Within and transgenerational immune priming in an insect to a DNA virus

Abstract

Invertebrates mount a sophisticated immune response with the potential to exhibit a form of immune memory through 'priming'. Increased immune protection following early exposure to bacteria has been found both later in life (within generation priming) and in the next generation (transgeneration priming) in a number of invertebrates. However, it is unclear how general immune priming is and whether immune priming occurs in response to different parasites, including viruses. Here, using Plodia interpuctella (Lepidoptera) and its natural DNA virus, Plodia interpunctella granulosis virus, we find evidence for both within generation and transgeneration immune priming. Individuals previously exposed to low doses of virus, as well as the offspring of exposed individuals, are subsequently less susceptible to viral challenge. Relatively little is known about the mechanisms that underpin viral immunity but it is probable that the viral immune response is somewhat different to that of bacteria. We show that immune priming may, however, be a characteristic of both responses, mediated through different mechanisms, suggesting that immune memory may be a general phenomenon of insect immunity. This is important because immune priming may influence both host-parasite population and evolutionary dynamics.

Figure 1.

Experimental design. (a) Within generation priming experiment. Second instar larvae (8 days) were collected from the food and starved. Half were orally primed with virus solution of concentration equivalent to LD₁ and the other half were primed with control solution. When these larvae reached fourth instar (14 days) they were orally challenged with virus solution of concentration equivalent to LD₅₀. To determine the level of infection that resulted from prime inoculation some larvae primed with virus were challenged with control solution. This figure outlines the procedure for one experimental block. This study was carried out in six blocks. (b) Transgeneration priming experiment. Third instar (11days) F₁ generation larvae were removed from six containers established from the same large outbred insect stock, kept separately and starved. Larvae from three containers were primed with virus of concentration equivalent to LD₁ and larvae from the other three containers were primed with a control solution. These primed larvae were left to develop and make six F₂ generations. The small number of larvae that became infected following the virus prime treatment were removed immediately once they showed symptoms. Third instar (11 days) F₂ generation larvae from each container were then challenged with virus solution of concentration equivalent to LD₅₀. This figure outlines the procedure for one experimental replicate. This study was carried out in six blocks with three replicates of virus prime and three replicates of control prime per block.

Figure 2.

Within generation priming, by exposure to low level virus, significantly reduced susceptibility of insects to a lethal virus challenge (F_1,10 = 9.22, p = 0.013). Open circles represent replicates, filled circles represent means ± s.e.

Figure 3.

Transgenerational immune priming, by exposing parents to low level virus, significantly reduced the susceptibility of offspring to lethal virus challenge (F_1,32 = 7.13, p = 0.012). Open circles represent replicates, filled circles represent means ± s.e.