First published online August 31, 2004
Journal of Experimental Biology 207, 3603-3617 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01183
Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locust
Stephen M. Rogers1,2,*,
Thomas Matheson1,
,
Ken Sasaki1,
Keith Kendrick3,
Stephen J. Simpson2 and
Malcolm Burrows1
1 Department of Zoology, University of Cambridge, Downing Street, Cambridge
CB2 3EJ, UK
2 Department of Zoology, University of Oxford, South Parks Road, Oxford OX1
3PS, UK
3 Laboratory of Cognitive and Developmental Neuroscience, Babraham
Institute, Babraham, Cambridge CB2 4AT, UK
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Fig. 1. Schematic of the nine stages of phase change analysed. Shown descending on
the left-hand side, cohorts of long-term crowded (gregarious-phase; stage 1)
locusts are taken and isolated for increasing periods, becoming increasingly
solitarious. Locusts that have been isolated for three whole generations
(long-term solitarious; stage 6) are then taken and crowded for increasing
periods, causing a progressive change to the gregarious phase, shown rising on
the right-hand side. Locusts that are crowded for long enough revert to the
gregarious phase state.
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Fig. 2. (A–M) Changes in the amounts of 13 chemicals in three different
regions of the central nervous system during successive stages (1–9) in
the isolation of long-term gregarious phase locusts (stage 1; darkest grey
background) and the gregarization of third generation solitarious locusts
(stage 6; white background). Values (mean ±
S.E.M.) are the amounts found in the brain
(red circles) excluding optic lobes, optic lobes (blue triangles) and the
thoracic ganglia (green squares) for final larval instar nymphs at the stages
of isolation or crowding indicated on the x-axis.
N=9–12 for each point. Note that the values for citrulline are
ln transformed. Stages as in Fig.
1.
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Fig. 3. Amino acids that increased on solitarization in final instar nymphs. (A)
Amino acids that exhibited large (over 2x) rapid changes. Aspartate,
glutamate and glycine showed rapid increases on the initial 24 h isolation of
gregarious locusts, before declining again in the first stadium of isolation.
Amounts increased again over a further 1–3 generations of isolation.
Crowding third generation isolated locusts led to a rapid decline in the first
4 h, but amounts had increased third generation isolated values by 24 h of
crowding. Values returned towards long-term gregarious values after 1 crowded
stadium. (B) Amino acids that exhibited smaller (maximum 1.8x) and
slower changes. Taurine, arginine and GABA did not change significantly during
the first 24 h of crowding or isolation, but increased only after 1 generation
of isolation. Values (mean ± S.E.M.)
are sum amounts in the three sampled regions of the central nervous system,
standardized to give the mean long-term gregarious value as 1. Stages as in
Fig. 1.
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Fig. 4. Chemicals that decreased on solitarization in final instar nymphs were
tyramine, citrulline and acetylcholine. Tyramine decreased to 30% of its
gregarious value within 24 h of isolation and remained low during all stages
of solitarization, but increased rapidly within 24 h of crowding. Citrulline
decreased to less than 10% of gregarious amounts after 24 h isolation and
remained low during all stages of isolation and gregarization monitored.
Acetylcholine declined slowly over a period of 24 h to 1 generation of
isolation and remained at approximately 80% of the gregarious amount during
further generations of isolation. It did not recover following 1 stadium of
crowding. Values (mean ± S.E.M.) are
sum amounts in the three sampled regions of the central nervous system,
standardized to give the mean long-term gregarious value as 1. Stages as in
Fig. 1.
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Fig. 5. Changes in the monoamines dopamine, serotonin and octopamine during phase
change. Dopamine (A) increased three- to fivefold throughout the central
nervous system following a 24 hperiod of isolation of gregarious locusts, but
declined to near gregarious values after 1 stadium of isolation. Locusts
isolated for longer periods had amounts just above those of gregarious
locusts. There was an increase in brain dopamine levels 4–24 h following
crowding, but a decline in the optic lobes and thoracic ganglia. Mean amounts
of optic lobe serotonin increased eightfold on initial isolation, accompanied
by more modest changes in the brain and no change in the thorax. Amounts
declined to near gregarious levels throughout the central nervous system on
further isolation. 4 h of crowding produced a ninefold increase in thoracic
serotonin, followed after 24 h by smaller (fourfold) increases in the brain
and optic lobes. There were no significant changes in octopamine (C) during
the entire isolation process, but crowding third generation solitarious
locusts for 24 h caused a 13-fold increase in the optic lobes and a sevenfold
increase in the thoracic ganglia. The amounts of octopamine in the optic lobes
remained high after 1 stadium of crowding. Values (mean ±
S.E.M.) are the amounts in the three sampled
regions of the central nervous system, standardized to give the mean long-term
gregarious value as 1. Stages as in Fig.
1.
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Fig. 6. Relative differences in the amounts of 12 chemicals in the brains and
thoracic ganglia of second generation solitarious and long-term gregarious
adult locusts. Values are standardized to give a mean gregarious value of 1;
the grey bars indicate ± S.E.M. of the
gregarious values. The circles shown the mean multiple of the gregarious value
found in second-generation isolated locusts (±
S.E.M.). Asterisks indicate significance of
post hoc comparisons, as detailed in
Table 2. NS, not
significant.
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Fig. 7. Summary of the neurochemical changes that occur on isolation of gregarious
and crowding of solitarious locusts. (A) Median values (dark blue circles and
line), interquartile range (dark blue region) and 95% data range (light blue
region) for all chemicals analysed, expressed as multiple of the difference
from long-term gregarious values. The inverse values were used for chemicals
that declined in solitarious locusts (cf.
Fig. 3). Outliers (data that
lie more than two interquartile ranges from the median) are shown as circles
and, for citrulline, as triangles. Selected data from Figs
3 and
4 (squares) are also plotted
for comparison with the overall pattern. Optic, optic lobes; thorax, thoracic
ganglia; OA, octopamine; 5-HT, serotonin; DA, dopamine. (B) Median changes in
the amounts of neurochemicals as in A (blue line), plotted against the change
in behavioural phase state associated with the same degrees of isolation and
crowding (stages 1–9; see Fig.
1), expressed as P (solitary) in a logistic regression
behavioural assay (orange, gregarious; green, solitarious). Data for
behavioural phase state taken from Roessingh et al.
(1993 ) and Roessingh and
Simpson (1994).
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© The Company of Biologists Ltd 2004
