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Juvenile hormone and methyl farnesoate production in cockroach embryos in relation to dorsal closure and the reproductive modes of different species of cockroaches.

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Archives of Insect Biochemistry and Physiology 66:159–168 (2007)
Juvenile Hormone and Methyl Farnesoate Production
in Cockroach Embryos in Relation to Dorsal Closure
and the Reproductive Modes of Different Species of
Cockroaches
Xinyi Li*
Juvenile hormone (JH), produced by the corpora allata (CA), is first detectable after dorsal closure, a conspicuous event in
embryogenesis. The present research found that the timing of dorsal closure was consistently at about 45% of the total
embryonic development time across most of the oviparous and ovoviviparous cockroach species examined. These included the
ovoviviparous cockroaches Blaberus discoidalis, Byrsotria fumigata, Rhyparobia maderae, Nauphoeta cinerea, Phoetalia pallida,
Schultesia lampyridiformis, and Panchlora nivea, as well as the oviparous cockroaches Blatta orientalis, Periplaneta americana,
Eurycotis floridana, and Supella longipalpa. However, the only known viviparous cockroach Diploptera punctata completed
dorsal closure at 20.8% of embryo development time. Methyl farnesoate (MF), the immediate precursor of JH III, is considered a functional molecule in crustaceans; however, in insects its function is still unclear. To understand the role of JH and MF
in cockroach embryos, I compared JH and MF biosynthesis and release in several cockroach species of known phylogenetic
relationships. Using a radiochemical assay, the present research showed that cockroach embryos representing all three reproductive modes produced and released both JH and MF, as previously shown for B. germanica, N. cinerea, and D. punctata.
Members of a pair of embryonic CA from B. discoidalis, B. fumigata, R. maderae, and D. punctata were incubated with and
without farnesol. MF accumulated in large amounts only in CA of R. maderae in the presence of farnesol, which indicates that
control of the last step of biosynthesis of JH, conversion of MF into JH by MF epoxidase, is probably a rate-limiting step in this
species. Arch. Insect Biochem. Physiol. 66:159–168, 2007. © 2007 Wiley-Liss, Inc.
KEYWORDS: juvenile hormone; methyl farnesoate; cockroach embryos; corpora allata; dorsal closure
INTRODUCTION
The corpora allata (CA) are a pair of endocrine
glands that synthesize and release juvenile hormones (JH) and JH precursors in many insects
(Judy et al., 1973; Pratt and Tobe, 1974). Juvenile
hormones regulate larval development and adult
reproduction. In immature insects, the presence of
a high JH titer brings about a subsequent larval
molt, whereas a low JH titer results in a metamorphic molt (reviewed by Truman and Riddiford,
2002). In adult female cockroaches, cycles of JH
biosynthesis correspond to reproductive cycles
(Schal and Chiang, 1995; Schal et al., 1997; Tobe
et al., 1984).
Insect CA become biosynthetically active after
the insect embryo reaches a structurally and physiologically differentiated state characterized by dorsal closure (DC) (Lanzrein et al., 1984). However,
few studies have been carried out to characterize
the timing of dorsal closure in cockroach embryogenesis (Imboden et al., 1978; Stay and Coop,
Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania
Abbreviations used: CA = corpora allata; DC = dorsal closure; JH = juvenile hormone; MF = methyl farnesoate; RCA = radio chemical assay.
*Correspondence to: Xinyi Li, Rm. 501, Institute of Pathology, Case Western Reserve University, 2085 Adelbert Rd., Cleveland, OH 44106.
E-mail: xinyi.li@case.edu
Received 30 December 2006; Accepted 3 May 2007
© 2007 Wiley-Liss, Inc.
DOI: 10.1002/arch.20207
Published online in Wiley InterScience (www.interscience.wiley.com)
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Li
1973). In hemimetabolous insects, the absence or
low titers of JH in the embryo allow them to secrete a pronymphal cuticle around dorsal closure
and high JH titers before the first nymphal molt
defines the nature of the molt (Truman and
Riddiford, 1999, 2002).
JH III is the homologue of JH found in many
cockroach species, including adult of the beetle
cockroach (Diploptera punctata), the German cockroach (Blattella germanica), brown-banded cockroach (Supella longipalpa), the Madeira cockroach
(Rhyparobia maderae), the lobster cockroach (Nauphoeta cinerea), the oriental cockroach (Blatta
orientalis), and the American cockroach (Periplaneta americana) (reviewed by Chiang et al., 1996).
A substantial amount of methyl farnesoate (MF),
the immediate precursor of JH III, has also been
found in embryos of N. cinerea (Bürgin and
Lanzrein, 1988; Lanzrein et al., 1984). A recent
study showed that a small amount of MF is synthesized and released by embryonic CA of D.
punctata by using a higher specific activity radiolabeled precursor than previous studies have used
(Holbrook et al., 1998; Stay et al., 2002).
In crustaceans, MF is suspected to play a role
similar to that of JH III in insects (Borst et al., 1987;
Laufer and Biggers, 2001; Tobe and Bendena,
1999). It is produced by the mandibular organs,
structures homologous to the insect CA. MF circulates in the hemolymph and regulates protein metabolism, the molt cycle and reproduction (Borst
et al., 2001; Homola and Chang, 1997; Laufer and
Biggers, 2001). Results in insects also provide some
evidence that MF has a JH-like function. It induces
vitellogenin synthesis and oocyte growth in decapitated adult females of N. cinerea (Brüning et al.,
1985). However, preliminary experiments using 3Hlabelled methyl farnesoate indicated there is no,
or only very little, conversion of MF into JH III in
N. cinerea adults, larvae, and embryos (Brüning and
Lanzrein, 1987; Lanzrein et al., 1984). Nevertheless, although it has been shown that JHs do function in embryos, it is also possible that MF acts as
a hormone per se in cockroach embryos.
Cockroaches have been grouped according to
three modes of reproduction. Oviparous cock-
roaches deposit the ootheca (egg case and its enclosed eggs) within one day of its formation and
the fertilized eggs develop outside the body of their
mother (Roth, 1970). Ovoviviparous cockroaches
extrude eggs covered by oothecal material, then retract them into a brood sac. There they remain until
the embryos mature, at which time the neonates
leave the brood sac as they break free from their
embryonic membranes and the ootheca. The embryos of ovoviviparous cockroaches, like those from
oviparous ones, are endowed with sufficient yolk to
complete embryonic development, but must absorb
water from their mother to complete development
(Roth, 1970). Viviparous cockroach reproduction
is similar to ovoviviparous forms, except that the
yolk provided to the eggs at oviposition is insufficient to support full development. The embryos
take up water and nutrients from their mother during gestation (Roth, 1970).
Whether MF is a hormone per se in insects is
still unknown and how JH evolved in insects is
an interesting question. To determine whether MF
is produced and released by embryonic CA in
cockroaches in an evolutionary context (i.e., in
relation to reproductive behavior) will help in understanding if MF is a functional hormone, or a
non-functional precursor of JH in the embryos. A
phylogenetic relationship among these cockroaches has been established by analyzing the DNA
sequence of mitochondrial ribosomal RNA genes
(Kambhampati, 1995) (Fig. 1). Using a radiochemical assay (RCA) in vitro and thin layer chromatography (TLC) methods, I investigated JH and
MF biosynthesis in embryonic CA of cockroach
species across three reproductive modes. The oviparous species examined include three blattids, Blatta
orientalis, Periplaneta americana, and Eurycotis
floridana, and two blattellids, Supella longipalpa and
Blattella germanica. The ovoviviparous cockroaches
studied include Blaberus discoidalis, Byrsotria fumigata, Phoetalia pallida, Schultesia lampyridiformis,
Rhyparobia maderae, Nauphoeta cinerea, and Panchlora
nivea, all of which are in the family Blaberidae.
Diploptera punctata, as is the only known viviparous cockroach (Roth, 1970) (Fig. 1).
Archives of Insect Biochemistry and Physiology
December 2007
doi: 10.1002/arch.
JH and MF in Cockroach Embryos
161
Fig. 1. The synthesis and release of juvenile hormone
(JH) and methyl farnesoate (MF) from the embryonic corpora allata (CA) of cockroaches (Blattaria) as related to
their phylogeny (modified from Kambhampati, 1995) and
their reproductive modes. *Species that are not included
in Kambhampati (1995). ND = JH and/or MF production
was not detected by the methods used in this study. JH
and MF indicate hormone gland-content and release into
medium (synthesis). JHR and MFR indicate only release
into medium (release).
MATERIALS AND METHODS
were obtained from pregnant females by applying
gentle posterior-directed pressure to the females’
abdomens.
Insects
Insect colonies were reared at 27 ± 1°C, under
a 12 h light:12 h dark photoperiod and insects were
provided rat chow and water ad libitum. Newly
emerged adult females were collected from the
colonies and maintained in groups of 2–5, along
with males, whose number exceeded the female
number by one. The insects were kept in large Petri
dishes or small cages, with an egg carton, under
the same conditions as the colonies. The females
were examined every day until they oviposited fertile eggs. Thereafter, the females were reared without males. Oviparous females were kept alone in
a Petri dish with a piece of egg carton. After it deposited its egg case, almost invariably on the egg
carton itself, the female was removed and the egg
case was collected from the Petri dish. For viviparous and ovoviviparous species, embryo broods
Archives of Insect Biochemistry and Physiology December 2007
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Reproductive Biology and Dorsal Closure
Broods of all species were partitioned with blunt
forceps into individual embryos under cockroach
saline modified to 360 mOsm/l (Holbrook et al.,
1998). The day of oviposition was recorded as day
0. Three embryos were randomly selected and dissected from each brood. The number of embryos
examined and the number of embryos that completed dorsal closure (DC) were recorded. The day
assigned as DC was the day when 100% of the embryos had undergone DC. The number of healthy
embryos in each brood was counted on the day of
DC. The day of hatch and the number of hatchlings
in each brood were also recorded. Percentages of
hatched embryos per brood were calculated as an
indicator of healthiness of the embryos.
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Li
Radiochemical Assay
Developmental stages of embryos are normally
described using percentage of total development
time (Stay and Coop, 1973). To identify CA of similar developmental stage, I used a post-dorsal closure time, which was based on a scale from DC to
hatch. For example, at 27°C in B. orientalis DC occurs 26 days after oviposition and total embryo development time (i.e., embryogenesis, or oviposition
to hatch) is 49 days. Then 40% post-dorsal closure
time would be at day 35, as calculated from the following: (49 – 26 days) × 40% + 26 days = 35.2 days.
The hormonal products of the CA were examined at the time when it was previously reported
that the embryonic CA produced large amounts of
both JH III and MF. This was in N. cinerea at 40%
post-dorsal closure (Brüning et al., 1985; Holbrook
et al., 1998), but at 65% post-dorsal closure time
in D. punctata. It was reported that the JH III titer
peaks in embryos after 35 to 40 days of embryo
development time in the B. orientalis as would be
predicted under conditions used in this investigation (Short and Edwards, 1992).
JH and MF release and synthesis were measured
with a rapid partition radio-chemical assay (Feyereisen and Tobe, 1981; Holbrook et al., 1997; Pratt
and Tobe, 1974). At one developmental stage, six
to seven embryos were randomly selected and dissected from a brood. At least three broods were
examined for each species. Embryos were individually dissected, and their heads were severed on a
dissecting plate under cockroach saline (Holbrook
et al., 1998). Upon isolating a CA-CC complex
from other tissues (nerves, fat, etc.), a CA pair (or
a CA-CC complex) were pre-incubated for at least
1 h in L-15 B medium lacking L-methionine
(Holbrook et al., 1997) supplemented with L-[methyl-3H]-methionine (diluted from 3.15TBq/mmol,
Amersham, Catalog number TRK705; diluted to a
final specific radioactivity of 74 GBq/mmol with
cold L-methionine; 100 µM methionine final concentration). The complex then was transferred into
20 µl fresh radiolabeled medium in 6 × 25 mm
borosilicate glass culture tubes, where the CA were
incubated for 6 h at 27°C with orbital shaking.
JH III and MF biosynthesis and release were
measured by the procedure described by Holbrook
et al. (1998). Briefly, to test for synthesis of JH III
and MF by insect CA (i.e., the amount retained in
CA and released into medium), 100 µl of isooctane was added to each culture tube and the medium with CA was vortexed at the highest intensity.
Then the culture tube was centrifuged at 4000g for
5 min and an aliquot of the isooctane was collected. The isooctane aliquots from six individual
pairs of glands were pooled and stored at –80°C
in a closed conical-bottomed tube filled with nitrogen until spectrometric quantification.
To measure the quantity of JH III and MF released into the medium by CA, 100 µl of non-radiolabeled medium was added to each 6 × 25 mm
borosilicate glass culture tube. The tubes were
vortexed at a low speed and then centrifuged at
2,000g for 5 min to spin down the CA. Then 100
µl of mixed media without CA was collected carefully from the top with a capillary tube and transferred into 6 × 50 mm borosilicate glass culture
tubes. After transferring 200 µl of isooctane to each
of the tubes, the tubes were vortexed and then centrifuged at 4,000g for 5 min, and the aliquots of
isooctane were collected. Aliquots from six individual pairs of glands were pooled and stored as
described above (Holbrook et al., 1998). Blank
controls were generated using the same procedure
without CA.
Split Pair Assay
Because members of a corpus allatum pair produce similar amounts of hormone (Holbrook et
al., 1996), the effect of farnesol could be determined by comparing an untreated with a treated
member of a pair of corpora allata. Using this technique, I studied JH and MF synthesis and release
with and without farnesol treatment in B. orientalis,
B. fumigata, B. discoidalis, N. cinerea R. maderae, and
D. punctata.
A CA-CC complex was pre-incubated in the
same medium as described previously. After preincubation, a pair of CA was separated and one
corpus allatum was incubated in radiolabeled meArchives of Insect Biochemistry and Physiology
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doi: 10.1002/arch.
JH and MF in Cockroach Embryos
dium (as described above) containing 100 µM
farnesol (Aldrich Inc., Milwaukee, WI) and the corresponding gland was incubated with the same
medium lacking farnesol. The tubes were incubated
for 6 h at 27°C with orbital shaking, then 100 µl
of cold medium was transferred into each tube.
After centrifuging CA down to the bottom, 80 µl
of medium was collected from the top and transferred into two clean 6 × 50 mm tubes with 200
µl of isooctane to calculate the amount of hormone
products released, and 100 µl of isooctane was
added to the tubes containing the CA to measure
the amount of hormonal products retained in CA
(the amount of hormone in 40 µl media was subtracted in calculation). All tubes were thoroughly
vortexed and 90% of the isooctane was collected
and stored as described above.
Analysis of Products of Embryonic CA by
Thin Layer Chromatography
To separate MF from JH III in samples, the solvent was first evaporated to a volume of less than
5 µl under a nitrogen stream. The samples were
spotted on a TLC plate (Silica gel IB2, J.T. Baker
4448-04, Phillipsburg, NJ), which was previously
developed twice in 1:1 chloroform:methanol and
then placed in an oven for a minimum of 24 h at
100°C. Authentic JH III and MF standards (a generous gift from Dr. Chih-Ming Yin at University of
Massachusetts) were also spotted on the plate. The
TLC plate was developed in 85:15 hexane:ethyl acetate and development was terminated when the
solvent front reached 2 cm from the top of the
plate. The plates were then developed in a sealed
glass chamber filled with iodine fume until the JH
and MF standards showed on the plate. Each
sample lane of the plate was cut into 0.5 by 2 cm
fractions and these were placed in scintillation vials, and vortexed with 5 ml Betamax scintillation
cocktail (ICN 880020, MP Biomedicals, Irvine,
CA), stored overnight in the dark, and examined
with a Beckman LS 6500 liquid scintillation
counter. The DPMs of two 1.5-cm regions corresponding to MF and JH III standards were used
Archives of Insect Biochemistry and Physiology December 2007
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163
for calculations. For analysis of JH and MF production of embryonic CA on TLC plates, the following formula was used to calculate rates of JH
and MF biosynthesis and release: 3H-dpm/(2.2
(dpm per pCi) × specific radioactivity of 3H-met
(pCi per pmol) × incubation time (h)) (Yagi and
Tobe, 2001).
Statistical Analysis
Statistical analysis was carried out in a MINITAB
version 13.0 or SAS 8.0.
For days of embryogenesis and the number of
eggs and the number of hatchlings, the data were
square root transformed. Species was considered
as a factor nested in reproductive mode.
For rates of JH and MF production, data were
transformed with logarithm to satisfy assumptions
of ANOVA, then analyzed in separate ANOVAs. Species was a factor nested in reproductive mode for
the ANOVAs. Release or synthesis of JH and MF by
CA was a fixed effect, and the interaction between
release, synthesis effect, and species was included
in the ANOVAs. Tukey pairwise comparisons were
used if the ANOVA indicated significant results.
Contrasts were established to compare JH and MF
biosynthesis between ovoviviparous and oviparous
cockroaches.
RESULTS
Comparison of Brood size, Hatching Success
and Dorsal Closure Time Related to Duration of
Embryonic Development
A summary of results by these observations are
presented in Table 1. The 13 species of cockroaches
studied have different numbers of eggs (ANOVA, F
= 267.93, df = 10, 397; P < 0.01) and different
numbers of hatchlings (ANOVA, F = 71.56, df =
10, 397; P < 0.01). P. nivea had the highest number of eggs (71.2 ± 1.5) and hatchlings (54.7 ±
3.4) per brood, whereas D. punctata had the lowest number of eggs (11.8 ± 0.2) and hatchlings (9.6
± 0.3) per brood (Tukey pairwise comparisons, P
< 0.01). The average hatching rate was about
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Li
TABLE 1. Parameters of Embryo Development in Different Cockroach Species at 27°C*
Day of embryo
Day of dorsal
Reproductive mode
Species
development (n)
closure (n)
Oviparous
Ovoviviparous
Viviparous
Number of hatchlings
per brood (n)
Number of embryos
in one brood (n)
Blatta orientalis
Periplaneta americana
Eurycotis floridana
Supella longipalpa
Blattella germanica
49.04 ± 0.16 (28)
43.32 ± 0.12 (37)
50.46 ± 0.22 (28)
52.71 ± 0.15 (41)
20.77 ± 0.08 (31)
26 (18)
21 (18)
27 (18)
25 (18)
8 (16)
14.14 ± 0.65 (28)
15.03 ± 0.36 (37)
13.75 ± 0.95 (28)
13.80 ± 0.66 (41)
39.32 ± 0.99 (31)
14.40 ± 0.19 (62)
14.66 ± 0.28 (56)
17.55 ± 0.50 (56)
15.27 ± 0.32 (56)
46.34 ± 0.53 (32)
Blaberus discoidalis
Byrsotria fumigata
Rhyparobia maderae
Nauphoeta cinerea
Phoetalia pallida
Schultesia lampyridiformis
Panchlora nivea
60.77 ± 0.39 (35)
58.15 ± 0.46 (23)
63.53 ± 0.43 (34)
40.21 ± 0.22 (33)
36.05 ± 0.12 (39)
33.06 ± 0.16 (47)
33.81 ± 0.36 (42)
29 (18)
30 (17)
32 (18)
20 (18)
20 (18)
19 (18)
17 (12)
33.35 ± 1.55 (35)
11.29 ± 1.09 (23)
27.33 ± 1.47 (24)
32.78 ± 0.66 (33)
28.13 ± 0.73 (39)
23.63 ± 1.06 (47)
54.69 ± 3.35 (42)
34.88 ± 0.86 (58)
23.37 ± 1.16 (30)
32.57 ± 0.87 (56)
35.75 ± 0.64 (57)
30.15 ± 0.62 (54)
25.24 ± 0.31 (54)
71.24 ± 1.50 (49)
Diploptera punctata
67.30 ± 0.23 (30)
14 (14)
9.60 ± 0.31 (30)
11.79 ± 0.21 (42)
*The day of dorsal closure was determined for three embryos randomly selected from each brood. Data points are mean ± SD. Number of broods examined is shown in
parentheses.
86.5%, which indicates hatching was highly successful in all cockroach species in this study. Interestingly, the ratio of the average number of eggs to
the average number of hatchlings in each brood is
consistent across all species (Regression, F = 161.64,
df = 1, 11; R2 adj. = 0.93, and P < 0.01).
The embryonic development times were significantly different among the 13 species of cockroaches (ANOVA, F = 2,721.15; df = 10, 397; P <
0.01), and among the three reproductive modes
(ANOVA, F = 3052.50; df = 2, 397; P < 0.01). Viviparous D. punctata had the longest development
time (67.3 ± 0.2 day) compared to the mean time
for oviparous (43.6 ± 0.9 day) and ovoviviparous
(44.0 ± 0.7 day) cockroaches. B. germanica had the
shortest (20.8 ± 0.1 days) development time; S.
lampyridiformis and P. nivea had similar development times (Tukey pairwise comparisons, P >
0.05), but those of the other species were all different from each other (Tukey pairwise comparisons, P < 0.05).
Within each species, DC occurred in more than
75% of the embryos during a 2-day period (data
not shown), indicating that the embryos developed
at a similar rate in each species. This suggests that
not only the embryos in the same brood but the
embryos in the same species developed at a similar pace.
The time of DC (day of DC) was significantly
correlated with the duration of embryonic devel-
opment (oviposition to day of hatch) (Correlation
analysis, F = 8.3; df = 1, 11; P = 0.015; R2 adj. =
37.8%) among all the cockroaches studied. However, D. punctata and B. germanica were different
from other species (outliers), and when these two
species were excluded the correlation was very significant (Correlation analysis, F = 145.85, df = 1,
9; P < 0.01; R2 adj. = 93.5%). This indicates that
the time of DC was very consistent, around 45.0%
of embryo development time, in most of the cockroach species studied. This suggests that the development time before DC was probably a conserved
developmental event in cockroaches. In other insect groups, DC occur at about 48–60% of the embryogenesis period (Truman and Riddiford, 1999,
2002). B. germanica is considered a link species between the oviparous and ovoviviparous groups
(Roth, 1970; Schal et al., 1997). The DC day of B.
germanica, 38.5% of the total embryogenesis time,
was the shortest among all species studied except
D. punctata.
Analysis of MF and JH Production by CA From
Post Dorsal Closure Embryos
Using the methods described, 13 species of
cockroaches were examined and JH and MF synthesis and release were detected in all except S.
longipalpa, B. germanica, P. pallida, S. lampyridiformis,
and P. nivea (Fig. 1).
Archives of Insect Biochemistry and Physiology
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JH and MF in Cockroach Embryos
The rates of JH production by embryonic CA,
shown in Figure 2A and B, were significantly different among the cockroach species with detectable JH (ANOVA, species term, F = 34.80; df = 5,
82; P < 0.01) and among the three reproduction
modes (ANOVA, reproductive mode term, F =
39.95; df = 2, 82; P < 0.01). Embryonic CA of different cockroach species synthesized and released
different amounts of JH (ANOVA, JH/MF term, F
= 9.82; df = 1, 82; P < 0.01). Similarly, they also
synthesized and released different amounts of MF.
(ANOVA, species term, F = 16.05; df = 5, 82; P <
0.01) (Fig. 2). However, when the CA synthesized
more JH, they released more JH (ANOVA, interaction term, F = 0.54; df = 2, 82; P < 0.75). In contrast, the release of MF was a species-dependent
process. When CA synthesized more MF, they did
not release more accordingly (ANOVA, interaction
term species by synthesis/release, F = 3.83; df = 5,
82; P < 0.01).
The ovoviviparous cockroaches examined (B.
discoidalis, B. fumigata, N. cinerea, and R. maderae)
produced more JH than the oviparous cockroaches
(B. orientalis, P. americana, and E. floridana) (Contrast analysis, P < 0.01). The level of MF produced
by the two types of cockroaches was not significantly different (contrast analysis, P > 0.05).
The embryonic CA of D. punctata produced and
released the largest amount of JH among the species studied and MF was also produced and released. The three oviparous species, B. orientalis, P.
americana, and E. floridana, produced and released
appreciable amounts of JH and trace amounts of
MF as well, whereas in the ovoviviparous cockroaches, N. cinerea and R. maderae, besides the production of JH, relatively large amounts of MF were
produced and released. In B. discoidalis and B.
fumigata, both JH and small amounts of MF were
produced and released (Fig. 2).
The effect of farnesol added to assay medium
of CA from four species of cockroaches showed that
the release of JH increased when CA were treated
with farnesol (Fig. 3). In D. punctata, the rate of
release of JH by CA increased threefold with the
farnesol treatment compared to untreated glands.
MF production was not significantly changed in
Archives of Insect Biochemistry and Physiology December 2007
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Fig. 2. Hormonal products of embryonic CA at 40% post
dorsal closure time in different cockroach species. A: JH
production. B: MF production. Data were graphed with
logarithmic y-axis. Columns represent mean ± S.E. Number of replicates ranged from 3 to 13 (6-pairs of CA per
replicate). Differences in JH and MF production were analyzed by ANOVAs separately (see Results). Release and synthesis and modes of reproduction as in Figure 1.
CA treated with farnesol compared to untreated
glands, except for CA of R. maderae, in which the
MF contained in CA increased after farnesol incubation (Tukey comparison, P < 0.05, Fig. 3).
DISCUSSION
In D. punctata and N. cinerea, my findings of
the days of DC and the length of embryogenesis
are consistent with previous reports (Stay et al.,
2002; Brüning et al., 1985). DC occurred at 47–
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Fig. 3. Comparison of JH and MF production by members of embryonic CA pairs, one treated with farnesol and
the other untreated. A: JH production. B: MF production.
Data were graphed with logarithmic y-axis. Bars represent
mean ± S.E. Replicates ranged from 6 to 16 pairs of CA. R
= release, C = content of products by untreated corpus
allatum. RF = released, CF = content of products after
farnesol treatment. Differences in JH and MF were analyzed by ANOVAs separately (see Results). Within each
species, Tukey pairwise comparisons were used between
treated and untreated glands. *Differences (P < 0.05).
57% of embryogenesis across all cockroach species except D. punctata, which was similar to the
48–60% reported for other hemimetablous insects
(Truman and Riddiford, 1999). Conserved time to
DC in oviparous and ovoviviparous species might
be controlled by nutrients availability to the embryos. The availability of nutrients is an important
factor in embryo-immature-adult development
theories (Truman and Riddiford, 1999). In the only
known viviparous cockroach, D. punctata, the day
of DC was relatively short (20.8% of embryo de-
velopment time), which is probably related to the
small amount of yolk supplied to the eggs.
Hemimetabolous insects start to produce their
pronymphal cuticle around dorsal closure (Truman
and Riddiford, 1999) and at the same time the corpora allata become physiologically active, for example in cockroaches (Lanzrein et al., 1984). A
high JH titer after DC precedes the prenymphal
molt in hemimetaboluous insects (Truman and
Riddiford, 1999). In addition to JH, the JH immediate precursor, MF, has also been shown to be
present in cockroach embryos (Brüning et al.,
1985).
In crustaceans, MF is suspected to play a similar role to JH III in insects (Homola and Chang,
1997). MF circulates in the hemolymph and regulates protein metabolism, the molt cycle, and reproduction (Homola and Chang, 1997). Moreover,
MF exerts JH-like effects when injected into N. cinerea larvae and female adults (Brüning and
Lanzrein, 1987). In the closely related R. maderae
and N. cinerea, relatively higher amounts of MF
were produced and released compared to other species, which suggests that the synthesis and release
of MF is probably phylogenically relevant. In the
eight species of cockroaches representing the diversity and evolutionary history of the order
Blattaria, MF was synthesized and released by embryonic CA in vitro, which suggests that this compound may circulate in the blood and may act as
a hormone per se. Although the amounts of MF
produced and released by embryonic CA varied
among the species studied and were much lower
compared to that of JH, the presence of MF in cockroach embryos presented here for primitive and
more highly evolved species together with previously reported presence of MF in crustaceans suggests that this molecule might be an ancient
hormone in arthropods.
It has been speculated that the accumulation
of MF in the CA could be the consequence of a
limited oxygen supply for conversion of MF to JH
III (Lanzrein et al., 1984). Since MF occur in D.
punctata whose embryos are continuously surrounded by a layer of air and whose chorion is
thin and ruptures early in embryogenesis, it is unArchives of Insect Biochemistry and Physiology
December 2007
doi: 10.1002/arch.
JH and MF in Cockroach Embryos
likely that the production of MF is due to a limited oxygen supply of embryos.
In the JH biosynthesis pathway, farnesol is converted into farnesoic acid and then into MF. In this
study, farnesol treatment resulted in the release of
large amounts of JH whereas little change occurred
in the amount of JH contained in the CA. These
results suggest that the amount of JH contained by
cockroach embryonic CA probably was determined
by factors such as CA volume or cell number or
was correlated with the amount of JH released.
In D. punctata, CA treated with farnesol released
a large amount of JH into the medium. However,
CA of R. maderae treated with farnesol accumulated MF within the glands. These results suggest
that in embryonic CA of D. punctata, MF does not
saturate MF epoxidase. This finding is similar to
results in adult female P. amaricana (Pratt et al.,
1975), which is also in agreement with the claim
that MF epoxidase is not a rate-limiting enzyme in
the JH-biosynthetic pathway in D. punctata (Holbrook et al., 1996; Schooley and Baker, 1985). In
contrast, in R. maderae, MF was retained in the CA.
In B. fumigata and B. discoidalis, there were no significant differences between the CA with and without farnesol treatment. These results suggest that
embryonic CA of different cockroach species respond differently to farnesol treatment, which has
also been observed for CA of adult bees belonging
to different castes (Rachinsky et al., 2000). The role
of MF in insect development and metamorphosis
warrants further study of MF production in larval
and adult stages of these cockroach species and in
embryos of related hemimetaboulous insects. The
data presented here illustrate the potential role for
MF in embryogenesis in ancestral insects such as
cockroaches.
ACKNOWLEDGMENTS
I thank Dr. Glenn Holbrook for his guidance
in this research design and methods. Thanks to Dr.
Kenneth Berger for technical support. I thank Dr.
Kambhampati for confirming the phylogenic tree
used in present paper. I also thank Dr. Stephen L.
Rathbun for providing comments on statistical
Archives of Insect Biochemistry and Physiology December 2007
doi: 10.1002/arch.
167
analysis. I am grateful to Drs. Coby Schal, Barbara
Stay, and Diana L. Cox-Foster for their comments
and editorial suggestions.
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Archives of Insect Biochemistry and Physiology
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doi: 10.1002/arch.
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