Abstract

Background Drosophila is an important model for studying the evolution of animal immunity, due to the powerful genetic tools developed for D. melanogaster. However, Drosophila is an incredibly speciose lineage with a wide range of ecologies, natural histories, and diverse natural enemies. Surprisingly little functional work has been done on immune systems of species other than D. melanogaster. In this study, we examine the evolution of immune genes in the speciose subgenus Drosophila, which diverged from the subgenus Sophophora (that includes D. melanogaster) approximately 25–40 Mya. We focus on D. neotestacea, a woodland species used to study interactions between insects and parasitic nematodes, and combine recent transcriptomic data with infection experiments to elucidate aspects of host immunity.ResultsWe found that the vast majority of genes involved in the D. melanogaster immune response are conserved in D. neotestacea, with a few interesting exceptions, particularly in antimicrobial peptides (AMPs); until recently, AMPs were not thought to evolve rapidly in Drosophila. Unexpectedly, we found a distinct diptericin in subgenus Drosophila flies that appears to have evolved under diversifying (positive) selection. We also describe the presence of the AMP drosocin, which was previously thought to be restricted to the subgenus Sophophora, in the subgenus Drosophila. We challenged two subgenus Drosophila species, D. neotestacea and D. virilis with bacterial and fungal pathogens and quantified AMP expression.ConclusionsWhile diptericin in D. virilis was induced by exposure to gram-negative bacteria, it was not induced in D. neotestacea, showing that conservation of immune genes does not necessarily imply conservation of the realized immune response. Our study lends support to the idea that invertebrate AMPs evolve rapidly, and that Drosophila harbor a diverse repertoire of AMPs with potentially important functional consequences.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0805-y) contains supplementary material, which is available to authorized users.

Highlights

  • Drosophila is an important model for studying the evolution of animal immunity, due to the powerful genetic tools developed for D. melanogaster

  • We found Mtk in the genomes of the subgenus Drosophila flies D. mojavensis, D. virilis, and D. albomicans, but not D. guttifera; we were unable to determine if it is truly absent in D. guttifera, or if this absence is instead an artefact of the current genomic assembly

  • We further found orthologues of this D. neotestacea drosocin in other subgenus Drosophila flies

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Summary

Introduction

Drosophila is an important model for studying the evolution of animal immunity, due to the powerful genetic tools developed for D. melanogaster. The ability to defend oneself from parasites and pathogens (natural enemies) is essential for life, and animals have conserved sophisticated mechanisms of defence referred to as the innate immune system. The innate immune response requires recognition, signaling, and activation of defensive mechanisms This defence response culminates in the synthesis and secretion of immune effectors, such as antimicrobial peptides (AMPs) – host-encoded antibiotics that directly combat invading microorganisms [1]. It is essential to overcome such host defences for success, setting the stage for antagonistic co-evolution. These evolutionary arms races have led to immune system genes typically evolving far more rapidly than other genes in the genome [2,3,4,5].

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