The parasitoid Exorista sorbillans exploits host silkworm encapsulation to build respiratory funnel for survival.

Abstract

Insect parasitoids have evolved sophisticated strategies to evade or modulate host immunity for parasitic infections. The precise mechanisms by which parasitoids counteract host anti-parasitic responses are poorly defined. Here we report a novel immune evasion strategy employed by the parasitoid Exorista sorbillans (Diptera: Tachinidae) to establish infection. We find that E. sorbillans larva construct a respiratory funnel that gradually increases in size as development progresses. This respiratory funnel, which connect to the parasitoid invasion aperture on the host silkworm epidermis, proves essential for E. sorbillans development, as sealing the invasion aperture results in complete mortality of larval parasitoids. Our investigation reveals that E. sorbillans infection reduces both host silkworms' hemocyte counts and the expression of hemocyte-specific genes, while simultaneously inducing varying degrees of host silkworm encapsulation at different parasitic stages. Nevertheless, more complete inhibition of host silkworm encapsulation through RNAi leads to parasitoid's defective respiratory funnel formation and increased mortality rates of the parasitoid. Further observations demonstrate that this suppressed encapsulation response triggers an enhanced activation of Toll/IMD pathways in the host silkworm. Take together, we show that E. sorbillans may utilize host silkworm encapsulation to construct a respiratory funnel for both respiration and immune evasion. Our findings provide new insights into the evasion tactics employed by parasitoids win out in the ongoing parasite-host evolutionary arms race.