Abstract

Parasitoids are ubiquitous in natural ecosystems. Parasitic strategies are highly diverse among parasitoid species, yet their underlying genetic bases are poorly understood. Here, we focus on the divergent adaptation of a specialist and a generalist drosophilid parasitoids. We find that a novel protein (Lar) enables active immune suppression by lysing the host lymph glands, eventually leading to successful parasitism by the generalist. Meanwhile, another novel protein (Warm) contributes to a passive strategy by attaching the laid eggs to the gut and other organs of the host, leading to incomplete encapsulation and helping the specialist escape the host immune response. We find that these diverse parasitic strategies both originated from lateral gene transfer, followed with duplication and specialization, and that they might contribute to the shift in host ranges between parasitoids. Our results increase our understanding of how novel gene functions originate and how they contribute to host adaptation.

Highlights

  • IntroductionBy combining multi-omics approaches and large-scale in vivo functional studies, we here successfully characterize two key genes that confer the active and passive parasitic strategies of Leptopilina heterotoma (Lh) and L. boulardi (Lb), respectively, and surprisingly find that they both originated from lateral gene transfer (LGT) and underwent subsequent gene duplication and expression specialization in the venom glands (VGs)

  • The difference in genome sizes between Leptopilina heterotoma (Lh) and L. boulardi (Lb) was likely determined by their repeat contents, as 51.47% of the Lh genome was annotated as repeat content in comparison with a 33.79% ratio in the Lb genome (Supplementary Table 4)

  • In comparison to dsGFP-injected wasps, we found a significant suppression of apoptosis in the host lymph gland and a correspondingly large population of lamellocytes in host larvae when parasitized by LhOGS20123knockdown wasps (Fig. 2e, f and Supplementary Fig. 14)

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Summary

Introduction

By combining multi-omics approaches and large-scale in vivo functional studies, we here successfully characterize two key genes that confer the active and passive parasitic strategies of Lh and Lb, respectively, and surprisingly find that they both originated from lateral gene transfer (LGT) and underwent subsequent gene duplication and expression specialization in the venom glands (VGs). We uncover their adaptive roles in driving the shifts in host range between parasitoids

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