Evolution of supercontraction in spider silk: structure–function relationship from tarantulas to orb-weavers

Abstract

SUMMARYSpider silk is a promising biomaterial with impressive performance. However, some spider silks also 'supercontract' when exposed to water, shrinking by up to ~50% in length. Supercontraction may provide a critical mechanism to tailor silk properties, both for future synthetic silk production and by the spiders themselves. Several hypotheses are proposed for the mechanism and function of supercontraction, but they remain largely untested. In particular, supercontraction may result from a rearrangement of the GPGXX motif within the silk proteins, where G represents glycine, P proline and X is one of a small subset of amino acids. Supercontraction may prevent sagging in wet orb-webs or allow spiders to tailor silk properties for different ecological functions. Because both the molecular structures of silk proteins and how dragline is used in webs differ among species, we can test these hypotheses by comparing supercontraction of silk across diverse spider taxa. In this study we measured supercontraction in 28 spider taxa, ranging from tarantulas to orb-weaving spiders. We found that silk from all species supercontracted, except that of most tarantulas. This suggests that supercontraction evolved at least with the origin of the Araneomorphae, over 200 million years ago. We found differences in the pattern of evolution for two components of supercontraction. Stress generated during supercontraction of a restrained fiber is not associated with changes in silk structure and web architecture. By contrast, the shrink of unrestrained supercontracting fibers is higher for Orbiculariae spiders, whose silk contains high ratios of GPGXX motifs. These results support the hypothesis that supercontraction is caused by a rearrangement of GPGXX motifs in silk, and that it functions to tailor silk material properties.

Wet webs work better: Humidity, supercontraction and the performance of spider orb webs

“…First, supercontraction of MA silk could prevent orb webs from sagging under the weight of dew drops by keeping the webs tense (Work, 1977). This hypothesis is consistent with the observation that, within Orbiculariae, orb-weaving spiders' silk supercontracts slightly more than silk from taxa that secondarily lost orb-weaving (Boutry and Blackledge, 2010). An alternative hypothesis argues that supercontraction plays an important role during the spinning of silk from liquid dopes by facilitating the alignment of molecules along the fiber axis, such that the water responsiveness of dry threads might be a 'non-adaptive by-product' for webs (Guinea et al, 2005).…”

“…This second hypothesis is supported by the observation that spiders using MA silk in a greater variety of contexts (e.g. in different web structures, as dragline and as safety lines versus only trailing draglines) produce silk that supercontracts more (Boutry and Blackledge, 2010).…”

“…During supercontraction, water infiltrates the silk and disrupts the hydrogen bonding that maintains much of the ordered tertiary structure in the amorphous regions of silk proteins (Eles and Michal, 2004;Grubb and Ji, 1999;Parkhe et al, 1997;Termonia, 1994). Unrestrained MA silk fibers consequently shrink by up to half their length, while restrained fibers instead develop high tension (Bell et al, 2002;Boutry and Blackledge, 2010;Savage et al, 2004). Supercontracted silk is also up to 1000 times more compliant and several times more extensible than dry silk (Guinea et al, 2005;Pérez-Rigueiro et al, 2003;Savage and Gosline, 2008a;Shao et al, 1999).…”

“…Furthermore, threads in webs are already under some tension (Wirth and Barth, 1992), while studies of isolated silk typically start with fully relaxed threads. The stress generated by supercontraction declines strongly with initial tension (Boutry and Blackledge, 2010). Thus, it is difficult to predict the behavior of a whole orb web from isolated threads.…”

Parasitoid suppression and life-history modifications in a wolf spider following infection by larvae of an acrocerid fly

“…The process is driven by increases in entropy, and the rearrangement of silk molecules occurs quite rapidly. Supercontraction can ultimately cause silk to shrink by up to 50% of its length or to generate substantial forces in confined threads (Work 1981;Boutry & Blackledge 2010). Once a thread has shrunk to its maximally contracted state, it can no longer supercontract unless external forces are applied (Blackledge et al 2009a), although the silk continues to show a cyclic swelling and contraction that has been implicated for biomimetics ).…”