Sex peptide receptor mediates the post‐mating switch in Helicoverpa armigera (Lepidoptera: Noctuidae) female reproductive behavior

Abstract

BACKGROUND: In Drosophila, the sex peptide receptor (SPR) in females to detect male sex peptide (SP) and trigger changes in female behavior including mating rejection and oviposition. In moths, the SPR had been identified and investigated the limited function by using RNA interference (RNAi). However, the detailed function of SPR after a normal mating in moths, especially the role in female sexual receptivity, remains to be elucidated.RESULTS: In this study, we use Helicoverpa armigera, an economically important pest worldwide, as a case study to verify the function of SPR in vivo by CRISPR/Cas9 gene editing system. Analyzing the post-mating behaviors in mutant females, we investigated that HarmSPR could mediate the long-term sexual receptivity (remating, sex pheromone production and calling behavior) switch in female, but not affect the short-term sexual receptivity and the duration time of remating. The oviposition of mated HarmSPR −/− females was significantly decreased by ∼70% comparing to wild-type (WT) mated females and there were more eggs staying in the ovary of mutant females. SPR also showed effect on female longevity, which is that the mated HarmSPR −/− females showed longer longevity than mated WT females. CONCLUSION:The results detailedly demonstrated the functional role of SPR in female post-mating behaviors and we could propose a pest control strategy in which developing an antagonist of SPR to reduce the oviposition of female.

RNAi‐mediated silencing of SlitPer disrupts sex pheromone communication behavior in Spodoptera litura

“…40 The sex peptide receptor probably mediated sex pheromone biosynthesis, calling, and oviposition behavior in Helicoverpa armigera. 41 Topical application of methoprene (a juvenile hormone analog) caused virgin Ephestia cautella to oviposit early. 42 The rearing on a juvenile hormone-supplemented diet reduced the calling behavior of Plodia interpunctella.…”

“…For example, pheromone biosynthesis activating neuropeptide can regulate sex pheromone production in female moths 40 . The sex peptide receptor probably mediated sex pheromone biosynthesis, calling, and oviposition behavior in Helicoverpa armigera 41 . Topical application of methoprene (a juvenile hormone analog) caused virgin Ephestia cautella to oviposit early 42 .…”

Sex peptide receptor is not required for refractoriness to remating or induction of egg laying inAedes aegypti

“…Spr ECFP knockout females oviposited a similar number of eggs as heterozygous females after mating and blood feeding, demonstrating that SPR is not required for this post-mating process. Knockdown or knockout of SPR in various insect systems have noted a reduced number of eggs laid (LI et al 2014;ZHENG et al 2015;GREGORIOU AND MATHIOPOULOS 2020;LIU et al 2021), although the degree of reduction varies and it often is not a complete lack of egg laying.…”

“…Although the Ae. aegypti genome does not contain a recognizable SP gene (our unpublished genome searches), neither does the genome of H. armigera, where SPR is necessary for inducing post-mating responses (HANIN et al 2012;LIU et al 2021).…”

“…Injection of D. melanogaster SP into the cotton bollworm, Helicoverpa armigera (which has no obvious SP gene in its genome) suppressed sex pheromone production leading to decreased calling behaviors; these effects did not occur if SPR was knocked down simultaneous with SP injection, indicating SP function is through SPR (HANIN et al 2012). Moreover, H. armigera females with little to no SPR laid significantly fewer eggs after mating and displayed altered pheromone calling behavior and remating rates after 24 and 48 h (HANIN et al 2012;LIU et al 2021). A reproductive role for SPR was also reported in the tobacco cutworm (Spodoptera litura): females with SPR knockdown laid fewer eggs than controls after injection of male accessory gland lysate and remained receptive to mating (LI et al 2014).…”