Abstract
It is becoming increasingly apparent that trans-generational immune priming (i.e. the transfer of the parental immunological experience to its progeny resulting in offspring protection from pathogens that persist across generations) is a common phenomenon not only in vertebrates, but also invertebrates. Likewise, it is known that covert pathogenic infections may become 'triggered' into an overt infection by various stimuli, including exposure to heterologous infections. Yet, rarely have both phenomena been explored in parallel. Using as a model system the African armyworm Spodoptera exempta, an eruptive agricultural pest and its endemic dsDNA virus (Spodoptera exempta nucleopolyhedrovirus, SpexNPV), the aim of this study was to explore the impact of parental inoculating-dose on trans-generational pathogen transmission and immune priming (in its broadest sense). Larvae were orally challenged with one of five doses of SpexNPV and survivors from these treatments were mated and their offspring monitored for viral mortality. Offspring from parents challenged with low viral doses showed evidence of 'immune priming' (i.e. enhanced survival following SpexNPV challenge); in contrast, offspring from parents challenged with higher viral doses exhibited greater susceptibility to viral challenge. Most offspring larvae died of the virus they were orally challenged with; in contrast, most offspring from parents that had been challenged with the highest doses were killed by the vertically transmitted virus (90%) and not the challenge virus. These results demonstrate that the outcome of a potentially lethal virus challenge is critically dependent on the level of exposure to virus in the parental generation-either increasing resistance at very low parental viral doses (consistent with trans-generational immune priming) or increasing susceptibility at higher parental doses (consistent with virus triggering). We discuss the implications of these findings for understanding both natural epizootics of baculoviruses and for using them as biological control agents.
Highlights
Until recently, it was generally assumed that the innate immune system of invertebrates lack the specificity and memory of the vertebrate adaptive immune response (Fearon, 1997; McFall-Ngai, 2007; Netea et al, 2015)
Offspring from parents challenged with low viral doses showed evidence of ‘immune priming’; in contrast, offspring from parents challenged with higher viral doses exhibited greater susceptibility to viral challenge
These results demonstrate that the outcome of a potentially lethal virus challenge is critically dependent on the level of exposure to virus in the parental generation— either increasing resistance at very low parental viral doses or increasing susceptibility at higher parental doses
Summary
It was generally assumed that the innate immune system of invertebrates lack the specificity and memory of the vertebrate adaptive immune response (Fearon, 1997; McFall-Ngai, 2007; Netea et al, 2015). Vertical baculovirus transmission can be an important factor impacting the dynamics of lepidopteran populations, especially those of economic and agricultural importance (Graham et al, 2012) One of these is the African armyworm, Spodoptera exempta, a major pest in sub-Saharan Africa, attacking cereals such as maize, rice, millet and pasture grasses (Rose et al, 2000). The aim of this study was to simultaneously study the effects of trans- generational viral transmission and immune priming (in its broadest sense, to include mechanisms not directly associated with the host innate immune defences) in the offspring of virally challenged parents. We addressed the following questions: (a) How is the covert viral load of adult moths affected by the magnitude of the viral challenge they receive as larvae? (b) What is the trans- generational impact of parental viral dose on offspring mortality, fitness and covert viral load? (c) What is the trans-generational effect of parental virus challenge (and covert viral load) on offspring susceptibility to subsequent challenge with a heterologous virus strain?
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