Differential Expression of Immune Genes between Two Closely Related Beetle Species with Different Immunocompetence following Attack by Asecodes parviclava.

Christopher W Wheat,Lisa Fors,Mahesh Binzer-Panchal,Peter A Hambäck,Tanja Slotte,Ulrich Theopold,Xuyue Yang

doi:10.1093/gbe/evaa075

Abstract

Endoparasitoid wasps are important natural enemies of many insect species and are major selective forces on the host immune system. Despite increased interest in insect antiparasitoid immunity, there is sparse information on the evolutionary dynamics of biological pathways and gene regulation involved in host immune defense outside Drosophila species. We de novo assembled transcriptomes from two beetle species and used time-course differential expression analysis to investigate gene expression differences in closely related species Galerucella pusilla and G. calmariensis that are, respectively, resistant and susceptible against parasitoid infection by Asecodes parviclava parasitoids. Approximately 271 million and 224 million paired-ended reads were assembled and filtered to form 52,563 and 59,781 transcripts for G. pusilla and G. calmariensis, respectively. In the whole-transcriptome level, an enrichment of functional categories related to energy production, biosynthetic process, and metabolic process was exhibited in both species. The main difference between species appears to be immune response and wound healing process mounted by G. pusilla larvae. Using reciprocal BLAST against the Drosophila melanogaster proteome, 120 and 121 immune-related genes were identified in G. pusilla and G. calmariensis, respectively. More immune genes were differentially expressed in G. pusilla than in G. calmariensis, in particular genes involved in signaling, hematopoiesis, and melanization. In contrast, only one gene was differentially expressed in G. calmariensis. Our study characterizes important genes and pathways involved in different immune functions after parasitoid infection and supports the role of signaling and hematopoiesis genes as key players in host immunity in Galerucella against parasitoid wasps.

Highlights

Parasitoid attack is a major cause of mortality in many insect species (Godfray and Shimada 1999; Asgari and Rivers 2011), exerting strong selection on traits that affect the likelihood or the outcome of an attack
De novo transcriptome assemblies were based on all the data for each species and yielded 262,505 transcript isoforms representing 195,422 unique transcripts (N50 1⁄4 1,428) for G. pusilla and 300,593 isoforms representing 224,904 unique transcripts for G. calmariensis (N50 1⁄4 1,070), before filtering
To test whether the transcriptional response to parasitoid infection differed between G. calmariensis and G. pusilla, we examined changes in gene expression between species and time points

Summary

Introduction

Parasitoid attack is a major cause of mortality in many insect species (Godfray and Shimada 1999; Asgari and Rivers 2011), exerting strong selection on traits that affect the likelihood or the outcome of an attack. Drosophila species show great variation in immunocompetence against the parasitoid Asobara tabida, where most species in the Drosophila obscura group show immune deficiency and no egg encapsulation, whereas other taxa show very strong immune responses Evol. 12(5):522–534. doi:10.1093/gbe/evaa Advance Access publication April 13, 2020

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