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First published online January 18, 2008
Journal of Experimental Biology 211, 370-376 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013458
Swarm formation in the desert locust Schistocerca gregaria: isolation and NMR analysis of the primary maternal gregarizing agent
1 School of Biological Sciences, The University of Sydney, Heydon-Laurence
Building A08, NSW 2006, Australia
2 Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1
3PS, UK
3 Department of Zoology, University of Rajshahi, Rajshahi 6205, Bangladesh
4 Department of Chemistry, University of Oxford, South Parks Road, Oxford, OX1
3QH, UK
* Author for correspondence (e-mail: stephen.simpson{at}bio.usyd.edu.au)
Accepted 12 November 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: gregarizing factor, L-dopa, locust phase, change, maternal effect, NMR spectroscopy, phenotypic plasticity
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
West-Eberhard, 2003). Locusts
express extreme polyphenism (Pener,
1991; Pener and Yerushalmi,
1998; Simpson and Sword,
2007; Uvarov,
1966); when subjected to high population densities, these insects
undergo changes in behaviour (Bouaichi et
al., 1995; Islam,
1996; Roessingh et al.,
1993; Rogers et al.,
2003; Simpson et al.,
1999), morphology (Dirsh,
1953) and colouration (Faure,
1932; Islam et al.,
1994b), as well as in reproductive features
(Schmidt and Albutz, 1999) and
other characteristics which reinforce further crowding and facilitate swarm
formation (Clynen et al., 2006;
Pener, 1991;
Pener and Yerushalmi, 1998;
Simpson and Sword, 2007;
Uvarov, 1966). In addition to
changing between extreme phases in response to crowding during their own
lifetime, locusts transmit information about their phase state to their
progeny (Hunter-Jones, 1958;
Islam et al., 1994a;
Islam et al., 1994b):
gregarious adults give rise to gregarious offspring, strongly influencing the
dynamics of locust plagues. This process is epigenetic, being
transgenerational, inducible and persistent for some duration in the absence
of inducing stimuli (Jablonka and Lamb,
2002; Jablonka and Lamb,
2005; Jablonka et al.,
2002).
Epigenetic transfer of phase state depends upon low molecular mass,
water-soluble chemicals within foam secreted by the reproductive accessory
glands at the time of oviposition
(Hägele et al., 2000;
McCaffery et al., 1998;
Rahman et al., 2002;
Simpson et al., 1999;
Simpson and Miller, 2007).
Although attempts to correlate egg foam chemistry with behaviour have been
made (Malual et al., 2001) and
some preliminary inquiries provided promising results
(Islam, 1997;
McCaffery et al., 1998),
bioactive foam components have yet to be identified
(Simpson and Miller, 2007).
Here we present the first direct evidence for a specific gregarizing compound
and provide data about its structure and possible phase-dependent
regulation.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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); p. 332.]
Solitarious mothers were second- or third-generation isolates reared in the
absence of conspecific stimuli, excepting a brief mating period, in
glass-fronted metal cages (10 cmx10 cmx25 cm) with upper and lower
compartments separated by 5 mm mesh grids. Gregarious adults were housed at a
density of 500–1000 insects per rearing bin (56 cmx76 cmx60
cm); females had continuous access to an oviposition box (27 cmx19
cmx12 cm) containing moist peat. Eggs for the study were collected in
plastic cylinders (3.5 cm diameterx8 cm high) filled with moistened sand
(10 g silver sand:1 ml water) placed either in the gregarious rearing bins,
where they temporarily replaced the peat box, or in the lower compartments of
the solitarious chambers beneath holes in the mesh grids. Incubation took
place in a room maintained at 30–32°C and 70–75% RH under a 12
h:12 h L:D cycle. Following eclosion, test hatchlings were either reared alone
(solitarious individuals) or in a group (gregarious individuals) until
subjected to behavioural assay on the day of hatching.
Logistic regression behavioural assay
Fifty-one hatchlings (<24-h old) reared in isolation from four
solitarious egg pods and 68 hatchlings (<24-h old) from the gregarious
culture (from an indeterminate number of egg pods) were used to construct the
logistic regression model. The protocol for assaying individuals during model
construction was identical to that used in later test assays on treatment
group hatchlings of unknown behavioural phase. Hatchlings were placed singly
into an arena (35.5 cmx15 cmx10 cm) and their behavioural
responses to a stimulus group of 50–70 conspecifics behind a perforated
plastic end wall were recorded for 10 min
(Islam et al., 1994a;
Islam et al., 1994b). Logistic
regression analysis, as previously discussed
(Simpson et al., 1999) is
appropriate to predict a binary outcome such as solitarious or gregarious
behavioural phase from a set of independent variables. Behavioural variables,
encapsulating both locomotory and non-locomotory movements and position in the
arena relative to the stimulus group, were recorded for each individual [see
Islam et al. (Islam et al.,
1994b) for a list of variables]. These served as independent
variables from which logistic regression assigned each test insect a value
between zero and one representing the probability of being considered
behaviourally gregarious (note that this differs from previous papers
describing
Psolitarious=1–Pgregarious).
Treatment of solitarious eggs with gregarious egg pod washes, gregarious crude foam extracts and solvent controls
Between 08:30 and 13:30 h, 12 egg pods (<5-h old) were collected from
crowd-reared females and separated into the foam plug and the remaining egg
mass (from which encasing foam was removed). The eggs were washed in distilled
water, ethanol or hexane (four pods per solvent, 2 ml each solvent). Resulting
solutions were filtered by Millex syringe-driven units (Millipore Corp.,
Billerica, MA, USA) and 50 µl aliquots were applied to 4.25 cm fluted
filter paper (Whatman, Maidstone, UK) pre-moistened with 5 µl distilled
water in 25 ml plastic containers. Water-moistened cotton wool was positioned
beneath each filter paper to maintain humidity. Within 5 min, individual eggs
(<2-h old) from solitarious mothers were sandwiched between the treated
filter paper and another untreated filter paper of the same size. The eggs
were then sealed within these plastic containers and incubated at
30–32°C until eclosion. Egg foam from the 12 gregarious pods was
also collected, cleaned of sand with a paintbrush, and homogenized using a
pestle and mortar in ethanol, distilled water or hexane at a concentration of
four plugs per 2 ml solvent. These crude foam extracts were syringe-filtered
and applied to filter paper identically to egg pod washes. Analogous
treatments for solvent controls (in which ethanol, distilled water or hexane
alone were placed on fluted filter paper beneath eggs) were also performed.
Egg washes, foam extracts and solvent controls were all prepared and deposited
onto filter paper immediately before eggs were added. A total of 41 and 40
hatchlings from nine solitary pods were used for egg pod wash and foam extract
treatments, respectively, and 43 hatchlings from the same pods were used as
solvent treatment controls.
HPLC analysis
Extracts were prepared by homogenization of foam plugs in a porcelain
mortar and pestle using 0.5 ml HPLC water (BDH, London, UK) per foam plug.
Each run was conducted using freshly isolated egg foam. Homogenates were
subjected to centrifugal filtration (10 000 g for 30 min) by
triple-rinsed polyethersulfone membranes (3 kDa molecular mass cut-off;
Vivascience AG, Hannover, Germany). Filtered extracts (500–1000 µl)
were loaded onto a HPLC system (Varian Inc., Palo Alto, USA) composed of three
components: a Varian 9012Q solvent delivery system, a Rainin Dynamax AI 200
automatic sample injector, and a Varian Prostar 330 photodiode array UV
detector (with range set to 190–350 nm). The arrangement was controlled
by a computer running Star Workstation v5.3. We utilized a 5 µm Spherisorb
ODS-2 25 cmx4.6 mm (Waters, Milford, MA, USA) separation column and a
flow rate of 1 ml min–1. Two solvents were chosen: (A) 0.1%
formic acid in H2O and (B) acetonitrile (BDH). Method 1 was used
for separation of samples related to the dose-dependence trial
(Fig. 1B) and for primary and
secondary separation runs (Fig.
2A,B,F,G): t=0.0 min, A:B=95:5; t=18.0 min,
A:B=32:68; t=18.1–22.0 min, A:B=0:100. Method 2 was used for
the tertiary separation run (Fig.
2C,E): t=0.0 min, A:B=95:5; t=12.0 min,
A:B=70:30; t=17.5–22.0 min, A:B=0:100. Method 3 was used for
the quaternary separation run (Fig.
2D,I): t=0.0 min, A:B=92:8; t=18.2 min,
A:B=72:28; t=19–24.0 min, A:B=0:100. Eluent collections were
made either of entire runs (Fig.
1B) or fractions thereof (Fig.
2, all treatments excepting some controls) into 50 ml round-bottom
flasks. Solvents were removed by rotary evaporation (Rotavapor, Switzerland)
under 3–6 kPa at 32–36°C until 5–10 µl solvent
remained; samples were then reconstituted to a total of 250–500 µl in
HPLC water for treatment of eggs. Peak integration was performed using
PolyView2000 (v5.3; Varian Inc.) on a total of 69 gregarious and 11
solitarious samples. Outliers (greater than 1.5 times the interquartile range
beyond upper or lower hinges) were excluded from statistical analysis.
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Nuclear magnetic resonance analysis
Samples for NMR were prepared identically to above, with several
modifications to increase yield. Fifty gregarious egg pods were separated from
sand cylinders and homogenized in 20 ml HPLC water. The resulting sand slurry
was transferred to a Buchner funnel fitted with a Whatman no. 4
analytical-grade filter paper wetted with 0.5 ml HPLC water and attached to a
vacuum flask. Sand was rinsed with a second volume of 20 ml, and the resultant
40 ml extract was centrifuged at 30 000 g for 5 min. The
supernatant was then centrifugally filtered through triple-rinsed
polyethersulfone membranes as previously described. Samples were flash-frozen
in liquid nitrogen and subjected to freeze-drying until solvents were removed
(2 days). This sample was then resuspended in 100 µl HPLC water and
separated by HPLC method 3. The gregarizing fraction (F3.2.1.2,
Fig. 2D,I) was then collected,
flash-frozen, and freeze-dried. This entire procedure was repeated with 100
egg pods, generating a replicate sample with more material. These two dried,
purified fractions were dissolved in 7 µl D2O; 6 µl were
placed into a 1 mm diameter NMR tube by centrifugation (the remainder was
subjected to high-resolution analysis on a Bruker ApexQ FT-ICR-MS with
Daltonics DataAnalysis 3.3, Billerica, MA, USA). Samples were analysed by 1H
NMR spectroscopy on a Bruker AVANCE DRX500 NMR spectrometer equipped with a 1
mm 1H/13C/15N TXI microprobe regulated at
25°C. There was insufficient material for the collection of 2D
1H-13C heteronuclear correlation spectra or NOE
spectra.
Statistical analysis
All data were analysed with SPSS 14 (SPSS Inc., Chicago, IL, USA).
Dose-dependence data were analysed by the distribution-free
Jonckheere-Terpstra test for categorically related groups. Other
Pgregarious values were rank normalized prior to
application of ANOVA and Dunnett's post-hoc analyses
(Conover and Iman, 1981). Peak
areas for solitary and gregarious foam were examined by Mann–Whitney
U-tests adjusted by the 
idák correction for multiple
comparisons (Abdi, 2007).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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2=102.88 at 6 d.f; P<0.001,
Table 1), and was chosen for
ascribing behavioural phase state to experimental and control insects in the
study. Gregarious nymphs tended to walk faster, sway more, spend less time in
the middle of the arena, end up closer to the stimulus group, spend more time
climbing the walls, and defecate less than did solitarious nymphs
(Table 1).
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Effects of dosage and solvents on egg foam efficacy
We applied extracts and washes created with different solvents to eggs and
assayed the behaviour of resultant hatchlings
(Fig. 1A,
Table 2) using the above
logistic regression model. Aqueous foam-extracts and egg-washes had
significant gregarizing activity when applied to solitarious eggs
(Table 2). Ethanolic
foam-extracts and egg-washes also significantly gregarized hatchlings from
solitarious eggs, but hexane treatments showed no significant effect on
behavioural phase state (Table
2). When water and increasing concentrations of aqueous foam
extract eluent were applied to solitarious eggs, a highly significant
dose-dependent response on hatchling behavioural phase was observed
(Fig. 1B, one-tailed
Jonckheere–Terpstra test, P=0.002). At a concentration of 0.4
FPE, the gregarizing effect of aqueous extract eluent was comparable to 0.1
FPE crude (pre-HPLC) extract.
Effect of HPLC fractions applied to eggs on hatchling behavioural phase
Some HPLC fractions applied to eggs affected their development; we
identified these bioactive fractions and iteratively examined increasingly
specific subfractions (Fig. 2).
The primary (Fig. 2A,F) run
served to identify fraction 3 (F3) as bioactive [a bioactive fraction, in this
context, is defined as one resulting in predominantly gregarious hatchlings
(i.e. a set of hatchlings whose median
Pgregarious
0.5) when applied to eggs]. Filtered foam
extract (FPE 0.1) and filtered extract HPLC eluent (FPE 0.4) were included as
positive controls. Although fraction 1
(Fig. 2A,F) was marginally
gregarizing (median Pgregarious=0.50), further assays
concentrated on F3 (median Pgregarious=0.62). The
behavioural phase state of hatchlings treated with F3 was not statistically
distinguishable from phase distributions of either filtered extract or
filtered extract HPLC eluent (Mann–Whitney U-tests,
P=0.94 and P=0.81, respectively). A secondary
(Fig. 2B,G) separation run
confirmed bioactivity of F3, and subfractions 3.1, 3.2, 3.3 and 3.4 were
further assayed for gregarizing potency. Fraction 3.2 (F3.2) was identified as
the sole gregarizing portion of F3; this subfraction resulted in a hatchling
phase distribution statistically indistinguishable from that induced by
application of the complete F3 (Mann–Whitney U-test,
P=0.18). F3.2, when further separated by HPLC method 2, was revealed
to consist of two very similar molecules
(Fig. 2C), only one of which
(F3.2.1, Fig. 2H) was
bioactive. The hatchling phase distribution resulting from HPLC subfraction
3.2.1 was not statistically distinguishable from that of F3.2
(Mann–Whitney U-test, P=0.59). In the final,
quaternary separation run, the solvent gradient was adjusted to separate more
finely F3.2.1 into three `sub-subfractions'. Only the second of these
(F3.2.1.2, Fig. 2D) was
bioactive, and the distribution of resulting hatchlings was not statistically
distinguishable from either filtered foam extract or filtered foam extract
HPLC eluent (Mann–Whitney U-tests, P=0.51 and
P=0.61, respectively).
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Peak area analysis: a comparison of gregarious and solitarious egg foam
Peak X (the bioactive peak) did not differ significantly in area between
solitarious and gregarious foam (idák-corrected
Mann–Whitney, P=0.22). However, peak Y was significantly
elevated in solitarious versus gregarious foam
(idák-corrected Mann–Whitney, P=0.03).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The presence of behaviourally gregarizing factors in polar (aqueous and
ethanolic) but not organic (hexane) solvents
(Fig. 1A) is consistent with
and extends earlier studies (Islam,
1997; McCaffery et al.,
1998) in which polar solvents were found to contain compounds
affecting gregarious colouration. As recently reviewed
(Simpson and Miller, 2007),
findings such as these discount the notion of bioactive unsaturated ketones
(Malual et al., 2001). The
dose-dependent effect of HPLC eluent upon behavioural phase
(Fig. 1B) further supports the
presence of bioactive agent(s) in aqueous extracts. Whether or not the same
compounds are involved in maternal transmission of colouration and behaviour
is a fascinating question worthy of further study.
Since peaks X (F3.2.1.2) and Z (F3.3) share nearly identical UV spectra (Fig. 2C,D) and retention times (Fig. 2A–E), they may represent conformational isomers. Interestingly, in contrast to its highly bioactive (Fig. 2H,I) putative isomer, peak Z is not bioactive (Fig. 2B,G). Peaks X and Y (F3.2.2), which are similar in retention time (Fig. 2A–D) and UV absorbance (Fig. 2C,D), are posited to be related through metabolic or oxidative pathways.
Spectroscopic details (Fig.
3A–C) of the maternal gregarizing agent suggest that an
alkylated L-dopa analogue (Fig.
3B) is responsible for transgenerational phase transmission. As an
extremely versatile and widespread component of invertebrate biochemical
systems, L-dopa can be synthesized from tyrosine by at least three
distinct enzymatic pathways (Waite,
1992). In invertebrates alone, L-dopa and its
metabolites are involved in processes as diverse as egg capsule formation
(Smyth and Clegg, 1959), silk
production (Kramer et al.,
1989), immunity (Nappi et al.,
1991) and predator defence
(Prota et al., 1981). Since
L-dopaminergic pathways are involved in both insect behavioural plasticity
(Goldstein and Camhi, 1991;
Kostowski et al., 1975) and
learning (Zhang et al., 2007),
perhaps it is not surprising that an L-dopa analogue is implicated
in locust phase transmission.
Although differences in gene expression have been found between locust
phases (Claeys et al., 2006;
De Loof et al., 2006;
Kang et al., 2004), our work
is the first to identify and demonstrate bioactive egg foam components capable
of causing such changes in gene expression. Using genetic arrays containing
locust expressed sequence tags, the effects upon gene expression of compounds
such as those in Fig. 3B could
be assayed and compared to the extreme expression profiles of solitarious and
gregarious specimens. An EST library for S. gregaria is currently in
preparation (De Loof et al.,
2006).
How might peak X (the bioactive compound) be regulated, given its presence
in equal amounts in solitarious and gregarious foam
(Fig. 4)? Differential
sensitivity due to differential receptor expression, such as occurs in the
tobacco hornworm (Manduca sexta) where ecdysterone sensitivity is
regulated via variable receptor expression
(Fujiwara et al., 1995), cannot
apply to gregarization in the locust since solitarious eggs are capable of
responding to gregarizing cues (e.g. Figs
1,
2). Rather, our data
(Fig. 4) are consistent with
inhibition of the active compound X by a second factor. We suggest peak Y may
be the inhibitory factor, based on two observations: peak Y is found in
significantly elevated (twice-median) concentrations in solitarious
versus gregarious egg foam (Fig.
2C), and peaks X and Y are likely to be close homologues since
they elute at similar times and share nearly indistinguishable UV spectra
(Fig. 2D). Owing to the
molecular similarity of the two peaks, peak Y may competitively inhibit the
action of peak X at the receptor level. Hence, gregarization is postulated to
result from reduced levels of peak Y in the egg foam of behaviourally
gregarized females. Such inhibitory effects are not uncommon in insect
development; for example, juvenile hormone can inhibit certain ecdysteroid
activity (Heming, 2003).
Finally, although we show peak X is sufficient to elicit behavioural
gregarization (Fig. 2I) and
provide NMR data (Fig. 3) about
the dominant molecule in this peak, we cannot exclude the possibility that
gregarization is reliant upon a co-eluting compound whose concentration is
beneath NMR detection thresholds.
Unfortunately we could not test for explicit inhibitory effects of peak Y or obtain conclusive mass spectral data because of unavailability of experimental S. gregaria in Australia. We suggest that investigation of the interactions of peaks X and Y are a matter of priority for those with access to S. gregaria in the laboratory. If our hypothesis is supported, future work might be directed toward blocking maternal gregarization (and consequently blocking perpetuation of locust swarms) by development of potent, specific inhibitors similar to peak Y.
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Acknowledgments |
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