Search performance and octopamine neuronal signaling mediate parasitoid induced changes in Drosophila oviposition behavior

Abstract

Making the appropriate responses to predation risk is essential for the survival of an organism; however, the underlying mechanisms are still largely unknown. Here, we find that Drosophila has evolved an adaptive strategy to manage the threat from its parasitoid wasp by manipulating the oviposition behavior. Through perception of the differences in host search performance of wasps, Drosophila is able to recognize younger wasps as a higher level of threat and consequently depress the oviposition. We further show that this antiparasitoid behavior is mediated by the regulation of the expression of Tdc2 and Tβh in the ventral nerve cord via LC4 visual projection neurons, which in turn leads to the dramatic reduction in octopamine and the resulting dysfunction of mature follicle trimming and rupture. Our study uncovers a detailed mechanism underlying the defensive behavior in insects that may advance our understanding of predator avoidance in animals.

Drosophilacells that express octopamine receptors can either inhibit or promote oviposition

“…We expressed the temperature-sensitive cation channel, dTrpA1, with the panel of Oa receptor MiMIC Gal4 lines and tested egg laying behavior at 29ºC, a temperature at which dTrpA1 activates neurons (Rosenzweig et al 2005;Hamada et al 2008). We hypothesized that activation of some if not all of the OaRNs might promote oviposition, similar to previously shown roles for Oa signaling in promoting ovulation (Deady and Sun 2015;White, Chen, and Wolfner 2021;Pang et al 2022;Cole et al 2005;Yoshinari et al 2020). However, we found that activation of OaRNs in female flies led to a significant decrease in egg laying rate compared to controls (Fig.…”

“…although it rescues the reduction in oviposition caused by exposure to parasitoid wasps (Pang et al 2022).…”

“…Although Oa regulates multiple processes within the reproductive tract, the most commonly reported phenotype for mutations that reduce octopaminergic signaling is a decrease in the release of eggs from the ovary (ovulation) with a resultant decrease in egg laying (White, Chen, and Wolfner 2021;Pang et al 2022). This phenotype has been observed with loss of function mutants or RNAi for the receptors Oamb (H.-G. Lee et al 2003;H.-G. Lee, Rohila, and Han 2009;Deady and Sun 2015) and Octβ2R (Lim et al 2014a;Li et al 2015), an enzyme required for Oa synthesis, tyrosine βhydroxylase (TβH) (Monastirioti, Charles E. Linn, and White 1996;Cole et al 2005;Monastirioti 2003) and the transporter responsible for its storage and release from secretory vesicles (Simon et al 2009).…”

The vitellogenin receptor gene contributes to mating and host-searching behaviors in parasitoid wasps

“…Indeed, our previous studies have shown that Leptopilina wasps have evolved multiple strategies to manipulate the hosts for successful parasitism. 13 , 14 , 15 , 16 Recently, several reports have revealed that the olfactory system plays key roles in the mating and host-searching behaviors of parasitoid wasps. 17 , 18 Those behaviors are necessary for the parasitoid reproduction, which is another key factor resulting in high parasitism.…”

Molecular and Pharmacological Characterization of β-Adrenergic-like Octopamine Receptors in the Endoparasitoid Cotesia chilonis (Hymenoptera: Braconidae)

“…Norepinephrine and OA are similar in structure and function, and they are generally considered counterparts in vertebrates and invertebrates, respectively [ 2 , 3 ]. OA is abundant in the central nervous system of insects [ 4 , 5 ], and regulates diverse processes of physiology and behaviors, such as feeding [ 6 , 7 , 8 ], aggression [ 9 , 10 , 11 , 12 ], sleep [ 13 , 14 ], courtship [ 15 , 16 ], post-mating [ 17 , 18 ], oviposition [ 19 , 20 , 21 ], learning [ 22 , 23 ], reward [ 24 ], immunity [ 25 , 26 ], exercise adaption [ 27 , 28 ], thermogenesis [ 29 ], and muscle contractility [ 30 ].…”