Sex, Guppies and Parasitism

By: Christina Tadiri

Most of my work focuses on understanding guppy-Gyrodactylus interactions in the lab, and I’ve talked about some of my previous work with them here. These parasites are interesting because they don’t fit neatly into the macro-microparasite dichotomy that most ecologists use. On the one hand, they’re worms like a macroparasite, but on the other, they reproduce directly on the host and transmit via direct contact, like a microparasite. The important thing about them is that they cause epidemics, which can have eco-evolutionary implications and are therefore worth understanding a bit better.

Figure 1: A female and male guppy (L) and their ectoparasite Gyrodactylus turnbulli (not to scale, obviously). Photo credit Paul Bentzen (guppies) and Joanne Cable (Gyrodactylus)

My PhD thesis involves looking at how differences among hosts can impact epidemic dynamics at the population and metapopulation level. For my first study, I focused on sex, and if sex-based parasitism could influence the way these parasites spread among groups. Since guppies are sexually dimorphic (males and females look really different) there's reason to believe that the sexes might respond differently to the pressures of parasitism parasitism (as shown here), which could affect parasite dynamics at a larger scale. There have been a few other studies that looked at differences in epidemics of this parasite between males and females (this one and this one, for example), but a lot of the results were inconsistent, and these studies didn’t necessarily look at the implications at multiple levels of analysis.

First, I had to determine if sex was associated with a difference in parasitism, so I isolated individual male and female guppies and infected them all with parasites and counted how many parasites they got over the course of their infections. Then I also assembled and infected single sex groups of male and female guppies, to determine if any differences in parasites by sex translated to the population level. Finally I assembled mixed-sex groups, to see how they parasite dynamics played out once males and females were put together. You can read a bit more about the methods and analysis in the paper, but I’ll just go over our most interesting results here.

Figure 2: Total parasite population numbers over the course of the experiment in group tanks for male groups (a), female groups (b) and mixed-sex groups (c). Data are square-root transformed for graphing purposes, but were not transformed for analysis. For all panels, “Day 0” indicates the day on which at least 3 parasites were first found in the tank.

First, we found that isolated female guppies did have much higher parasite loads than isolated males. This could either be due to their larger size making it easier for them to harbor more parasites, or a difference in innate immune response. However, when we put fish in groups, we found no difference between males and females in the number of parasites per fish, nor the total number of parasites in the population, nor any of our other epidemic parameters. This of course meant that we also found no difference between our mixed and single-sex groups, since our single-sex groups were the same anyway. We also found that no matter what, parasites reached their peak earlier on males than on females (graph below).  We also found that relative condition (the metric we used for fish size) only influenced parasite load on isolated males (with larger ones having more parasite than smaller ones).

Figure 3: Mean peak burden (±SE) vs. mean time to peak (±SE) for individual fish in each treatment. SF: single (isolated) females, SM: single (isolated) males, FG: female groups, MG: male groups, MIX: mixed groups.

While these results seem a little underwhelming, we were surprised to find that differences that had mattered for isolated fish (sex, size) had no effect on parasite dynamics at the group level. These findings highlight the importance of studying host-parasite relations at a broader level, and can help to inform future experiments and models with this system. Of course, the pattern we observed may differ with fish from other populations, and further work is necessary to understand the dynamics of this unique host-parasite system. For the full story, you can check out the paper in Parasitology here.