Abstract

The immunological interaction between Drosophila melanogaster and its larval parasitoids has been thoroughly investigated, however, little is known about the interaction between the host and its pupal parasitoids. Pachycrepoideus vindemmiae, a pupal ectoparasitoid of D. melanogaster, injects venom into its host while laying eggs on the puparium, which regulates host immunity and interrupts host development. To resist the invasion of parasitic wasps, various immune defense strategies have been developed in their hosts as a consequence of co-evolution. In this study, we mainly focused on the host immunomodulation by P. vindemmiae and thoroughly investigated cellular and humoral immune response, including cell adherence, cell viability, hemolymph melanization and the Toll, Imd, and JAK/STAT immune pathways. Our results indicated that venom had a significant inhibitory effect on lamellocyte adherence and induced plasmatocyte cell death. Venom injection and in vitro incubation strongly inhibited hemolymph melanization. More in-depth investigation revealed that the Toll and Imd immune pathways were immediately activated upon parasitization, followed by the JAK/STAT pathway, which was activated within the first 24 h post-parasitism. These regulatory effects were further validated by qPCR. Our present study manifested that P. vindemmiae regulated the cellular and humoral immune system of host D. melanogaster in many aspects. These findings lay the groundwork for studying the immunological interaction between D. melanogaster and its pupal parasitoid.

Highlights

  • Parasitoids are unique venomous organisms among hymenopteran insects, with an estimated number of species ranging from 150,000 to 600,000 (Mrinalini and Werren, 2017)

  • Immune suppression is usually related to virulence factors, including venom (Asgari and Rivers, 2011), polydnaviruses (PDVs) (Gundersen-Rindal et al, 2013), virus-like particles (VLPs) (Grgacic and Anderson, 2006) and ovarian secretion (MabialaMoundoungou et al, 2010), and they work alone or cooperate with each other to regulate the cellular and humoral immune responses of hosts (Burke and Strand, 2014)

  • Our results demonstrated that great changes took place in cellular and humoral immunity of the host, including cell adherence, cell viability, hemolymph melanization and the Toll, immune deficiency (Imd), and JAK/STAT immune pathways

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Summary

Introduction

Parasitoids are unique venomous organisms among hymenopteran insects, with an estimated number of species ranging from 150,000 to 600,000 (Mrinalini and Werren, 2017). There is great potential for developing parasitoids as a crucial means of biological control They lay eggs into the hemocoel (endoparasitoids) or on the surface (ectoparasitoids) of hosts (Moreau and Asgari, 2015). Immune evasion occurs when wasp eggs are either covered with a fibrous layer or tightly adhered to host tissue, and the hosts fail to recognize it as non-self (Asgari et al, 1998; Eslin and Prévost, 2000; Hu et al, 2003). Both strategies are how parasitic wasps outwit their hosts

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