Parasitoid wasp venom manipulates host innate behavior via subtype-specific dopamine receptor activation

Abstract

The subjugation strategy employed by the jewel wasp is unique in that it manipulates the behavior of its host, the American cockroach, rather than inducing outright paralysis. Upon envenomation directly into the central complex (CX), a command center in the brain for motor behavior, the stung cockroach initially engages in intense grooming behavior, then falls into a lethargic sleep-like state referred to as hypokinesia. Behavioral changes evoked by the sting are due at least in part to the presence of the neurotransmitter dopamine in the venom. In insects, dopamine receptors are classified as two families, the D1-like and the D2-like receptors. However, specific roles played by dopamine receptor subtypes in venom-induced behavioral manipulation by the jewel wasp remain largely unknown. In the present study, we used a pharmacological approach to investigate roles of D1-like and D2-like receptors in behaviors exhibited by stung cockroaches, focusing on grooming. Specifically, we assessed behavioral outcomes of focal CX injections of dopamine receptor agonists and antagonists. Both specific and non-specific compounds were used. Our results strongly implicate D1-like dopamine receptors in venom-induced grooming. Regarding induction of hypokinesia, our findings demonstrate that dopamine signaling is necessary for induction of long-lasting hypokinesia caused by brain envenomation.

Parasitoid wasp venom re-programs host behavior through downmodulation of brain central complex activity and motor output

“…In addition to GABA, wasp venom contains dopamine ( Banks and Adams, 2012 ; Moore et al, 2018 ; Weisel-Eichler et al, 1999 ), which is shown to induce intense and prolonged grooming behavior. A recent study shows that the D1-like dopamine receptor (dopR) is the venom target responsible for grooming evoked by the sting into the CX ( Nordio et al, 2022 ). Furthermore, studies from Drosophila demonstrated that dopR receptors are highly expressed in the fly CX ( Kong et al, 2010 ; Pitmon et al, 2016 ).…”

“…However, pharmacological studies extend the functional roles of the CX beyond locomotion, implicating its involvement in almost all the behavioral changes induced after the wasp sting. For example, pharmacological block of dopR receptors in the CX prior to the wasp sting prevents sting-induced grooming behavior ( Nordio et al, 2022 ) without affecting spontaneous walking. Likewise, focal injection of opiate agonists mimics venom effects on spontaneous walking and the escape threshold, but does not affect grooming behavior.…”

“…The first potential weapon deployed by the wasp is presumably GABA, which reduces neuronal activity of the CX sharply, though briefly. As the actions of GABA wear off, dopamine present in the wasp venom triggers intense and prolonged grooming ( Nordio et al, 2022 ). Subsequently, the other proteins and peptides in the venom suppress neuronal activity in the CX ( Arvidson et al, 2019 ), leading to reduced DIN influences on thoracic ganglia circuitry.…”