Evolutionary shifts in gene expression decoupled from gene duplication across functionally distinct spider silk glands

Abstract

Spider silk synthesis is an emerging model for the evolution of tissue-specific gene expression and the role of gene duplication in functional novelty, but its potential has not been fully realized. Accordingly, we quantified transcript (mRNA) abundance in seven silk gland types and three non-silk gland tissues for three cobweb-weaving spider species. Evolutionary analyses based on expression levels of thousands of homologous transcripts and phylogenetic reconstruction of 605 gene families demonstrated conservation of expression for each gland type among species. Despite serial homology of all silk glands, the expression profiles of the glue-forming aggregate glands were divergent from fiber-forming glands. Also surprising was our finding that shifts in gene expression among silk gland types were not necessarily coupled with gene duplication, even though silk-specific genes belong to multi-paralog gene families. Our results challenge widely accepted models of tissue specialization and significantly advance efforts to replicate silk-based high-performance biomaterials.

Structural Characterization of Black Widow Spider Dragline Silk Proteins CRP1 and CRP4

“…Transcriptomic studies of the silk-producing glands from L. hesperus have detected CRP1, CRP2, and CRP3 transcripts in the MA gland [36]. However, based upon our proteomic studies we have…”

Conservation of a pH-sensitive structure in the C-terminal region of spider silk extends across the entire silk gene family

“…Moreover, this conservation has persisted despite the diversification of other spider traits. For example, terrestrial spiders such as the mygalomorphs produce two to three silk proteins from a large, undifferentiated silk gland whereas the Orbiculariae have evolved several specialised glands from which different types of silk are extruded (Blackledge and Hayashi 2006 ; Blamires et al 2017 ; Clarke et al 2017 ; Garb 2013 ; Garb et al 2010 ; Perez-Rigueiro et al 2010 ; Rising et al 2007 ; Stark et al 2007 ).…”

Major ampullate silk gland transcriptomes and fibre proteomes of the golden orb-weavers, Nephila plumipes and Nephila pilipes (Araneae: Nephilidae)

“…clavipes , Babb et al characterised spidroin expression within the distinct silk glands [ 27 ]. Significant transcriptome coverage has also been achieved by Prosdocimi and colleagues in their infraorder comparative study of expressed RNAs of the spinning glands [ 30 ]; by Clark et al, based on multi-tissue de novo transcriptome assemblies of closely related cob-weavers [ 31 – 33 ]; and Correa-Garhwal et al examined silk expression in male spiders of the family Theridiidae [ 34 ].…”