Evolutionary ecology of host-parasite interactions

A while back I wrote a blog post (check it here) on how host adaptation to the predation environment could influence host-parasite coevolution. This happened to be my first blog post, and also my first chapter for my thesis. I specifically explored how guppy (Poecilia reticulata) adaptation to its ectoparasite, Gyrodactylus, can be influenced by their adaptation to predation. In that study, I found that both predation and Gyrodactylus parasitism induce similar phenotypic responses in guppies (i.e. reduction in growth and higher reproductive allocation), which led me to conclude that guppy adaptations to predation could reinforce adaptations to Gyrodactylus parasites, and vice versa. Another important point, which will be evident later in this blog post, is that there were also strong and repeated variations in guppy-Gyrodactylus dynamics across the different rivers, which was independent of predation – at the end of this series of blogs, you might come to realize I have a frustration with river effects!

Given the particular experimental design of my first study (for specifics check the published paper here), I was unable to disentangle the confounding effects between highly resistant hosts and highly virulent parasites, with those from low-resistant hosts and low-virulence parasites. This restricted any potential inferences on host-parasite adaptation. Thus, I decided to build on the previous experiment to assess local adaptation of guppies and Gyrodactylus, and to determine if such adaptation is influenced by the environment (i.e., predation) or evolutionary history (i.e., river).

The mesocosms where I performed the experiments.

In the so called arms race between parasites and their hosts, parasites have generally been expected to have an evolutionary advantage over their hosts due to short generation time and potentially high host specificity, and, thus, be locally adapted to their host. Yet this has been far –really far– from a universal rule. Studies on how additional sources of mortality could influence host-parasite local adaptation, and whether they prevent or facilitate host-parasite adaptation, are still largely missing– despite that they would help to better understand the mechanisms of local adaptation. For example, in the case of predation, we could expect that under increased guppy mortality (high-predation: HP), higher Gyrodactylus’ infectivity and transmission (i.e., virulence) would evolve, and this of course would in turn select for higher resistance in HP guppies. Thus, a priori, one would expect that local adaptation is facilitated in high-predation environments.

Of course, based on the results of my previous study –more on my fixation with river effects– differences between rivers could also be important drivers of guppy-Gyrodactylus local adaptation. This is because guppy populations from different rivers are genetically diverged, in part because they originated from independent colonization events, but also because different guppy evolutionary histories (i.e., selection, genetic bottlenecks and drift) could similarly influence guppy-Gyrodactylus coevolution in the various rivers in different ways. The predatory fauna in rivers from the northern and southern slopes is also drastically distinct: visual predators of the Cichlidae family are only present in the southern drainages, whereas the main predators in the northern drainages belong to the Eleotridae, a family of generalist ichthyophagous predators. Such differences in community composition could strongly influence the relative fitness costs associated with Gyrodactylus infections in the different rivers and, hence, guppy-Gyrodactylus local adaptation. If you are still wondering what I mean by guppy-Gyrodactylus local adaptation, I refer to locally adapted Gyrodactylus when they show higher performance when infecting their sympatric than with allopatric hosts, and locally adapted guppies when guppy performance is higher when infected with sympatric than with allopatric parasites.

 I will only briefly summarize the methods for this experiment, but if you are really eager to know more details you can check the published article here.

I used fully reciprocal cross infections with two guppy populations from the Marianne (one HP and one LP), and two from the Aripo river (one HP and one LP), and their corresponding sympatric Gyrodactylus ectoparasites. This design led to four sympatric pairs (hosts and parasites from the same locations) and 12 allopatric pairs (hosts and parasites from different locations) (Fig. 1).

Experimental design with Gyrodactylus infection dynamics.

We found that Gyrodactylus performance on their sympatric host was generally similar across populations (Fig. 2), but their performance when infecting allopatric guppies was dramatically different! In particular, Gyrodactylus from the Aripo performed the best (both as mean number of parasites/fish, as parasite population growth) when infecting guppies from the Marianne, but did poorly when infecting guppies from their own river.  This could indicate a higher infectivity, virulence and/or reproductive success of the Aripo parasites. Gyrodactylus from the Marianne, on the other hand, performed similarly on all hosts, or even slightly better when infecting their sympatric guppies.

Gyrodactylus performance on sympatric vs. allopatric hosts.

We found similar differences in guppy performance (Fig. 3). Aripo guppies were able to better limit Gyrodactylus population growth than guppies from the Marianne River, indicating their strong ‘‘resistance’’ to Gyrodactylus regardless of the source of the parasite. Surprisingly, predation environment had no detectable influence on host–parasite population dynamics of sympatric or allopatric combinations. The much stronger effect of river than predation emphasizes its importance in driving local co-evolutionary dynamics. Damn you, river effects!

Guppy performance when infected with sympatric vs. allopatric Gyrodactylus

At the end of the day, I think that this study demonstrates that, contrary to a priori expectations, Gyrodactylus coevolution is not deterministic, and could be influenced by historical demographic and evolutionary processes. This is an important aspect of host-parasite interactions that has been commonly neglected in studies of local adaptation, and this study demonstrates the need to incorporate them into future research on host-parasite coevolution.

The actual paper:

Pérez-Jvostov, F., Hendry, A. P., Fussmann, G. F. and Scott, M. E. 2015. Testing for host-parasite local adaptation: an experiment with Gyrodactylus ectoparasites and guppy hosts. Int J Parasitol, 45: 409-417.