The Interaction of Immune Priming with Different Modes of Disease Transmission

Immune priming in invertebrates is most commonly described as an increase in survival (Roth et al., 2010) or the strength of an immune response (Moret, 2006) against a microbe to which the host has been previously exposed. Because priming alters epidemiologically relevant parameters like disease-induced mortality and recovery, priming is likely to impact the spread, and persistence of diseases in invertebrate populations. Early modeling efforts have explicitly incorporated priming into disease transmission frameworks by allowing exposed (Tidbury et al., 2012) or previously infected but recovered (Tate and Rudolf, 2012) individuals to transition into a primed compartment. There, they are less likely to become infected and infectious upon subsequent exposure, but may suffer reproductive or developmental costs stemming from the physiological costs of maintaining a primed immune response. Conflating infected and infectious states, however, obscures the impact of priming on the correlative and dynamical relationships (Day, 2003; Berenos et al., 2009) between parasite replication, pathology, and transmission. In directly transmitted infections, for example, parasite replication tends to be correlated with transmission, while pathology is often a byproduct of exploitation rather than a means of securing transmission (Roode et al., 2008). In fact, excessive pathology may curtail transmission by killing the host. In cases where peak pathology and peak transmission exhibit a time lag, an SEI (Susceptible-Exposed-Infectious)-type framework can be adapted to reflect different host fitness costs in infected and infectious states by allowing the latent “Exposed” compartment to experience pathology and disease-induced mortality. However, many pathogens of insects are obligate killers (Ebert and Weisser, 1997), meaning that they must kill the host in order to achieve transmission. There, the infected and infectious states are entirely separate, and pathology exerts a binary response on transmission (killing the host or not), although parasite replication will quantitatively affect transmission rates (Raymond et al., 2009) in hosts that do succumb. While priming is often modeled in the context of direct transmission (Tate and Rudolf, 2012; Tidbury et al., 2012; Best et al., 2013), many microbes against which priming has been successfully demonstrated, including Bacillus thuringiensis in beetles (Roth et al., 2010; Milutinović et al., 2013; Tate and Graham, 2015), Paenibacillus larvae in bees (Hernández López et al., 2014), and baculoviruses in moths (Tidbury et al., 2010), exhibit obligate killer dynamics in nature (Tate, 2016).To illustrate the impact of transmission mode on the stability of a disease-free equilibrium (DFE) in insect populations in the context of parameters thatmight reflect priming, we can consider an analytically tractable model of three ordinary differential equations: