Redox chemistry, involving the transfer of electrons and hydrogen atoms, is central to energy conversion in respiration, and the control of gene expression by redox state commonly occurs in bacteria, allowing rapid responses to environmental changes, for instance, in the food supply. Colonial metazoans often encrust surfaces over which the food supply varies in time or space; hence, in these organisms, redox control of the development of feeding structures and gastrovascular connections could be similarly adaptive, allowing colonies to adjust the timing and spacing of structures in response to a variable food supply. To investigate the possibility of redox control of colony development, the redox states of hydractiniid hydroid colonies were manipulated experimentally. As in many colonial animals, hydractiniid hydroids display a range of morphological variation from sheet-like forms (i.e. closely spaced polyps with high rates of stolon branching) to runner-like forms (i. e. widely spaced polyps with low rates of stolon branching). In the runner-like Podocoryna carnea, azide, a blocker of the electron transport chain, and dinitrophenol, an uncoupler of oxidative phosphorylation, diminished the largely polyp-driven gastrovascular flow to a similar extent. Measures of the redox state of the polyp epitheliomuscular cells using the fluorescence of NAD(P)H suggest that azide shifts the redox state in the direction of reduction, while dinitrophenol shifts the redox state in the direction of oxidation. Colony development corresponds to redox state in that azide-treated colonies were more runner-like, while dinitrophenol-treated colonies were more sheet-like. Nevertheless, the functional role of polyps in feeding and generating gastrovascular flow probably contributed to a trade-off between polyp number and size such that azide-treated colonies had few large polyps, while dinitrophenol-treated colonies had many small polyps. Regardless of the treatment, P. carnea colonies developed to maturity and produced swimming medusae in the normal fashion. In the sheet-like Hydractinia symbiolongicarpus, treatment with azide resulted in complete suppression of the development of both the stolonal mat and the blastostyles, the reproductive polyps. Azide-treated H. symbiolongicarpus colonies therefore developed in a juvenilized, runner-like manner and much resembled colonies of P. carnea. Following cessation of azide treatment in H. symbiolongicarpus, normal colony development ensued, and both a stolonal mat and blastostyles formed. In both hydroid species, relative oxidization favors sheet-like growth, while relative reduction favors runner-like growth. Since feeding triggers strong contractions of polyp epitheliomuscular cells and results in relative oxidation, this experimental evidence supports the hypothesis of adaptive redox control of colony development and evolution.

REFERENCES

REFERENCES
Allen
J. F.
(
1993
).
Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes
.
J. Theor. Biol
165
,
609
–.
Allen
J. F.
,
Balin
A. K.
(
1989
).
Oxidative influence on development and differentiation: an overview of the free radical theory of development
.
Free Rad. Biol. Med
6
,
631
–.
Blackstone
N. W.
(
1996
).
Gastrovascular flow and colony development in two colonial hydroids
.
Biol. Bull
190
,
56
–.
Blackstone
N. W.
(
1997
).
Dose—response relationships for experimental heterochrony in a colonial hydroid
.
Biol. Bull
193
,
47
–.
Blackstone
N. W.
(
1998
).
Morphological, physiological and metabolic comparisons between runner-like and sheet-like inbred lines of a colonial hydroid
.
J. Exp. Biol
201
,
2821
–.
Blackstone
N. W.
,
Buss
L. W.
(
1991
).
Shape variation in hydractiniid hydroids
.
Biol. Bull
180
,
394
–.
Buss
L. W.
,
Blackstone
N. W.
(
1991
).
An experimental exploration of Waddington's epigenetic landscape
.
Phil. Trans. R. Soc. Lond B
332
,
49
–.
Cartwright
P.
,
Bowsher
J.
,
Buss
L. W.
(
1999
).
Expression ofa Hox gene, Cnox-2 and the division of labor in a colonial hydroid
.
Proc. Natl. Acad. Sci. USA
96
,
2183
–.
Chance
B.
(
1991
).
Optical method
.
Annu. Rev. Biophys. Biophys. Chem
20
,
1
–.
Chance
B.
,
Baltscheffsky
H.
(
1958
).
Respiratory enzymes in oxidative phosphorylation
.
J. Biol. Chem
233
,
736
–.
Dudgeon
S. R.
,
Buss
L. W.
(
1996
).
Growing with the flow: on the maintenance and malleability of colony form in the hydroid Hydractinia
.
Am. Nat
147
,
667
–.
Dudgeon
S. R.
,
Wagner
A.
,
Vaisnys
J. R.
,
Buss
L. W.
(
1999
).
Dynamics of gastrovascular circulation in the hydrozoan Podocoryne carnea: the 1-polyp case
.
Biol. Bull
196
,
1
–.
Eto
K.
,
Tsubamoto
Y.
,
Terauchi
Y.
,
Sugiyama
T.
,
Kishimoto
T.
,
Takahashi
N.
,
Yamauchi
N.
,
Kubota
N.
,
Murayama
S.
,
Aizawa
T.
,
Akanuma
Y.
,
Aizawa
S.
,
Kasai
H.
,
Yazaki
Y.
,
Kadowaki
T.
(
1999
).
Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion
.
Science
283
,
981
–.
Fanburg
B. L.
,
Massaro
D. J.
,
Cerutti
P. A.
,
Gail
D. B.
,
Berberich
M. A.
(
1992
).
Regulation of gene expression by O2tension
.
Am. J. Physiol
262
,
235
–.
Foyer
C. H.
,
Noctor
G.
(
1999
).
Leaves in the dark see the light
.
Science
284
,
599
–.
Hajnoczky
G.
,
Robb-Gaspers
L. D.
,
Seitz
M. B.
,
Thomas
A. P.
(
1995
).
Decoding of cytosolic calcium oscillations in the mitochondria
.
Cell
82
,
415
–.
Heineman
F. W.
,
Balaban
R. S.
(
1993
).
Effects of afterload and heart rate on NAD(P)H redox state in the isolated rabbit heart
.
Am. J. Physiol
264
,
433
–.
Jantzen
H.
,
Hassel
M.
,
Schulze
I.
(
1998
).
Hydroperoxides mediate lithium effects on regeneration in Hydra
.
Comp. Biochem. Physiol
119
,
165
–.
Nijhout
H. F.
(
1990
).
Metaphors and the role of genes in development
.
BioEssays
12
,
441
–.
Pfannschmidt
T.
,
Nilsson
A.
,
Allen
J. F.
(
1999
).
Photosynthetic control of chloroplast gene expression
.
Nature
397
,
625
–.
Polyak
K.
,
Xia
Y.
,
Zweier
J. L.
,
Kinzler
K. W.
,
Vogelstein
B.
(
1997
).
A model for p53-induced apoptosis
.
Nature
389
,
300
–.
Poyton
R. O.
,
McEwen
J. E.
(
1996
).
Crosstalk between nuclear and mitochondrial genomes
.
Annu. Rev. Biochem
65
,
563
–.
Pralong
W.-F.
,
Hunyady
L.
,
Várnai
P.
,
Wollheim
C. B.
,
Spät
A.
(
1992
).
Pyridine nucleotide redox state parallels production of aldosterone in potassium-stimulated adrenal glomerulosa cells
.
Proc. Natl. Acad. Sci. USA
89
,
132
–.
Pralong
W.-F.
,
Spät
A.
,
Wollheim
C. B.
(
1994
).
Dynamic pacing of cell metabolism by intracellular Ca2+transients
.
J. Biol. Chem
269
,
27310
–.
Rohács
T.
,
Nagy
G.
,
Spät
A.
(
1997
).
Cytoplasmic Ca2+signalling and reduction of mitochondrial pyridine nucleotides in adrenal glomerulosa cells in response to K+, angiotensin II and vasopressin
.
Biochem. J
322
,
785
–.
Schierwater
B.
,
Piekos
B.
,
Buss
L. W.
(
1992
).
Hydroidstolonal contractions mediated by contractile vacuoles
.
J. Exp. Biol
162
,
1
–.
Scholz
R.
,
Thurman
R. G.
,
Williamson
J. R.
,
Chance
B.
,
Bucher
B.
(
1969
).
Flavin and pyridine nucleotide oxidation—reduction changes in perfused rat liver
.
J. Biol. Chem
244
,
2317
–.
Springer
M. L.
,
Patterson
B.
,
Spudich
J. A.
(
1994
).
Stage-specific requirement for myosin II during Dictyostelium development
.
Development
120
,
2651
–.
Stebbins
G. L.
,
Basile
D. V.
(
1986
).
Phyletic phenocopies: a useful technique for probing the genetic and developmental basis of evolutionary change
.
Evolution
40
,
422
–.
Sundaresan
M.
,
Yu
Z.-X.
,
Ferrans
V. J.
,
Irani
K.
,
Finkel
T.
(
1995
).
Requirements for generation of H2O2for platelet-derived growth factor signal transduction
.
Science
270
,
296
–.
Tardent
P.
(
1963
).
Regeneration in the Hydrozoa
.
Biol. Rev
38
,
293
–.
Vander Heiden
M. G.
,
Chandel
N. S.
,
Schumacker
P. T.
,
Thompson
C. B.
(
1999
).
Bcl-xLprevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange
.
Molec. Cell
3
,
159
–.
Wagner
A.
,
Dudgeon
S. D.
,
Vaisnys
R. J.
,
Buss
L. W.
(
1998
).
Nonlinear oscillations in polyps of the colonial hydroid Podocoryne carnea
.
Naturwissenschaften
85
,
1
–.
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