Inter- and intra-species variation in genome-wide gene expression of Drosophila in response to parasitoid wasp attack

Abstract

BackgroundParasitoid resistance in Drosophila varies considerably, among and within species. An immune response, lamellocyte-mediated encapsulation, evolved in a subclade of Drosophila and was subsequently lost in at least one species within this subclade. While the mechanisms of resistance are fairly well documented in D. melanogaster, much less is known for closely related species. Here, we studied the inter- and intra-species variation in gene expression after parasitoid attack in Drosophila. We used RNA-seq after parasitization of four closely related Drosophila species of the melanogaster subgroup and replicated lines of D. melanogaster experimentally selected for increased resistance to gain insights into short- and long-term evolutionary changes.ResultsWe found a core set of genes that are consistently up-regulated after parasitoid attack in the species and lines tested, regardless of their level of resistance. Another set of genes showed no up-regulation or expression in D. sechellia, the species unable to raise an immune response against parasitoids. This set consists largely of genes that are lineage-restricted to the melanogaster subgroup. Artificially selected lines did not show significant differences in gene expression with respect to non-selected lines in their responses to parasitoid attack, but several genes showed differential exon usage.ConclusionsWe showed substantial similarities, but also notable differences, in the transcriptional responses to parasitoid attack among four closely related Drosophila species. In contrast, within D. melanogaster, the responses were remarkably similar. We confirmed that in the short-term, selection does not act on a pre-activation of the immune response. Instead it may target alternative mechanisms such as differential exon usage. In the long-term, we found support for the hypothesis that the ability to immunologically resist parasitoid attack is contingent on new genes that are restricted to the melanogaster subgroup.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3697-3) contains supplementary material, which is available to authorized users.

Differential activation of JAK-STAT signaling in blood cell progenitors reveals functional compartmentalization of theDrosophilalymph gland

“…To gain further evidence for increased activity of STAT92E in the posterior lobes of parasitized larvae, we also assessed the expression of the STAT target Tep1. Indeed JAK overactivation as well as L. boulardi infection were shown to induce the expression of this opsonin (Lagueux et al, 2000, Wertheim et al, 2005, Salazar-Jaramillo et al, 2017. RNA in situ hybridization revealed a basal level expression of Tep1 in the primary and posterior lobes in the wild type unparasitized larval lymph glands ( Figure 5K).…”

DoesDrosophila sechelliaescape parasitoid attack by feeding on a toxic resource?

“…In a comparative transcriptomic study, we further revealed evidence of the failure of a functional 91 immune response in D. sechellia to parasitoid attack (Salazar-Jaramillo et al, 2017). Although D.…”

“…homologs of Mtk, DptB, PGRP-SB1), it failed to upregulate most of the genes that were upregulated 94 during the cellular immune response against parasitoids in the closely related species D. melanogaster 95 and D. simulans(Salazar-Jaramillo et al, 2017). These genes included TepI, PPO3, CG4259, CG4793, 96…”

“…Figure 1 summarizes the relevant previous genomic and transcriptomic results. Based 97 on these combined results we proposed the hypothesis that D. sechellia possesses the "machinery" for 98 melanotic encapsulation, but that it does no longer function properly in response to parasitoid attack 99 (Salazar-Jaramillo et al, 2017). This would signify a case of trait loss.…”

Long-Read Genome Sequencing and Assembly of Leptopilina boulardi: A Specialist Drosophila Parasitoid

“…Nevertheless, the virulence of the parasitoid is a key factor in determining the fate of an infected host. Although, studies have explored the cause of genetic variance (intra-or inter-specific) and identified the genes involved in the host resistance (A R Kraaijeveld, Van Alphen, and Godfray 1998;Hita et al 1999;Schlenke et al 2007;Howell et al 2012;Salazar-Jaramillo et al 2017), our understanding of the genetic and epigenetic basis of variation seen in the counter-resistance/virulence of the parasitoids is limited (Alex R. Kraaijeveld and Godfray 2009;Colinet et al 2010). Another factor that affects the outcome of the host-parasitoid association is the symbiotic partners they harbor, such as Leptopilina boulardi Filamentous Virus (LbFV) and Wolbachia.…”