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Foot Silk: Probably the Last Volley

Remember the controversy over whether tarantula feet produce silk? We posted a summary of the back and forth here last year. Rainer Foelix, Bruno Erb, and Bastian Rast have now published transmission electron micrographs that refute the foot-silk claim in Arthropod Structure and Development. Although the article is behind a paywall, you can look at their figures for free, and it's hard not to be struck with wonder at the complexity of some of these tiny structures.  Read More 
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At Last: Mesothele Silk

I’ve been waiting for years to learn something about mesothele silk genes and silk proteins. The 90 or so species of mesothele make up the oldest surviving spider lineage. They now live only in Southeast Asia. As we explain in Spider Silk, mesotheles are sometimes considered living fossils (a term biologists don’t like nowadays; it gives the false impression that the organism hasn’t evolved at all since some distant point in the past) because they display characteristics so similar to the characteristics found in a 290-million-year-old fossil mesothele and so dissimilar from more “modern” spiders. For one thing, unlike other spiders, their abdomens are segmented, an outward display of spiders’ descent from segmented ancestors. If we want a full picture of spider silk evolution, mesothele silk genes and proteins are an obvious place to focus.

James Starrett, Jessica Garb, Amanda Kuelbs, Ugochi Azubuike, and Cheryl Hayashi have, for the first time, looked at the sequence of mesothele silk proteins by synthesizing cDNAs from the silk glands of Liphistius malayanus, a mesothele. They also looked at the sequences of silk proteins of six species of mygalomorph spider—these are the spiders in the second major spider lineage, which includes the tarantulas.

Neither mesotheles nor mygalomorphs spin the kinds of webs most non-arachnologists think of when we think “web.” They are incapable, for example, of spinning the kind of silk araneomorph spiders (the third major lineage) use as dragline or rapelling rope. (This largely accounts for silk researchers’ relative neglect of mesotheles and mygalomorphs: there’s no obvious industrial or other money-making application of this research). Instead, these spiders use silk to create linings for their burrows, or above-ground tubes such as pursewebs, or sheets that spread away from the spider’s hiding place to create a prey detector.

The research team also looked at the sequence of silk proteins produced by Hypochilus thorelli, a lampshade spider, one of the earliest-evolved still-surviving araneomorph spiders. Unlike the mesotheles and mygalomorphs, Hypochilus produces different kinds of silk strands specialized for different tasks. The researchers state that the motive for their study is the belief that “characterizing silk transcripts in mesotheles, mygalomorphs, and a basal araneomorph lineage allows for a better understanding of the evolutionary transition from substrate-borne, general-use silk fibers to aerial webs with task specific fibers spun by orb-weavers.” In other words, ancient spiders may have produced multiple silk proteins, but they seem to have used them interchangeably. Later in spider evolution, spiders use specific silks for specific jobs. Can silk protein sequences tell us how spiders got from there to here?

Previous to this research, two different classes of silk protein had been identified: spidroins, or spider fibroins, which make up the bulk of spider silk fibers, and egg case proteins (ECPs). ECPs were identified only in 2005 (whereas spidroins have been studied for decades) and only in Latrodectus hesperus, the Western black widow. (Given how few spider families have been sampled, though, it’s quite possible other spiders also produce them.)

Back in the early 1990s, Joachim Haupt and Jacqueline Kovoor conducted histology and histochemical studies on mesothele silk glands that showed that these spiders produced more than one kind of fibrous protein. What makes Starrett’s team’s findings so interesting is not just that they confirm Haupt and Kovoor’s study, but also that they found such a large variety of recognizable silk proteins in the mesothele: a spidroin plus six ECP-like proteins.

This appears to confirm the hypothesis that spidroins evolved very early in spider evolutionary history. Arachnologists have long assumed that the “original” spider produced just one spidroin, and that the genes scripting later-evolved spidroins probably evolved from the gene scripting that original spidroin. This study found just one spidroin in a mesothele, which makes that assumption seem more likely.

At the same time, the presence of the ECP-like proteins in addition to the spidroin shows that silk proteins started to diversify quite early in spider evolutionary history. These mesothele ECP-like proteins, like the mesothele spidroin, contain little repetition compared to the araneomorph black widow ECPs. But the selection pressures on mesothele silks are quite different from the selection pressures on black widow silks. Mesotheles live underground in burrows, and their eggs are laid and covered in silk underground. Mesothele silk proteins may be selected to cope with dampness or dangers such as mold or interfacing with soil or underground predators and parasites, whereas black widow silks may be selected to cope with sunlight, aridity, attack by above-ground predators and parasites, and wind forces, among other challenges.

The big question is: Why did these silk proteins start to diversify in the first place? It’s possible that mesotheles are not quite so indiscriminate in their use of different silk proteins as we think. In black widows, the ECPs knit with a specialized spidroin called tubuliform silk to form egg casing. Neither mesotheles nor mygalomorphs produce tubuliform silk. The research team believes that, because both ECPs and the ECP-like proteins are rich in the amino acid cysteine, and because cysteine plays a role in the knitting together of black widow ECPs and tubiliform spidroin, the mesothele ECP-like proteins may knit with that spider’s spidroin. Does the mesothele tailor its protein mix to lay down, for example, an egg blanket versus a trap door?

That isn’t an easy question to answer. Araneomorphs’ specialized silks are produced in specialized glands, and they can be observed as they emerge from distinct spinnerets. Mesothele glands don’t seem much different from each other. And closely observing a mesothele laying down silk requires unusual dedication: they undertake housekeeping chores in the dark, stop when exposed to light, and also, unlike mygalomorphs and araneomorphs, their spinnerets are inconveniently (for observers, not for the spiders) placed under their abdomens instead of exposed out at the end. So whether he or she chooses dissection and RNA extraction or focused observation or both, some researcher is going to have to contract an obsession with this question before we get an answer.

It’s also possible that the early diversification of these proteins is related to the different amounts of energy required for their synthesis. Spiders not entirely dependent on any one protein in their heavy dependence on silk may have been able to weather fluctuations in prey capture more easily.

What is clear is that this early diversification of silk proteins shows once again that silk genes are evolvable; that is, they have a propensity for evolution—they can duplicate and change slightly but still be useful. Eventually, under the right circumstances, accumulated changes may result in proteins suited to specific tasks.

The research team’s analysis of the mesothele spidroin, the newly found mygalomorph spidroins, the newly found Hypochilus spidroin, and previously known spidroins supports this scenario. They believe that their analysis shows that the common ancestor of the opisthotheles (the combined mygalomorphs and araneomorphs) had a minimum of five related spidroin genes, meaning that this gene duplication occurred before the mygalomorphs and araneomorphs went their separate ways. Mygalomorphs, like mesotheles, have pretty uniform silk glands. So this would mean that spidroins diversified before glands evolved to be specialized.

ECPs and ECP-like silk proteins are probably also much more diverse—it strains belief that they are produced only by mesotheles and black widows, which are pretty distant relatives. It’s much more likely that, due to the way the cDNA synthesis process works, it’s possible the team sampled their mygalomorph and Hypochilus specimens at a time when the genes scripting ECP-likes or ECPs weren’t being expressed. We’ll only know for sure when genome sequences—rather than just cDNA sequences—are available for various spiders. Then we’ll also be able to see what, if any, evolutionary connections there are between ECPs and spidroins.

Besides these basic findings, this study found a number of other interesting details that should be of interest to silk specialists. And like all good research, it points the way to a number of further research questions, which the authors point out: We know that the number of repeats has an influence on silk fiber formation and mechanical properties, but what influence does the length of repeats have? Do the silks of different mygalomorphs have different mechanical properties, and how are those properties related to the molecular architecture of their silk proteins? And finally, once the mechanical properties and functional properties of mesothele and different mygalomorph silks are understood, how have those properties been influenced by the natural selection pressures exerted by life underground?

Once you get tangled up in spider silk research, there’s really no end to its fascination. Read More 
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Foot Silk Redux: Nope

In what looks to be the last word on the tarantula foot-silk controversy, Fernando Perez-Miles and David Ortiz-Villatoro take a firm stand with the title of their new paper in the Journal of Experimental Biology: "Tarantulas do not shoot silk from their legs." In our last post, we outlined why Rainer Foelix and his team contend that the supposed silk spigots described by research teams supporting the pro-foot-silk position are most likely chemoreceptor hairs. Now, Perez-Miles and Ortiz-Villatoro also dispute the earlier findings of foot-silk; they contend that the silk those researchers found is actually spinneret silk.

Back in 2009, Perez-Miles, Ortiz-Villatoro and two other colleagues challenged the original claim that the zebra tarantula produces foot silk, reporting that when they sealed the tarantula's spinnerets with paraffin before having it cling to vertical pieces of glass, they couldn't find any silk. When yet another team of researchers claimed to have found foot-silk left behind on glass by four different kinds of tarantula, they suggested that the Perez-Miles team might not have shaken the glass enough. In other words, maybe the spiders didn't feel the need to produce foot silk.

Now, Perez-Miles and Ortiz-Villatoro have more closely repeated the procedure of previous foot-silk finders, with four tarantula species. When they left the spinnerets unsealed, they found silk threads in the "footprints" left behind on the glass. When they sealed the spinnerets, they found none. Their conclusion: the footprints became contaminated with spinneret silk, which easily travels from spinneret to leg because it's so light.

In combination with the facts that no one can find silk glands in the spiders' feet and that the "spigots" have more in common with chemoreceptors than with spinneret spigots, this latest piece of research makes it seem highly unlikely that anyone will find spiders whose feet produce silk. Read More 
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Foot Silk: True or False?

Last summer, a team of researchers reported they had indeed found that tarantulas secrete silk from their feet. This appeared to settle a controversy that had started in 2006 when a different team reported finding foot silk. The original finding was bound to be controversial: no one had ever before observed the secretion of silk from the feet of any kind of spider. In 2009, a team investigating the first claim couldn't find evidence of foot silk. Last summer's report, which included a micrograph that seemed to show a blob of silk protein forming at the tip of a purported foot silk spigot, appeared to validate the 2006 report. (For a discussion of these three reports and of the questions concerning silk evolution they raise, see this earlier Spider Silk blog post.)

Well, there is now more evidence that tarantulas actually DON'T produce foot silk. Rainer Foelix is a leading spider anatomist and author of the must-have Biology of Spiders. When he examined the micrographs included in last summer's report, the alleged foot silk spigots looked like chemoreceptor hairs he had studied intensively in the 1970s. Kathryn Knight summarizes what Foelix did next. He, Bastian Rast, and Anne M. Peattie report their full findings in the April 1, 2012, issue of the Journal of Experimental Biology.

Foelix, Rast, and Peattie explicity address the questions concerning silk evolution that these earlier studies raised for us. They note that--even if the silk allegedly secreted through the foot "spigots" really is silk--all the tarantulas tested tend to stay close to the ground. It's not clear, then, what survival advantage foot silk would give them, particularly when the tiny amounts produced would add little cling compared to the spiders' already clingy adhesive setae, or hairs.

Most interesting to us, the team compared the feet of the tarantulas in their study to the feet of Liphistius desultor, a mesothele. As readers of Spider Silk know, mesotheles make up the oldest extant branch of the spider family tree. They live in burrows, rarely venturing more than a few inches beyond the burrow's trap door. Foelix, Rast, and Peattie state that Liphistius has no adhesive hairs on its feet. But it does have the same hairs that earlier researchers identified as silk spigots but that Foelix et al. are pretty convinced are chemoreceptors. The tiny amounts of "silk" produced from the hairs in question wouldn't allow the mesotheles to climb, even if they wanted to.

Next step in deciding whether the hairs in question on tarantula feet are silk spigots or chemoreceptors: testing them for sensory innervation with transmission electron micrography. Down the road, we wonder whether anyone will find any evolutionary connection at all--given the evolutionary relationship between limbs and spinnerets--between the proteinaceous fluid that apparently oozes from these hairs (which are also found on the spinnerets and all extremities) and the protein silk that is secreted through spinneret spigots.

As usual, the best research leads to more questions.  Read More 
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A neat little video from a couple of years ago that we somehow missed. Jonathan Coddington is one of the world's foremost arachnologists, and here he explains how photography gives today's araneologists an advantage over araneologists of the past. One quibble: Despite what Jonathan says, flying insects often do see webs. Why they still fly into them is a big research question we discuss in Chapter 10 of Spider Silk, "Now You See It, Now You Don't." Thanks to Bug Girl for bringing this video to our attention. Read More 
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Silkworms and Spider Genes

If you don't already follow Ed Yong's great Not Exactly Rocket Science, you've been missing some of the best science blogging around. Check out his latest post, on research involving the insertion of spider silk genes into the genome of silkworms. These silkworms produced silk that's an improvement (in human terms; silkworm silk works just fine for silkworms) over normal silkworm silk, but not really up to spider dragline silk standards. There are all sorts of possible reasons for this result; I give some of them in the comments section below the post.  Read More 
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Silk was one of the first fibrous proteins to be investigated in the early 20th century. Spider silk's exceptional properties have long inspired researchers from fields ranging from mechanical engineering to biotech. Now three MIT researchers from the Departments of Mathematics and Civil and Environmental Engineering have used a new concept called ontology logs, from the category theory branch of mathematics, to examine the relationship between spider silk's structure and function.

The really different aspect of this research? They conducted their examination by comparing spider silk and classical music. And they present their findings as a demonstration of a new way of gaining insight into various structures built on smaller and smaller substructures. Read more at MITnews.

The original paper, by Tristan Giesa, David I. Spivak, and Markus J. Buehler, is published in BioNanoScience. Read More 
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Feet and Glue

[This post contains later amendments that may be instructive to other science writers. See the later posts on purported tarantula foot silk to see why.]

Three papers published this summer might at first seem unrelated. But read together, they pull the entire arc of spider silk evolution into sharper focus. Two papers indirectly address the evolutionary origins of spider silk production. The other demonstrates that the evolution of silk proteins has been central to spider evolution even after the extraordinary proliferation of silks that made the vertical orb web possible.

First, F. Claire Rind and colleagues reported that at least some tarantulas (which belong to the family Theraphosidae) do indeed secrete silk from their feet. This report appears to settle a controversy that first broke out in 2006, when a team of researchers led by Stanislav Gorb announced that they had persuaded a Costa Rica zebra tarantula, Aphonopelma seemanni, to walk on a nearly vertical surface covered with glass microscope slides. The researchers claimed that as the tarantula started to slip, it left behind “footprints” made up of miniscule silk fibers. If this observation held true, it could have important implications concerning the origin of spider silk production. Like all spiders, tarantulas secrete silk through abdominal spinnerets, small appendages ending in multiple spigots that are the outlets for the abdominal silk glands. Genetic studies have shown that spider spinnerets are the evolutionary descendants of the gill branches of ancient arthropod limbs. If spiders secreted silk from their limbs as well as through their spinnerets, this fact might not only cement the limb-spinneret connection but also suggest new hypotheses for the earliest origins and survival value of spider silk.

The Gorb report left some questions open, however.  Read More 
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Here are links to two interesting blog posts about spiders likely to be encountered in many parts of the US at this time of year:

Bill Hilton, Jr., writes about a variety of spiders and their webs at This Week at Hilton Pond in a post titled "Spiders of August: The Case for Arachnophilia."

Bug Eric writes about Argiope aurantia. Eric writes about spiders most Sundays. Read More 
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Breathing, Underwater

A fascinating new study published in the Journal of Experimental Biology has found that the silk diving bell of the European water spider, Argyroneta aquatica, is more than just a bubble-holding net: it actually functions like a gill, drawing oxygen from the surrounding water.

You can watch a water spider in action here. Notice how it pops its abdomen above the water surface to gather more air to drag back to the diving bell. Read More 
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