From Inquilines to Gall Inducers: Genomic Signature of a Life-Style Transition in Synergus Gall Wasps.

Erik Gobbo,Yoshihisa Abe,Nicolas Lartillot,Christopher W Wheat,Jack Hearn,Fredrik Ronquist,Tatsuya Ide,Graham N Stone,Enard David

doi:10.1093/gbe/evaa204

Abstract

Gall wasps (Hymenoptera: Cynipidae) induce complex galls on oaks, roses, and other plants, but the mechanism of gall induction is still unknown. Here, we take a comparative genomic approach to revealing the genetic basis of gall induction. We focus on Synergus itoensis, a species that induces galls inside oak acorns. Previous studies suggested that this species evolved the ability to initiate gall formation recently, as it is deeply nested within the genus Synergus, whose members are mostly inquilines that develop inside the galls of other species. We compared the genome of S. itoensis with that of three related Synergus inquilines to identify genomic changes associated with the origin of gall induction. We used a novel Bayesian selection analysis, which accounts for branch-specific and gene-specific selection effects, to search for signatures of selection in 7,600 single-copy orthologous genes shared by the four Synergus species. We found that the terminal branch leading to S. itoensis had more genes with a significantly elevated dN/dS ratio (positive signature genes) than the other terminal branches in the tree; the S. itoensis branch also had more genes with a significantly decreased dN/dS ratio. Gene set enrichment analysis showed that the positive signature gene set of S. itoensis, unlike those of the inquiline species, is enriched in several biological process Gene Ontology terms, the most prominent of which is “Ovarian Follicle Cell Development.” Our results indicate that the origin of gall induction is associated with distinct genomic changes, and provide a good starting point for further characterization of the genes involved.

Highlights

Gall wasps (Hymenoptera: Cynipidae) are plant parasites that induce the development of highly modified plant tissues, termed galls, in which their immature stages feed and grow (Abrahamson and Melika 2002; Stone et al 2002)
Genes from 141 orthogroups were seemingly present in two copies in S. itoensis but only in a single copy in the other three species; this does not necessarily imply a duplication, since genes that are split between two contigs are included in this count
We think our results demonstrate that comparative phylogenomic studies can serve as an important complementary tool to experimental studies, and can help identify candidate genes involved in the gall induction process

Summary

Introduction

Gall wasps (Hymenoptera: Cynipidae) are plant parasites that induce the development of highly modified plant tissues, termed galls, in which their immature stages feed and grow (Abrahamson and Melika 2002; Stone et al 2002). Diversity of a trait of interest in closely related species allows us to use selection analysis to identify genetic factors associated with evolutionary changes in the trait (Suzuki 2010). Even if ratios >1.0 are likely to be rare, the origin of a trait of interest should be accompanied by increased dN/dS ratios in the genes coding for the trait compared with background levels (Yang and Nielsen 2002) It is, worth noting that these kind of methods are subject to many errors (Markova-Raina and Petrov 2011), and the implementation of many levels of control is recommended. To use selection analysis to identify genes associated with the origin of gall induction in cynipids, we need to pinpoint where on the tree the ability to induce galls evolved

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Conclusion