VENOM COMPONENTS OF Asobara japonica IMPAIR CELLULAR IMMUNE RESPONSES OF HOST Drosophila melanogaster

Abstract

The endoparasitoid wasp Asobara japonica has highly poisonous venom: the host Drosophila larvae are killed by envenomation at a dose that is naturally injected by the female wasp at parasitism. This insecticidal venom is neutralized, however, because A. japonica introduces lateral oviduct components soon after venom injection at oviposition. Although the venom and lateral oviduct components of this parasitoid have been partially characterized, how the venom components favor successful development of wasp eggs and larvae in the host remains ambiguous. Here, we demonstrated that A. japonica venom did not affect host humoral immune responses, determined as expression of antimicrobial peptide (AMP) genes, but significantly diminished two cellular responses, spreading and phagocytosis, by host hemocytes. Moreover, venom components drastically elevated a serine protease-like activity 4 h after its injection. The lateral oviduct components did not negate the detrimental effects of the venom on host cellular immunities, but significantly reduced the venom-induced elevation of protease activity. Both active factors in venom and lateral oviduct components were roughly characterized as heat-labile substances with a molecular mass of at least 10 kDa. Finally, venom of A. japonica, with a wide host range, was found to be much more toxic than that of Asobara rossica, which has a limited host range. These results reveal that A. japonica venom toxicity allows exploitation of a broader range of host insects because it is essential to overcome cellular immune responses of the host for successful parasitism.

Toxicity of venom of Asobara and Leptopilina species to Drosophila species

“…Asobara japonica has venom that exhibits a toxic effect on host species if its injection is not followed by an injection of lateral oviduct components (Mabiala‐Moundoungou et al ., ; Furihata et al ., ). However, the venom of the other three Asobara species investigated in the present study does not have such toxic effects.…”

“…Thus, vibration of the ovipositor is an indication of egg laying (Vet & Bakker, ; van Lenteren et al ., ; Dubuffet et al ., ). In parasitism experiments using A. japonica and some host species such as Drosophila melanogaster Meigen and Drosophila simulans Sturtevant, interruption of oviposition after injection of venom but before egg laying kills host larvae (Furihata & Kimura, ; Mabiala‐Moundoungou et al ., ; Furihata et al ., ). However, this toxic action of the venom is suppressed by lateral oviduct components that are injected to the host by the parasitoid female along with egg laying (Mabiala‐Moundoungou et al ., ; Furihata et al ., ).…”

“…Tel. : +81 11 706 2236; e-mail: tetsuo_kohyama@ees.hokudai.ac.jp as Drosophila melanogaster Meigen and Drosophila simulans Sturtevant, interruption of oviposition after injection of venom but before egg laying kills host larvae (Furihata & Kimura, 2009;Mabiala-Moundoungou et al, 2010;Furihata et al, 2013). However, this toxic action of the venom is suppressed by lateral oviduct components that are injected to the host by the parasitoid female along with egg laying (Mabiala-Moundoungou et al, 2010;Furihata et al, 2013).…”

“…: +81 11 706 2236; e-mail: tetsuo_kohyama@ees.hokudai.ac.jp as Drosophila melanogaster Meigen and Drosophila simulans Sturtevant, interruption of oviposition after injection of venom but before egg laying kills host larvae (Furihata & Kimura, 2009;Mabiala-Moundoungou et al, 2010;Furihata et al, 2013). However, this toxic action of the venom is suppressed by lateral oviduct components that are injected to the host by the parasitoid female along with egg laying (Mabiala-Moundoungou et al, 2010;Furihata et al, 2013). Additional studies showed that the venom of A. japonica is much less toxic to certain Drosophila species that kill A. japonica embryos or larvae at high rates, such as Drosophila bipectinata Duda and Drosophila ficusphila Kikkawa & Peng (Furihata & Kimura, 2009;Furihata et al, 2013).…”

“…However, this toxic action of the venom is suppressed by lateral oviduct components that are injected to the host by the parasitoid female along with egg laying (Mabiala-Moundoungou et al, 2010;Furihata et al, 2013). Additional studies showed that the venom of A. japonica is much less toxic to certain Drosophila species that kill A. japonica embryos or larvae at high rates, such as Drosophila bipectinata Duda and Drosophila ficusphila Kikkawa & Peng (Furihata & Kimura, 2009;Furihata et al, 2013). These 'resistant' Drosophila species may have evolved some mechanisms to detoxify lethal components of A. japonica venom along with the acquisition of capacity to kill A. japonica embryos and/or larvae in the course of their coevolutionary interactions.…”