Pathogen persistence in migratory insects: high levels of vertically-transmitted virus infection in field populations of the African armyworm
- 259 Downloads
Pathogens face numerous challenges to persist in hosts with low or unpredictable population densities. Strategies include horizontal transmission, such as by the production of propagules that persist in the environment, and vertical transmission from adults to offspring. While many pathogens are capable of horizontal and vertical transmission little is known of their relative roles under realistic conditions of changing population densities. Insect baculoviruses can be transmitted both horizontally and vertically, although much of the work on baculovirus transmission has focussed on horizontal transmission that can be effective at high host densities. Here, we examine the prevalence of a vertically-transmitted, covert infection of nucleopolyhedrovirus (NPV) in field populations of the African armyworm, Spodoptera exempta, in Tanzania. African armyworm is a major pest of graminaceous crops in Africa and despite its migratory nature and boom and bust dynamics, NPV epizootics are common and can be intense at the end of the multi-generation armyworm season. We found that virtually all the insects collected in the field were positive for S. exempta NPV (SpexNPV) DNA and 60% of these insects had transcriptionally active virus. This suggests that SpexNPV is transmitted vertically at extremely high levels in field populations of S. exempta and can maintain a persistent infection without obvious symptoms. Similarly high levels of virus DNA and RNA were detected in a S. exempta colony that had been maintained in continuous culture for 5 years. This study provides an insight into mechanisms of pathogen persistence in migratory populations where hosts are unpredictable and indicates that covert infection may be more common and more relevant in disease dynamics of insects than had previously been thought.
KeywordsCovert infection Latency NPV Persistence Sublethal Epizootic
We would like to thank Tim Carty for rearing the laboratory colony of S. exempta and for producing insect diet and John Burden for advice on PCR. We are also very grateful to Wilfred Mushobozi and colleagues in Arusha, Tanzania, for their input and support in the field and David Gryzwacz for his encouragement and support throughout the project. We would also like to thank David Grzywacz and Judy Myers for their comments on the manuscript and Hilary Lauzon for help with Fig. 2. This work was funded by NERC grant NER/A/S/2000/01141 to JSC and KW and partly funded by the United Kingdom Department for International Development (DFID) for the benefit of developing countries. The views expressed are not necessarily those of the DFID R7954 Crop Protection Research Programme. JSC would also like to acknowledge the support of the NSERC Canada Research Chair program.
- Chao Y-C, Lee S-T, Chang M-C et al (1992) Differential expression of Hz-1 baculovirus genes during productive and persistent infections. J Virol 63:1442–1448Google Scholar
- Federici BA (1997) Baculovirus pathogenesis. In: Miller LK (ed) The baculoviruses. Plenum Press, NY, pp 301–339Google Scholar
- Funk CJ, Braunagel SC, Rohrmann GF (1997) Baculovirus structure. In: Miller LK (ed) The baculoviruses. Plenum Press, NY, pp 7–32Google Scholar
- Herniou EA (2003) Use of comparative genomics and phylogenetics to study the evolution of the Baculoviridae. Imperial College, University of London, Unpublished Ph.D. thesisGoogle Scholar
- Hunter FR, Crook NE, Entwistle PF (1984) Viruses are pathogens for the control of insects. In: Grainger JM, Lynch JM (eds) Microbiological methods for environmental biotechnology. Academic Press, NY, pp 323–347Google Scholar
- Lively CM, Clay K, Wade MJ et al (2005) Competitive co-existence of vertical and horizontally transmitted parasites. Evol Ecol Res 7:1183–1190Google Scholar
- Lu A, Miller LK (1995) The roles of eighteen baculovirus late expression factor genes in transcription and DNA replication. J Virol 69:475–482Google Scholar
- Moore J (2002) Parasites and the behaviour of animals. Oxford University Press, OxfordGoogle Scholar
- Rose DJW, Dewhurst CF, Page WW (2000) The african armyworm handbook: the status, biology, ecology, epidemiology and management of Spodoptera exempta (Lepidoptera: Noctuidae), 2nd edn. Natural Resources Institute, ChathamGoogle Scholar
- Stewart AD, Logsdon JM, Kelley SE (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evol Int J Org Evol 59:730–739Google Scholar