Chance and predictability in evolution: The genomic basis of convergent dietary specializations in an adaptive radiation

Abstract

The coexistence of multiple eco-phenotypes in independently assembled communities makes island adaptive radiations the ideal framework to test convergence and parallelism in evolution. In the radiation of the spider genus Dysdera in the Canary Islands, species diversification occurs concomitant with repeated events of trophic specialization. These dietary shifts, to feed primarily on woodlice, are accompanied by modifications in morphology (mostly in the mouthparts), behaviour and nutritional physiology. To gain insight into the molecular basis of this adaptive radiation, we performed a comprehensive comparative transcriptome analysis of five Canary Island Dysdera endemics representing two evolutionary and geographically independent events of dietary specialization. After controlling for the potential confounding effects of hemiplasy, our differential gene expression and selective constraint analyses identified a number of genetic changes that could be associated with the repeated adaptations to specialized diet of woodlice, including some related to heavy metal detoxification and homeostasis, the metabolism of some important nutrients and venom toxins. Our results shed light on the genomic basis of an extraordinary case of dietary shift convergence associated with species diversification. We uncovered putative molecular substrates of convergent evolutionary changes at different hierarchical levels, including specific genes, genes with equivalent functions and even particular amino acid positions. This study improves our knowledge of rapid adaptive radiations and provides new insights into the predictability of evolution.