AMER. ZOOL., 33:303-307 (1993)
Hormonal Control of Growth and Reproduction in the Arthropods:
Introduction to the Symposium*
MARCIA J. LOEB
Insect Neurobiology and Hormone Laboratory, U.S. Department of Agriculture, ARS,
Beltsville, Maryland 20705
SYNOPSIS. An overview of hormonal control of growth and reproduction
in the arthropods is presented.
Arthropod endocrinology and neuroendocrinology has been examined in major
classes, including insecta, Crustacea, and
arachnida. Data suggest that there are more
similarities than differences in endocrine
systems regulating growth, metamorphosis
and reproduction in all of the arthropod
phylum. I will use this opportunity to summarize the highlights of these endocrine
activities, and hope that the symposium will
provide a platform for a more unified
approach to research in this field in the
future.
The growth of arthropods is intimately
tied to molting, since all members sport
exoskeletons rather than internal bones, and
must cast off the old superstructure in order
to expand. Arthropods usually undergo
developmental and maturational changes as
they proceed through each genetically destined molt. Therefore, molting is complex,
often involving changes in gene expression,
cellular commitment, mitotic and secretory
activity (Riddiford, 1982), endocrinology
(Bollenbacher, 1988), behavior, and cell
death (Truman and Morton, 1987). Molting
is stimulated by ecdysteroid hormones in
all arthropods studied, correlated with a drop
in juvenile hormone (JH), methyl farnesoate (MF) or farnesoic acid (FA) levels
(Spindler et ai, 1980; Riddiford, 1982;
Sonenshine et ai, 1986; Bollenbacher, 1988;
Hopkins, 1988; Descamps etai, 1990; Cusson et ai, 1991). Although stimulation of
the prothoracic nerve can release ecdysteroids from insect prothoracic glands (Rich-
ter, 1990), most studies have implicated
brain-derived peptides in insects and crustacea as regulators of glandular synthesis of
ecdysteroids (Bollenbacher et al., 1988;
Chang, 1989) or, in ticks, epidermal synthesis of ecdysteroids (Zhu et al., 1991).
However, the method by which the peptides
control steroid synthesis is different in
insects and Crustacea. In insects the prothoracicotropic hormones induce several
sharp increases in secretion of ecdysteroids
by prothoracic glands prior to a molt (Bollenbacher, 1988). However, the molt inhibiting hormone of Crustacea (MIH) continually inhibits ecdysteroid secretion by the
Y organs; synthesis of ecdysteroid and subsequent molting occur only after MIH secretion ceases (Mattson and Spaziani, 1985).
Physiological downregulation of ecdysteroid action and secretion, and, at other times,
enhancement of ecdysteroid action, is mediated by the JHs of insects (Bollenbacher et
ai, 1988) or MF or FA of Crustacea (Laufer
and Borst, 1988; Cusson et ai, 1991). Several simultaneous or sequential processes
provide exquisite regulation of circulating
titers of JH or MF. In insects, JH synthesis
by the corpora allata can be depressed via
transmitters released by nerve tracts from
the brain (Rankin et ai, 1986), by brain
neuropeptides (allatostatins) (Woodhead et
ai, 1989), and by feedback factors from the
ovary (Rankin and Stay, 1985). The corpus
allatum can be stimulated by neurohormonal allatotropins (Granger et al., 1984;
Kataoka et ai, 1989). Juvenile hormone can
be quickly eliminated from the insect system by a specific blood-borne esterase. Its
synthesis by fat body tissue can be initiated
1
From the Symposium on Hormonal Control of
a neurosecretory product of the brain,
by
Growth and Reproduction in Arthropods of the Division
of Comparative Endocrinology presented at the Annual and later sustained by positive feedback
Meeting of the American Society of Zoologists, 27-30 from blood JH (Jones et ai, 1981; Roe and
December 1991, at Atlanta, Georgia.
303
304
MARCIAJ. LOEB
Venkatesh, 1990). In Crustacea, MF synthesis is increased by eyestalk ablation and
reduced by adding eyestalk extract, suggesting negative control over MF production (Landau et al, 1989). However, red
pigment concentrating hormone, until
recently associated with mobilization of
crustacean pigment cells (Fingerman, 1956),
stimulates MF synthesis in the crayfish,
Procambarns clarkii; inhibition of MF synthesis has been attributed to pigment dispersing hormone in this animal (Landau et
al, 1989), suggesting muliple roles for eyestalk peptides. Crustacean pigment dispersing hormone has been found in various
orthopteran insects (Rao and Riehm, 1989);
it may play a role in circadian rhythm-regulated events (Homberg et al, 1991).
The interaction between ecdysteroids and
JH or MF is vital to reproduction in arthropods. The female system has received most
attention by researchers because of the
destructive impact of rapidly reproducing
insect pests and the positive commercial
importance of edible Crustacea. At the
appropriate time, JH in several species of
female insects (Engelmann, 1979), ecdysteroid in some crustacean species (Payen,
1986), and MF in others (Laufer and Borst,
1988) induce the fat body or hepatopancreas, respectively (and in some cases, the
ovary as well), to synthesize yolk proteins,
the vitellogenins. In the mosquito, JH must
"prime" the fat body before ecdysteroid,
secreted by the ovarian follicular epithelium
(Goltzene et al., 1978), initiates vitellogenogen synthesis by the fat body (Hagedorn et
al, 1975; Kelly et al, 1987) by activating
vitellogenin genes (Racioppi et al, 1986).
JH also activates Na + -K + ATPase in ovarian follicular epithelium, inducing enough
shrinkage in follicle cell volume to allow the
large vitellogenins to enter the resulting
spaces between follicle cells, and thus
approach the oocytes (Ilenchuk and Davey,
1987). The major portion of ecdysteroids
secreted by ovaries of insects (Hoffmann and
Lagueux, 1985), Crustacea (Laufer and Deak,
1990), and arachnids (Dotson et al, 1991)
are converted to conjugates and sequestered
in the eggs where, later, they are believed
to regulate early embryonic development
(Thompson et al, 1986). As in molting, cen-
tral control of ovarian ecdysteroid secretion
is dependent on brain peptides; in insects,
the egg development neurohormone elicits
ecdysteroid secretion by ovaries and vitellogenesis by fat body after the fat body has
been primed by JH (Lea, 1972; Hagedorn
et al, 1979). However, in Crustacea, the eyestalk neuropeptide, vitellogenin inhibiting
hormone, restrains vitellogenic secretion and
ovarian maturation (Juchault et al, 1989)
until it is overridden by a vitellogenesis
stimulating hormone from the thoracic ganglion (Payen, 1986). Red pigment concentrating hormone may be a gonad stimulating hormone (Landau et al, 1989).
The testes of insects (Loeb et al, 1982)
and myriapods (Descamps et al, 1990) also
synthesize ecdysteroids in response to a
brain peptide, testis ecdysiotropin (Loeb et
al, 1987). Ecdysteroid in turn stimulates
mitosis in spermatocytes of insects (Dumser, 1980), arachnids (Dumser and Oliver,
1981) and myriapods (Beniouri et al, 1983).
However, meiosis and elongation proceed
independent of ecdysteroids (Leloup, 1969);
local factors, elaborated by the testis sheath
and fat body in the absence of ecdysteroid,
direct these events (Giebultowicz et al,
1987). Fetal calf serum, which contains the
macromolecular factor described by Kambysellis and Williams (1972; Kiss and Williams, 1976) is essential to the initiation of
meiosis (Giebultowicz et al, 1987). Later
in development, testis sheaths and fat body
must be exposed to ecdysteroid (probably
locally synthesized) to secrete factors which
elicit the growth and development of the
adult male genital tract (Loeb, 1991). However, after distinct parts of the genital tract
have differentiated, ecdysteroid alone can
promote functional development (Grimnes
and Happ, 1987). JH promotes synthesis of
accessory gland proteins in several insect
species, once the tract is fully formed (Gillott and Venkatesh, 1985). A similar
arrangement may exist in Crustacea in the
form of the androgenic gland. This organ
elaborates a peptide, the androgenic hormone, which controls spermatogenesis, male
development, and maintains male sexual
and secondary sexual characteristics (Charniaux-Cotton, 1954;Hasegawa£-/a/., 1987).
It also secretes an analogue of MF which
INTRODUCTION TO THE SYMPOSIUM
305
in insects and crustaceans: The search for a unican inhibit protein synthesis in the crab
fying arthropod endocrinology. Insect Biochem.
ovary (Andrieux et ai, 1989). The activity
21:1—6.
of the androgenic gland is inhibited by a DeLoof,
A. 1987. The impact of vertebrate-type steneurohormone from the eyestalks; another
roids and peptide hormone-like substances in
factor, released by neurosecretory cells disinsects. Entomol. exp. appl. 45:105-113.
persed throughout the central nervous sys- Descamps, M., M. Charlet, and B. Leu. 1990. Conversion of 2,22,25-trideoxyecdysone (5b-Ketotem, stimulates the release of androgenic
diol) by body parts and gonads of Lithobius forhormone (Payen, 1986).
ficatus M. (Myriapoda, Chilopoda). Invert. Reprod.
Many of the endocrine and neuroendoDevel. 18:111.
crine interactions in arthropods parallel Dotson, E. M., J. L. Connat, and P. A. Diehl. 1991.
Cuticle deposition and ecdysteroid titers during
those in vertebrate systems. For example,
embryonic and larval development of the argasid
regulation of steroid production by central
tick Ornithodoros moubata. Gen. Comp. Endonervous system peptides in insects and Cruscrin. 82:386-400.
tacea may be analogous to regulation of ste- Dumser, J. B. 1980. The regulation of spermatogenesis in insects. Ann. Rev. Entomol. 25:341-369.
roid production in vertebrates by ACTH
and LH. Hormone-receptor interactions, Dumser, J. B. and J. H. Oliver, Jr. 1981. Kinetics of
spermatogenesis, cell cycle analysis, and testis
second messenger cascades (Smith et ai,
development in nymphs of the tick, Dermacenter
1987) and subsequent gene activation (Horvariabilis. J. Insect Physiol. 27:743-753.
odyski and Riddiford, 1989) proceed in Engelmann, F. 1979. Insect vitellogenin: Identification, biosynthesis and role in vitellogenesis. Adv.
similar fashion. The small forms of the
Insect Physiol. 14:49-108.
Bombyx prothoracicotropes are structurally
M. 1956. The physiology of the melainsulin-like, and the sequences of bombyxin Fingerman,
nophores of the isopod Ligia exotica. Tulane Stud.
genomic DNA are similar to preproinsulin
Zool. 3:137-148.
(Nagasawa et ai, 1986). Vertebrate steroids Giebultowicz, J. M., M. J. Loeb, and A. B. Borkovec.
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cally in insect neurosecretory cells (DeLoof, Gillott,
of secretory proteins in the accessory reproductive
1987). Therefore, arthropod systems may
glands of the male migratory grasshopper Melanalso serve as models for vertebrate systems.
oplus sanguinipes: A developmental study. J. Insect
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