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Annu. Rev. Entomol. 1997. 42:231–67
c 1997 by Annual Reviews Inc. All rights reserved
Copyright EVOLUTION OF ARTHROPOD SILKS
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Catherine L. Craig
The Bunting Institute of Radcliffe College, Harvard University, Cambridge,
Massachusetts 02198
KEY WORDS:
spider, insect, spinneret, spinning, Onychophora
ABSTRACT
Silks belong to the class of molecules called structural proteins. The ability to
produce silk proteins has evolved multiple times in the arthropods, and silk secreting glands have evolved via two different pathways. The comparative data and
phylogenetic analyses in this review suggest that the silk-secreting systems of spiders and insects are homologous and linked to the crural gland (origin of systemic
pathway to silk production) and cuticular secretions (origin of surficial pathway
to silk production) of an onychophoran-like ancestor. The evolution of silk secreting organs via a surficial pathway is possible in adult and larval hexapods,
regardless of their developmental mode. Silk secretion via a systemic pathway is
possible in either adult or larval hexapods, but only larval insects have dedicated
silk producing glands. Spiders, however, have evolved silk producing systems via
both systemic pathway and surficial pathways, and a single individual retains both
throughout its lifespan. Early in the evolution of spiders, silk glands were undifferentiated, suggesting that the number of silk secreting glands of any individual
was related to the spider’s energetic need to produce large quantities of protein.
However, the complex silk-producing systems that characterize the aerial web–
building spiders and the diverse types of proteins they produce suggest that their
silks reflect the diverse and increasing number of ways in which spiders use them.
Because the muscular and innervated spinnerets and spigots of spiders allow them
to control fiber functional properties, silk proteins represent an avenue through
which animal behavior may directly affect the molecular properties of a protein.
INTRODUCTION
Silks are produced solely by arthropods and only by animals in the classes
Insecta, Arachnida, and Myriapoda. Collectively, insects produce many different types of silk proteins, although individual species produce only one type.
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Table 1 Comparison of ways insects and spiders use silks
Function
Protective shelter
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Structural
support
Reproduction
Foraging
Dispersal
Example for insects
Cocoon silks produced by
Lepidoptera (93)
Silk egg stalk produced by
Neuroptera (93)
Restriction of female
movement during mating by
Thysanoptera (91)
Underwater silk prey capture
nets produced by Trichoptera
(93)
Dispersal of new hatched
Lepidoptera (93)
Example for spiders
Retreat silks produced by all
spiders (65a)
Egg sac suspension threads
produced by Araneidae (32)
Sperm web produced by all
male spiders (49)
Aerial nets produced by
Araneidae (32)
Dispersal of newly hatched
spiderlings (40)
Spiders also produce a variety of silks, but in contrast to insects, an individual spider may produce as many as eight different types of silk thread (49).
Nevertheless, the purposes for which insects and spiders use silks are similar
(Table 1). The silks produced by myriapods are uncharacterized.
The goal of this review is to outline and compare the molecular properties
of silks produced by arthropods, the purposes for which they are used, and
their evolution and probable origins. Because most of the information available on the structure of silk proteins has been gathered for silks produced by
insects, the analyses presented here focus on insects. However, the proposed
monophyletic origin of the arthropods (104) and the molecular and functional
similarity of silks and their uses across arthropod taxa suggest that the silks
produced by insects and spiders may have evolved from a common ancestor.
Rudall & Kenchington (82) proposed that molecular variations among silks
produced by insects were the result of random processes. They reasoned that,
because silks are used outside an insect’s body, they are not subject to the
stringent selection pressures acting on proteins used for intracellular functions.
However, the cladistic analysis presented below suggests there has been selection for the production of silks characterized by parallel-β configurations that
correlate with the uses to which they are put and the developmental mode of the
insects producing them. A recent study comparing silks spun by spiders across
phylogenetic groups shows that their structural properties are also variable (19).
Here too, analyses of the variations of silks and glands reveal that differences in
the structural organization of silk proteins correlate with the evolution of spider
foraging behaviors as well as their ecological radiation.
This review is divided into three parts. The first section summarizes the production of silks and their physical and chemical properties. The crystalline silks
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EVOLUTION OF ARTHROPOD SILKS
233
include the α-helical silks and the β-pleated sheet fibroins. Less ordered materials include random-coil proteins (polymeric secretions that cannot be spun
or stretched) and related fibrous materials. The discussion of mixed secretions
and fiber bundles describes ways of altering the mechanical properties of silk
threads without changing the primary (and, likely, the secondary) structures
of the component protein domains. This set of classifications is intended to
provide an understanding of the physical-chemical properties of silks, their interrelationships, and how they are used by the organisms that secrete them. The
classifications used here encompass early groupings based on X-ray diffraction
patterns (102).
The second section of the review presents two new cladistic analyses. The
first analysis addresses the evolution of silk secreting glands, silk molecular
structure, and the functional uses of silks spun by insects and spiders. The
second analysis addresses the evolution of secreted proteins across arthropod
groups and their proposed sister group, the Onychophora (104).
The third section of the review presents current hypotheses regarding the
origin of the silk glands and spinnerets of spiders and insects. Using these
data and the analyses presented in section two, a new hypothesis is proposed.
Silk producing glands in both insects and spiders evolved via two pathways, a
surficial (epidermal) gland pathway and a systemic gland pathway. Although
insects produce silks via one or the other pathway, spiders retain both types
of silk producing systems and, unlike the insects [exceptions: Embiidina and
Gryllacridoidea (75)], produce silks throughout their lives. Furthermore, although none of the insects has a spinneret that represents more than a cuticular
hardening or process (68), all spiders have muscular and innervated spinnerets
and spigots. As a result, spiders are able to control the protein composition,
fiber diameter, and rate at which the fiber is drawn. All of these factors affect
the mechanical and physical properties of silks and the diversity of ecological
uses to which they are put. The data presented here suggest that the origin of the
secreted silk proteins produced by all arthropods lies in the crural gland and dermal secretions of the common, onychophoran-like ancestor of the Arthropoda.
DEFINITION OF SILK
Silks are fibrous proteins containing highly repetitive sequences of amino acids
and are stored in the animal as a liquid and configure into fibers when sheared
or “spun” at secretion. This definition excludes keratin and collagen.
The Molecular Backbone
The molecular backbone of all proteins consists of a chain of amino acids
(Figure 1a), each of which is built of four components. Three of the compo-
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nents, an amine group (−NH2 ), a carboxyl group (−COOH), and a hydrogen
group (−H), are common to all amino acids and are bound to a carbon molecule
designated as the α-carbon. The backbone of the protein forms when a terminal carboxyl group of one amino acid binds with a terminal amine group of
an adjacent amino acid, eliminating water to make an amide bond. The fourth
component of each amino acid, designated the “R” group or side chain, is variable, and the diversity of proteins derives from the different size, shape, charge,
hydrogen-bonding capacity, and chemical reactivity of these distinctive side
chains. Furthermore, rotation around the α-carbon of the amino acid affects
the interactions among the R groups (determines the polarity of the molecule)
and allows the protein to fold in a variety of ways.
The 20 different R groups give rise to 20 different amino acids and from
these, all proteins are built. Silk proteins, however, are composed primarily of
the three amino acids: glycine, alanine, and serine. Glycine (Figure 1b), the
simplest amino acid, has just one hydrogen atom (−H) as its side chain, and
alanine (Figure 1c), the next simplest amino acid, has a single methyl group
(−CH3 ) as its side chain. Serine (Figure 1d) is similar to alanine, but instead of
having three hydrogen atoms bound to the carbon molecule of the methyl group,
one of the hydrogen molecules is replaced by a hydroxyl group (−CH2 OH).
These three amino acids dominate the polypeptide chains that make up silks.
The remainder of the amino acids in silk protein sequences is highly variable
(55).
Identifying the Diverse Macromolecular Configurations
of Silk Proteins
Recent application of nuclear magnetic resonance spectroscopy (NMR) (3),
circular dichroism (CD) and small-angle X-ray scattering (SAXS) (11), solid
state NMR and Raman spectroscopy (34), and characterization of silks by insitu synchrotron X-ray studies (63) have provided detailed information on the
behavior of the molecules and amino acid sequences that make up silk proteins
Figure 1 (a) All amino acids are composed of an amine group, a carboxyl group, and a hydrogen
group. The R group, or side chain, is variable. Among silks, the amino acids are usually (b)
glycine, (c) alanine, or (d) serine.
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EVOLUTION OF ARTHROPOD SILKS
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Figure 2 Schematic representation of silk structures.
spun by the golden orb-spinning spider Nephila clavipes and the silk worm
larvae Bombyx mori. However, these silks represent only a small sample of
the diverse types of silks that arthropods spin. The most powerful technique
for studying the macromolecular structure of large molecules, and the approach
used most extensively to explore silk proteins, is X-ray diffraction or crystallography. X-ray crystallographic studies on silks spun by over 100 insect species
have revealed several classes of protein chain conformation that correlate with
their amino acid composition. The X-ray crystallographic analyses, completed
in the 1950s (101), 1960s (53, 55, 102), and 1970s (82), together with ecological studies on silk mechanical properties and the functional uses of silks,
provide enough data for a first analysis of the evolution of silk proteins and
their ecological importance across insect groups.
Physical, Chemical, and Mechanical Properties of Silk
α-HELICAL STRUCTURE The primary unit of an α-helical protein is a polypeptide chain that assumes the conformation of a rod-like coil stabilized by hydrogen bonds that form between the amine and carboxyl groups within the
backbone (Figure 2a). The amino acid side chains (the R groups) extend away
from the coil in a helical array and are stabilized by H-bonds that form between
polypeptide chains within protein sheets (95). The α-helical silks have a relatively low glycine content but are high in acidic residues such as aspartic acid
and glutamic acid (82). Silks composed entirely of proteins in an α-helical
conformation are not produced by a dedicated silk gland but by glands that
assume some other primary function, such as the colleterial glands.
Alpha-helical silks are produced by a disparate array of insects in the orders Dictyoptera, Siphonaptera, and Hymenoptera (55, 82, 102). For example,
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honey bees (Hymenoptera) produce α-helical silks in their colleterial glands
(accessory to insect genital glands) and the adults use them to reinforce their
wax combs (43, 44). Larval Siphonaptera (fleas) produce α-helical silks in
their labial glands and use them to construct nests, pupation cases, and individual and group cocoons (55, 82, 93, 102). Mantids use this kind of silk
to construct a parchment-like ootheca (77). Insects producing α-helical silks
appear to use them in combination with other materials, and sometimes with
other silks, suggesting that α-helical proteins provide only some of the material
properties needed by the structures into which they are incorporated. The silks
of species of the suborders Aphaniptera of the Siphonaptera and Aculeata of
the Hymenoptera (55, 82, 102) are characterized by reduced glycine and a high
proportion of glutamic acid residues. At least some α-helical proteins, for example those produced by the sawfly Arge ustulata (Symphyta: Hymenoptera), can
be transformed into antiparallel β-fibroin crystallites upon stretching (54, 57).
This suggests that the processing of silk proteins, i.e. how they are extruded and
deposited, may be as important to their evolutionary diversity as the protein’s
molecular sequence.
None of the silks produced by spiders are known to be entirely α-helical in
conformation. This may be a result of preferential sampling in that the only
silks to have been studied so far are those that can be easily drawn from spider
spinnerets. Some spiders, as well as insects, do secrete silk-like compounds by
ejecting or extruding them instead of “spinning” (which involves pulling and
shearing). For example, spiders in the family Scytodidae, the spitting spiders,
use modified salivary glands to produce what is thought to be a fibrous protein
that they eject or spit onto passing insects, matting them to the surface on which
they were walking. The structure of this material has not been determined but
only described as a gluey, fibrous glycoprotein (49). If this material proves to
be crystalline, then the fact that it is ejected, not drawn, suggests it may have
the α-helical form rather than the shear-induced ordering of crystallites that
characterizes β-pleated sheet silks.
PARALLEL–β-PLEATED SHEET STRUCTURE A second type of protein structure,
and the structure that characterizes the majority of silk proteins that have been
described, is the β-pleated sheet (Figure 2c). This type of silk is produced
by both insects and spiders. It differs from the α-helical proteins in that the
polypeptides are stabilized by H-bonds that form between amino acid chains,
not within chains (95). The secondary unit of the protein, the polypeptide chains
that compose the β-pleated sheets, are aligned side by side in a parallel or antiparallel direction in four possible configurations: polar-antiparallel sheet (proposed in 58), polar-parallel sheet (methyl groups of alanine residues grouped on
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EVOLUTION OF ARTHROPOD SILKS
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just one side), antipolar-antiparallel sheet (methyl groups pointed alternately
to opposite sides of the sheet), and antipolar-parallel model (98). Both the
direction of adjacent polypeptide chains and the polarity of the molecules composing them determine how the protein sheets stack into a three-dimensional
crystalline matrix. Mixed parallel- and antiparallel-β protein sheets such as
those spun by the tussock moth (55) are relatively common (100).
The structure of fibrous proteins, proposed by Marsh, Corey & Pauling (58),
is illustrated by the cocoon silks spun by B. mori. The silks of this species
assume a polar-antiparallel structure in which all of the polypeptide’s methyl
groups project to one side of the protein sheet. The protein sheets of these silks
stack closely (intersheet distances are 3.5 Å for glycine-glycine interactions and
5.7 Å for alanine-alanine interactions) and in a regular orientation (48, 55, 102).
In contrast, when the protein chains comprising β-pleated sheets run parallel,
the hydrogen bonds between the sheets are distorted. In this type of silk the
spacing between all protein sheets is about 5.27 Å. The internal strain generated
by parallel packing may destabilize such silks. In fact, parallel-β sheets of less
than five polypeptide chains are rare, possibly because of this distortion.
The β-pleated sheet proteins, described as the classical silk proteins, were
originally characterized as having a polar, antiparallel structure. Warwicker
classified them into three different groups on the basis of the structure of the silk
crystallites (102). The molecular symmetries of silks in Warwicker’s Groups
1–3 differ by increased spacing between the peptides of adjacent chains (Table 2), which may result from increased amounts of alanine (82) and decreased
amounts of glycine. The three types of “classical” silk proteins produced by
Lepidoptera include the following:
1. The cocoon silks spun by B. mori (Bombycoidea: Bombycidae), characterized by an intersheet packing distance of 9.3 Å and polypeptide strands of
alternating amino acids of glycine and alanine or serine (55);
2. The cocoon silks spun by the caterpillar Anaphe moloneyi (Bombycoidea:
Thamoetopoeidae), characterized by an intersheet packing distance of 10 Å
and polypeptide strands whose repeating unit is ((Gly-Ala)x -Ala)n (54, 55);
3. The cocoon silks spun by the caterpillar Antheraea mylitta (Bombycoidea:
Saturniidae), characterized by an intersheet packing of 10.6 Å and polypeptides primarily composed of alanine. The dragline silk (ampullate gland)
produced by the spider Nephila madagascariensis is also characterized as
this configuration (55).
The additional β-pleated silks that Warwicker classified into Groups 4 and 5
are considered atypical. Group 4 silks, illustrated by the cocoon silks spun by
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Table 2 Types of proteins deposited, ejected, or spun by insects and spiders
Protein type
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Random coil proteins (2, 100)
(Insects and spiders)
α-Helical structure (54, 55, 82,
102) (Insects and spiders)
Parallel-β pleated sheet (53,
82, 101, 102) (Insects
and spiders)
Cross-β structure (54)
(Insects, unidentified in
spiders)
Collagen (54, 82)
(Insects, unidentified in
spiders)
Protein characteristics
High content of basic amino
acids
Randomly coiled before and
after secretion
Reconfigures into parallel-β
proteins under stress
Low glycine, high in acidic
residues
Helical coil stabilized by H
bonds forming between
polypeptide chains, secreted
Reconfigures into parallel-β
protein under stress
Low tensile strength, high elasticity
Five primary groups
characterized by increasing
length of side chain and
decreasing glycine, sheared
Warwicker Groups 1–3
Intersheet distance—9.3 Å–
10.6 Å; High tensile strength
Warwicker Groups 4–5
Intersheet distance 15 Å–
15.7 Å; High tensile strength
and elasticity
Warwicker Group 6—Parallel-β
sheets grouped in threes
and including α-helical
component. Mechanical
properties not measured
45% serine
Polypeptide chain oriented
perpendicular to fiber axis
Reconfigures to parallel-β
chain when stretched to six
times its original length
30% glycine, 50% glycine,
alanine and serine
Three polypeptide chains
twisted into triple helix
stabilized by steric repulsion
Tightly packed structure
characterized by high strength
Glandular origin
Insects—unknown
Spiders—suspected
piriform, aggregate
Insects—colleterial
glands
Spiders—unidentified
Insects—labial
glands
Spiders—ampullate,
flagelliform, tubullar
pseudoflagelliform,
paracribellar
Malpighian tubules,
adults and
larvae; peritrophic
membrane
Salivary glands
(Continued)
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Table 2 (Continued)
Protein type
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Chitin (82)
(Insects, unidentified in
spiders)
Cuticulin silk (82)
(Insects, unidentified in
spiders)
Polyglycine II (82)
(Insects, unidentified in
spiders)
Protein characteristics
A nitrogenous polysaccharide
(C8 H13 NO5 )n
Appears to be silk but is
actually composed of cells
Highly oriented fibrous
protein of α-helical
orientation
20% more glycine than
Warwicker Group 1 silks
Glandular origin
Procuticle
Dipteran epithelial cells
Hymenopteran salivary
glands
Thaumetopoea pitycocampa (Bombycoidea: Thaumetopoeidae) and silks spun
by Avicularia avicularia, are characterized by an intersheet packing distance of
15 Å, and they contain high amounts of the amino acids serine and glycine (55).
Unlike the amino acid side chains of polypeptides in Groups 1–3, the longer
side-chains that compose Group 4 and 5 silks are thought to fit into the matrix
of the protein crystals (54, 55). Group 5 silks are characterized by an intersheet
packing distance of 15.7 Å (53, 102) and are illustrated by the cocoon silks
produced by Nephila senegalensis (tubiliform glands) (102), as well as a silk
of unidentified origin spun by A. diadematus.
Later investigators identified two more groups of silk proteins with unique
X-ray crystallographic patterns. Group 6 silks, spun by the sawflies in the families Perigidae, Argidae, and Tenthredinidae, are characterized by a parallel-β
structure, but the pleated sheets are arranged into repeating units of three and
include a well-defined α-helical component (53, 54, 82).
Takahashi (98) recently identified an additional molecular conformation for
the hydrogen-bonded, β-pleated sheet proteins in which the alanine residues
of the polypeptides alternately point to opposite sides of the sheet. As a result,
the crystalline region of the silk is composed of irregularly stacked, antipolarantiparallel sheets with different orientations (98). This more recent model
may help in understanding the diversity of silk protein structures, in particular
the “new” silks, or those spun by the derived, aerial web-spinning spiders. It
may be that the conformational shifts such as thosedescribed for Group 4 and
5 structures are only possible if silks have an anti-polar antiparallel structure
as in the model proposed by Takahashi (98). Takahashi’s model allows for a
greater diversity of silk molecular structure and thus differs from the classical
silk models proposed in the 1960s and 1970s.
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Information on the molecular conformation of silks produced by spiders has
been limited to proteins drawn from the tubuliform (origin of egg-sac silks),
ampullate (origin of dragline silks), and flagelliform (origin of prey-capture
threads spun by araneoids) glands of only a few spider species (55). All of
these proteins are characterized by different types of parallel-β structure.
CROSS–β-PLEATED SHEET STRUCTURE A third conformation for crystallite proteins, and a subset of the parallel fibroins, is the cross-β configuration. Here
polypeptide strands are oriented perpendicular to, instead of parallel to, the
silk fiber axis (33) (Figure 2b). Upon stretching, the cross-β proteins reconfigure into a parallel-β structure similar to that of the Group 3 fibroins defined
by Warwicker (54). Although thought to be common among arthropod silks
and silk-like materials (46), relatively few cross-β silks have been identified.
All of these are produced by Endopterygote insect larvae in the orders Neuroptera [Chrysopa (44, 54)], Coleoptera [Hydrophilus, Hypera (46, 81)], and
Diptera [Arachnocampa; (26, 53, 81)], and all are produced in larval Malpighian
tubules or are derived from the peritrophic membrane. In one case, the lacewing
Chrysopa flava (Chrysopidae), cross-β proteins are produced in the colleterial
glands of adults and used to attach eggs to the underside of leaves (54).
Cross-β silks reconfigure to parallel-β silks when stressed or stretched.
For example, when the silks spun by the weevil Hypera spp. (Curculionidae:
Coleoptera) are stretched beyond six times their original length and released,
there is a partial molecular transformation to a parallel-β form. This transition is an intramolecular phenomenon and the degree of shift is proportional
to the degree of fiber extension (46). The conformational shift from cross-β
to the parallel-β form suggests again that the behavior by which the silk is
released from the animal can contribute greatly to the evolution of the proteins’
macromolecular conformation. Natural selection for silks that exhibit high extensibility may have exploited the cross-β to parallel-β transition in lieu of a
gross change in the molecular composition of the silk protein. For example, the
New Zealand glowworm Arachnocampa luminosa (Mycetophilidae) intercepts
flying midges (76) with suspended silk threads that exhibit a cross-β conformation (53, 81). Although the biomechanical properties of these silks and their
role in intercepting prey have not been explored, the high thread extension
achieved through the process of unfolding represents a mechanical means that
could greatly enhance the silks’ ability to absorb insect impact. In contrast,
the high extensibility of the flagelliform silks produced by the araneoid spiders, the orb-spinners, results from the composite nature of the silk material
(35, 36). Much less silk protein is needed to produce a material that extends
elastically than is needed for a thread that extends mechanically by unfolding.
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The composite nature of the araneoid’s flagelliform silk allows the threads to
withstand the impact of fast-flying, heavy-bodied prey at a lower energetic investment than that which would be required if the impact-absorbing capacity
were achieved just through the sixfold increase in fiber length of the threads
produced by A. luminosa. Furthermore, although the transition from a cross-β
to a parallel-β conformation, and hence extended silk length, is permanent, the
araneoid silks are plastic and largely able to regain their original conformation
and length after deformation (22, 110).
RANDOM COIL PROTEINS Proteins characterized by a random coil configuration have not been identified with certainty from the silk-secreting glands of
insects. However, histological and amino acid analyses suggest that spiders
secrete proteins that are not characterized by an α-helical or parallel-β secondary structure. Nevertheless, random coil silks can be transformed into α,
β, and well-oriented β forms by mechanical shearing and treatment in organic
solvents under various reaction conditions (57).
The amino acid residues of parallel-β silk proteins drawn from the tubuliform,
ampullate, and flagelliform glands are primarily glycine, serine, and alanine,
which are amino acids characterized by short side-chain functional groups (2).
Histological analyses show that these silk proteins are primarily acidic. In
contrast, the piriform glands (common to all araneomorph or true spiders) and
aggregate glands (found in only araneoid spiders) produce protein secretions
characterized by a high content of basic amino acids, particularly lysine (2).
These silk polymers are unlikely to exhibit the α-helical configuration because
of their high proline content and are unlikely to assume a β-conformation because of their low content of amino acids with short side chains (97). These
proteins probably occur in a randomly coiled state both before and after secretion, and thus it is reasonable to infer that they are not pulled from the tip
of the spinneret but rather deposited. The interactions among these types of
molecules and between the protein and the substrate suggest that the random
coil proteins are likely to be good glues (2).
The protein secretions from the piriform and aggregate glands yield glues
with different affinities for water. The piriform gland proteins, used to bind
materials or cement threads to a substrate, dry quickly. Proteins secreted from
the aggregate glands of the orb-spinning spiders (glands unique to the araneoids)
yield proteins that do not dry (2), probably because of a high concentration of
hygroscopic, low-molecular weight compounds, and hence result in a viscid
catching thread that retains prey after interception.
Piriform and aggregate gland proteins contribute to the paper-like quality of
some silk materials produced by spiders when used in combination with fibrous
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proteins, such as those secreted from the tubuliform, the flagelliform, and ampullate glands. For example, the outer shell that characterizes the egg sacs produced by the garden spiders Argiope spp. may be analogous to the paper-like
silk secretions produced by wasps in the labial glands of wasps of the superfamily Vespoidea. These secretions harden to form fibers and plates, and vespids
use them to bind organic and mineral matter into a nest wall (90, 93). Argiope
spp. also use piriform gland secretions to bind materials, but instead of collected
exogenous materials, spiders bind silk threads drawn from other glands (8).
MIXED SECRETIONS AND THREADS Spiders have been grouped as generalists
or specialists on the basis of their silk producing systems. Generalist spiders
are defined as those that produce one to three kinds of fibers but use them
indifferently for the construction of burrows, egg sacs, or sperm webs (49).
Specialist spiders produce four to nine kinds of silks (distinguished by their
glandular origin) that they use specifically to construct burrows, egg sacs, sperm
webs, or feeding nets. These are characterized by different fiber compositions
and they include several types of proteins. In fact, among the araneomorph
spiders, the only threads not characterized by a mixed fiber composition are the
dragline silks that emerge from the ampullate glands (49). Nevertheless, even
these silks are used in conjunction with piriform gland secretions that cement
them to the substrate on which the spider walks.
The Mesothelae (42) are the most ancestral living spiders. Anatomical and
histological studies show that they are characterized by three or four different kinds of silk glands that secrete one to three distinct protein products. The
Mesothelae use their silks indiscriminately to line their burrows or cover their
eggs (42) suggesting that differentiation among protein types has little functional value. No other spiders have evolved an analogous system of protein
differentiation. The Mesothelae gland system may reflect the need for a particular amount of silk protein but not for any particular type silk.
The Opisthothelae (which includes both the Mygalomorphae, ancestral spiders such as tarantulas and trap-door spiders, and the Araneomorphae, or the
“modern” spiders) also produce silks composed of more than one type of protein. The simplest silk producing system, that of the mygalomorph spider
Antrodiatus unicolor (68), is characterized by only one type of silk gland, an
acinous gland, that produces two types of proteins secreted through spigots on
two pairs of spinnerets (69). The distal cells of the silk glands produce a basic
protein rich in sulfhydryl groups that may function in the cross-binding of the
protein’s crystallites. These silks have a double composition consisting of a
core and outer coating (49).
Although even the simplest of the spider silk-producing systems makes
threads that contain multiple types of protein, the production of mixed protein
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EVOLUTION OF ARTHROPOD SILKS
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threads is described only for the most derived of the silk producing insects, the
Lepidoptera. The apparently specialized nature of lepidopteran silks may have
been recognized, however, because they are better studied than the labial gland
silks produced by other insects.
The diverse nature of the types of silks and silk-producing glands of spiders
suggests that silk fibroins may have evolved under selection for the expanded
uses to which spiders put them. The diversity of gland type further suggests that
the silk produced by spiders may have evolved through more than one pathway.
By producing threads with a sheath-core structure (96), varying the proportions
of the sheath and core (49), combining fibrils with different tensile strengths
and extensibilities (96), producing composite materials (35), and making use
of a diverse set of silk-spinning techniques (e.g. Ref. 57) spiders produce silks
with mechanical properties suitable for a wide variety of ecological functions.
SILKS AS COMPOSITE MATERIALS The parallel-β silks produced by insects have
been identified by the structure of their crystallite components (102). Close to
100% of the silk protein spun by B. mori is characterized as an antiparallel-β
sheet, and recent analysis suggests that no residues of either an α-helical or
random coil conformation are present (36, 88). The specialized silks produced
by the araneoid spiders, however, contain three structural domains: an amorphous domain, an α-helical domain, and a parallel-β domain. This complexity
differentiates them from silks produced by all other arthropods.
The proportion of the silk protein devoted to each of these three structural
motifs greatly affects the fiber’s mechanical behavior (and hence its potential
selective value to the organism). Individual fibrils of dragline silk spun by
the golden orb-weaver Nephila clavipes have a composite structure containing
crystalline regions equaling 30% of the dry silk volume that are embedded in
an amorphous matrix comprising 70% of the remaining dry silk volume (35).
A recent model for spider dragline silks suggests that some of the residues are
present in a classical crystalline phase and that the remainder are protocrystals,
possibly preformed β sheets (89). Crystallites confer tensile strength on the
polymers, and the amorphous protein regions provide a stiff, energy-absorbing
matrix of cross–β links, in some cases strongly reinforced by the β crystallites
(35, 37, 99). The poorly oriented β sheets may be important in coupling the
highly oriented crystalline domains and the amorphous regions (89). As a result
of its high tensile strength and extendibility, more energy is required to break
the same volume of silk protein produced by Nephila spp. than that of any other
biological material (22, 35, 36).
SILK MECHANICAL PROPERTIES In a 1980 review Denny classified the mechanical properties of silks spun by arthropods into three groups on the basis of their
extensibility. Although he notes that his groupings based solely on mechanical
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properties are somewhat artificial, it is informative to review his findings in the
context of protein structure, silk functional properties, and origins. Denny’s
Group 1 silks (crystallite Group 1 and packed at 9.3 Å) include those produced
by the silk worm B. mori as well as the dragline silks produced by garden spider
Araneus spp. These silks are comparable in strength to other biological fibers,
such as cellulose, collagen, and chitin, and are stronger than keratin. However,
they differ from other fibrous proteins in their ability to extend to 50% of their
resting length before failure. As a result, these silks are five to ten times more
extensible than chitin and cellulose and twice as extensible as collagen (21, 22).
In comparison to other silks, however, they are stiff.
The second group of silks Denny defined are those that extend up to 100%
of the thread’s resting length. These include the cocoon silks spun by the wax
moth larvae Galleria mellonella (crystallite Group 2 and packed at 10 Å) as
well as the cocoon silks spun by A. diadematus (probably crystallite Group 3
and packed at 10.6 Å).
The third functional group defined by Denny, in which fibers extend from 200
to 1600%, includes silks with two different types of molecular organization.
Among these are silks composed only of α-helical protein that are produced
in the colleterial glands by adult Apis mellifera and Chrysopa flava (43, 44).
Denny does not include the viscid silks spun by Araneus sericatus, which
extend up to 2.3 times their resting length (22), in this group. A. sericatus
silks contain a mixed structural motif that includes both β-pleated sheet and
α-helical regions. In contrast to the silks produced by the insects, the highly
extensible silks produced by these spiders exhibit both high tensile strength and
high extensibility.
Although silk strength and extensibility are not necessarily mutually exclusive (22), only spiders that spin protein composites produce silks characterized
by both of these properties. Furthermore, these properties are variable among
silks spun by spiders and provide a focus on which natural selection might act.
For example, the tensile strength of the dragline silks produced by A. diadematus are an order of magnitude higher than the tensile strength of that spider’s
cocoon silks, but their extensibilities are of the same order of magnitude. In
contrast, the capture silks produced by the closely related A. sericatus are similar in strength to the dragline and cocoon silks spun by A. diadematus but are
characterized by greater extensibility differing by an order of magnitude (22).
Related Fibrous Proteins
Silks are not the only support proteins produced by arthropods. For example, a
collagen-like silk is produced by sawflies in the family Perigidae (Hymenoptera)
(82). True collagen, found only in vertebrates, is composed of three polypeptide
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EVOLUTION OF ARTHROPOD SILKS
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chains that run parallel to one another and intertwine to form a triple-helical
structure. The collagen polypeptide differs from that of the β-pleated sheet
fibroin protein in that every third residue is constrained to glycine, the only
amino acid whose side chain can fit in the interior position of the helix. Unlike
the intrachain H-bonds that stabilize the α-helical proteins and the interchain
H-bonds that stabilize the β-pleated sheet proteins, the three helical chains
comprising the collagen molecule are fixed in place by steric repulsion between
pyrrolidine rings of proline and hydroxyproline residues that flank each glycine
(100). This staggered arrangement allows the tight packing of the collagen
structure and gives it its high tensile strength. Although some spiders produce
twisted cables of silk threads (96), these are fiber bundles of β-pleated sheet
proteins encased in a sheath and not held together by steric interactions within
and between polypeptides. Arthropod collagens are cross-β silks superimposed
on a collagen pattern and are produced in a dedicated silk gland, exemplified
by the salivary gland proteins produced by the currant-worm (or sawfly larvae)
Nematus ribessi (Nematinae: Tenthredinidae) (86).
Another alternative structural material, polyglycine, is produced by sawflies
in the families Argidae and Perigidae (Hymenoptera) (53, 82). Polyglycine,
the least constrained polypeptide, has the basic structural motif of collagen
and is considered the molecular precursor of collagen; however, it lacks the
triple-helical conformation and thus collagen’s high tensile strength (100).
Chitin, a third type of fibrous protein, is found in the cocoon threads of the
beetle Ptinus tectus and the weevil Iprionmerus calceatus. Chitin is produced
in the peritrophic membrane and is thus a product of insect excretory systems
(cited in 82).
Overview of Silks Produced by Insects and Spiders
In summary, insects in almost all orders secrete some type of fibrous protein
(Table 2), and most insect silks are secondary products of organs that evolved
for some other primary purpose (68). The ancestral hexapods, Diplura and
Thysanura, secrete fibrous proteins from anal and colleterial glands that they
use during reproductive displays. The paurometabolous insects produce fibrous
proteins—some identified as silks—from portions of their Malpighian tubules,
colleterial glands, or peritrophic membranes. These silks are used largely for
protection. The silks produced by the adult holometabolous insects (Lepidoptera, Diptera, Siphonaptera, Hymenoptera) are variable in structure, and all
except one (Empidiidae: Diptera) are produced in colleterial glands. Larval
holometabolous insects produce labial gland silks. These have been studied
most extensively probably because they are produced in large quantities and
easy to collect. Labial gland silks include those of an α-helical and cross-β and
parallel-β configurations.
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In contrast to insects that produce silks in glands modified from some other
purpose, the Embiidina, an order of phylogenetically primitive insects, produce silk proteins in specialized tarsal glands that seem to have evolved solely
for this purpose. Embiid silks, like those spun by the derived holometabolous
Lepidoptera and Trichoptera larvae, are characterized by a parallel-β configuration.
Only the insects in the Embiidina, Hymenoptera, and Lepidoptera have
evolved spinning behaviors, a process in which the protein is stressed at secretion, forcing the molecules to shear and orient into the parallel-β conformation. Silk proteins characterized as random coil, α-helical, β-fibroin, and
cross-β configurations may be simply secreted, deposited or ejected; parallel-β
proteins are pulled. This suggests that the most important link between the
evolution of silks in primitive and derived forms lies not only in the amino acid
sequence of the protein but also in the behavior by which the silk is manipulated
or spun at secretion.
Spiders have as many as nine different silk glands (42) and some spiders are
able to produce as many as nine different types of silk protein (49). Unfortunately, so little information is available on the diversity of spider silk proteins
that it is not possible to determine if there have been any particular patterns
suggesting how silk molecular structure evolved.
PHYLOGENY-BASED RECONSTRUCTION
OF SILK EVOLUTION
When viewed within the Insecta and Araneae, silks seem to have evolved multiple times. Silks are produced in different glands and have diverse molecular
structures and diverse functions. This section presents a series of cladistic tests
and analyses that were carried out to better understand the apparently sporadic
appearance of silks across insect taxa, and to gain insight into the overwhelming
effect silks have had on the biology and evolution of spiders. First, to determine if there was any pattern suggesting how the protein might have evolved,
the molecular structure of silks, the gland from which they are derived, and
their function were mapped onto a recent phylogeny of the insect orders (50;
Figure 3). A comparable analysis on the molecular configuration of silks spun
by spiders is not available. Furthermore, detailed studies of spider spinnerets
and spigots have been used to draw the most recent phylogenies of spider taxa
(13a, 41, 72), thus prohibiting an independent test of their evolution. However,
data on the reflectance properties (due to structural color) of spider silks, suggesting differences in the molecular organization of the protein, have recently
been analyzed and are reviewed.
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EVOLUTION OF ARTHROPOD SILKS
247
Recent systematic analyses making use of both morphological and molecular
data suggest that the arthropods are a monophyletic clade and that their sister
group is the Onychophora (104). Therefore, information regarding the production of fibrous proteins was superimposed on this recent phylogeny to determine
if the fibrous proteins produced by insects and spiders might have a common
evolutionary origin. All results are dependent on the phylogenies used.
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Silks Spun by Insects
The cladograms in Figures 3–8 represent a conservative hypothesis of the higher
order relationships among the Hexapoda (subsequently broadly referred to as
insects) (50). Because the phylogenetic relationships among the insect orders
Orthoptera, Dermaptera, Plecoptera, and Dictyoptera are unresolved, they were
excluded from the final analysis. In addition, the analyses also excluded the insect orders Mecoptera, Raphidoptera, Strepsiptera, and Megaloptera for which
the data were incomplete. Although fibrous proteins are secreted by both ancestral and derived insects, most X-ray crystallographic data are only available
for insects in the neuropteroid orders. Therefore, when an insect was known to
secrete extracellular fibrous proteins but of unknown structure, it was coded as
“fibrous” (see Appendix for data matrix).
The ancestral character states for silk structure, function, and gland were
inferred using MacClade 3.05 (56) and its Equivocal Cycling procedure was
Figure 3 Insect phylogeny used. Redrawn from Ref. 50.
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Figure 4 Presence or absence of secreted fibrous proteins across hexapod taxa. The ability to
secrete fibrous proteins has evolved multiple times across hexapod taxa.
used to determine the most parsimonious reconstruction for each. Some of the
insect orders included (a) taxa that produce silks characterized by more than
one macromolecular configuration, (b) taxa that produce silks as larvae and
adults but in different glands, and (c) taxa that used silks for more than one purpose. When terminal taxa were polymorphic for a given character, all character
states were encoded to correctly infer ancestral states (66). Polymorphisms in
the molecular configuration of silks were found among the Hymenoptera and
Diptera and the type of silk-producing larval gland in the Hymenoptera, Neuroptera, and Coleoptera, but ancestral character tracing yielded only one most
parsimonious evolutionary reconstruction.
Phylogenetic comparison across insect taxa suggests that the ability to secrete fibrous proteins is a primitive feature of the hexapods (Figure 4). More
specifically, silk production evolved first among adult hexapods, reflecting its
use in reproduction and was later lost and regained multiple times (Figure 5).
Among larvae, silk production evolved sporadically (Figure 6). However, all of
the most derived holometabolous insect larvae produce silk proteins that they
use for protection (Figure 7).
The evolution of silk producing glands is equally complex. At least five
taxa of adult insects produce silks in colleterial glands, and colleterial silk
production has been lost and regained at least once (Figure 5). Among larvae,
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EVOLUTION OF ARTHROPOD SILKS
249
silk production in Malpighian tubules evolved early in the Ephemeroptera, was
lost and later reappeared sporadically (Neuroptera, Coleoptera) across the insect
orders. Labial silk glands evolved only twice, once in the Psocoptera and later
in the derived, holometabolous insect larvae (Figure 6). Only the Embiidina
and the Diplura have the ability to produce silks throughout their lifespan. The
Diplura produce silks in their anal glands and the Embiidina draw silks from
specialized dermal glands.
The phylogenetic analyses suggest two evolutionary origins of the parallel-β,
fibrous proteins (Figure 8). First, silks of this highly ordered β-configuration
evolved in Embiidina where they are produced in specialized dermal cells.
The β-fibroin silks are produced by most holometabolous larvae, but it is only
in the Trichoptera and Lepidoptera that larvae have evolved the specialized
spinning behavior that allows them to draw the silks into parallel-β–pleated
sheet crystallites.
SILK PROTEINS AS SECONDARY SECRETIONS For most insect groups, silks evolved as secondary products of insect reproductive and excretory systems and
were first used for reproductive purposes (77). For example, males in the
Figure 5 Silks produced by adult hexapods (12 reconstructions). Silk production among adult
hexapods is less common than among larvae, and all silks are secreted from glands that evolved for
some other primary purpose. Most frequently silks are produced by adults in colleterial glands.
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Figure 6 Silks produced by hexapod larvae. Silk production is common among hexapod larvae.
The most prolific silk producers, the Embiidina and Lepidoptera, have evolved dedicated silk
glands.
primitive Apterygote order Thysanura (the bristletails) produce protein secretions in accessory genital glands. The secretions are drawn into threads used
to restrict females during mating (84). Female mantids (Dictyoptera : Mantoidea, not included in final systematic analysis because of polytomy) produce colleterial gland silks they use to protect their eggs, as do Hydrophilus
piceus (Coleoptera : Hydrophilidae) (82, 93). Adult Chrysopa flava (Neuroptera : Chrysopidae) produce colleterial gland silks from which they construct an egg sac stalk (54, 82, 86). Colleterial gland silks are characterized as
having either a cross-β [Coleoptera (82)] or α-helical configuration. With the
exception of those produced by male Thysanura (91), none of the colleterial
gland silks are delivered through a specialized spinning organ. Furthermore,
only adult insects produce silks in their colleterial or accessory genital glands,
perhaps a reflection of their uses and their link to a mature reproductive physiology.
Silks as secondary secretions are also produced in some insect excretory systems, primarily by larval insects in the orders Coleoptera and Neuroptera. In
most cases their silks are used for protection. Larvae of the phylogenetically
ancestral stingless bee, Plebeia droryana, and the bumble bee, Bombus atratus,
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EVOLUTION OF ARTHROPOD SILKS
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produce cocoon silks, making use of Malpighian tubule secretions (38). In contrast, Hypera postica [Coleoptera (46, 86)] produce cocoons from Malpighian
silks (cross-β conformation) that are characterized by loosely fabricated networks of coarse brown fibers. Larvae in the phylogenetically primitive neuropteran suborders of Megaloptera and Raphidioidea produce Malpighian silks
as well (13, 93); their conformations have not been identified. Insects in the
Neuroptera produce silks both as larvae and adult, but they are products of different organs. For example, Malpighian silks are produced by larval chrysopids
whereas colleterial gland silks are produced by adults. Like most colleterial gland silks (with the exception of the Thysanura), none of the silks produced in insect Malpighian systems are delivered through a specialized spinning
organ.
Orthopterans in the superfamily Gryllacridoidea (not included in the final
analysis because of polytomy) are unique among in the Orthoptera in that they
produce labial gland secretions throughout their lives (75). Although, like many
fibrous proteins, their molecular structure has not been determined, they have
been identified as silks on the basis of their general appearance. Camptonotus
carolinensis use silks to roll and bind leaves together; Cnemotettix sp. constructs
Figure 7 Function of silks produced by hexapods. Silks were first used for reproductive purposes
and later for protection. Only the Trichoptera (which make aquatic capture nets) and the Lepidoptera
(which manipulate plant resources) have evolved to use silks in foraging.
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Figure 8 Structural configuration of silks produced by hexapods (2 reconstructions). In most
cases the structural configuration of silks produced by hexapods has not been determined. The
Hymenoptera produce the greatest diversity of silks. Parallel-β silks only evolve in hexapods that
are able to produce both their peculiar molecular sequence and a means of shearing the protein
upon secretion.
a vertical, cylindrical burrow in which it “sews” small packets of sand grains
that it fits into the burrow ceiling or wall (64). Bothriogryllacris brevicauda
uses silks to tie a pebble or soil cap to seal off its burrow to protect against
desiccation.
SILK PROTEINS AS PRIMARY SECRETIONS Silks produced in dedicated silk
glands (glands that serve solely to produce silk) are used mainly for protection.
Character reconstruction shows that with the exception of the silks produced by
Siphonaptera, all labial gland silks are some type of parallel-β fibroin. Furthermore, with the exception of the Embiidina and a few Psocoptera, the only insects
that produce labial gland silks are those whose development is holometabolous
(Figure 6). Labial gland silks have evolved in some of the Paraneoptera, and
insects in the Psocoptera have silk glands similar to those of caterpillars (77).
In particular, Psocidae cover their eggs with silks, Philotarsidae spin webs
singly or gregariously in small groups, and Archipsocidae spin extensive webs
covering trunks and branches of large trees (92, 93). Representatives of all endopterygote insect orders (Hymenoptera, Diptera, Siphonaptera, Trichoptera,
and Lepidoptera) are characterized by the ability to produce labial gland silks.
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EVOLUTION OF ARTHROPOD SILKS
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In summary, all silk proteins are produced in cells whose lineage is ectodermal. Most insects produce silk proteins in glands that have been modified from
some other function. Silks evolved first for reproductive purposes and were produced in the anal and colleterial glands. Later, silks were used for protection and
were derived from larval Malpighian tubules and labial glands. Although more
ancestral insects produce silks in colleterial glands and Malpighian tubules (77)
that are characterized by an α-helical or cross-β conformation, holometabolous
larvae produce labial gland silks characterized by parallel-β conformations.
Only the paurometabolous Embiidina are able to produce silks characterized
by a parallel-β conformation throughout their lifespan.
All of the parallel-β silks are pulled (spun) from a specialized orifice, in
contrast to the α-helical and cross-β silks that are deposited, secreted, or ejected.
It is significant to note that among insects, labial gland silks evolved late in
the hexapod clade and that these glands are found only among the larvae of
insects characterized by holometabolous development. The tarsal silk glands
of the Embiidina represent a unique evolutionary event in the history of the
hexapods. All hexapod silk delivery systems (or spinnerets) are simple cuticular
hardenings or pores (68).
Silks Spun by Spiders
The most prolific silk producing glands of the spiders are located in the opisthosoma (posterior portion of the body behind the cephalothorax or prosoma) and
are tubular or acinous in form. The opisthosomal silk glands include the piriform, aciniform (both acinous), ampullate, aggregate, flagelliform, and tubuliform (all tubular glands). All of these glands are dedicated to the production of
silk proteins and are thought to have evolved de nova, i.e. antecedent glands are
unknown (68). The spinnerets through which these silks are spun are located on
the fourth and fifth opisthosomal segment. Acinous, epiandrous (abdominal)gland silks, common to most males, are located on the anterior rim of the
epigastric furrow and open through simple spigots. Although the histochemical characteristics of the epiandral glands are the same for all spiders that have
been studied (49), the characteristics of all other glands are variable among
spider taxa.
The cribellate spiders belong to several unrelated families and are differentiated from other araneomorphs by the presence of a cribellum. The cribellum,
a sclerotized plate located in front of the anterior spinnerets, is covered with
hundreds of very fine spigots (66a), each of which is supplied with silk from
a small acinous gland at its base (71). The capture threads produced by these
spiders include two or four axial fibers (24) that may be produced in the sinuous
pseudoflagelliform gland and are surrounded by masses of tiny silk fibrils. The
tiny silk fibrils are brushed from the cribellar spigots by means of a calamistrum,
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a series of stout setae, located on each fourth leg. A third component of the capture thread, the paracribellar fibrils, are drawn from acinous paracribellar glands
that open through long articulated spigots on the posterior median spinnerets
(49) and link the two axial threads (71).
The modified cheliceral glands of spiders in the family Scytodidae produce
fibrous proteins of undetermined structure. These glands, unique to this family
of spiders, are homologous to insect labial glands (49). The cheliceral glands
are the only silk glands of spiders that are thought to be derived from the
modification of an existing gland, the labial glands. A possible reflection of
this is that the abdominal spigots (and presumed glands) of the Scytodidae
are highly reduced to include primarily piriform and aciniform spigots (72).
Prosomal glands have also evolved independently in the Acariformes as well
as in all pseudoscorpions (49).
Cladistic analysis of silks produced in the ampullate, tubuliform, cribellar,
pseudoflagelliform, paracribellar, and flagelliform gland silks of mygalomorph
and araneomorph spiders shows great variation in their optical properties and
would most likely show the same degree of variation in their molecular conformations (Figure 9). Reflectance of silks in the ultraviolet (UV) region of the
spectrum seems to vary systematically. In particular, the prey capture silks and
retreat silks produced by the ancestral mygalomorph spiders, ancestral araneomorph spiders, and ancestral, aerial web-spinning spiders are characterized by
high UV reflectance. In contrast, the prey capture silks produced by the more
derived araneomorph spiders, as well as some of the derived web-spinning spiders, are spectrally flat. Other derived web spinners produce catching threads
characterized by reduced UV-reflectance. Multiple silk producing glands allow the derived spiders to spin multiple kinds of silks (17, 18). The derived,
aerial web spinners have a unique set of glands, the flagelliform glands, from
which a new type of protein is drawn. The evolution of the flagelliform silks
and aggregate glands correlates with a 37-fold increase in species number and
apparent habitat expansion among the araneoids (19).
Fibrous Proteins Produced by Other Members of the Phylum
Arthropoda and Their Probable Sister Taxon, the Onychophora
In the phyletic hypotheses proposed by Wheeler (104), the Arthropoda include
the Trilobita, Chelicerata, Crustacea, Myriapoda, and Hexapoda. The Crustacea secrete collagens that are considered proteins (100), but are not silks.
The Trilobita, also marine, are known only from the fossil record, and whether
they secreted protein or not is unknown. Male myriapods secrete fibrous proteins from their accessory glands that they use to produce sperm webs, sperm
stalks, and mating threads. Females in the Diplopoda and Symphyla also
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EVOLUTION OF ARTHROPOD SILKS
255
produce fibrous proteins they use for moulting, egg cocoons, defense, and
communication. Regrettably, none of the macromolecular configurations of
any of the fibrous proteins produced by the myriapods have been identified
(68). The slime gland secretions of the Onychophora, sister group of the monophyletic arthropod clade, are also of unknown molecular configuration but may
be classified as fibrous on the basis of scanning electron and transmission electron photomicrographs of ejected threads. These secretions are stored and
ejected as a fluid that solidifies into sticky white threads when exposed to air
(94).
The available data do not lend cladistic support to a hypothesis suggesting that silks produced by the arthropod taxa are derived from their proposed
onychophoran-like ancestor (Figure 10). However, this may reflect the lack
Figure 9 Spectral properties of silks and spider foraging environments mapped onto a cladogram
of the order Araneae (from Ref. 19).
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of information available and, in particular, the fact that only recently have the
molecular tools needed to test this idea become available. In particular, information on the molecular processes that regulate silk gland development are
needed. If these data were available, they might suggest that the structural
and functional diversity of arthropod silk systems, like the diversity of arthropod appendages (70), result from regulatory shifts in the expression of genetic
information.
The glands in which silks are produced and the structural types of silk have
evolved multiple times across the insect taxa. Silk production is not a defining
character of the insects. In contrast, silk production is an identifying feature of
the spiders, and silks are produced by even the most primitive spiders throughout their lives. Spiders, too, produce silks in many different glands, suggesting multiple evolutionary origins. However, unlike the insects, spiders retain
glands that are both primitive and derived within a single species and individual.
X-ray crystallographic data on most silks are lacking, but samples on silks drawn
from the ampullate, tubuliform, and flagelliform glands suggest that these are
characterized by parallel-β configurations.
Silk proteins flow from a reservoir in which they are stored through a narrow constriction or nozzle (47). A pressure gradient between the reservoir and
nozzle, plus tension applied to the silk as it is drawn or “spun,” orients and
shears the molecules, causing them to polymerize (47) into a fiber (57). Shear
rate (force · area−1 · time−1 ) is a function of the morphology of the silk
Figure 10 Presence of secreted fibrous proteins among members of the monophyletic clade
Arthropoda and their sister outgroup, the Onychophora.
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EVOLUTION OF ARTHROPOD SILKS
257
gland (for example, globular, tubular, or sinuous), the morphology of the spigot
(length and cross-sectional area of the aperture through which the protein is
expelled), and the speed at which the protein is pulled. The animal’s ability to
control the shear rate influences the regularity of the thread surface, the diameter
of the fiber, and the phase composition of the protein (57). Even though some
insects, like Diptera and Coleoptera, are able to produce silks in a β-fibroin
conformation, insects in neither of these groups have evolved a means of spinning or shearing the protein to orient its molecules into a parallel-β pleated
configuration.
Insects in only four different orders, the Lepidoptera, Trichoptera, Hymenoptera, and Embiidina, produce silk in the highly ordered, parallel-β configuration, and in each of these groups, a different method of spinning has
evolved. Among the most derived silk-spinning insects, the Lepidoptera, a vigorous, repeated figure-eight motion of the silkworm’s head draws the viscous
protein from the spinneret, stretches, and shears it (57). Although the Lepidoptera are able to regulate the release of the silks and shape of the emerging
threads, they are unable to stop the flow of silk by any means other than biting or breaking the silk strand (30). Although larval weaver ants (Oecophylla;
Hymenoptera) have not evolved the ability to spin silks, parallel-β fibroins are
produced when mature ants hold silk-secreting larvae in their mandibles while
shuttling them back and forth across a surface (45). By manipulating a larva
that is releasing liquid silk, tension is applied to the protein stream; this orients
the molecules in the direction in which the larvae are drawn. The resulting
silk threads pull and bind nest leaves together. The third group of insects able
to produce parallel-β silks are the Embiidina. Specialized dermal cells located
on the insect’s foretarsi are armed with setae-like ejectors. Silk proteins are
expelled when the setae are swept across a stone, grass, or bark surface (79),
and the subsequent mechanical shear causes the silk protein to organize into
the parallel-β configuration.
The ability to produce silks throughout their lives defines the uniqueness of
the clade Araneae (49). Some types of spider spinnerets, for example those
that serve the specialized labial, cribellar, and epiandral glands, seem to be
hollow setae and thus are similar to the fixed cuticular extensions or epidermal
modifications that are characteristic of all insect spinnerets as well as those of
the Acarina and Pseudoscorpiones (see references in 49, 87). However, the
key feature that distinguishes spiders from all other silk secreting arthropods
is the muscular, innervated spinnerets that serve the opisthosomal silk glands
that the mygalomorph and araneomorph spiders hold in common. The sensory
capability of these, their ability to move independently of the spider’s body,
and the spider’s ability to adjust the size of the spigot allow great control over
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the rate at which the proteins are released and the properties of the threads that
are spun. As a result, spiders have great flexibility with respect to the types and
character of the threads they spin. Insects are constrained to produce a much
more limited kind of thread.
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Current Hypotheses Regarding the Evolution of Silk Glands
and Spinnerets in Spiders and Insects
In 1932, Bristowe proposed that spider spinnerets evolved from modified leg
segments and the spigots through which silks were delivered derived from
simple hairs (9). Recent studies have suggested that silk producing glands
of spiders are derived from epidermal invaginations (49, 68). This view has
been supported by the proposal that the protein-secreting, epiandral glands of
most male spiders are known to be derived from dermal glands (49). Several
investigators have proposed that these are homologous with the “true” silk
glands of spiders, the opisthosomal or abdominal glands (reviewed in 87).
This hypothesis has been further extended to suggest that the silk-producing
systems of spiders are most similar to the dermal silk-producing system of the
Embiidina (68). A third hypothesis also proposes that the glands are epidermal
invaginations but suggests that the spigots originated as sensory hairs and not
simple hairs. This is based on the fact that the silk spigots of mygalomorph
spiders are morphologically similar to chemoreceptors and are characterized
by well-developed slit sensilla at their base (68).
Proposed Evolution of Arthropod Silks
The production of highly ordered, parallel-β silk proteins, requires the confluence of three events: the evolution of the protein, the evolution of a spinneret,
and the evolution of a specialized spinning behavior. The data accumulated in
this article indicate that although both spiders and insects have met these requirements, spiders have been more successful in silk production, as reflected
in number and types of proteins they spin. Three groups of insects, however, may match, if not exceed, spiders in the energy they invest in fibroin
production: the Embiidina (phylogenetically primitive, paurometabolous and
flightless), the Trichoptera, and larval Lepidoptera (phylogenetically derived,
holometabolous, and having larval silk production). Because dedicated silkproducing glands, reproduction, and flight are high energy activities, it may be
that arthropods cannot meet all three energetic demands at once. Instead they
can either reproduce and spin silk (Embiidina, Siphonaptera, and spiders) or reproduce and fly (Paraneoptera). However, after insects evolved holometabolous
systems in which flight and reproduction are isolated from development, silk
production once again became accessible and important.
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EVOLUTION OF ARTHROPOD SILKS
259
Figure 11 Proposed pathways for the evolution of silk proteins produced by insects and spiders.
Glands indicated in bold are dedicated to the production of silk; glands indicated in italics produce
silk as a secondary function.
PROTEIN-PRODUCING GLANDS I propose that silk producing systems seem to
have evolved via two different pathways (Figure 11): a surficial pathway (for
example, epidermal invagination and dermal cell modifications) and a more
complex, systemic pathway (for example, a dedicated silk producing system
such as the salivary glands). The morphological similarities of the following groups suggest that these glands are homologous and may characterize
a surficial silk production system: the simple undifferentiated glands of the
liphistiomorph and mygalomorph spiders; the differentiated piriform, acinous,
cribellar, and epiandral silk glands of the araneomorph spiders; and the dermal glands of the Embiidina, Empiidae (Diptera), and some Hemiptera. The
proteins produced in these glands appear fibrous, but not all exhibit the highly
ordered, parallel-β configuration. Silk production via a surficial pathway is
possible among arthropods with all types of development, and dermal silk producing glands have evolved in adults or larvae.
Silk production seems also to have evolved via a systemic pathway (Figure 11) and includes both primary glands (dedicated silk glands) and secondary
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glands (produced in an organ with some other primary function). All of the
silks produced in primary systems are characterized by a parallel-β configuration. These include the ampullate, tubuliform, and flagelliform glands of
spiders and the labial glands of the holometabolous insects. All of these glands
are characterized by an elongated, and in some cases sinuous, morphology that
is likely to be important in protein processing and storage. Additional silks are
produced via a secondary, systemic pathway. Silks produced by these pathways
are characterized by α-helical or cross-β configurations. In these cases silks
are produced in some region of a gland that serves some other primary function. Secondary systemic systems include the Malpighian tubules, colleterial
and anal glands.
SPINNERETS Silks are delivered in two ways, via cuticular spigots (present in
all insects and spiders) or through a flexible spinneret and spigot (present in no
insects but in all spiders, Figure 11). The proposed surficial and systemic origins
of silk producing glands outlined above, however, do not track directly with
the evolutionary origins of these systems. In particular, insects deliver their
silks through spigots derived from cuticular pores, hardenings, or modified
hairs; none of their spigots are muscular and none are innervated. Only the
Lepidoptera are able to control fiber diameter via a “silk press” or muscle
located between the anterior silk gland and the cuticular spinneret. After passing
through the press, the larva has no further control of the silk and is only able to
stop protein flow by jerking its head or using its forelegs to break the thread.
Thus, insects spin silks in the absence of any sensory feedback.
In contrast, all spiders are characterized by muscular spinnerets that function
in association with a spigot. These systems could have evolved in two ways.
Some spigots seem to be derived from simple hairs (68) and are likely to include
those associated with the epiandral, cribellar (surficial), and labial (systemic)
glands. Other spigots are probably derived from sensory hairs (68) and are likely
to include those associated with the tubiliform, ampullate, and flagelliform
glands. Spigots that are innervated supply sensory feedback regarding protein
type, stream diameter, and flow rate. This information, coupled with a muscular
spinneret that moves independently of the animal’s body, allows great flexibility
in fiber production.
SPINNING The third event critical to the evolution of silk production in arthropods is the evolution of silk-spinning behavior. The Lepidoptera have evolved
the most complex uses of silks for communication (31), manipulating their
environment (6), and protection (83), yet they have not evolved diverse silkspinning behavior. This may follow from the similar mechanical requirements
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EVOLUTION OF ARTHROPOD SILKS
261
of lepidopteran silks (68); once the protein evolved, further modifications do
not seem to have been important. In contrast, the derived, aerial web spinners
vary over an order of magnitude in body size and produce nets that also vary
over an order of magnitude in size and kinetic properties (15, 16). All of the
aerial web spinners have evolved a rich repertoire of spinning behavior that
determines the rate that the proteins are sheared, which contributes to their
material properties. In fact, consistent variations in spinning behavior across
spider systematic groups (13b, 23) suggests that spinning behavior is a likely
target for evolution by natural selection.
Proposed Crural Gland Hypothesis
The Onychophora, considered by some authors to be the connecting link between the Annelida and Euarthropoda (94), are considered to be the sister
outgroup of the monophyletic clade that includes the Arthropoda and Chelicerata (70, 104). The onychophorans have a cylindrical body 5 mm to
15 cm long and a trunk bearing 13–43 pairs of short, conical, unsegmented
legs (lobopods). The cuticle is chitinous and covered with large and small
papillae, the larger terminating in a sensory bristle and the smaller terminating
with a simple hair.
Multiple crural glands are characteristic of this ancient phylum. These glands
are located at the base of each leg and secrete an acidophilic compound. The crural glands have been a source of evolutionary innovation for the Onychophora.
For example, the crural glands of the anterior appendages are modified into
labial slime glands that eject protein glues used for defense and predation. The
glands of posterior segments are modified to be accessory genital glands and
anal glands (males only) (94). All of these systems have been modified for silk
production in the insects, i.e. the labial glands, colleterial glands, anal glands,
and Malpighian tubules, implying that they may have shared a common evolution with crural glands. Furthermore, it may be that the proteins the crural
glands secrete are homologous with the proteins secreted by arthropod systemic
silk systems, including insect labial gland silks and spider cheliceral, tubuliform, ampullate, flagelliform, and pseudoflagellar silks. Therefore, protein
secretions for defense, reproduction, and foraging must have evolved multiple
times, been lost multiple times, and, in some cases, reappeared.
Spinnerets, the muscular, conical organs on which the spigots sit, are a
specialized component of spider silk delivery systems not found in insects.
Embryological data show that spinnerets are homologous with other arachnid, prosomal appendages, including chelicerae, pedipalps, and walking legs
(20). On this basis, investigators have proposed that spinnerets have arisen
from segmented appendages later modified for silk delivery (87). The lateral
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spinnerets of the spider, Liphistius spp., however, are not similar to the segmented appendages of arthropods but instead are more similar to a lobopod appendage (68) as exemplified by their probable sister group, the Onychophora (104). These two views are reconciled with the current finding
that the diverse limbs of the insects, crustaceans, myriapods, and chelicerates can all be attained through temporal and spatial control of the homeotic
gene Distal-less (Dll) (70). Therefore, both segmented and lobate spinnerets
can be derived from a primitive lobopod appendage such as that of the Onychophora.
In summary, the comparative approach taken in this study, together with
recent information on the developmental and molecular regulation of arthropod systems, suggests that the silk secreting systems of spiders and insects
are linked to the crural and cuticlar sections of an onychophoran-like ancestor.
Silk secretion has evolved multiple times and through two different pathways,
a surficial pathway or a systemic pathway. Silk secreting glands that evolved
via a surficial pathway are possible in adult and larval arthropods, regardless
of their developmental mode. Silk secretion glands that evolved via a systemic
pathway are possible only in adults when development is paurometabolous, and
these are only found in the spiders. In holometabolous insects, systemic silkproducing systems are limited to larvae. In addition, spiders differ from insects
in the number and types of silk producing glands. Insects have either systemic
or surficial silk-producing pathways; mygalomorph and araneomorph spiders
retain both. Hence, there is a correlation between silk production method and
developmental mode that may reflect the energetic demands of flight, reproduction, and silk production. Finally, the evolution of muscular and innervated
spinnerets and their probable derivation from a primitive lobate appendage
suggests that the temporal and spatial expression of the homeotic gene Dll that
is responsible for the diversity of arthropod limbs has also been important to
the evolution of the spinnerets and hence the diverse silk-spinning systems of
spiders.
ACKNOWLEDGMENTS
I am grateful to RS Weber for our many discussions on the molecular properties of proteins and the evolution of silks and to P Jennings, A Brower, JA
Coddington, J Haupt, BD Opell, and NE Pierce for comments on the manuscript.
This work was supported by the AP Sloan Foundation, the John Simon Guggenheim Foundation, the Office of Naval Research, and the Mary Ingraham Bunting
Institute of Radcliffe College, Harvard University.
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APPENDIX
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Data matrix for cladistic analysis
Taxa
Silk present Adult glands Larval glands
Collembola
Protura
Diplura
Absent
Absent
Present
Absent
Absent
Anal
Absent
Absent
Anal
Microcoryphia
Thysanura
Ephemeroptera
Odonata
Embiidina
Zoraptera
Psocoptera
Pthiraptera
Hemiptera
Present
Present
Present
Absent
Present
Absent
Present
Absent
Present
Thysanoptera
Neuroptera
Present
Present
Unknown
Colleterial
Absent
Absent
Dermal
Absent
Labial
Absent
Absent
Dermal
Absent
Colleterial
Coleoptera
Present
Colleterial
Siphonaptera
Diptera
Present
Present
Absent
Absent
Dermal
Absent
Absent
Malpighian
Absent
Dermal
Absent
Labial
Absent
Absent
Dermal
Absent
Absent
Malpighian
Absent
Malpighian
Labial
Labial
Absent
Labial
Trichoptera
Present
Colleterial
Labial
Lepidoptera
Present
Absent
Labial
Hymenoptera
Present
Colleterial
Absent
Labial
Function
Absent
Absent
Reproduction
Protection
Reproduction
Reproduction
Protection
Absent
Protection
Absent
Protection
Absent
Protection
Silk type
Reference
Absent
Absent
Fibrous
39
39
14
Fibrous
Fibrous
Fibrous
Absent
Parallel-β
Absent
Fibrous
Absent
Fibrous
93
84, 91
93
93
25, 26, 93
93
43
93
77
Protection
Fibrous
Reproduction Cross-β
Protection
Protection
Cross-β
Protection
Reproduction
Protection
Foraging
Protection
Foraging
Protection
Foraging
Dispersal
α-Helical
Fibrous
Cross-β
Protection
Fibrous
α-Helical
Parallel-β
Parallel-β
Parallel-β
93
10, 13, 54, 82,
86, 93
46, 59, 62, 82,
85, 86
55, 82, 93, 102
5, 26, 46, 51, 53
74, 76, 81, 82
86, 93, 103, 106
38, 67, 82, 93,
105, 107
6, 7, 12, 29, 52,
54, 55, 73, 78
82, 83, 93, 102
109
1, 4, 27, 28, 30,
43, 53, 54,
60, 61, 80, 82,
86, 90, 93, 108
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Annual Review of Entomology
Volume 42, 1997
CONTENTS
Annu. Rev. Entomol. 1997.42:231-267. Downloaded from arjournals.annualreviews.org
by University of California - Irvine on 05/16/09. For personal use only.
J. S. KENNEDY (1912–1993): A Clear Thinker in Behavior's Confused
World, John Brady
1
ADAPTATIONS IN SCALE INSECTS, Penny J. Gullan, Michael
Kosztarab
23
ECOLOGY AND EVOLUTION OF GALLING THRIPS AND THEIR
ALLIES, Bernard J. Crespi, David A. Carmean, and, Thomas W.
Chapman
51
DIPTERA AS PARASITOIDS, Donald H. Feener Jr, Brian V. Brown
73
WILD HOSTS OF PENTATOMIDS: Ecological Significance and Role in
Their Pest Status on Crops, Antônio R. Panizzi
99
BEHAVIORAL MANIPULATION METHODS FOR INSECT PESTMANAGEMENT, S. P. Foster and, M. O. Harris
123
VISUAL ACUITY IN INSECTS, Michael F. Land
147
INTERACTIONS AMONG SCOLYTID BARK BEETLES, THEIR
ASSOCIATED FUNGI, AND LIVE HOST CONIFERS, T. D. Paine, K.
F. Raffa, T. C. Harrington
179
PHYSIOLOGY AND ECOLOGY OF DISPERSAL POLYMORPHISM
IN INSECTS, Anthony J. Zera, Robert F. Denno
207
EVOLUTION OF ARTHROPOD SILKS, Catherine L. Craig
231
INSECTS AS TEACHING TOOLS IN PRIMARY AND SECONDARY
EDUCATION, Robert W. Matthews, Lynda R. Flage, and, Janice R.
Matthews
269
LIFE-STYLES OF PHYTOSEIID MITES AND THEIR ROLES IN
BIOLOGICAL CONTROL, J. A. McMurtry, B. A. Croft
291
PHOTOPERIODIC TIME MEASUREMENT AND RELATED
PHYSIOLOGICAL MECHANISMS IN INSECTS AND MITES, Makio
Takeda, Steven D. Skopik
323
SYSTEMATICS OF MOSQUITO DISEASE VECTORS (DIPTERA,
CULICIDAE): Impact of Molecular Biology and Cladistic Analysis,
Leonard E. Munstermann, Jan E. Conn
351
HOST PLANT INFLUENCES ON SEX PHEROMONE BEHAVIOR OF
PHYTOPHAGOUS INSECTS, Peter J. Landolt, Thomas W. Phillips
371
MIGRATORY ECOLOGY OF THE BLACK CUTWORM, William B.
Showers
393
PHYLOGENY OF TRICHOPTERA, J. C. Morse
427
THE BIOLOGY, ECOLOGY, AND MANAGEMENT OF THE CAT
FLEA, Michael K. Rust, Michael W. Dryden
451
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by University of California - Irvine on 05/16/09. For personal use only.
BEHAVIOR AND ECOLOGICAL GENETICS OF WIND-BORNE
MIGRATION BY INSECTS, A. G. Gatehouse
475
BIONOMICS OF THE FACE FLY, MUSCA AUTUMNALIS, Elliot S.
Krafsur, Roger D. Moon
503
PERITROPHIC MATRIX STRUCTURE AND FUNCTION, M. J.
Lehane
525
GENETIC DISSECTION OF SEXUAL BEHAVIOR IN DROSOPHILA
MELANOGASTER, Daisuke Yamamoto, Jean-Marc Jallon, Akira
Komatsu
551
BIOLOGY OF WOLBACHIA, John H. Werren
587
BIOLOGICAL MEDIATORS OF INSECT IMMUNITY, Jeremy P.
Gillespie and, Michael R. Kanost, Tina Trenczek
611