Costs of resistance and infection by a generalist pathogen

Abstract Pathogen infection is typically costly to hosts, resulting in reduced fitness. However, pathogen exposure may also come at a cost even if the host does not become infected. These fitness reductions, referred to as “resistance costs”, are inducible physiological costs expressed as a result of a trade‐off between resistance to a pathogen and aspects of host fitness (e.g., reproduction). Here, we examine resistance and infection costs of a generalist fungal pathogen (Metschnikowia bicuspidata) capable of infecting a number of host species. Costs were quantified as reductions in host lifespan, total reproduction, and mean clutch size as a function of pathogen exposure (resistance cost) or infection (infection cost). We provide empirical support for infection costs and modest support for resistance costs for five Daphnia host species. Specifically, only one host species examined incurred a significant cost of resistance. This species was the least susceptible to infection, suggesting the possibility that host susceptibility to infection is associated with the detectability and size of resistance cost. Host age at the time of pathogen exposure did not influence the magnitude of resistance or infection cost. Lastly, resistant hosts had fitness values intermediate between unexposed control hosts and infected hosts. Although not statistically significant, this could suggest that pathogen exposure does come at some marginal cost. Taken together, our findings suggest that infection is costly, resistance costs may simply be difficult to detect, and the magnitude of resistance cost may vary among host species as a result of host life history or susceptibility.

age at pathogen exposure and the relative difference in total reproduction, mean clutch size, and lifespan between exposed-uninfected and infected individuals of the same age (infection costs), and exposed-uninfected and resistant hosts of the same age (resistance costs). We found no evidence that host age at pathogen exposure influenced resistance ( Figure S3) or infection ( Figure S4) costs, except for a positive relationship between host age and the magnitude of resistance cost in terms of total reproduction for D.
pulicaria. This means that there was a greater difference in total reproduction between resistant and control hosts when hosts were older. The fact that Daphnia pulicaria, a host that has never, to our knowledge, been observed to be infected, incurred such a great cost of resistance, is curious and seemingly maladaptive, when the probability of becoming infected is low (or null).

The potential relationship between host susceptibility and resistance costs
The relative per-species difference between exposed-uninfected host individuals and control individuals (i.e. resistance cost size) was dependent on host species susceptibility ( Figure S5), but not when including data from D. dentifera ( Figure S6). This difference was calculated by sampling control and resistant hosts of a single species, truncating the control host samples to be the same length as the resistant host samples, and taking the difference between the means. This was performed 1000 times for each host species and fitness metric combination, which allowed the plotting of both mean and standard deviation of the mean difference between control and resistant hosts.
The use of a single clone of each host species examined makes interspecific comparisons difficult, as there could be large intraspecific variation in physiological responses to pathogen exposure. We therefore do not make any claims regarding the generality of the relationship between resistance cost and host susceptibility. However, this is an interesting open question, as the answer could potentially provide a more mechanistic or evolutionary perspective on interspecific differences in resistance costs. Specifically, perhaps host species are less susceptible because they mount such a large resistance effort.
Understanding the mechanistic basis of interspecific variation in resistance costs is an interesting, and currently largely unexplored research area.
2 Table S1: Mean and standard error for fitness measures (reproductive output, lifespan, and mean clutch size) for control, exposed-uninfected, and infected individuals. Host species are ordered from most to least susceptible to infection by M. bicuspidata.

Host
Infection   Figure S2: Costs of resistance and infection to a generalist fungal pathogen. This is the same as the main text Figure 1, but includes D. dentifera, who was excluded because of high mortality observed.  Figure S4: Infection costs along a gradient of host age at pathogen exposure. Infection costs were unrelated to host age at pathogen exposure, except for reproduction of D. dentifera, though this host was excluded from analyses, and the age effect on change in total reproduction is small. 7  Figure S5: Resistance costs scale with host susceptibility. The difference between means (calculation described above) is plotted for 1000 bootstrapped samples. Plotted points are mean differences +-1 standard deviation. Grey lines are linear models for illustrative purposes, though the relationship is significant for lifespan (adj. R 2 = 0.911, p = 0.03).  Figure S6: Resistance costs scale with host susceptibility, but not when D. dentifera is included. The difference between means (calculation described above) is plotted for 1000 bootstrapped samples. Plotted points are mean differences +-1 standard deviation. Here, we include D. dentifera, though this host species suffered enhanced mortality early in the experiment, and was subsequently removed from our analysis.