Variation in Infection Prevalence

Why do we see so much infection in some places, some hosts, some species, and much less in others? What are the ecological and genetic drivers of this variation?

Fine-scale spatial variation in infection prevalence

My study lake, Lake Alexandrina, is not big, only 6.4 square kilometers (shown below). Some of our study sites are within 150 meters of one another. Nonetheless, decades of field sampling show dramatic spatial and temporal variation in the proportion of snails infected with Microphallus along the shoreline of Lake Alexandrina (Jokela et al. 2009, Gibson et al 2016 Am Nat). For example, nearly 70% of snails may be castrated by Microphallus at one site, while, at a nearby site, practically 0% are infected. What explains such variation between nearby sites?

Lake Alexandrina

Do hosts from different sites vary in how susceptible they are, genetically, to local Microphallus? Given the high rates of gene flow between snails from different sites at Lake Alexandrina (shown by analysis of neutral markers – Fox et al. 1996, Paczesniak et al. 2014), we might expect that migration and gene flow between nearby sites would erode genetic variation for susceptibility. Hence environmental variables should be a bigger factor in explaining variation in Microphallus prevalence at this spatial scale.

Not so! (see Gibson et al. 2016 Am Nat) There is up to 6.5-fold variation in susceptibility of snails from different sites to local Microphallus. Moreover, mean susceptibility explains one-third of the variation in infection prevalence between sites: sites with a greater proportion of snails susceptible to Microphallus also had higher prevalence of Microphallus, on average. Because susceptibility has a strong genetic basis, we take this as evidence for a substantial contribution of host genetic variation to variation in infection prevalence.

We have preliminary data suggesting that the remaining ~2/3 of the variation in infection prevalence between sites may arise from spatial variation in exposure, with snails at some sites getting exposed to more parasites than others. Snails acquire Microphallus from duck feces – we currently know relatively little about how duck distribution and behavior contributes to the distribution of Microphallus eggs in the water.

life cycle
Potamopyrgus antipodarum (left) and its trematode parasite Microphallus. In the center, you can see a healthy snail (shell removed) vs. an infected snail, which is packed full of larval trematodes or metacercariae. They have replaced the snails gonads, castrating it!  Microphallus is a complex life cycle parasite – it travels trophically from snails to duck guts to duck poop back to snails. Image on the left courtesy of Bart Zjilstra. Central image courtesy of Gape Harp, used under Creative Commons BY-SA 4.0. Modified from originals: images combined, line and text elements added.

Escaping smut

I asked similar questions for the fungus Microbotryum violaceum, which causes anther-smut disease in the Caryophyllaceae family (learn more here). To briefly summarize here:

Microbotryum is absent from rare species in the Silene genus, and this seems to be due to limited transmission opportunities in small, fragmented populations. We find that this pattern is quite general: federally endangered plant taxa have lower fungal pathogen richness than non-endangered relatives (Gibson et al. 2010 Oikos).

Anther smut is also noticeably absent from annual species – 80% of perennial Silene host species are host to M. violaceum, while no annual Silene species is known to naturally host the disease (Thrall et al. 1993, Hood et al. 2010). We showed that annuals can acquire the disease via direct inoculation – in other words, they’re susceptible to infection. Their lack of infection in the wild is thus very likely to be a direct result of their ecology. The life cycle of Microbotryum is such that the annual habit prevents transmission. We also show that this “ecological protection” selects against other forms of costly resistance in annual taxa (Gibson et al. 2013 Ecol Evol).

Silene-Microbotryum is also a fascinating system to study host shifts, hybridization, and speciation. These are particularly important topics in fungal pathogens – hybridization has led to the formation of new fungal species that emerge to devastate novel hosts (e.g. strains of Batrachochytrium dendrobatidis causing amphibian chytrid epidemics). Gibson et al.(2012 Evolution) shows that host shifts, hybridization and speciation are limited by 1) selfing in M. violaceum and 2) competition between selfed and hybrid lineages (which the hybrid tends to lose). Gibson et al. (2014 Int J Plant Sci) shows that hybrids in M. violaceum don’t necessarily have novel host ranges – rather, there’s a clear host-parasite genotype interaction that determines hybrid success.



  • Fox, J., M. F. Dybdahl, J. Jokela, and C. M. Lively. 1996. Genetic structure of coexisting sexual and clonal subpopulations in a freshwater snail (Potamopyrgus antipodarum). Evolution 50:1541-1548.
  • Hood M.E., J.I. Mena-Alí, A.K. Gibson, B. Oxelman, T. Giraud, R. Yockteng R, M.T.K. Arroyo, F. Conti, A.B. Pedersen, P. Gladieux, and J. Antonovics. 2010. Distribution of the anther-smut pathogen Microbotryum on species of the Caryophyllaceae. New Phytol. 2010;187:217–229.
  • Jokela, J., M. F. Dybdahl, and C. M. Lively. 2009. The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. Am Nat 174:S43-S53.
  • Paczesniak, D., S. Adolfsson, K. Liljeroos, K. Klappert, C. M. Lively, and J. Jokela. 2014. Faster clonal turnover in high-infection habitats provides evidence for parasite-mediated selection. J Evol Biol 27:417-428.
  • Thrall P.H., A. Biere , and J. Antonovics J. 1993. Plant life-history and disease susceptibility–the occurrence of Ustilago violacea on different species within the Caryophyllaceae. J Ecol 81:489–498.




parasites coevolution sex