Abstract
Silk spinning is essential to spider ecology and has had a key role in the expansive diversification of spiders. Silk is composed primarily of proteins called spidroins, which are encoded by a multi-gene family. Spidroins have been studied extensively in the derived clade, Orbiculariae (orb-weavers), from the suborder Araneomorphae (‘true spiders’). Orbicularians produce a suite of different silks, and underlying this repertoire is a history of duplication and spidroin gene divergence. A second class of silk proteins, Egg Case Proteins (ECPs), is known only from the orbicularian species, Lactrodectus hesperus (Western black widow). In L. hesperus, ECPs bond with tubuliform spidroins to form egg case silk fibers. Because most of the phylogenetic diversity of spiders has not been sampled for their silk genes, there is limited understanding of spidroin gene family history and the prevalence of ECPs. Silk genes have not been reported from the suborder Mesothelae (segmented spiders), which diverged from all other spiders >380 million years ago, and sampling from Mygalomorphae (tarantulas, trapdoor spiders) and basal araneomorph lineages is sparse. In comparison to orbicularians, mesotheles and mygalomorphs have a simpler silk biology and thus are hypothesized to have less diversity of silk genes. Here, we present cDNAs synthesized from the silk glands of six mygalomorph species, a mesothele, and a non-orbicularian araneomorph, and uncover a surprisingly rich silk gene diversity. In particular, we find ECP homologs in the mesothele, suggesting that ECPs were present in the common ancestor of extant spiders, and originally were not specialized to complex with tubuliform spidroins. Furthermore, gene-tree/species-tree reconciliation analysis reveals that numerous spidroin gene duplications occurred after the split between Mesothelae and Opisthothelae (Mygalomorphae plus Araneomorphae). We use the spidroin gene tree to reconstruct the evolution of amino acid compositions of spidroins that perform different ecological functions.
Highlights
Silk is vital to the ecology of spiders, being used throughout their lifetime for a wide array of essential functions
While most silk research has focused on derived members of Araneomorphae (‘‘true spiders’’), we present silk genes from Paleocribelletae, increase sampling for Mygalomorphae, and record silk sequences from Mesothelae
We found a considerable diversity of silk associated cDNAs in the mesothele species, Liphistius malayanus; in particular, we discovered homologs to Egg Case Proteins (ECPs) that are otherwise only known from the orbicularian species, Latrodectus hesperus
Summary
Silk is vital to the ecology of spiders, being used throughout their lifetime for a wide array of essential functions. There are over 42,000 described species of spiders [1], and they are taxonomically diverse and ecologically diverse in their silk biology. Few species have been sampled for their silk genes. Mesotheles and mygalomorphs exhibit profound differences in silk use compared to most araneomorph spiders [3,4]. Mesotheles and mygalomorphs produce general-purpose fibers and apply silk in a sheet-like manner to a burrow or other substrate, which is believed to be most similar to silk use in the common ancestor of extant spiders that lived .380 million years ago [2,5,6,7,8,9,10,11]
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