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Terrestrial Arthropod Reviews 6 (2013) 257–333


Insect hormones: more than 50-years after the discovery of
insect juvenile hormone analogues (JHA, juvenoids)
Karel Sláma
Institute of Entomology, Czech Academy of Sciences, Drnovská 507, 16100 Praha 6, Czech Republic
e-mail: slama@entu.cas.cz
Received on5 May 2013. Accepted on15 October 2013. Final version received on 17 February 2014

This review describes the over half-centennial history of research on insect juvenile hormone (JH) as well
as its natural and synthetic bioanalogues (JHA or juvenoids).The leading theories of insect hormone
action in growth and metamorphosis were created more than 50 years ago by the pioneers of insect
endocrinology, V. B. Wigglesworth, C. M. Williams, V. J. A. Novák, H. Piepho, H. A. Schneiderman and
L. I. Gilbert. There are two principal categories of hormones released from the central neuroendocrine
system (neurosecretory cells of the brain, corpora cardiaca, corpora allata) that regulate insect growth and
metamorphosis. The first is a complex set of neurohormones (neuropeptides) originating in the neurosecretory cells of the insect brain, which are released from the neurohaemal organs, the corpora cardiaca.
These neuropeptides are responsible for stimulation of various developmental events, such as the release of
the activation hormone, AH. The second category of centrally produced hormones in insects is the morphogenesis inhibiting hormone, or juvenile hormone (JH), produced by the associated endocrine glands,
the corpora allata. JH is responsible for induction of the somatic larval growth in young instar larvae and
stimulation of reproduction in the feeding adult stages.
Wigglesworth (1935) first described JH as an inhibitory hormone; Williams (1957) discovered its
active extracts. Sláma (1961) discovered the hormonomimetic or pseudojuvenile effects of various lipid
extracts and free fatty acids. In addition to lipid extracts with JH activity, a phenomenon found in various
human organs, microorganisms and plants, JH-mimetic materials were found in American paper products
in 1964. The source of the so-called “paper factor” was the wood of the Canadian balsam fir. The potential
use of these and other analogues of JH as nontoxic, selectively acting “third generation pesticides” stimulated an enormous boom of activity among industrial and academic institutions all over the world, in the
pursuit of synthetic JH analogues for replacement of toxic insecticides.
For practical reasons, in this review the chemical structures of the synthetic juvenoids have been
divided into three categories: a) natural and synthetic, predominantly terpenoid juvenoids known before
1970; b) terpenoid and nonterpenoid juvenoids synthesized and tested before 1980, and; c) predominantly nonterpenoid, polycyclic juvenoids with relatively high JH activity, found and selected for practical
use after 1980. Chemical structures of several juvenoids of theoretical or practical importance, together
with the essential structure-activity relationships, are outlined in several figures and tables. The total number of all juvenoids reported active in one or more insects species has been estimated to be more than 4000
compounds. A juvenoid molecule has, more or less, a similar molecular size, roughly equivalent to a chain
of 15 to 17 carbon atoms, with the presence of some slightly polar functional groups and a more or less
© Koninklijke Brill NV, Leiden, 2014

DOI 10.1163/18749836-06041073


K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333

lipophilic physico-chemical properties. Beyond these similarities, there are many variations in the structural types of juvenoids, including, derivatives of acyclic terpenoids, arylterpenoids, peptides, heterocyclic
and polycyclic juvenoids, phenoxyphenyl juvenoids, juvenoid carbamates, and pyridyl-derivatives.
In addition to the generally known and intensively studied effects of juvenoids, such as inhibition of
metamorphosis, inhibition of embryogenesis, and stimulation of ovarian growth, there are certain less
remarkable and largely unexplored biological effects of juvenoids. Some of those phenomena, which are
briefly described in this review, are: a) the effects of juvenoids on embryonic development (ovicidal effects);
b) delayed effects of JH on metamorphosis from egg stage; c) sexually transmitted female sterility caused
by juvenoid treatments of the males; d) the nonvolatile, biochemically activated juvenogen complexes,
generating hormonally active juvenoids by enzymatic hydrolysis of the complex, and; e) antihormones
with antijuvenile activity.
There are two basic hormonal theories on the regulation of insect metamorphosis by JH that have been
proposed during the past 50 years. The first is the theory of Gilbert-Riddiford, which has been widely
disseminated at universities worldwide, through textbooks on insect physiology, biochemistry and endocrinology. The second, less renowned, hormonal theory of insect development is that of Novák-Sláma.
Briefly, the Gilbert-Riddiford theory is based on several fundamental principles. These are: a) the brain
hormone-prothoracic gland (PG) concept created more than 50 years ago and later disproved by Williams;
b) the conclusions of Piepho, who suggested that a large concentration of JH would cause a single epidermal cell to develop larval patterns, pupal patterns at medium concentrations, and adult epidermal patterns
at zero concentration; c) small amounts of JH are necessary in the last larval instars of endopterygote
insects for preventing precocious proliferation of imaginal discs; d) metamorphosis is stimulated by PG
through a small endogenous peak of ecdysteroid preceding the large prepupal one; e) ecdysteroids are
released from the PG in response to superimposed prothoracicotropic hormone (PTTH) from the brain;
f ) the true juvenile hormone of the corpora allata is a sesquiterpenoid compound known as epoxy homofarnesoate (JH-I), isolated from the adult male abdomens of the Cecropia silkmoths, and; g) physiological
functions of JH and other hormones are regulated at the peripheral level by enzymes (esterase) or genes
(methoprene tolerant, Met or a Broad complex gene).
The Novák-Sláma theory is based on completely different building blocks. Briefly, these are: a) the PG
represent a peripheral organ which is not involved in the regulation of the moulting cycles, instead; b) the
PG are a subordinated target of JH (not PTTH), they are inactive during the last larval instar and their
removal does not abolish the cycles of moults; c) the PG are used to generate metabolic water during the
growth of young larval instars by secreting of an adipokinetic superhormone, which stimulates total combustion of the dietary lipids; d) small, medium, or large concentrations of JH are unimportant, the hormone only needs to be present in the minimum, physiologically effective concentrations; e) an imperative
condition for metamorphosis to occur is a virtual absence of JH starting from the second half of the
penultimate larval instar; f ) JH acts according to an “all-or-none” rule at the single cell level, and the
temporal sensitivity to JH is strictly limited to a narrow period at the beginning of the moulting cycle,
before the cells begin to divide; g) the corpus allatum never produces JH in a nonfeeding stage, and the
sesquiterpenoid juvenoid JH-I cannot be the true JH of insects (it has very low JH activity, 100,000-fold
smaller in comparison to human made peptidic juvenoids); h) the developmental cycles are stimulated
exclusively by neuropeptides produced by the brain’s neurosecretory cells (AH); i) developmental stimulation by AH has nothing in common with the PTTH or PG; j) when environmental interventions in the
hormonal system become obsolete, the regulation of moulting cycles becomes autonomic (hormone independent), supported by the stereotypic instructions coded on the genome; k) during the millions of years
of insect evolution, the central neuroendocrine system acquired the superimposed, epigenetic ability to
adapt gene functions and synchronize them with essential changes in the environment. A model based on
the regulation of insect metamorphosis by simple combination of two hormones (AH, JH) of the central
neuroendocrine system is outlined. A possibility that the 4000 known juvenoid molecules act as the feedback or homeostatic factors affecting permeability of the epidermal cell membranes has been suggested.
Speculations about possible peptidic or proteinic nature of the corpus allatum hormone have been

K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333


Juvenile hormone (JH); activation neurohormone (AH) pseudojuvenile effects; terpenoid juvenoids;
nonterpenic juvenoids; peptidic juvenoids; epoxyhomofarnesoate (JH-I); inhibition of morphogenesis;
“all-or-none” rule in JH action; epigenetic action of JH; autonomic development; Gilbert-Riddiford theory; Novák-Sláma theory; history of juvenoids; “paper factor”; antijuvenile Met gene; JH-esterase enzymes

Over fifty years ago there were no computers and there was no Internet. It was a great
task to compile a research paper using mechanical typewriters. In addition to English,
papers were usually published in German, French, Spanish, Russian or Japanese. Thus,
to retrieve essential data, scientists were obliged to know these languages or to have the
articles translated. Unfortunately, for many, the elementary textbooks on insect hormones were written in German (Pflugfelder, 1958, containing 2074 references; Novák,
1959, containing 1512 references; Gersch, 1964, containing 850 references). In
English, a new and very ambitious set of theories on insect hormone action were created by Williams (1952) and his students, Schneiderman and Gilbert (1959, 1964).
These theories are still maintained as the general concepts of JH action (Riddiford,
1994, 1996a, 1996b, 2008, 2012; Jindra et al., 2013). Those theories have been
included in the recent insect hormone textbooks by Nijhout (1994), Nation (2002),
Klowden (2007) and Devillers (2013a). Although alternative views on the mode of
insect hormone action have also been published throughout the 50-year history of JH
research (Novák, 1956, 1959, 1966; Sláma, 1962, 1975, 1980b, 1985) those views are
generally not well known.
The original papers have often disappeared from library shelves to be placed
into depositories, making access to them more difficult. From the library of the late
Dr. V. J. A. Novák, I inherited extensive collections of reprints on insect hormones,
containing the data thus far inaccessible through the Internet. The original papers
enable me to offer a retrospective revision of the data on which the old hormonal concepts were grounded. The total amount of scientific publications and online presentations has recently increased enormously. Furthermore, the topic of insect hormones
has been transferred from physiology to biochemistry and molecular biology. However,
the current theories on insect hormones are still based on the old data that are repeated
in numerous review articles. In my opinion, the most utilized hormonal theories have
never been properly experimentally verified, because it is practically impossible to
uncover a false theoretical grounding without access to the original publications.
During the past 50 years of investigation on natural and synthetic analogues of
insect JH, we have prepared and tested more than 2000 synthetic juvenoids, and a
similar number of other JH active compounds were found in other laboratories (reviews
by Sláma, 1971, 1985, 1999; Sláma et al., 1974; Henrick, 1982). First, the results of
these studies have provided clear experimental evidence that insect JH, and all of
its structural bioanalogues, affects metamorphosis only during a narrow period at the
beginning of the moulting cycle, before the epidermal cells begin to divide. Second,


K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333

we found that the action of JH followed an “all-or-none” rule. The heterogeneous
populations of cells found in the JH-induced larval-adult, or larval-pupal intermediates revealed a mosaic distribution of the new, affected, and the old, unaffected, cells.
These “yes” or “no” responses of epidermal cells to JH (Sláma and Weyda, 1997) are in
serious conflict with other theories (Piepho, 1951; Schneiderman and Gilbert, 1964;
Riddiford, 2008, 2012; Jindra et al., 2013), which are based on qualitatively discriminated developmental outcomes of large, medium or zero concentrations of JH.
The data obtained from insect hormones have resulted in two alternative and fundamentally different explanations for the mode of action of insect JH: 1) the widespread
Gilbert-Riddiford theory, which claims that the moulting cycles are stimulated by a
moulting hormone from the PG and that the larval, pupal and adult epidermal structures are determined by the large, medium or zero concentrations of JH, respectively,
and; 2) the lesser known theory of Novák-Sláma, which postulates that the larvalpupal-adult transformation proceeds in complete absence of JH, according to a genetically programmed schedule. The arguments in favour or against each of these theories
have been carefully investigated by extensive bioassays for hundreds of JH analogues
(Sláma, 1971, 1999; Sláma et al., 1974). A brief description of the results can be found
in the text below.

A brief history of juvenile hormone (JH) and its bioanalogues
Wigglesworth (1935, 1936) first elucidated the inhibition of insect metamorphosis by
the secretory product of the endocrine gland, the corpus allatum, in a hemipteran
insect Rhodnius prolixus Stål. Initially, the hormone was called the inhibitory hormone,
in the sense of maintaining the status quo and preventing the realization of the latent
adult characters (Wigglesworth, 1935). Later, when he believed that the corpus allatum hormone could also bring about a partial reversal of metamorphosis from the
adult back to the larval structures, Wigglesworth (1940) abandoned the term inhibitory hormone and proposed the term juvenile hormone (Wigglesworth, 1940, 1970).
Although existence of the reversal of metamorphosis has never been experimentally
confirmed (Sláma, 1975, 1985), the term juvenile hormone (JH) persisted and became
generally used. The pioneering work of Wigglesworth on the effects of the corpus allatum hormone on metamorphosis in Rhodnius was corroborated and extended to the
pupal stages of the commercial silkworms, Bombyx mori (Bounhiol,1938; Fukuda,
1944) and Cecropia silkworms, Hyalophora cecropia (Williams, 1952). Hinton (1951)
extensively reviewed the historical data on insect hormones and endocrine glands
known before the second half of the 20th century.
The first stride in juvenile hormone research was the preparation of lipid extracts
with JH activity from abdomens of the adult male Cecropia silkworms (Williams,
1956, 1959). In addition, the availability of a bioassay stimulated the search for
JH activity in other insect species and in other organisms. Insect JH activity was found
in human thymus, human placenta, other vertebrate organs and even in cream from
ordinary milk (Williams et al., 1959). Hormone activity was also encountered in the

K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333


lipid extracts prepared from the adrenal cortex of vertebrates (Gilbert and Schneiderman,
1958), various invertebrates and vertebrates (Schneiderman and Gilbert, 1958), microorganisms and plants (Schneiderman et al., 1960) and from various species and developmental stages of insects (Gilbert and Schneiderman, 1961; Williams, 1967; review
by Sláma, 1971; Sláma et al., 1974).
The second important step in JH research was the chemical identification of an
active JH principle, made more than 50-years ago. Karlson and Schmialek (1959)
found JH-active materials in the yeast and excrement of the mealworm beetle, Tenebrio
molitor. The active principle was identified by Schmialek (1961) as a common sesquiterpenoid alcohol farnesol (3,7,11-trimethyldodeca-2,6,10-trien-1-ol), which was the
first JH-active compound with a determined chemical structure. Farnesol, its derivative farnesylmethylether (Schmialek, 1963b) and the related sesquiterpenoids
(Schmialek, 1963c) brought JH research into the field of terpenoid chemistry. Chemists
soon prepared a number of related sesquiterpenoid derivatives, which were tested for
JH activity in insects (Bowers and Thompson, 1963; Schmialek, 1963c; Schneiderman
et al., 1965). The compounds responsible for JH activity in the lipid extracts of
Cecropia silkworms remained unknown until Schmialek (1963a) identified 3,7,11-trimethyl-2,6,10-tridecatrien-1-ol and, subsequently, Rőller and Bjerke (1965) and
Rőller et al. (1965, 1969) identified the JH-active compound from the Cecropia
extract as an ester of the related sesquiterpenoid acid, 10,11-epoxy-7-ethyl, 3,11dimethyltrideca-2,6,-dienoic acid, named JH-I. Thereafter, JH-I has been generally
considered the true JH of insect corpora allata (Rőller and Dahm, 1970; Nijhout,
1994; Gilbert et al., 2000; Nation, 2002; Riddiford, 1996a; Jindra et al., 2013;
Devillers, 2013a).
Among the synthetically prepared isoprenoid mimics of JH, the first potent
bioanalogue of JH was prepared by the action of hydrochloric acid on 3,7,11trimethyldodeca-2,6,10-trienoic (farnesenic) acid (Law et al., 1966). This preparation
was commonly known as the “Law-Williams mixture”. The most active compound
with JH activity was identified as 7,11-dichlorodihydrofarnesoate (Romaňuk et al.,
1967), which was considered to be the most active synthetic analogue of JH for a
short time. This compound acted in nanogram quantities per specimen when administered externally to the cuticle of the last instar larvae of the hemipteran fire bug,
Pyrrhocoris apterus. After the discovery of a “paper factor”, where JH activity was
found in American paper products and in the wood of Canadian balsam fir, Abies
balsamea (L.) Mill. (Pinaceae) (Sláma and Williams, 1965, 1966a), the effects of insect
JH became widely publicized. The find was soon followed by a boom in the search
for similar, JH-active compounds with the potential new status of non-toxic pesticides of the third generation (Williams, 1967; Williams and Robbins, 1968). Between
1965 and 1975, hundreds of new isoprenoid and non-isoprenoid compounds with
JH activity (juvenoids) were synthesized and tested on different insect species (review
by Sláma, 1971; Sláma et al., 1974; Henrick, 1982). The study of insect hormones,
or insect endocrinology, attracted a number of industrial insecticide chemists and
biochemists who dominated the field, creating new interpretations of JH action (see


K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333

State of the art in JH research some 50 years ago
Insect endocrinology became part of the established discipline of insect physiology in
the first half of the 20th century, when Kopeč (1917, 1922) discovered the brain hormone and Wigglesworth (1936, 1940, 1964; review 1970) discovered the inhibition of
metamorphosis (inhibitory hormone) in the kissing bug, Rhodnius prolixus. As has
already been mentioned, the conclusions of Wigglesworth were confirmed by Bounhiol
(1938) and Fukuda (1944) in the mulberry silkworm. Great progress in insect hormones was achieved by Williams (1947, 1952, 1956, review 1959), who documented
induction of development in diapausing pupae of the Cecropia silkworm, Hyalophora
cecropia, by transplantations of “active” brains from the chilled, developing pupae. The
brilliant surgical maneuvers performed by Williams in Cecropia, with practical
demonstration of the effects of insect brain hormone (Kopeč, 1922), led Williams
(1947, 1952) to create the “brain – PG” theory of insect development. Williams found
that implantation of the PG alone was inactive and assumed that it had to be activated
by a brain hormone. This “moulting hormone theory” of Williams (1952) became the
leading theoretical concept of insect hormones for 50 years (Nijhout, 1994; Nation,
2002; Klowden, 2007; Jindra et al., 2013) and it is still used as the theoretical ground
stone of insect hormone action, especially in the fields of insect biochemistry and
molecular biology (Riddiford et al., 2010; Jindra et al., 2013; Devillers, 2013a).
The favourite objects of hormonal studies between the years 1930 and 1952 were
larvae and adults of the pyralid, known as the Greater waxmoth, Galleria mellonella ,
investigated by a number of outstanding German scientists (reviewed by Hinton,
1951; Pflugfelder, 1958). Piepho (1951) compared the developmental regulation of
metamorphosis in this species to a “playing ball” of different concentrations of JH.
According to this interpretation, a large concentration of JH caused the insect cells to
develop specific larval characteristics, a medium concentration caused appearance of
the pupal characteristics and no JH resulted in development of the adult structures.
This highly simplified outline of insect hormone action was derived from light-microscopic investigations of the cyst-like regenerates of epidermal implants in Galleria.
Nobody had used this technique before or after Piepho. Perhaps the most curious
interpretation of these experiments was that extremely large dosages of JH caused a
reversal of metamorphosis, namely backward development from pupal to larval structures, which was supported by several authors (Wigglesworth, 1970; Sehnal and
Schneiderman, 1973; Sehnal, 1984). We have carefully reinvestigated the enigmatic
conclusions of Piepho (1951) in Galleria and found that they were not experimentally
substantiated (Sláma, 1975; Sláma and Weyda, 1997). Nevertheless, the large, medium
or zero concentration JH theory of Piepho (1951) is still taught at universities worldwide as part of the common hormonal theory of Schneiderman and Gilbert (1959,
1964, and see below).
In Diptera, intensive hormonal studies were carried out 50 years ago in the blowfly,
Calliphora erythrocephala Meigen, 1826 by Thomsen (1952) (this taxon has been synonymized under C. vicina Robineau-Desvoidy, 1830) and reviewed by Possompés
(1953). Vogt (1943) and Bodenstein (1953) described the role of the ring gland,

K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333


located in the anterior part of the larva, in hormonal regulation of metamorphosis in
Drosophila melanogaster.
There were also intensive endocrinological studies by Novák (1956, 1959, review in
1966) on the hemipteran, Oncopeltus fasciatus, and by Pflugfelder (review by Pflugfelder,
1958) on the Indian stick insect (Phasmatodea) Dixippus morosus and other insects.
Important investigations on insect neurohormones and neurosecretions, associated
with the discovery of peripheral neurohaemal organs (perisympathetic organs) of
insects were carried out by Raabe and her co-workers (review by Raabe, 1982). Finally,
there were outstanding hormonal studies carried out by Scharrer (1953), as well as
Bodenstein (1953), on cockroaches and by Pfeiffer (1945) on grasshoppers.
Endocrinology of invertebrate animals, including insects, was extensively studied and
reviewed by Gersch (1964). According to these data, a substantial portion of our
knowledge concerning physiology of insect hormones was actually obtained a long
time ago (see reviews by Pflugfelder, 1958; Gersch, 1964; Novák, 1966, 1975;
Wigglesworth, 1964, 1970; Raabe, 1982; Sláma et al., 1974). Unfortunately, these
endocrinological data have been systematically underscored and overwhelmed by the
interpretations of Piepho (1951) and the associated theory of Schneiderman and
Gilbert (1964 for a review).
Brief recapitulation of the old hormonal concepts
The two latent developmental systems of Wigglesworth
Wigglesworth created what perhaps is the most important theory of insect JH action
in 1940, before he accepted the conclusions of Piepho (1951). His theory assumed the
existence of two latent developmental systems within each epidermal cell; a larval or
immature system stimulated and sustained by JH, and an adult system responsible for
development and metamorphosis in the absence of JH. Wigglesworth was most familiar with the work on the exopterygote kissing bug, Rhodnius. He had limited experience with the pupal stage of endopterygote insects, which he learned to recognize
during his visit to Piepho’s laboratory in Gőttingen, Germany. Fascinated by the
straightforward explanation of JH action by large-larval, medium-pupal and zero-adult
interpretations of Piepho (1951), Wigglesworth abandoned his original concept of the
two latent developmental systems. In combination with the brain-PG theory of
Williams (1952), he published a series of developmental schemes (Wigglesworth,
1954, 1957, 1964, 1970), which were incorporated as a basis for the creation of the
hormonal theory by Schneiderman (1967, 1969) and Schneiderman and Gilbert
(1958, 1959, 1964). I consider the approval of Piepho´s (1951) interpretations by
Wigglesworth’s authority (Wigglesworth, 1954, 1957, 1964, 1965) an unfortunate
event in the history of insect physiology and endocrinology. Ironically, a simple transformation of the two latent developmental systems of Wigglesworth (1940) into the
inhibition of morphogenesis by JH and stimulation of development by AH neuropeptides could make the secret of insect metamorphosis very simple.


K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333

The large, medium and zero JH concentration theory of Piepho
The confusion caused among insect physiologists by the theory of Piepho (1951) shows
how difficult it may be to disprove an incorrect interpretation of relatively simple
developmental features. Piepho (1951) used to implant Galleria mellonella pupal epidermal fragments into the larval body cavity. After the next moults, he inspected the
cyst-like regenerates and found that the original pupal cells, when transferred into
the JH-rich larval milieu, produced a larval-like cuticle without the characteristic pupal
pigmentation. At the time, Piepho did not realize that the pigmentation of the pupal
cuticle is a very efficient oxidative substrate in Lepidoptera. Oxidation could have
never taken place in the oxygen-deficient, cyst-like regenerates within the liquid larval
haemolymph (Sláma and Weyda, 1997). He apparently confused the unpigmented
(and unoxidized) pupal cuticle with the transparent cuticle of the larval cells and concluded, therefore, that the pupal cells of the implants dedifferentiated back into
the larval structures in a larval milieu containing relatively large concentrations of
JH. Piepho (1951) speculated further that a single epidermal cell, such as a pupal cell,
could develop alternatively into: a) larval structures under large concentrations of
JH; b) pupal structures under medium concentrations of JH, and; c) adult structures
in the absence of JH. The conclusions of Piepho (1951) were taken with reservations
by his co-workers (A. Heims, personal communication to K.S.) and by some endocrinologists (Novák, 1959; Bodenstein, 1953; Sláma, 1962; Wigglesworth, 1970).
Furthermore, those conclusions were in conflict with the common biological law of
Haeckel (repetition of phylogenetic stages in animal ontogenesis) and with Dollo´s
principle of irreversibility of evolutionary changes. Nevertheless, the interpretations of
Piepho (1951) and the associated theory of Schneiderman and Gilbert (1959, 1964)
have dominated the field of insect hormones for more than 50 years (Fig. 1).
Later reinvestigations of the Piepho´s theory in Galleria (Sláma, 1975, 1982, 1985,
1995; Sláma and Weyda, 1997) revealed that the light microscopic method used by
Piepho (1951) did not make it possible to distinguish the cuticles of the larval cells
from the unpigmented pupal cuticle of the cyst-like epidermal implants. It was not
known at that time that both the larval and pupal epidermal cells of Galleria have the
same size and occupy identical cuticular areas. Sláma and Weyda (1997) found this
fact more than 45 years later. The JH theory of Piepho (1951) as well as Schneiderman
and Gilbert (1964) remained unchanged as long as for 50 years (Riddiford, 1994,
1996b, 2008, 2012; Jindra et al., 2013). Alternative interpretations of insect hormone
action represented, for example, by a concentration independent, all-or-none rule for
JH action (Sláma, 1975, 1995, 1999; Sláma and Weyda, 1997; Sláma et al., 1974)
were underestimated or rejected (Willis, 1996; Willis et al., 1982; Sehnal, 1984).
The brain-PG theory of Williams
Williams (1947, 1952) created his theory of insect hormone action based on
his elegant experimental work with transplantation of the brain in the Cecropia
silkworms. Earlier work on the commercial silkworm (Hachlow, 1931; Bounhiol,
1938; Fukuda, 1944) suggested that, in addition to the brain, there was another
development-stimulating centre located within the thoracic region. Initially, the results

K. Sláma / Terrestrial Arthropod Reviews 6 (2013) 257–333


Figure 1.  Schematic diagram of hormonal theory of insect metamorphosis, proposed more than 50 years
ago by Schneiderman and Gilbert (1959, 1964) and Schneiderman (1969) after modification of
Wigglesworth (1957) model based on JH theory of Piepho (1951). The larval, pupal or adult developmental programme was determined in each epidermal cell by the respectively large, medium or zero concentrations of juvenile hormone. The moult cycles were stimulated by the moulting hormone released from the
prothoracic glands in response to brain hormone. This figure is published in color in the online version.

indicated that it was located in the mesothoracic segment (Hachlow, 1931). However,
there is no endocrine organ in this segment and thus the suspicion fell on the prothoracic segment with a relatively large, usually ramified PG. With regard to some positive
results by Fukuda (1944), Williams assumed that the “growth and differentiation hormone” could be released from the PG, despite the fact that the gland alone was ineffective. He concluded that in order to be active, the PG had to be activated by the brain
hormone (Williams, 1947, 1952). This attractive hormonal idea could hardly be challenged because PG had to always be implanted with the brain. The PG theory of
Williams was accepted and disseminated, mainly by biochemists (Karlson, 1966),
especially by the group of “ecdysonists” after the discovery of ecdysone.
The activation and inactivation of PG by the brain hormone (Williams, 1952;
Karlson, 1966) could not be experimentally verified due to the branched structure of
the PG. The hormonal scheme presented in Fig. 1 has been widely used as the leading
hormonal concept, especially in the fields of insect biochemistry and molecular biology
(Nijhout, 1994; Nation, 2002; Riddiford, 1996a, 2012; Goodman and Granger, 2009;
Devillers, 2013a; Jindra et al., 2013).

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