Two novel venom proteins underlie divergent parasitic strategies between a generalist and a specialist parasite

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.

Neofunctionalization of an ancient domain allows parasites to avoid intraspecific competition by manipulating host behaviour

“…how to synchronise development with the host and how to combat with the host immune system. Correspondingly, a related study showed that the more powerful active immune suppression, which is absent in the specialist, allows broad parasitisation in the generalist Lh 34 .…”

“…Both strains were checked with Lb filamentous virus (LbFV) by mapping whole-genome sequencing reads with the virus reference. Genome sequencing reads of Lb is the sequencing data for polishing the assembly of long reads (see below), and the reads of Lh was generated by the previous study 34 .…”

“…Local InterProScan v5.13 99 was performed with all involved databases to search functional domains, Gene Ontology terms, and KEGG Orthology (KO) terms for each gene. Previously published transcriptome data 34 were used to profile the expression pattern of each protein-coding gene. These data covers most representative developmental stages of parasitoid wasps, including Egg, Larva-1 (days 1–3 larvae), Larva-2 (days 4–6 larvae), Larva-3 (days 7–9 larvae), Pupa-1 (days 1–3 pupae), Pupa-2 (days 4–7 pupae), Pupa-3 (days 8–10 pupae), Adult-F (day 3 adult females) and Adult-M (day 3 adult males).…”

“…These data covers most representative developmental stages of parasitoid wasps, including Egg, Larva-1 (days 1–3 larvae), Larva-2 (days 4–6 larvae), Larva-3 (days 7–9 larvae), Pupa-1 (days 1–3 pupae), Pupa-2 (days 4–7 pupae), Pupa-3 (days 8–10 pupae), Adult-F (day 3 adult females) and Adult-M (day 3 adult males). Transcriptome data of venoms was generated independently 34 , in which the venom glands of 3-day-old adult female wasps were independently dissected in Ringer’s saline solution on an ice plate under a stereoscope (Nikon). To quantify the expression profiles, Salmon v0.12.0 100 was used to determine the expression level as Transcripts Per Million (TMP) for each sample.…”

A parasitoid wasp of Drosophila employs preemptive and reactive strategies to deplete its host’s blood cells

“…Lb infection activates many components of humoral and cellular immunity: Toll-NF-κB, JAK-STAT, and the melanization pathways and their target genes are transcriptionally upregulated; there is a burst of hematopoietic proliferation and differentiation of blood cells (also called hemocytes) in the lymph gland and in circulation. If the immune responses are strong and sustained, macrophages and lamellocytes encapsulate and kill wasp eggs [7][8][9][10][11]. Lh infection in contrast suppresses immune gene expression and kills immature and mature larval hemocytes [12,13].…”