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First published online February 1, 2008
Journal of Experimental Biology 211, 548-554 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.009233
Cuticular hydrocarbons as maternal provisions in embryos and nymphs of the cockroach Blattella germanica
Department of Entomology and W. M. Keck Center for Behavioral Biology, Box 7613, North Carolina State University, Raleigh, NC 27695 7613, USA
* Author for correspondence (e-mail: coby_schal{at}ncsu.edu)
Accepted 1 December 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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50%) of radiolabeled maternal hydrocarbons was
transferred to oocytes and persisted through a 20-day embryogenesis and the
first two nymphal stadia. The maternal hydrocarbons were not degraded or lost
during this protracted period, except for significant losses of cuticular
hydrocarbons starting with the first-to-second instar molt. Thus, although
embryos and nymphs can produce their own hydrocarbons, maternal hydrocarbons
provide a significant fraction of the cuticular and hemolymph hydrocarbons of
both stages. These results show, for the first time in any insect, that a
mother provides a significant complement of her offspring's cuticular
hydrocarbons. Further research will be needed to determine whether
provisioning hydrocarbons to eggs is a general strategy among insects and
other arthropods or if this strategy is limited to taxa where eggs and early
instars are susceptible to desiccation.
Key words: cuticular hydrocarbons, maternal investment, waterproofing, communication, cockroach, Blattella germanica
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Material provisions of oviparous females in eggs are
nevertheless extensive and costly because all provisions are gathered,
processed and sequestered within a short pre-ovulatory period. The greatest
investment is represented by proteins – mainly vitellogenin and other
glycolipoproteins – that are metabolized during early embryogenesis to
release products that are used to biosynthesize embryonic and neonate tissues.
In marine invertebrates, a group in which egg-size evolution has been
extensively researched, protein content of the egg increases in direct
proportion to egg size (Jaeckle,
1995), highlighting the pivotal role of proteins in
embryogenesis.
Nevertheless, large amounts of maternal lipids are also sequestered in
oocytes (Kunkel and Nordin,
1985; Speake and Thompson,
1999; Ziegler and van
Antwerpen, 2006), and lipids too, like proteins, are metabolized
during embryogenesis to serve as components of membranes (i.e. phospholipids)
and as metabolic fuel sources (i.e. most neutral lipids, such as di- and
triacylglycerols). There are few quantitative studies on the provisioning and
metabolic fate of apolar lipids in eggs, and this is especially surprising in
insects, where all life stages require extensive deposition of long-chain
hydrocarbons on the cuticle to prevent desiccation. Indeed, a recent
minireview of lipid uptake by insect oocytes
(Ziegler and van Antwerpen,
2006) makes no mention of hydrocarbon uptake. In some marine
invertebrates, lipid biomass (mainly wax esters) is higher than expected in
large eggs, and the adaptive value of increased lipids is thought to involve
greater buoyancy and higher energy content
(Emlet, 2001;
Emlet and Hoegh-Guldberg,
1997). But the embryonic strategies involved in processing
maternal lipids are poorly understood. In this report, we investigate the
patterns of maternal provisioning of long-chain hydrocarbons in oocytes and
the metabolic fate of the maternal hydrocarbons in embryos and nymphs of a
terrestrial insect. We show that, unlike other maternal nutriments,
hydrocarbons are not metabolized as an energy source, but rather are conserved
for waterproofing the cuticle across several larval molts.
Long-chain cuticular hydrocarbons waterproof insect cuticle and serve as
pheromones or as pheromone precursors
(Gibbs, 1998;
Howard and Blomquist, 2005;
Nelson and Blomquist, 1995;
Schal et al., 1998;
Schal et al., 2003). In the
oviparous German cockroach, Blattella germanica L., hydrocarbons are
biosynthesized only by specialized cells (oenocytes) of the abdominal
integument and they accumulate in the hemolymph and the cuticular surface of
all life stages (Fan et al.,
2003; Gu et al.,
1995). In the adult female cockroach, surprisingly large amounts
of hydrocarbons are found within the ovaries, and because the ovaries do not
biosynthesize hydrocarbons, all ovarian hydrocarbons are delivered to the
maturing oocytes by lipophorin, a high-density hemolymph lipoprotein
(Fan et al., 2002;
Gu et al., 1995;
Schal et al., 1994;
Schal et al., 1998). The
adaptive value of hydrocarbons on the external surface of the eggs is
apparent: the specific hydrocarbon blend on the eggs has a melting temperature
that is 15.4°C and 21.5°C higher than the melting temperature of
female's own cuticular hydrocarbons and lipophorin-bound hydrocarbons,
respectively (Young et al.,
2000). However, the hydrocarbons within the oviposited eggs are
similar to those of the mother. Although the location, metabolic fate and
adaptive value of maternally derived hydrocarbons within the developing
embryos are unknown, it is likely that, as hypothesized for wax esters in
marine invertebrates, hydrocarbons may serve physical functions (i.e.
waterproofing) or as nutrients and energy reserves. We now provide the first
empirical support for the proposal that maternal hydrocarbons are conserved
during embryogenesis, they coat the embryonic and nymphal cuticles and are
slowly lost, mainly during successive molts, as nymphs ingest more food and
are able to produce their own hydrocarbons.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Insect colony
The German cockroach, Blattella germanica L., colony was
maintained at 27±0.5°C, 50% relative humidity and 12 h:12 h
light:dark photoperiod and was provided with a continuous supply of rat chow
(Purina Mills, St Louis, MO, USA) and water. Newly emerged adult females were
separated from the colony on the day of adult eclosion (day 0), and maintained
in separate plastic cages. Females were always maintained in groups of
10–50 individuals because solitary females are reproductively repressed
(Gadot et al., 1989;
Holbrook et al., 2000).
Females were mated on day 6, they oviposited on day 9, and embryos hatched
from egg cases when females were 29 days old, or 20 days after oviposition
under these conditions. During the 20-day embryogenesis, the proximal part of
the egg case is held in the female's genital vestibulum and is provisioned
with water (Mullins et al.,
2002).
Ovarian, embryonic and cuticular hydrocarbons
Surface lipids were extracted from egg cases as described previously
(Young and Schal, 1997). Each
egg case was immersed in 2 ml n-hexane containing 15 µg
n-hexacosane as an internal standard, agitated gently for 5 min, and
the solvent was decanted into a clean vial. This procedure was repeated and
the egg case was subjected to a final rinse with 1 ml hexane. The three hexane
extracts were combined and the hydrocarbons were purified and quantified by
GC.
Internal lipids were extracted by a modified Bligh and Dyer
(Bligh and Dyer, 1959)
procedure (Gu et al., 1995).
For samples to be analyzed by GC, 15 µg n-hexacosane was added as
an internal standard. Lipids were extracted from various tissues by
homogenization in water for 30 s (Kontes micro ultrasonic cell disruptor,
Vineland, NJ, USA) in a glass vial, and the homogenate was extracted with
hexane/methanol/water (2:1:1). Samples were vortexed vigorously and
centrifuged at 2000 g for 10 min. An aliquot of the hexane
phase was loaded on a 500 mg silica gel (100–200 mesh, type 60A;
Fisher, Fairlawn, NJ, USA) mini-column in a Pasteur pipette, and hydrocarbons
were eluted with 6 ml hexane. The solvent was reduced with a gentle stream of
N2, and hydrocarbons were quantified by GC or by liquid
scintillation spectrometry (LSS; LS5801; Beckman, Fullerton, PA, USA).
For GC analysis, the hexane was reduced to 1–2 µl with N2 and analyzed on a HP5890II GC (Agilent, Palo Alto, CA, USA) equipped with a flame-ionization detector and interfaced with a HP ChemStation (Rev. A.09.03). Splitless injection was made into a 30 mx0.32 mmx1 µm HP-5 capillary column operated at 100°C for 2 min, increased at 20°C min–1 to 150°C, then at 5°C min–1 to 310°C and held at this temperature for 5 min. The injector and detector were held at 300°C and 310°C, respectively.
In vitro hydrocarbon synthesis by embryos and first-instar nymphs
Methylmalonyl-CoA, derived from propionate, can serve as a methyl-branch
donor in the synthesis of methyl-branched hydrocarbons in B.
germanica (Chase et al.,
1990). Since over 80% of Blattella's hydrocarbons are
methyl-branched (Jurenka et al.,
1989) this allows us to track overall de novo hydrocarbon
biosynthesis with [1-14C]propionate. An egg case or individual
first-instar nymphs were bisected with a sharp razor and incubated in 500
µl L-15B medium [adjusted to 410 mOsm by the addition of 55 mmol
l–1 NaCl and 40 mmol l–1 Hepes, pH 7.4 and
sterilized by filtration through a 0.22 µm low protein binding filter
(Millipore, Bedford, MA) just prior to use] and 37 kBq
[1-14C]propionate. All incubations were at 27°C with constant
shaking on an orbital waving shaker (VWR, Atlanta, GA, USA) to oxygenate the
tissues. After 3 h, the tissues were removed and analyzed for labeled
hydrocarbons. Hydrocarbons were purified and radioactivity in the hydrocarbon
fraction analyzed by LSS.
Tracking radiolabeled hydrocarbons
Three-day-old females were injected with 111 kBq sodium
[1-14C]propionate in 1 µl Blattella saline
(Kurtti and Brooks, 1976) and
mated on day 6 with 15-day-old males. Another group of 3-day-old females were
injected with 3.36 kBq [3H]3,11-dimethylnonacosane in 1 µl
Blattella saline containing 0.02% Triton X-100 and also mated on day
6. External lipids of embryos and nymphs at different developmental stages
were extracted followed by extraction of internal lipids in
chloroform/methanol/water (2:1:0.9, v/v). The chloroform phase was dried under
nitrogen, hydrocarbons purified and subjected to LSS.
Thin-layer chromatography (TLC) of lipids
Aliquots of 0.336 kBq of extracted lipids were analyzed by TLC (Silica gel
60–F254; Merck, Damstadt, Germany) using hexane/ethyl
ether/acetic acid (80:20:2, v/v). Lipid classes were identified by comparing
their mobilities with those of authentic standards. Radioactive lipids were
scanned with a BioScan system 200 image scanner (Washington, DC, USA).
Statistical analyses
Statistical analyses were performed using SAS statistical analysis software
(version 9.1, SAS Institute, Cary, NC, USA).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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40 basal oocytes synchronously mature between
days 0 and 9 of the first ovarian cycle (reviewed in
Schal et al., 1997). Females
oviposit on day 9, and although B. germanica is considered oviparous,
females exhibit functional ovoviviparity: fertilized eggs are oviposited into
an egg case that remains attached to the genital vestibulum of the female
between days 9 and 29 (see Fig.
1A for events of the reproductive cycle). During this `pregnancy',
embryogenesis proceeds and the new basal oocytes in the ovaries are prevented
from growing. After hatching, the female resumes a new vitellogenic cycle (not
shown).
During the preoviposition period, the female amasses about 450 µg of
hydrocarbons internally, about half of which accumulate in the ovaries
(Fan et al., 2002). The
ovarian hydrocarbons sharply decline at oviposition on day 9 and,
subsequently, the ovaries do not accumulate hydrocarbons during `pregnancy'
(days 9–29) (Fig. 1A).
While the exterior of the newly formed egg case contained only
18.7±1.20 µg (s.e.m., N=7) hydrocarbons, its interior
contained 224.6±8.52 µg (N=7), which approximately
represented the difference between ovarian hydrocarbons before and after
oviposition (231.6 and 8.2 µg, respectively). Thus, copious amounts of
hydrocarbons accumulate in the ovaries and are then transferred into the egg
case with the oviposited eggs. Because the ovaries do not synthesize
hydrocarbons (Gu et al.,
1995), hydrocarbons must be shuttled to the ovaries through the
hemolymph.
The external hydrocarbons of the egg case remained relatively constant but
with a slight decline towards the end of embryogenesis
(Fig. 1A). By contrast, 225
µg of embryonic hydrocarbons were recorded on the first day, they remained
unchanged for 6 days (to mother's age 15 days), then significantly increased
by 19% to 268±6.01 µg (N=7) through embryo age 11 days
(mother's age=20 days) and remained constant until hatching (one-factor ANOVA,
F=15.43, d.f.=3,23, P<0.001).
The elevation in hydrocarbon titer was coincident with the onset of de
novo hydrocarbon biosynthesis (Fig.
2A) around dorsal closure (day 7–8)
(Tanaka, 1976), when embryonic
oenocytes become differentiated and competent to produce their own lipids.
Hydrocarbon production in embryos increased significantly on day 7 (mother's
age 16 days) to a broad peak lasting about 7 days and then gradually declined
to non-detectable levels shortly before hatching on day 20. A similar cycle
was evident in first-instar nymphs, where hydrocarbon production was low early
in the stadium, peaked on days 2–4 and declined to extremely low levels
of hydrocarbon synthesis by the final day before the molt
(Fig. 2B,C).
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), transported by lipophorin to the ovaries and then
incorporated in embryos and first- and second-instar nymphs. About 7.05% of
the injected propionate was used for hydrocarbon production. Some radiolabeled
hydrocarbons (58.8%) were retained in the female's interior and transported to
the female's cuticular surface, and 41.2% was provisioned into the eggs.
Interestingly, maternal (i.e. radiolabeled) hydrocarbons in the embryo
remained relatively unchanged throughout embryogenesis
(Fig. 3A), indicating that (1)
no new maternal hydrocarbons were provisioned to embryos after oviposition, as
expected in oviparous reproduction, and (2) little, if any, metabolism of
maternal hydrocarbons occurred during embryogenesis.
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),
transfer of radiolabeled propionate to the oocytes is extremely unlikely.
Thus, it appeared that maternal hydrocarbons were not degraded at any
embryonic or post-embryonic stage.
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Surprisingly little loss of maternally provisioned hydrocarbons was evident
during the first instar (Fig.
3A), despite an expected loss at hatching, in association with the
molted embryonic cuticle. This is because immediately after hatching the
neonates ingest the embryonic cuticle (C.S., personal observation), resulting
in a highly efficient recycling of both maternal and embryonic cuticular
hydrocarbons (Fig. 1B,
Fig. 3A). The first substantial
loss of maternally provisioned hydrocarbons occurs during the first-to-second
instar molt. About 153.8 µg hydrocarbons was found in internal tissues of
newly hatched first instars, while 90.3 µg hydrocarbons (37% of total)
was associated with their cuticular surface
(Fig. 1B). By contrast,
16.0% of the total radiolabeled (maternal) hydrocarbons, representing
38.1±1.5% of first-instar nymph's labeled hydrocarbons, were
provisioned to the external cuticular surface, showing that most of the
maternal hydrocarbons are retained internally within the first-instar nymph,
while only a fraction is externalized. The cuticular hydrocarbons were then
shed during the molt to the second instar. The newly molted second-instar
nymph, in turn, ingested less of the shed cuticle, resulting in a substantial
loss of maternal hydrocarbons. Of the remaining maternal hydrocarbons (34.3%
of the total 14C-hydrocarbons), 9.9% was then found on the
cuticular surface of the second-instar nymph (equivalent to only
28.9±0.9% of radiolabeled hydrocarbons of the nymph) whereas 24.4% of
the total maternal hydrocarbons (71.1±0.9% of radiolabeled nymphal
hydrocarbons) were allocated to the internal hydrocarbon pool
(Fig. 3A). Because internal
– including maternal – hydrocarbons continue to be shunted to the
cuticular surface throughout each intermolt period
(Young et al., 1999), it is
not surprising that 16.6% of maternal hydrocarbons are lost after the
second molt, and this loss is expected to continue in successive molts of
well-fed insects. Nevertheless, the steady-state hydrocarbon composition of
early nymphs suggests a `last in/first out' hypothesis, whereby maternal
hydrocarbons (first in) tend to be more retained internally than are newly
biosynthesized nymphal hydrocarbons, which are more rapidly externalized.
Consequently, maternal hydrocarbons appear to be used over many stadia as an
internal reserve.
A second, independent confirmation of this pattern was obtained by injecting [3H]3,11-dimethylnonacosane, a native B. germanica hydrocarbon, into vitellogenic females and tracking its metabolic fate in embryos and nymphs. As before, TLC indicated that little hydrocarbon was metabolized (data not shown). The pattern of utilization of maternal 3H-hydrocarbon by embryos and nymphs was nearly identical to that of 14C-hydrocarbon derived from propionate (Fig. 3A,B). Both patterns clearly show that a large fraction of maternal hydrocarbons is provisioned to eggs and subsequently to the interior of nymphs, to serve mainly for coating the external cuticular surface of nymphs at each molt and during the intermolt period.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). In addition to proteins, large stores of lipids are found
in mature insect eggs (Chino et al.,
1977). Studies with Manduca sexta, Locusta migratoria,
Rhodnius prolixus and B. germanica have described the lipid
transport processes (Arrese et al.,
2001; Ryan et al.,
1986; Schal et al.,
2003; Schal et al.,
1998). In M. sexta, 1% of the lipid in the oocyte is
biosynthesized by the egg itself, while 5% of the lipid is delivered by
vitellogenin. Lipophorin – both low- and high-density – is the
major vehicle for lipid delivery during vitellogenesis
(Kawooya and Law, 1988;
Kawooya et al., 1988;
Liu and Ryan, 1991;
Ziegler and van Antwerpen,
2006).
Maternally provisioned proteins and lipids are metabolized during
embryogenesis to release nutrients and a metabolic fuel supply. Along with
other lipids, a large amount of hydrocarbons, constituting about 4.85% of egg
lipids, is found in newly oviposited eggs of the German cockroach
(Fan et al., 2002). The fate
and function of maternal hydrocarbons within the embryo have not been
investigated in any insect. Our radiotracer results showed clearly the
intriguing fact that hydrocarbons were not metabolized during embryogenesis.
Rather, maternal hydrocarbons remained intact to aid in waterproofing the
cuticles of the first, second and even later instar offspring. Quantification
of embryonic hydrocarbons and in vitro studies of hydrocarbon
production showed that embryos began to make hydrocarbons approximately 30%
into embryonic development (Fig.
1). This is also the stage in B. germanica when the
oenocytes, the only cell type that biosynthesizes hydrocarbons
(Fan et al., 2003), become
differentiated and when deposition of the first embryonic cuticle is initiated
(Rinterknecht, 1985). It is
possible that maternal hydrocarbons might be used to coat the embryonic
cuticle before the embryo is capable of making its own hydrocarbons. Towards
the end of embryogenesis, a second embryonic cuticle – that of the
pharate first instar – is deposited. After formation of the pharate
first-instar cuticle, the oenocytes show signs of regression
(Rinterknecht, 1985),
coinciding with a sharp decline in production of hydrocarbons
(Fig. 2A) and molting
hormone.
But why does the mother provide later instars with hydrocarbon provisions
when they are fully able to biosynthesize hydrocarbon? The answer may lie in
the allometric scaling relationship between the cuticle and the fat body, as
well as in insects' cyclic loss of competency to make hydrocarbons. It is
possible that small nymphs, with a high surface area to volume ratio, are
limited in their capacity to make sufficient hydrocarbons to thoroughly coat
their cuticle and would experience high evaporative water loss. Maternal
hydrocarbons would thus offset such deficiencies and serve to protect young
nymphs from excessive water loss. Moreover, only a fraction of each intermolt
period is dedicated to hydrocarbon synthesis
(Fig. 2B)
(Cripps et al., 1988;
Young and Schal, 1997) and
this process is significantly constrained by both availability of food
(Young et al., 1999) and
cyclic cellular competency of the oenocytes to produce hydrocarbons
(Schal et al., 2003).
Interestingly, the first instar of the German cockroach is the only mobile
stage that can proceed to the next molt largely independent of food intake
(Kopanic et al., 2001). It is
quite likely that this lack of dependence upon food intake by the first instar
is conferred by the mother's nutrient and hydrocarbon investment in the
eggs.
Some marine invertebrates that provision their oocytes with large amounts
of nutrients might represent a remarkably similar scenario. While elevated egg
proteins free echinoderm larvae from the need to feed, extra provisions of
lipid appear not to be utilized during embryonic and larval development.
Rather, maternal lipids – mainly wax esters – appear to be
reserved for the postmetamorphic juveniles
(Emlet and Hoegh-Guldberg,
1997; Rinterknecht,
1985; Villinski et al.,
2002), and it is thought that provision of maternal lipids to
postlarval stages is an adaptive response to a particularly vulnerable
juvenile stage in a complex biphasic life cycle
(Byrne and Cerra, 2000).
Unfortunately, however, because the studies on marine invertebrates utilized
mass measurements, microscopy and GC, they did not examine de novo
lipid production nor clearly differentiated between maternal and newly
biosynthesized embryonic and larval lipids. Nevertheless, the convergence of
maternal lipid provisioning strategies of marine invertebrates and terrestrial
insects suggests that maternal waterproofing of neonates has played a central
role in the evolution of oviparity. If proven correct, it would appear that
wax esters in marine invertebrates, in addition to serving in buoyancy, as
previously suggested, might also be used for waterproofing.
The evolution of the amniotic/cleidoic egg of reptiles and birds also
represents a case where the transition of embryogenesis to a terrestrial
environment required adaptive changes, including prevention of desiccation and
greater maternal yolk provisions (Speake
and Thompson, 1999). As in marine invertebrates, greater yolk
provisions allow embryos of vertebrates, for example precocial birds, to
develop to a relatively advanced, active state, independently of the parents.
Bird vitellogenin is limited in its ability to deliver lipids to oocytes, and,
as in the cockroach, the plasma lipoprotein system is recruited to accomplish
this task. But in addition to providing energy, some maternal provisions
– for example the 18-carbon polyunsaturated fatty acid 
-linolenic
acid and docosahexenoic acid, a 22-carbon fatty acid derived from it –
are preferentially transferred from yolk to the embryo in birds, or across the
placental membrane in mammals (Speake and
Thompson, 1999); they are required for neuronal and retinal
development and cannot be synthesized by the embryo. Both fatty acids, like
hydrocarbon provisions in the cockroach, resist metabolic degradation in the
embryonic tissues; the fatty acids are instead targeted for delivery to the
developing embryonic brain.
A potential implication of our findings is that, as in the cockroach, some
social insects might endow their embryos with cuticular hydrocarbons as
trophic provisions. In many social insects, hydrocarbons play important roles
in species and nestmate recognition
(Howard, 1993), and nestmates
exchange and share cuticular hydrocarbons through mutual licking and passive
contact (Soroker et al.,
1994). These exchanges create a colony-specific odor, the
so-called gestalt chemical signature [ants
(Crozier and Dix, 1979); bees
(Breed and Julian, 1992)].
Thus, studies of hydrocarbon transfer among social insects have concentrated
on the homogenization of colony odors (i.e. hydrocarbons) through reciprocal
exchanges among sterile workers. It is possible that the demands of egg
production by queens also require that hydrocarbons biosynthesized by workers
might also be vectored to the queen, to serve as maternal trophic provisions
in eggs. Consequently, transfer of hydrocarbons throughout the colony might
serve to both homogenize nestmate recognition cues and deliver hydrocarbons to
the queens to provision to eggs. Therefore, it is important for researchers on
cuticular hydrocarbons in arthropods, especially in social insects, to
consider the multiplicity of hydrocarbon functions. For hydrocarbons to serve
solely as recognition cues, only nanogram amounts would be needed per
individual. Yet, small insects weighing just several mg may carry on their
cuticular surface and internally 2–5 orders of magnitude more
hydrocarbons than are needed as recognition signals. Clearly, waterproofing
and trophic contributions to progeny have played important roles in the
evolution of cuticular hydrocarbon profiles.
A number of intriguing issues remains to be addressed. First, how are
maternal hydrocarbons provisioned into oocytes? Second, how are hydrocarbon
reserves stored and partitioned in the embryo without interfering with growth
and cellular differentiation and without undergoing chemical cleavage, like
other maternal provisions? Third, what is the metabolic fate and function of
maternally provisioned hydrocarbons? Fourth, what happens to
hydrocarbon-deficient embryos? And finally, are there other maternal
provisions that withstand embryonic catabolism? To our knowledge, such
provisions have not been described in any animal or plant, but these questions
are readily tractable with radio- and mass-labeling approaches. Also, it will
be of interest to determine whether interference with maternal provisions
might constitute a new target for environmentally responsible management of
cockroach pest populations, which are now known to be a major source of
allergens that cause childhood asthma
(Rosenstreich et al.,
1997).
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Acknowledgments |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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