Are Abdominal Prolegs Serially Homologous With the Thoracic Legs in Panorpidae (Insecta: Mecoptera)? Embryological Evidence

Abstract

It is a long standing question whether the abdominal prolegs of holometabolous insect larvae are serially homologous with their thoracic legs. The histology and ultrastructure of proleg embryonic development in the scorpionfly Panorpa magna were studied using light and scanning electron microscopy. During the early embryonic development, paired primary abdominal appendages appeared laterally in line with the thoracic legs. Several hours later, a pair of proleg primordia arose along the midventral line on each of the first eight abdominal segments mesial to the primary abdominal appendages, which then ceased to grow and eventually degenerated into flat vestiges. Histological observation showed that the thoracic legs were obviously connected with lateral thoracic muscle cells, whereas the abdominal prolegs resembled secondary outgrowths. No apparent contact was observed between the lumen of abdominal prolegs and the hemocoel. After dorsal closure, each thoracic segment bore a pair of well-developed five-jointed legs, whereas the prolegs were unjointed, fleshy structure. The remnants of the primary abdominal appendages could still be clearly seen in the mature embryo. On the basis of the histological and morphological observation of the embryonic development, we confirm that the abdominal prolegs of Panorpidae lack the characters of the primary appendages; hence they are not serially homologous with the thoracic legs. The reasons why the primary abdominal legs are reduced in scorpionflies are briefly discussed.

Full text

Are Abdominal Prolegs Serially Homologous With the
Thoracic Legs in Panorpidae (Insecta: Mecoptera)?
Embryological Evidence
Chao Yue and Baozhen Hua*
Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, Entomological Museum,
Northwest A&F University, Yangling, Shaanxi 712100, China
ABSTRACT It is a long standing question whether
the abdominal prolegs of holometabolous insect larvae
are serially homologous with their thoracic legs. The
histology and ultrastructure of proleg embryonic devel-
opment in the scorpionfly Panorpa magna were studied
using light and scanning electron microscopy. During
the early embryonic development, paired primary ab-
dominal appendages appeared laterally in line with the
thoracic legs. Several hours later, a pair of proleg pri-
mordia arose along the midventral line on each of the
first eight abdominal segments mesial to the primary
abdominal appendages, which then ceased to grow and
eventually degenerated into flat vestiges. Histological
observation showed that the thoracic legs were obvi-
ously connected with lateral thoracic muscle cells,
whereas the abdominal prolegs resembled secondary
outgrowths. No apparent contact was observed between
the lumen of abdominal prolegs and the hemocoel. After
dorsal closure, each thoracic segment bore a pair of
well-developed five-jointed legs, whereas the prolegs
were unjointed, fleshy structure. The remnants of the
primary abdominal appendages could still be clearly
seeninthematureembryo.Onthebasisofthehisto-
logical and morphological observation of the embryonic
development, we confirm that the abdominal prolegs of
Panorpidae lack the characters of the primary appen-
dages; hence they are not serially homologous with the
thoracic legs. The reasons why the primary abdominal
legs are reduced in scorpionflies are briefly discussed.
J. Morphol. 271:1366–1373, 2010. Ó2010 Wiley-Liss, Inc.
KEY WORDS: Mecoptera; proleg; homology; eruciform
larva; embryogenesis
INTRODUCTION
Holometabolous insects have four life stages: the
egg, larva, pupa, and adult. Some primitive holome-
tabolous larvae possess several pairs of abdominal
prolegs besides three pairs of thoracic legs and are
generally called eruciform larvae or caterpillars
(Stehr, 2003). In glossatan Lepidoptera (moths and
butterflies), the larvae usually bear five pairs of pro-
legs on abdominal segments 3–6 and 10 (Scoble,
1995). The symphytan Hymenoptera larvae (sawflies)
possess 6–8 pairs of abdominal prolegs (Birket-Smith,
1984). In Mecoptera (scorpionflies and hangingflies)
larvae, eight pairs of prolegs are present on the first
eight abdominal segments (Byers and Thornhill,
1983; Tan and Hua, 2008, 2009; Du et al., 2009; Hua
and Cai, 2009). The larvae of Trichoptera (caddisflies),
Coleoptera (beetles), and some Hymenoptera lack ab-
dominalprolegsandwerepostulatedtobeevolved
from caterpillars by loss of legs (Williamson, 2009).
Legs, antennae, and mouthparts are long consid-
ered serially homologous structures in insects
(Snodgrass, 1935; Angelini and Kaufman, 2005b).
However, whether the prolegs of the eruciform lar-
vae are derived from the primary appendages of
abdomen and thus serially homologous with the
thoracic legs is a long-standing and controversial
problem, which has not yet been satisfactorily
resolved (Suzuki and Palopoli, 2001). Earlier
researchers supposed that the larval abdominal
prolegs originate from the limb-like rudiments in
the embryo that correspond to the rudiments of
the thoracic legs, thus treated them as parts at
least of true segmental appendages by their struc-
ture and musculature (Snodgrass, 1935). Similarly,
Matsuda (1976) claimed that the embryonic ab-
dominal appendages in the lower holometabolous
insects tend to persist into the larval stage,
strongly supporting the appendicular nature of the
embryonic and larval abdominal legs in insects.
According to the expression pattern of Distal-less
gene (Dll), Panganiban et al. (1994) demonstrated
that ventral and anal prolegs of the butterfly Pre-
cis coenia are homologous with thoracic legs. How-
ever, Hinton (1955, 1958) assumed that the larval
Contract grant sponsor: The National Natural Science Founda-
tion of China; Contract grant number: 30670255.
*Correspondence to: Baozhen Hua, Entomological Museum,
Northwest A&F University, Yangling, Shaanxi 712100, China.
E-mail: huabzh@nwsuaf.edu.cn
Received 24 January 2010; Revised 30 April 2010;
Accepted 4 June 2010
Published online 16 August 2010 in
Wiley Online Library (wileyonlinelibrary.com)
DOI: 10.1002/jmor.10879
JOURNAL OF MORPHOLOGY 271:1366– 1373 (2010)
Ó2010 WILEY-LISS, INC.

prolegs were secondary adaptive structures not
serially homologous with the thoracic legs and
evolved independently in different orders. On the
basis of embryological work, Suzuki (1990) con-
cluded that the median larval abdominal legs of
Panorpa pryeri and Bittacus laevipes in Mecoptera
were not homologous with the thoracic legs.
In general, there are two approaches currently
applied to determine the relationship between the
abdominal prolegs and the thoracic legs (Suzuki,
1990). The first and modern approach is to use mo-
lecular techniques of developmental Hox genes,
which play a key role in determining the presence
or absence of insect limbs (Lewis, 1978). The Dll
gene, one of Hox regulatory targets, is required for
the development of distal limb structures in
arthropods (Panganiban et al., 1995). Although
genetic technology is an effective method to dis-
cover the origin of appendages, not all aspects of
limb patterning may be as universal as initially
inferred from the widely conserved pattern of Dll
expression (Angelini and Kaufman, 2005b). Sev-
eral recent researchers (Prpic et al., 2003; Jock-
usch and Ober, 2004; Angelini and Kaufman,
2005a; Tomita and Kikuchi, 2009) have suggested
that limb specification mechanisms described for
the fruit fly Drosophila could not be representative
of insects in general.
Alternatively, the second and classical approach
is to apply morphological methodology, including
comparative anatomy and comparative embryol-
ogy, which can contribute a lot to current direction
in revealing the possible serial homologues of the
prolegs with other appendages (Richter, 2005;
Scholtz, 2010). If one observes the embryogenesis
of insect appendages, focusing in particular on the
development of the thoracic legs and abdominal
appendages by comparing the relative position and
morphology between them, a simpler and more
direct evidence for the homology of abdominal pro-
legs could be disclosed. However, the homology of
the abdominal prolegs is poorly documented in the
embryonic stage thus far. The muscles connected
with larval thoracic legs and abdominal prolegs,
and their relative position during embryogenesis
play a key role in deducing their homology
(Birket-Smith, 1984; Suzuki, 1990). In some
respects, using the connected muscles of larval
thoracic legs and abdominal prolegs as homologous
evidence is not fully reasonable, because it fails to
uncover the entire process of the embryonic devel-
opment, which may contain some important fea-
tures to indicate their development and evolution.
In this case, the embryological method appears to
be more reliable to elucidate the serial homology of
the larval abdominal prolegs.
The aim of this study is to discover whether the
abdominal prolegs are serially homologous with
the thoracic legs in the larvae of Mecoptera
through the embryological observation on the de-
velopment of abdominal prolegs in the scorpionfly
Panorpa magna Chou.
MATERIALS AND METHODS
Insects and Eggs
Adults of P. magna Chou were collected at the Daguanzi For-
est Farm in the Qinling Mountains, 16 km south of Taibai
County, Shaanxi Province, central China in late August, 2008.
The adult scorpionflies were reared in a net cage and fed
freshly killed orthopterans to the mountain area. Gravid
females were transferred into a covered transparent plastic cup
containing 4 cm of humid soil. Newly laid egg batches were
transferred into plastic cups containing humid tissue paper and
incubated at approximately 208C.
Sample Preparation
For light microscopy (LM) observation, eggs were fixed in the
Bouin’s fixative solution (saturated picric acid: formaldehyde:
glacial acetic acid 515:5:1 v/v) for 12 h every 2 hours beginning
from the time of oviposition before being stored in 70% ethanol.
For scanning electron microscopy (SEM) observation, the
embryos of different periods were fixed in 2.5% glutaraldehyde
solution in phosphate buffer (0.1 mol l
21
, pH 7.2) for 12 h at
48C.
Light Microscopy
LM was used to observe the embryonic structure of different
developmental stages. The embryos were dissected out of the
chorion under a Motic SMZ-168 stereo microscope, then dehy-
drated in a series of graded acetone (from 30% to 100% v/v),
infiltrated in a serial mixture of Epon 812 and acetone, and
finally embedded in Epon 812. Then, the specimens were cut
into semi-thin sections using a LKB2088 microtome. Semi-thin
sections were mounted on glass slides, routinely stained with
0.5% toluidine blue, and examined with an Olympus BX-51
microscope. Images of the sections were taken with a digital
camera mounted on the microscope.
Scanning Electron Microscopy
SEM was used to obtain detailed images of the external mor-
phology of the embryos. After dehydration in a graded acetone
series (from 30% to 100% v/v), the specimens were treated with
isoamyl acetate, critical-point dried in liquid CO
2
, sputtered
coated with gold, and examined with a JEOL JSM-6360 LV
scanning electron microscope at 15 kV.
RESULTS
The whole period of the embryonic development
of P. magna is roughly 160 h at about 208C. Our
observations mainly focused on the external mor-
phology and the formation process of the abdomi-
nal prolegs during this period. In the first 60 h
after oviposition, egg cleavage and blastoderm
formation occur successively. At 74 h after oviposi-
tion, germ band with a bilobed protocephalon in
the anterior pole and a slender protocorm extend-
ing to the posterior pole of the egg is present on
the surface of the yolk, this type of superficial
embryo allowing it to be observed with ease.
At 80 h after oviposition, primary abdominal
appendages appear soon after the germ band begins
SERIAL HOMOLOGY OF PROLEGS IN PANORPIDAE 1367
Journal of Morphology

to separate into 6 cephalic, 3 thoracic, and 10 ab-
dominal segments. At 96 h, a pair of thoracic leg
rudiments appears on each thoracic segment. They
further develop into limb-like structures at 100 h.
Paired primary abdominal appendage primordia
arise on the first eight abdominal segments and are
arranged in line with the rudiments of the thoracic
legs but much smaller (Fig. 1A,C). They develop
slowly and retain their previous shapes. At 110 h
after oviposition, a pair of new primordia appears
mesial to the primary abdominal appendages along
the midventral line of the abdomen (Fig. 1C). These
new primordia eventually give rise to the future ab-
dominal prolegs on the first eight abdominal seg-
ments (Fig. 1C,D). At 120 h after oviposition, the
thoracic legs differentiate further and could be dis-
cerned as three joints, and the details could be
observed more clearly (Fig. 3A). In the longitudinal
section of the thoracic legs (Fig. 2A), the lumen of
the columniform thoracic legs is continuous with
the hemocoel (or body cavity), a character of the pri-
mary appendages sensu Snodgrass (1935). In the
developing thoracic legs, there exist lateral thoracic
muscle cells connected to the thoracic wall. There is
no separation between the thoracic legs and the
hemocoel (Fig. 2A). The proleg primordia along the
midventral line of the abdomen develop further,
forming abdominal prolegs that are quite different
from the thoracic legs in this stage (Fig. 3B). The
proleg is unsegmented, lacking distinct cell struc-
ture and looking like a cytoplasmic process (Fig.
2B). Each abdominal proleg is an independent out-
growth and not directly continuous with the hemo-
coel (Fig. 2B), and an interspace is readily observed
between the abdominal proleg and the abdominal
ganglion (Fig. 3C,D). The primary abdominal
appendages cease to grow and degenerate into flat
vestiges during this stage (Fig. 3B). After dorsal clo-
sure, the thoracic legs are well demarcated, and
each consists of five joints: the coxa, femur, tibia,
tarsus, and apical pretarsus (Fig. 4A). The basal
coxa is the thickest segment with two long setae.
Fig. 1. Scanning electron micrographs of P. magna embryo. (A) Ventral view of the embryonic abdomen at 96 h, showing the ab-
dominal appendage primordia (AAP). Scale bar 550 lm. (B) High magnification of the third thoracic and the first two abdominal
segments of the embryo at 96 h. Scale bar 510 lm. (C) Overview of the embryo at 110 h, showing the lateral primary abdominal
AAP and the mesial abdominal proleg primordia (PP) on the sternum. Scale bar 525 lm. (D) High magnification of the third ab-
dominal segment of the embryo shown in C. Scale bar 510 lm. A1–7, abdominal segments 1–7; DrP, dorsal protuberance; Sp, spir-
acle; TL1–3, thoracic legs 1–3; Y, yolk.
1368 C. YUE AND B. HUA
Journal of Morphology

The longest is the femur, which is slightly thinner
than the coxa. The tibia, tarsus, and pretarsus are
much shorter and thinner than the first two joints.
The anterior margins of the tibia and tarsus are fin-
gernail shaped, and the both joints are covered with
dense hairs. The apical pretarsus is pointed and
curved upward, extending from the tarsus (Fig. 4A).
On the first eight abdominal segments, the rem-
nants of the primary abdominal appendages can
still be clearly observed at the late stage of the
embryonic development (Fig. 4B). They are trian-
gular prominences on the subventral part of the
abdominal segments (Fig. 4B,D). Two clavate
setae are situated on a pinnaculum of the trian-
gular remnants (Fig. 4B,D). The position, shape,
and chaetotaxy of the remnants are almost identi-
cal with the coxa of thoracic legs (Fig. 4C). Com-
pared with the thoracic legs, the tapering prolegs
are much smaller and unsegmented along the
midventral line and mesial to the remnants of the
primary abdominal legs (Fig. 4B,C). The prolegs
are transversely wrinkled and bear on their outer
side rows of minute setae, including abundant
spinal prominences, which are present around the
basal part of the abdominal prolegs, and some
wispy hairs and one spine at the anterior part
(Fig. 4D). The apical part of the proleg is slightly
flexed, somewhat claw-like.
There are not any swellings or limb-like struc-
tures on the ventral part of the ninth and tenth
abdominal segments during the whole embryogen-
esis of P. magna. Neither primary abdominal leg
remnants nor prolegs were observed on these two
segments. However, four protuberances arose from
telson and gradually developed into the anal fork
of the larva (data not shown). Several hours before
eclosion, the gross morphology of the first-instar
larva is formed fully (Fig. 4C).
DISCUSSION
Insects have three thoracic appendages (or legs)
judged from their analogical structure, constant num-
ber, segmentation, and derivative origin. However, the
abdominal prolegs vary considerably both in segmen-
tal arrangement and number in the larvae of different
insect groups, even being absent in some orders (Nagy
and Grbic, 1999). Based on the distribution of prolegs
in holometabolous insects, Nagy and Grbic (1999)
assumed that prolegs evolved independently in differ-
ent lineages. Based on the absence of the Dll gene
from the abdominal prolegs in sawflies and the pres-
ence both of proximal and distal portions in lepidop-
teran prolegs during embryogenesis, Suzuki and Palo-
poli (2001) suggested that sawfly prolegs may be limb
bases, corresponding to the coxal segment of a thoracic
leg, and that lepidopteran prolegs appear to have both
proximal and distal portions, concluding that the
larval prolegs had evolved independently between the
Lepidoptera and Hymenoptera. They believed that
although the prolegs in different orders may share
mechanisms of limb development, the particular
mechanisms by which the derepression of appendage
development occurs in the abdomen independently
among various insect lineages are likely to make some
difference. Williamson (2009) claimed that onycho-
phorans were the evolutionary source of eruciform lar-
vae, and therefore, the prolegs of eruciform larvae are
equivalent to the stub feet of onychophorans.
There are two conflicting hypotheses about the
larval prolegs of holometabolous insects as to
whether they are serially homologous with tho-
racic legs (Birket-Smith, 1984). Abdominal prolegs
were regarded as secondary adaptive structures
that are not homologous with the thoracic legs in
panorpoid insects (Hinton, 1955). However, some
researchers (Applegarth, 1939; Matsuda, 1976;
Birket-Smith, 1984) claimed that thoracic legs and
abdominal prolegs were serially homologous in hol-
ometabolous insects.
According to the innervations of larval muscles,
Birket-Smith (1984) concluded that the thoracic
legs and abdominal prolegs are homodynamous in
the lepidopterans Hepialus humuli, Noctua pro-
nuba, and the hymenopteran Arge pullata. Even
for some insects that lack prolegs, there exist some
other structures that could be homologous with the
Fig. 2. Micrographs of the semi-thin section of Panorpa
magna embryo at 120 h. (A) Longitudinal section of the third
thoracic legs; arrowheads indicate the boundaries of leg tissue
and the tissue of ganglion. Scale bar 520 lm. (B) Longitudinal
section of the abdominal prolegs. Scale bar 520 lm. AAP, ab-
dominal appendage primordia; AG, abdominal ganglion; MC,
muscle cell; PL, abdominal proleg; Pt, proctodaeum; Sp, spira-
cle; TG3, third thoracic ganglion; TL3, third thoracic leg; Y,
yolk. [Color figure can be viewed in the online issue, which is
available at wileyonlinelibrary.com.]
SERIAL HOMOLOGY OF PROLEGS IN PANORPIDAE 1369
Journal of Morphology

thoracic legs. Suzuki (1990) put forward a criterion
to determine the relationship between the abdomi-
nal prolegs and thoracic legs, suggesting that if the
paired abdominal prolegs in each segment arranged
in line with the thoracic legs and developed histo-
logically in the same manner as the thoracic legs
during embryonic development, they could be con-
sidered as serially homologous. On the basis of this
criterion, he inferred that the abdominal prolegs of
the lepidopteran Diacrisia and the hymenopteran
Athalia were homologous with the thoracic legs
from their identical position (Suzuki, 1990). Judg-
ing from the position of pleuropodia on the first ab-
dominal segment of the primitive moths Neomicrop-
teryx and Endoclita and several heteroneurous
moths, Kobayashi and Ando (1990) suggested that
pleuropodia should be considered as appendage or a
part of them is homologous with their thoracic legs.
They appear as a pair of appendage-like projections
and degenerate before hatching. During the early
stage of embryonic development in the tussah moth
Antheraea pernyi, all of its abdominal segments
except the hindmost carry a pair of appendages.
Some segments lost their appendages, whereas the
remaining appendages develop further to be seg-
mented into abdominal prolegs with two articula-
tions (Saito, 1934). In the embryo of the sawfly
Pteronidea ribesii, abdominal prolegs as appen-
dages appear on the second to seventh and the
tenth abdominal segments (Shafiq, 1954).
In Mecoptera, eight pairs of appendages are pres-
ent on ventral side of the first eight segments in
Apterobittacus (Applegarth, 1939), Harpobittacus
(Currie, 1932), Bittacus (Tan and Hua, 2009), Pan-
orpa (Miyake, 1912; Rottmar, 1966; Hua and Cai,
2009), and Neopanorpa (Cai and Hua, 2009). After a
simple comparison of the position and structure of
the larval prolegs with those of thoracic leg apices in
Apterobittacus,Applegarth(1939)incorrectly
claimed that the prolegs are vestigial legs. Ando and
Fig. 3. Panorpa magna embryo close to dorsal closure. (A) Ventral view of the embryonic thorax at 120 h, showing the early de-
velopment of the thoracic leg that consists of coxa, femur, and tibia. Scale bar 525 lm. (B) Ventral view of the embryonic abdomen
at 124 h. The mesial swellings along the midventral line grow further, developing into abdominal prolegs (PL), while the primary
abdominal appendages (APP) degenerate. Scale bar 510 lm. (C) Longitudinal section of the embryo, focusing on the structure of
abdominal prolegs before dorsal closure. Scale bar 520 lm. (D) High magnification of the abdominal prolegs shown in C. Scale bar
510 lm. A1–9, abdominal segments 1–9; AAP, abdominal appendage primordia; AG2–4, abdominal ganglia 2–4; Cx, coxa; Fm, fe-
mur; H, head; Tb, tibia; TL, thoracic leg; TL1–3, thoracic legs 1–3; Y, yolk.
1370 C. YUE AND B. HUA
Journal of Morphology

Haga (1974) also suggested that although the ab-
dominal prolegs of P. pryeri are not quite homotopous
with thoracic legs because of their different position
at the early embryologic stage, they probably devel-
oped into larval legs that are serially homologous
with the thoracic legs. Du et al. (2009) also argued
that the primary abdominal appendages degenerate
and the abdominal prolegs developed from the sec-
ondary mesial rudiments in Panorpa emarginata.
The embryonic developmental process of the ab-
dominal prolegs in P. magna is consistent with
those in P. pryeri,B. laevipes (Suzuki, 1990), and
P. emarginata (Du et al., 2009). According to their
identical positions and successive appearances, it
is evident that the earlier lateral primordia are
the primary abdominal limbs, which are serially
homologous with the thoracic legs. Conversely, the
mesial anlagen that appeared chronologically later
along the midventral line are the future abdominal
prolegs, which are obviously secondary outgrowths
of the body wall and should not be confused with
the primary abdominal appendages.
Snodgrass (1935) stated that the lumen of insects
enlarges upward with the growth of the mesoderm
around the yolk or the alimentary canal, penetrates
into the appendages, and eventually forms the con-
tinuous body cavity. The appendages are continuous
with the hemocoel, this feature being present on the
primary appendages such as thoracic legs, anten-
nae, and mouthparts. Based on the longitudinal sec-
tions in early embryonic development (Figs. 2 and
3C,D), the thoracic legs are hollow cylindrical out-
growths of the body wall, the lumen being continu-
ous with the hemocoel and closely related with the
thoracic ganglion, and are connected to the lateral
thoracic muscle cells. The abdominal prolegs are
evidently secondary outgrowth of the body wall and
not directly continuous with the hemocoel (Fig. 2B).
No distinct abdominal muscle cells connected to ab-
dominal prolegs were observed, because at this
Fig. 4. Scanning electron micrographs of Panorpa magna embryo just before hatching. (A) Lateral view of thoracic legs, which
consist of five joints. Scale bar 550 lm. (B) Lateral view of abdomen, showing the well-developed abdominal prolegs (PL) and the
remnants of the primary abdominal legs (ALR). Note that some setae were lost during preparation, thus only the setal cavities are
left. Scale bar 550 lm. (C) Lateral view of the larva before hatching, showing the PL and the ALR. Scale bar 5500 lm. (D) High
magnification of the abdominal prolegs of third and forth abdominal segments, lateral view. Scale bar 550 lm. A1–8, abdominal
segments 1–8; AF, anal fork; ALR, abdominal leg remnant; CE, compound eye; Cx, coxa; DrP, dorsal protuberance; Fm, femur; Pta,
pretarsus; Sp, spiracle; Ta, tarsus; Tb, tibia; TL, thoracic leg; TL1–2, thoracic legs1–2.
SERIAL HOMOLOGY OF PROLEGS IN PANORPIDAE 1371
Journal of Morphology

stage, the prolegs simply looked like cytoplasmic
processes (Suzuki, 1990). No apparent contact
exists between the abdominal prolegs and the hemo-
coel (Fig. 3D). Judged from this, abdominal prolegs
apparently lack characters of true appendage in
scorpionflies. It is interesting to note that a similar
feature of a limb-bud like structure is situated pos-
terior to the mandible in Crustacea during their
embryogenesis, and this appendage (the so-called
paragnaths) was considered to be a sternal out-
growth of the ventral ganglion region and not a
limb (Wolff and Scholtz, 2006), very similar to what
happens in Panorpidae.
The primary abdominal appendages gradually
cease to grow and eventually degenerate, similar
to the abdominal appendages of the primitive
moth Neomicropteryx after revolution of the em-
bryonic development (Kobayashi and Ando, 1981).
In addition, the remnants of the primary abdomi-
nal appendages were observed during late embryo-
genesis, confirming that their degeneration does
occur during late embryonic development. Compar-
ing the appendicular structure of the abdomen
with that of the thorax, we find that both the sub-
coxa and coxa of the abdominal appendages
become part of the pleuron in the future larval ab-
domen (Fig. 4B,C). Miyake (1912) claimed that
each fully developed thoracic leg of Panorpa klugi
larva consists of four visible joints: coxa, trochan-
ter, femur, and tarsus. However, Hinton (1958)
argued that the thoracic leg in Mecoptera larva
consists of five segments: coxa, trochanter, femur,
the fused tarsus and tibia, and pretarsus. Hinton’s
(1958) point of view receives support from our ob-
servation on the larval thoracic legs in P. magna.
In addition to the Mecoptera, eruciform larvae
also include those of sawflies in the Hymenoptera
and caterpillars in the Lepidoptera. The abdominal
prolegs of sawfly larvae and caterpillars have been
considered to be serially homologous with the tho-
racic legs (Snodgrass, 1935; Suzuki, 1990; Suzuki
and Palopoli, 2001), quite different from the situa-
tion in hangingflies and scorpionflies in the Mecop-
tera (Suzuki, 1990; Du et al., 2009). This means
that the so-called eruciform larvae are not consist-
ent with respect to the nature of prolegs.
The abdominal prolegs are originally adapted to
grasp substrates to assist movement (Birket-Smith,
1984; Headrick and Gordh, 2003). The larvae of saw-
flies and glossatan lepidopterans are phytophagous,
living on the leaves of plants. The strong abdominal
prolegs of a sawfly larva can be everted as holdfasts
when the larva walks on the edge of a leaf. Similarly,
as the locomotory organs of caterpillars, the abdomi-
nal prolegs are used to hold the entire body and act
as the center of movement when the larva stays on
the surface of plant. Conversely, the larvae of Mecop-
tera are saprophagous and live on the ground with
no leaves to grasp (Byers and Thornhill, 1983).
Under this condition, the original grasping function
of the primary abdominal legs seems to be redun-
dant, and thus, they degenerate gradually during
their evolution. However, the larvae of scorpionflies
and hangingflies still need to forage dead arthropods
as their food, so limited movement is definitely neces-
sary. If this is the case, the abdominal prolegs
evolved secondarily to assist the movement of the
larvae, and more likely help to support the long ab-
domen. Otherwise, the ventral abdomen will be in
direct contact with the ground and will be more vul-
nerable to abrasive injury. The prolegs on the first
abdominal segment are greatly reduced and seta-like
in Bittacus larvae (Tan and Hua, 2008). We assume
that this reduction is derived from their reduced role
in keeping the larval abdomen off the ground
because of the longer thoracic legs. Similarly, the pro-
legs on the eighth abdominal segment are also very
small because of the development of a four branched
anal fork on the last segment.
This study provides more details of the develop-
ment of abdominal prolegs in the family Panorpi-
dae. The manner of development, morphology, and
structure of the abdominal prolegs are completely
different from those of the thoracic legs. The rem-
nants of the primary abdominal appendages were
still observed on the embryo after revolution dur-
ing embryogenesis, further confirming that the ab-
dominal prolegs are not serially homologous with
the thoracic legs in Panorpidae, and possibly also
in the whole order Mecoptera.
ACKNOWLEDGMENTS
The authors thank Miss Sha Xie and Baorong
Yan for their valuable comments on the early manu-
script draft and Dr. Yankai Li for his assistance in
insect rearing. Two anonymous reviewers are
greatly appreciated for their valuable comments
and suggestions in the revision of manuscript.
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SERIAL HOMOLOGY OF PROLEGS IN PANORPIDAE 1373
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