera two
g
roups are
especiall
y
diverse, the Curculionoidea and the Chr
y
someloidea, which collectivel
y

total
more than 130,000 species (see Chapter 10, Section 5). The ancestor of these groups likely
f
e
d
on pr
i
m
i
t
i
ve p
l
ants suc
h
as pter
id
op
h
ytes, cyca
d
san
d
con
if
ers. T
h
e spec
i
es “exp

l
os
i
on
”
th
at
l
e
d
to t
h
emo
d
ern curcu
li
ono
id
san
d
c
h
rysome
l
o
id
s
b
egan
i

nt
h
e post-Jurass
i
c per
i
o
d
and closel
y
paralled the evolution of the an
g
iosperms (Farrell, 1998).
The evolution of the proboscis enabled adult Lepidoptera to easil
y
in
g
est water, hence
av
oid desiccation, and to obtain nectar, often stored cr
y
pticall
y
b
y
the plants with whic
h
th
ey coevo
l

ve
d
.D
i
ptera, too, w
i
t
h
t
h
e
i
r spec
i
a
li
ze
d
mout
h
parts
h
ave
b
een a
bl
etoexp
l
o
i

t
part
i
cu
l
ar
li
qu
id f
oo
d
sources, nota
bl
y nectar,
j
u
i
ces
f
rom
d
ecay
i
ng mater
i
a
l
s, an
d
an

i
ma
l
ti
ssue
fl
u
id
s. It
i
s
g
enera
lly
cons
id
ere
d
t
h
at t
h
era
di
at
i
on o
f
t
h

e Lep
id
optera an
d
D
i
pter
a
closel
y
paralleled that of the flowerin
g
plants and while this ma
y
be correct, Labandeira
and Sepkoski (1993) noted that the accelerated radiation of insects be
g
an 100 million
y
ear
s
b
e
f
ore t
h
at o
f
t
h

e ang
i
osperms, an
d
t
h
at t
h
e great ma
j
or
i
ty o
f
mout
h
part types were
i
n
ex
i
stence
b
yt
h
eM
iddl
e Jurass
i
c. In La

b
an
d
e
i
ra an
d
Sep
k
os
ki
’s v
i
ew
i
t may
h
ave
b
een
th
eevo
l
ut
i
on o
f
see
d
p

l
ants
i
n genera
l
,an
d
not spec
ifi
ca
ll
yt
h
e ang
i
osperms, t
h
at was t
he
d
rivin
g
force behind the explosive evolution of the Insecta.
The H
y
menoptera, the
g
reat ma
j
orit

y
of which are small to minute, have “pi
ggy
backed”
on the success of other insect groups, by becoming parasitoids, especially on larvae or eggs
,
th
roug
h
t
h
e
d
eve
l
opment o
f
t
h
eov
i
pos
i
tor as a para
l
yz
i
ng organ. In a
f
urt

h
er step, man
y
spec
i
es evo
l
ve
d
s
i
mp
l
e
f
orms o
f
parenta
l
care (e.g.,
b
yp
l
ac
i
ng t
h
e prey
i
n spec

i
a
l
ce
ll
sa
l
ong
w
ith their e
gg
), leadin
g
eventuall
y
to cooperative nest care and true socialit
y
.
S
everal features of insects have contributed therefore to their success
(
diversification
).
I
tisim
p
ortant to realize that these features have acted
i
n
co

m
bi
n
atio
n
t
o effect success
,
an
d
,
f
urt
h
ermore,
li
tt
l
eo
f
t
hi
s success wou
ld h
ave
b
een poss
ibl
e except
f

or t
h
ec
h
ang
i
ng
en
vi
ronmenta
l
con
di
t
i
ons
i
n
whi
c
h
t
h
e
i
nsects e
v
o
lv
e

d.
4.2. The Importance of Environmental Chan
g
e
s
T
h
e
i
mportance o
f
env
i
ronmenta
l
c
h
anges
i
nt
h
e process o
f
evo
l
ut
i
on, act
i
ng t

h
roug
h
natura
l
se
l
ect
i
on,
i
swe
ll k
nown. T
h
ese c
h
anges can
b
e seen act
i
ng at t
h
e popu
l
at
i
on or
spec
i

es
l
eve
l
onas
h
ort-term
b
as
i
s, an
d
man
y
examp
l
es are
k
nown
i
n
i
nsects, per
h
aps t
h
e