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First published online February 15, 2008
Journal of Experimental Biology 211, 780-789 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014043
The functional morphology of color changing in a spider: development of ommochrome pigment granules
Université de Tours, Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 6035, Av. Monge, Parc Grandmont, 37200 Tours, France
* Author for correspondence (e-mail: tere.insausti{at}univ-tours.fr)
Accepted 13 December 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: animal color, epidermis, zoochromes, kynurenine, 3-OH-kynurenine, mimetism, crab-spider, Misumena vatia
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Needham, 1974;
Fuzeau-Braesch, 1972;
Fuzeau-Braesch, 1985;
Kayser, 1985). Scattered work
has been carried out since then, related to the developmental biology of
butterfly wing patterns (e.g. Koch,
1993; Nijhout,
1997; Reed and Nagy,
2005) or in the context of tryptophan metabolism (e.g.
Han et al., 2007;
Kato et al., 2006). The eye
pigmentation pathway of Drosophila based on ommochrome synthesis and
deposition has been extensively analyzed, mainly in the context of genetic and
epigenetic work (e.g. Phillips and
Forrest, 1980; Lloyd et al.,
1998; Lloyd et al.,
1999; Mackenzie et al.,
2000). Ommochrome pigments are the main chromogenic class in the
pathway from tryptophan. They range from gold (xanthommatin X) through red,
purple and violet, up to black. The reduced form is red and the oxidised form
usually yellow. The characteristic properties of ommochromes, i.e. redox
behavior, absorption of ultraviolet and visible light, and low solubility,
enable them not only to act as authentic functional pigments (eyes,
integument), but also as an electron accepting or donating system and as
metabolic end products (Needham,
1974). Ommochromes, principally xanthommatin, are widely
distributed in arthropods as screening pigments in the accessory cells of the
eyes and are also present in the retinula cells
(Linzen, 1974).
The functions of ommochromes are diverse and several complementary and
non-exclusive hypotheses have been suggested for their common occurrence;
these have been well reviewed in the general references cited above.
Hypothesis 1: the ommochrome pathway is the main pathway for avoiding excess
accumulation of highly toxic tryptophan. Insects and other spiralian phyla
have never possessed or have lost the simpler vertebrate catabolism pathway
for tryptophan based on the glutarate pathway. Supporting this hypothesis is
the observation that ommochrome formation is strongly correlated with the
massive breakdown of proteins at the onset of metamorphosis. This is the
oldest and most popular view for the existence of ommochromes. Hypothesis 2:
it is believed that the major function of ommochrome eye pigments is
protection of photosensitive visual cells against excessive scattered light,
and also to protect them against photodestruction by intense ultraviolet light
(Langer, 1975;
Stavenga, 1989). Ommochromes
participate in the antioxidative system in invertebrate photoreceptors, like
melanin in the eyes of vertebrates (Dontsov
et al., 1984; Dontsov,
1999; Ostrovsky et al.,
1987; Sakina et al.,
1987). The ommochromes are effective inhibitors of free radical
induced lipid peroxidation. Lipid peroxidation is also produced by
photo-oxidation and is indicative of photoreceptor damage, manifested in the
retina by deterioration of photoreceptor membranes
(Ostrovsky and Fedorovich,
1994). Hypothesis 3: the color of ommochromes is believed to be
used in signalling, mimicry and crypsis. This is the hypothesis supported by
most of the community working on color changing insects such as stick insects
and mantids (Fuzeau-Braesch,
1985), including Mantis religiosa, Sphodromantis viridis
and Locusta migratoria
(Vuillaume, 1968), and spiders
(Rabaud, 1918;
Rabaud, 1919; Gabritschevsky,
1927; Chittka, 2001;
Schmalhofer, 2000;
Théry and Casas, 2002;
Heiling et al., 2003;
Heiling et al., 2005;
Théry et al., 2005;
Théry, 2007).
The reversibly color changing crab-spiders of the family Thomisidae have
been studied since 1891 (Heckel,
1891) with respect to pigmentation. Older works assumed that the
yellow color of Misumena vatia was due to carotenoids
(Millot, 1926), but
ommochromes were later found to be the pigments responsible for this color
change (Seligy, 1972). This
spider is unusual, as it is able to change color reversibly, within a few
days, from white to yellow and back. Both food and light quality have recently
been found to increase the degree of color change, but the variability in the
response level was very high, with many individuals remaining white despite
strong stimuli (Théry,
2007). The matching to background that these spiders can produce
is astonishing at times, for example below the discrimination ability of bees
(Chittka, 2001;
Théry and Casas, 2002;
Théry et al., 2005).
This form of mimetism has therefore been interpreted as potentially both a
defensive (hiding from predators) and aggressive (luring prey) one. While the
defensive color change hypothesis is still waiting for experimental and
observational studies of predation by birds and may well eventually be proved
wrong, bees and other flower-visiting insects are common prey. Finally, the
occasional striking match between the colors of flowers and spider found in
naturally occurring situations in the field is unlikely to be due to chance
alone.
The aim of the present study was to describe the ultrastructural changes occurring during the color change from white to yellow, using several microscopic techniques, and to describe the ontogeny of the ommochrome pigment granules, in order to lay the necessary physiological foundations for the numerous statements about the adaptiveness of the color change that are being currently made.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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For the morphological analysis, transmission electron and light microscopy
were performed on the spiders following the technique described
(Ribi, 1987). Briefly, a
spider was fixed for 3 h in a mixture of 2.5% glutaraldehyde and 2.0%
paraformaldehyde in phosphate buffer (pH 7.3) with glucose and
CaCl2 added. Subsequently, the pieces were postfixed with buffered
1% osmium tetroxide for 1–2 h. After dehydration, they were embedded
via propylene oxide in Durcupan ACM (Electron Microscopy Sciences no.
14040). Blocks were serially sectioned at 1.5–5 µm using glass knives
mounted in a microtome. The sections were stained on a hot plate with
Toluidine Blue–Basic Fuchsin or mounted unstained on a slide with DPX
(Electron Microscopy Sciences no. 13510). The unstained sections were observed
under a light microscope and a fluorescence microscope (using a USH102D
burner, DM400 dichroic mirror, a BP330–385 excitation filter and a BA420
barrier filter; Olympus, Japan). The same sections were observed with a linear
polarizer.
For electron microscopy, ultrathin sections were cut with an ultramicrotome using a diamond knife. The sections were doubly stained by uranyl acetate and lead citrate and observed using a JEOL 1010 transmission electron microscope.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The epidermal pigment granules
We first describe the content of epidermal cells for white spiders, then
for yellow spiders and finally for the red stripes on both color forms. A
synopsis of the different granule types is given in
Table 1.
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White spiders
In the opisthosoma, pigment granules are scattered in the cytoplasm of
epidermal cells. They emit light-blue fluorescence and do not differentiate
with the polarizer filter. They consist of poorly osmiophilic ellipsoidal
granules, bound by a unit of membrane, with a section of 0.8 µmx1.4
µm (Fig. 2A,B). This type of
pigment granule, denoted type I, is the only type of granule present
in the epidermal cells in the white zone of the opisthosoma. Glycogen rosettes
are scattered in whole cytoplasm (Fig.
2B, inset). We have not found Golgi bodies close to the granules.
Striking structures of rough endoplasmic reticulum (RER), organized into
several concentric rings, were found in close association with granules
(Fig. 2C,D). The granules are
enclosed by membranes, which are also intimately associated with those of the
structure of RER (Fig. 2D,
arrow). High densities of mitochondria are observed to be associated with
these structures (Fig. 2C,
arrows).
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Yellow spiders
The nature of pigment granules in the epidermal cells of the opisthosoma of
yellow spiders (Fig. 4) differs
according to the intensity of the color. In light-yellow tinted spiders we
found two types of granules: pale yellow granules and brown granules
(Fig. 5A). We denote these
granules as type II and type III, respectively. Type
II granules emit light-blue fluorescence
(Fig. 5B) and remain dark under
observation with a polarizer filter. The fine structure of these granules
revealed that they are not homogeneous, in contrast to the type I
granules, and are confined within a unit of membrane
(Fig. 5C). They revealed an
heterogeneous electron-opaque content with vesicular electro-lucent material.
We observed that some granules contained small vesicles only, whereas others
contained some small vesicles surrounding a bigger one located in the centre
of the granule. Other granules have an electron-lucent center and an
electron-dense ring border (Fig.
5C). A high density of glycogen rosettes occurs in the cytoplasm
of the cell (Fig. 5F). Golgi
bodies and smooth endoplasmic reticulum are frequently present
(Fig. 5C inset, F). Brown
granules of type III are the only ones present in bright yellow
spiders (Fig. 5D). They can be
found in the same cell of yellowing spiders as type II. They emit no
fluorescence and remain unaffected by the polarizer filter. The type
III granules are electron-dense, with a diameter of 0.8–1 µm and
a spherical section. Their content is homogeneous and they are enclosed by
membranes (Fig. 5E,F). They are
sometimes broken up by the microtome cutting.
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Epidermal cells of the prosoma of yellow spiders do differ in their pigment content according to the location of the cell. Cells in the opaque region contain two types of granules: type III granules, located at the top of the cells, and granules with microcrystal inclusions (already described in the prosoma of the white spider), located at the base of the cell (Fig. 6A–D). Sometimes microcrystals tend to group together, forming structures surrounded by rough endoplasmic reticulum (Fig. 6E). Cells located in the yellow translucent tegument of the prosoma contain type III granules only.
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Red stripes in white and yellow spiders
The epidermal cells are rich in granules in the red stripes. In the white
spider, two types of granules were observed: dark red granules in the basal
and medial zone of the cell, and translucent granules in the apical zone of
the cell (Fig. 7A).
Observations of this region by fluorescence microscopy revealed that the
apical and medial zones of the cell emit light-blue fluorescence (type
I granules), whereas the basal zone emits no fluorescence (type
III granules) (Fig. 7B).
The ultrastructure of this region confirmed the presence of two types of
granules: type III at the basal region of the cell and type
I at the apical region (Fig.
7C).
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In the red stripe of the yellow spiders, yellow and red tinted granules are mixed through the whole cell (Fig. 7D). This zone emits no fluorescence (both types of granules are type III granules) (Fig. 7E, left). When observed through a linear polarizer, the granules did not behave differently from the surroundings. These characteristics are typical of type III. The ultrastructural study of this region confirmed the presence of type III granules only (Fig. 7F, left).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Weigel, 1941;
Seitz, 1972;
Oxford, 1998). Guanine, a
purine compound stored in intestinal cells, was the only pigment so far
identified as responsible for the white coloration of spiders
(Holl, 1987;
Oxford and Gillespie, 1998).
Because guanine emits no fluorescence (under our lightning conditions) and is
not birefringent, we rule out its presence in the prosoma region, in which we
observed a second white pigment, different from guanine. Pterin, a very common
pigment in the white tegument of insects, is not present in detectable
quantities in the epidermis of spiders, particularly M. vatia
(Seligy, 1972). The granules
that we observed were electron-dense, with electron-lucent inclusions of
micro-crystals with a characteristic fluorescence and birefringence. This
suggests that these abundant granules contain uric acid. Guanine and uric acid
are still present in yellow spiders. The combination of a yellow granule layer
(type III) with crystals of either nature leads to the brilliant
yellow color we observe.
Chemical identity of the pigment granules: ommochromes and their precursors
We identified two types of progranules (type I and type
II) and a complete granule (type III), and their developmental
relationship (Fig. 8). These
granule types can occur seperately or combined in the same cell. The
characteristics and structure of the type III granules allow us to
conclude that they are carriers of ommochrome pigment, which have been
extensively chemically characterized
(Stamm Menendez and Galarza Basanta,
1961; Linzen,
1967; Linzen,
1974; Seligy,
1972; Holl, 1987).
Ommochromes are derivatives of the amino acid trytophan via
kynurenine and 3-OH-kynurenine. They are responsible for yellow (oxidized
xanthommatin) and red (reduced form) colors found in many invertebrates
(Needham, 1974;
Oxford and Gillespie, 1998).
The different granules that we found in the epidermis of the spider are very
similar to the ommochrome granules type 1–3 described in locust
epidermis (Bouthier and Lhonoré,
1984). Five morphological categories were defined, corresponding
to different developmental stages of pigment granules. Ommochromes are
progressively deposited onto the homogeneous matrix of type 1 progranules of
unknown chemical nature. The final granule (type 3) contains the true pigment.
Granules types 4 and 5 corresponded to successive steps of mineral deposition
in the matrix (calcium phosphate and uric microcrystals)
(Bouthier and Lhonoré,
1984).
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Chemical identification of the final granule type, ommochromes, enabled us
to work back through their metabolic pathway to hypothesize the chemical
composition of the progranules. All metabolites of the ommochrome pathway can
easily be detected under ultraviolet light, as they retain the fluorescence
due to their aromatic ring (Linzen,
1967). The natural fluorescence of kynurenine and 3-OH-kynurenine,
the two major precursors of ommochromes, provides a convenient means of
localizing these metabolites intracellularly. The characteristic fluorescence
and the fine structure of progranules of type I and type II
suggest that they could contain both precursors. The content of type
I progranules is homogeneous, so we assume that type I
progranules contain kynurenine only. During the change in color from white to
yellow, the vesiculated progranule type II could be an intermediate
form between the progranule type I and the ommochrome granules. The
different states of the type II progranules (heterogeneous content)
suggest that the vesicles could contain both kynurenine and 3-OH-kynurenine,
and also the final product (ommochrome) in their electro-dense regions.
There is ample evidence from other studies to support our inference
regarding the chemical identity of the progranules. In the stick insect
Carausius morosus, for example, all the metabolites of the ommochrome
pathway are found in the epidermis
(Stratakis, 1980). All
tryptophan metabolites have been shown to be present in the eyes of Apis
mellifera (Dustmann,
1975). In the insects Schistocerca gregaria and C.
morosus, 3-OH-kynurenine was found to occur in the epidermis
(Pinamonti et al., 1973;
Stratakis, 1980). Finally, the
spiders Argiope aurantia and A. trifasciata accumulate both
kynurenine and 3-OH-kynurenine in their opisthosomal hypodermis
(Seligy, 1972). Our current
biochemical HPLC studies tend to confirm the presence of large amounts of
these two metabolites in M. vatia epidermis (J.C., unpublished
observation). Even though our hypothesis is supported by morphological
observations, further work is necessary to elucidate the biochemical nature of
the granules.
The granule formation is associated to endoplasmic reticulum
The cytological origin of ommochrome pigment granules has often been
associated with Golgi vesicles. In particular, Shoup
(Shoup, 1966) reported the
presence of immature granules adjacent to Golgi regions of developing fly eyes
and concluded that these granules originate as vesicular secretions of Golgi
apparatus. By contrast, Fudge (Fudge,
1967) observed that the granules arise from the small cisternae of
the smooth endoplasmic reticulum (SER) in the eyes of Drosophila
melanogaster. Taking an intermediate position, Bouthier and
Lhonoré (Bouthier and
Lhonoré, 1984) related the formation of initial progranules
with Golgi vesicles found in the epidermal cells of Locusta migratoria
cinerascens, but could not conclude whether these progranules were
derived from dictyosomes or from rough endoplasmic reticulum (RER). Recently,
a unique pathway for screening granule formation in the retina of the opilion
Eumesosoma roeweri was proposed
(Johnson and Gordon, 1990). An
endoplasmic reticulum network is at work in the formation of each granule.
Each site is composed of concentric, interconnected rings of SER that are
filled with spherical pigment particles. The formation of screening pigment
granules occurs in the middle of these rings and begins with the release of
particles from the innermost rings of carrier reticulum.
A common origin of vertebrate pigment cells, melanophores, xanthophores and
iridophores, was proposed by Bagnara et al.
(Bagnara et al., 1979). These
cells contain pigmentary organelles known, respectively, as melanosomes
(melanins), pterinosomes (pteridines) and reflecting platelets (purines).
These authors suggest the existence of a primordial organelle derived from the
endoplasmic reticulum. This preorganelle may be a vesicle formed from the RER,
and may represent an early structural component in the genesis of each
pigmentary organelle. In the formation of melanosomes, the premelanosome is
derived from cisternae of the RER, and then fuses with vesicles containing
tyrosinase enzymes, considered to be derived ultimately from the Golgi complex
(see also Palumbo et al.,
1997).
The ontogeny of ommochrome granules bears strong similarities to that
described above for vertebrate pigment cells. We observed a strong
relationship between the structure of concentric rings of RER, the relative
high density of mitochondria and the glycogen rosettes with the pigment
granules in M. vatia. The external layer of the ring structure
appears to be continuous with the outer membrane of a granule. While there is
a close morphological analogy between the RER structure of M. vatia
and the SER structure observed by Johnson and Gordon
(Johnson and Gordon, 1990),
the presence of RER suggests a closer functional analogy with the model
described by Bagnara et al. (Bagnara et
al., 1979). The type I granules present in the white
spider are probably primordial vesicles derived from RER. We have so far
failed to detect Golgi vesicles, despite intensive search in the vicinity of
progranules of type I. However, we found that Golgi bodies are
frequently present near the type II granules (yellowing spiders),
which suggests that they might have a role in the transformation of
progranules to ommochrome pigment granules.
Mechanisms and significance of color change
Our understanding of pigment granule development and the presence of
different stages of granule formation in different color morphs enable us to
revisit the three main hypotheses for the arthropod ommochrome formation
described in the Introduction.
The epidermis of white spiders is full of granules containing ommochrome
precursors, most likely kynurenine. White spiders with red stripes have large
amounts of ommochromes localised precisely and only in these stripes. Hence,
the absence of a change of color from white to yellow is not due to a lack of
precursors, nor a lack of enzymes [as found in the white eyes clones of
Drosophila melanogaster
(Mackenzie et al., 2000)].
This clear conclusion invalidates the common hypothesis stating that the
ommochrome production is due to the necessity of avoiding high cellular
concentrations of tryptophan (hypothesis 1), since it is already neutralized
as the ommochrome precursor in granules of type I (before changing to
yellow). Storing this toxic compound as kynurenine might be sufficient.
However, hypothesis 1 could hold true for other tissues or organs, such as
Malpighian tubules. The photoprotection role of ommochromes, another common
hypothesis for the role of ommochromes due to their widespread occurrence as
screening pigments in insect eyes (hypothesis 2), deserves much more
attention. Indeed, M. vatia is quite original in being both exposed
for days to direct solar radiation on the top of flowers and in having a
transparent cuticle exposing the epidermal cells to direct radiation.
Ommochrome precursors could however be sufficient as screening pigments, as in
the group of chartreuse mutants of Apis mellifica
(Linzen, 1974). Indeed, the
mutant group accumulates the yellow tinted but still translucent
3-OH-kynurenine in a granular form in the pigment cells of the compound eyes.
That pigment precursor therefore assumes a pigment function
(Linzen, 1974). The intensity
of the yellow hue of spiders, a result of the mix between 3-OH-kynurenine and
ommochromes, might reflect the amount of screening against radiation. As
indicated in the Introduction, in addition to this optical function, given
their antioxidant properties, ommochromes constitute protective agents against
UV-induced photodamage.
The final and most favored hypothesis from the ecologist's point of view for the formation of ommochromes (hypothesis 3) is mimetism and crypsis. A cost–benefit analysis of ommochrome production is, however, required to understand the fitness gain from the change of color in an evolutionary context. It can only be based on a precise nutritional budget, at present lacking for this class of pigment. It also requires the measurement of some fitness-related trait, such as increased fecundity, survival or simply higher prey capture rate, as a function of the degree of flower color matching, a main piece still missing in the puzzle. Furthermore, while the basic metabolic pathway and enzymes for the anabolism of ommochromes are partially identified, the catabolism of these pigment granules, which is relevant when spiders revert from yellow to white, is unknown. We therefore lack a dynamic vision of this highly reversible phenomenon. In conclusion, any claim concerning physiological costs and ecological benefits of color change must be considered with extreme care. While our work tends to reject one hypothesis and support another, too many key assumptions remain untested for its acceptance and decisions about further hypotheses. Results from ultrastructural studies offer us a sobering reminder of how tenuous the functional basis is of most of the discussions and claims over the last century.
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Acknowledgments |
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