Resistance, Tolerance and Host CompetenceSubmitted by editor on 17 August 2021.Get the paper!
Parasite spread in experimental metapopulations: Resistance, Tolerance and Host Competence
Understanding why some individuals transmit infectious disease more than others has been a goal of epidemiologists and disease ecologists for quite some time, however most of the focus thus far has been on behaviour and contact rates. We suspected that host defense against parasites would also play an important role in their competence (ability to transmit infection). In theory, a more resistant host (one that is able to limit/fight off infection more easily) would have fewer parasites and therefore a lower probability of transmitting them when contacting another individual. A tolerant host (one that is better able to limit the damage caused by infection) on the other hand, may be infected with more parasites for a longer period of time, and therefore increase its probability of infection (See Fig. 1).
Figure 1: Resistance and tolerance to parasites in relation to host fitness and parasite burden
Our study system, guppies and Gyrodactylus turnbulli is a pretty good candidate for investigating whether resistance and tolerance influence competence because these live on the skin of the host and are easily quantifiable without destructive sampling, meaning that we can track infection burdens on individuals over time However, we did hit one snag: the parasites are identical and therefore cannot be traced from individual to individual. Luckily, we had a data set from a previous metapopulation experiment (See Fig. 2 for design) that could help get around this issue. Since fish were moved one at a time into a new tank, we could use the number of previously uninfected fish that became infected immediately after an individual’s introduction as an estimate of that individual’s competence (making some adjustments to account for an individual’s “opportunity” to transmit to an uninfected hosts).
Figure 2: Experimental design of metapopulation. For a full description of the experiment see (1)
We found that resistance was negatively correlated with competence, as we expected given our hypothesis that less resistant fish have more parasites and therefore a greater probability of transmission, which was also consistent with previous work done in this system (2). However, we also found that tolerance was negatively correlated with competence, opposite to our hypothesis. We consider two possible explanations for this finding that would be interesting to follow-up. One, we also found that more tolerant fish were larger, and it’s possible that these fish may serve as a better resource for the parasite, making them less likely to transfer. This would be consistent with previous work in this system that found when parasites were introduced on fish of high relative body condition, they tended to aggregate on that fish rather than spread throughout the population (3). The second potential explanation has more to do with the design of our experiment. We found that parasite load when moved, a significant predictor of the number of new infections and the hypothetical mechanism through which defense against parasites may influence competence, was actually negatively correlated with tolerance. It is possible that fish that survived longer were more likely to be moved with lower parasite loads than less tolerant fish that died earlier in the experiment. A follow-up experiment designed specifically around testing the relationship between tolerance and competence would be useful, as would one that examined the role of induvial behaviour in competence, which was excluded from this study. This project underlines the importance of individual host defense against parasites and its impacts on epidemic dynamics, and was also in interesting exercise in thinking about how these terms (resistance, tolerance and competence) are defined and selecting the best methods for measuring them within this system.
Figure 3: Always counting parasites
1. Tadiri CP, Scott ME, Fussmann GF. Microparasite dispersal in metapopulations: A boon or bane to the host population? Proceedings of the Royal Society B: Biological Sciences. 2018;285(1885).
2. Stephenson JF, Young KA, Fox J, Jokela J, Cable J, Perkins SE. Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts. Philosophical Transactions of the Royal Society B: Biological Sciences. 2017;372(1719):20160093.
3. Tadiri CP, Dargent F, Scott ME. Relative host body condition and food availability influence epidemic dynamics: a Poecilia reticulata-Gyrodactylus turnbulli host-parasite model. Parasitology. 2013;140(3):1-9.