Expansion and intragenic homogenization of spider silk genes since the Triassic: evidence from Mygalomorphae (tarantulas and their kin) spidroins.

Spiders spin a diverse array of silk fibers that are predominately composed of repetitive proteins (spidroins) encoded by a gene family. Characterization of this gene family has focused on spidroins synthesized by the Araneomorphae (true spiders), whereas only a single sequence is known from the Mygalomorphae (tarantulas and their kin). To better understand the diversity and evolution of the spidroin gene family, we surveyed the silk gland transcriptomes of 4 divergent mygalomorph species. Through expressed sequence tag screening and probing of silk gland cDNA libraries, we discovered 6 novel mygalomorph spidroins and an approximately 8-kb cDNA of the previously reported Euagrus chisoseus fibroin 1. Mygalomorph spidroin cDNAs encode tandem iterations of sequence repeats, followed by a nonrepetitive carboxy-terminal domain. Though highly homogenized at the nucleotide level within a cDNA (89-100% identical), these repeats exhibit extensive variation across spidroins, consistent with intragenic repeats evolving in concert. Extreme homogeneity of intragenic repeats is also characteristic of araneomorph spidroins, suggesting that modular architecture and its maintenance through concerted evolution have persisted since the mygalomorph/araneomorph split (> or =240 MYA). Phylogenetic analyses of C-terminal sequences grouped all mygalomorph spidroins, except Aliatypus fibroin 1, in a clade. Aliatypus fibroin 1 was instead more closely related to a subset of araneomorph spidroins, including those used in prey wrapping. Our results suggest that spidroin paralogs existed prior to the divergence of mygalomorphs and araneomorphs, followed by a far greater expansion of this gene family in araneomorphs, paralleling the dramatic functional diversification of their silk gland anatomy.