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

Thomas H Clarke,Cheryl Y Hayashi,R Crystal Chaw,Robert A Haney,Nadia A Ayoub,Jessica E Garb

doi:10.1038/s41598-017-07388-1

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.

Highlights

Spiders (Araneae) owe their ecological success as keystone predators[1, 2] in large part to their usage of silk[3,4,5]
Spider silk synthesis presents a valuable model for studying the evolution of tissue-specific gene expression and the role of gene duplication in functional novelty
Some paralogs are expressed in multiple gland types confirming previous indications that not every spidroin paralog is restricted to a single gland type[33,34,35,36]

Summary

Introduction

Spiders (Araneae) owe their ecological success as keystone predators[1, 2] in large part to their usage of silk[3,4,5]. Transcriptome evolution in specialized tissues has primarily been examined in mammals[13,14,15,16,17,18,19] These studies largely found that gene expression profiles of thousands of orthologous genes were most similar among homologous tissues from different species, supporting a long held assumption that conserved patterns of gene expression “underlie tissue identity in mammals”[16]. The relationship among morphological specialization of silk glands, gene duplication, and gene expression evolution has only been investigated for spidroins We address these issues by profiling gene expression patterns across the different silk glands and non-silk gland tissues of three cobweb weaving spider species (Theridiidae). Our results expand models of the evolution of tissue specialization and will improve efforts to artificially recreate spider silks

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Conclusion