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Silk Genes Support the Single Origin of Orb Webs

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Science  23 Jun 2006:
Vol. 312, Issue 5781, pp. 1762
DOI: 10.1126/science.1127946

Abstract

The orb web is a spectacular evolutionary innovation that enables spiders to catch flying prey. This elegant, geometric structure is woven with silk fibers that are renowned for their superior mechanical properties. We used silk gland expression libraries to address a long-standing controversy concerning the evolution of the orb-web architecture. Contrary to the view that the orb-web design evolved multiple times, we found that the distribution and phylogeny of silk proteins support a single, ancient origin of the orb web at least 136 million years ago. Furthermore, we substantially expanded the repository of silk sequences that can be used for the synthesis of high-performance biomaterials.

The spider orb web is an impressive example of animal architecture. This silken net consists of a frame and supporting radii overlaid with a sticky capture spiral. Because an orb web must absorb the enormous kinetic impact of flying prey, silks composing the web have exceptional mechanical properties (1). Orb weaving is characteristic of species in two lineages: Araneoidea and Deinopoidea (Fig. 1A). Araneoid and deinopoid orb weavers use nearly identical behavioral sequences and spinning apparatuses to produce architecturally similar webs. However, there are notable differences between the adhesive mechanisms of capture spirals spun by araneoids (aqueous glue) and deinopoids (dry fibrils) (2). Thus, the two types of orb webs were widely considered a dramatic example of convergent evolution (3).

Fig. 1.

Relationships of orb-weaving spiders and spidroins. (A) Deinopoid (purple) and araneoid (green) lineages (2), depicting inferred ancestral web and spidroins. Orb-web frame and radii composed of MaSp1 (blue) and MaSp2 (brown) are shown along with temporary spiral with MiSp (black) and capture spiral with Flag (red). (B) Summarized phylogeny of spidroin family members. The full tree is shown in fig. S2.

Spider silks are composed of proteins (spidroins) synthesized in specialized abdominal glands. Three types of glands produce the fibers used in orb-web construction: (i) major ampullates for frame and radial fibers, (ii) minor ampullates for temporary spiral scaffolding, and (iii) flagelliforms for capture spiral axial fibers (4). Whereas silk cDNAs were described from these glands in araneoids, none are known from deinopoids. If Araneoidea and Deinopoidea are sister taxa (Orbiculariae), then the simplest explanation for similarities between their orb webs is that they were acquired from a common orb-weaving ancestor (2). Thus, deinopoids are expected to have counterparts to araneoid silk proteins used in orb-web construction. To test this hypothesis, we characterized silk gland cDNAs from representatives of both deinopoid families: a net-casting spider, Deinopis spinosa (Deinopidae), and a feather-legged orb weaver, Uloborus diversus (Uloboridae) (5).

Among the deinopoid cDNAs, we identified the following orthologs of araneoid silks used in orb webs: (i) MaSp1 and MaSp2, major ampullate proteins of the frame and radii, (ii) MiSp, minor ampullate scaffolding protein, and (iii) Flag, flagelliform protein of capture spirals (4) (fig. S1). Given the diversification of silk glands and fiber types that accompanied spider evolution (6), the distribution of certain spidroins should uniquely define particular clades. Spidroins have been reported from six nonorbicularian species (4), but MiSp and Flag are exclusively known from araneoids, and major ampullate cDNAs that encode MaSp1-like spidroins but not MaSp2 are known from nonorbicularians. Because minor and major ampullate gland spigots are broadly distributed in nonorbicularians (6), the use of MiSp and MaSp1 by araneoids and deinopoids is interpreted as plesiomorphic. However, araneoids and deinopoids are united by their shared use of MaSp2. Moreover, araneoids and deinopoids are the only spiders that have flagelliform-like spigots and make capture spirals with silk from these spigots (2). The discovery of Flag and MaSp2 in deinopoids consequently identifies these spidroins as molecular synapomorphies (shared derived traits) supporting orbicularian monophyly.

Phylogenetic analyses of spidroin C-termini substantiate close relationships between deinopoid and araneoid spidroins used in orb webs (Fig. 1B). The analyses do not consistently recover a grouping of MiSp-like sequences, but the resulting trees do contain clades of the following: (i) deinopoid and araneoid Flag, (ii) deinopoid and araneoid MaSp1 and MaSp2, (iii) deinopoid and araneoid AcSp1 (prey-wrapping silk protein), and (iv) deinopoid and araneoid TuSp1 (egg-case silk protein). The collective combination of Flag, MiSp, MaSp1, and MaSp2 in araneoid and deinopoid spiders implies that the orbicularian ancestor was equipped with the molecular elements necessary for orb-web construction. Based on fossil evidence, this ancestor minimally dates from the Lower Cretaceous, 136 million years ago (7). Accordingly, the birth of Flag, MiSp, MaSp1, and MaSp2 must have occurred by this time. Since their ancient origins, these silks have diversified during the subsequent radiation of Orbiculariae (>10,000 species) (2), thus greatly expanding the designs available for the production of high-performance biomimetic materials.

Supporting Online Material

www.sciencemag.org/cgi/content/full/312/5781/1762/DC1

Materials and Methods

Figs. S1 and S2

References

References

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