The regulation of daily activity and feeding rhythms of the economically impactful lepidopteran pest Plutella xylostella

Abstract

Life forms have evolved mechanisms to remain ‘in time’ with the daily cycles of the planet. These circadian rhythms are often maintained via highly conserved molecular components called circadian clocks. These clocks regulate numerous physiological responses to both abiotic and biotic factors that can determine the effectiveness of pest management strategies. The diamondback moth, Plutella xylostella, is arguably the most economically impactful and widespread lepidopteran pest, having achieved a cosmopolitan distribution, causing ~$5 billion worth of damage annually. P. xylostella specializes in feeding on Brassica host plants and cruciferous crops while adult moths spread to fresh fields in a seasonally expanding range. Unique glucosinolate sulfatase enzymes allow P. xylostella to neutralize the glucosinolate/myrosinase defence system, which their host plants employ in a rhythmic fashion. Given the widespread impact of daily timekeeping on both plant and insect physiology, it is important to understand how both P. xylostella adult activity and larval feeding are controlled by internal and environmental rhythms. Our results showed that daily locomotor activity rhythms of adult moths resulted from a combination of light-mediated repression and homeostatic control of activity levels with little reliance on the circadian clock. However, qPCR results demonstrated the presence of molecular circadian clock components in adults that were maintained into constant conditions. Larval feeding rhythms also showed signs of light-mediated suppression, showing typical nocturnal feeding rhythms across conditions, however, they also exhibited circadian control under constant light conditions where they damped out gradually. This indicated circadian clock-controlled herbivory which when in-phase with host plants showed minimal feeding around dawn and maximal around dusk. Comparison of herbivory on in-phase versus out-of-phase leaves indicated that both the phase of the larval and host plant clocks helped determine recorded daily feeding rhythms. Moreover, similar circadian rhythms to adults were demonstrated for P. xylostella larval transcripts encoding core molecular clock components. In addition, the above-mentioned glucosinolate sulfatases were also shown to maintain relative expression at particular times of day in larvae, suggesting a mechanism underlying the timing of herbivory. Herbivory rhythms were also maintained across host plants, however, when clock and jasmonic acid mutant hosts were used, feeding was significantly altered. This demonstrates that the phase and rhythm of host plant clocks significantly affect P. xylostella feeding, potentially through defence volatile signalling. These findings have potential implications for the temporal control of reproduction, migration and crop damage by P. xylostella and may be useful for informing integrated pest management strategies.

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ORCID for Connor Tyler: orcid.org/0000-0002-9849-4074

ORCID for Herman Wijnen: orcid.org/0000-0002-8710-5176

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