High-resolution analysis of baculovirus-induced host manipulation in the domestic silkworm, Bombyx mori.

Susumu Katsuma,Hiroyuki Hikida

doi:10.1017/s0031182020001924

Abstract

Many parasites manipulate host behaviour to enhance their transmission. Baculoviruses induce enhanced locomotory activity (ELA) combined with subsequent climbing behaviour in lepidopteran larvae, which facilitates viral dispersal. However, the mechanisms underlying host manipulation system are largely unknown. Previously, larval locomotion during ELA was summarized as the distance travelled for a few minutes at several time points, which are unlikely to characterize ELA precisely, as ELA typically persists for several hours. In this study, we modified a recently developed method using time-lapse recording to characterize locomotion of Bombyx mori larvae infected with Bombyx mori nucleopolyhedrovirus (BmNPV) for 24 h at 3 s resolution. Our data showed that the locomotion of the mock-infected larvae was restricted to a small area, whereas the BmNPV-infected larvae exhibited a large locomotory area. These results indicate that BmNPV dysregulates the locomotory pattern of host larvae. Furthermore, both the mock- and BmNPV-infected larvae showed periodic cycles of movement and stationary behavior with a similar frequency, suggesting the physiological mechanisms that induce locomotion are unaffected by BmNPV infection. In contrast, the BmNPV-infected larvae exhibited fast and long-lasting locomotion compared with mock-infected larvae, which indicates that locomotory speed and duration are manipulated by BmNPV.

Highlights

Manipulation of host behaviour is a strategy commonly used by parasites to enhance their proliferation in the environment (Moore, 2002)
Each mock- or B. mori nucleopolyhedrovirus (BmNPV)-infected larva was placed in a cell culture dish with a portion of artificial diet and its locomotion was recorded for 24 h from 72 hpi when typical enhanced locomotory activity (ELA) was not observed
BmNPV-infected larvae subsequently moved around the peripheral area of the dish and were rarely found at the centre at late stages of infection, whereas mock-infected larvae remained primarily at the centre of the dish (Fig. 2A and B)

Summary

Introduction

Manipulation of host behaviour is a strategy commonly used by parasites to enhance their proliferation in the environment (Moore, 2002). Hairworms cause crickets to jump into the water, where the hairworms can search for their mates (Thomas et al, 2002), and Ophiocordyceps fungi make ants to bite onto vegetation at an elevated position, which is thought to enable the fungi to disperse their spores (Andersen et al, 2009). Baculovirus-infected larvae exhibit horizontal hyperactivity, which is called enhanced locomotory activity (ELA), followed by vertical movement, which is known as climbing behaviour (CB) or tree-top disease. These virus-induced host manipulations lead the larvae to the upper plant foliage, where they die. The combination of larval death at an elevated position, and liquefaction of their body is thought to facilitate viral dispersal with rainfall or avian predation (Entwistle et al, 1993; D’Amico and Elkinton, 1995)

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Conclusion