Wednesday, October 17, 2012

Guppies, predators, and parasites

As many people who follow the blog know, there is a lot of work being done on Trinidadian guppies. Just in case you don't know about guppies, a quick overview. Guppies are native to Venezuela and Trinidad, and in the northern mountain range of Trinidad, it so happens that there is a lovely playground for evolutionary biologists. Starting with Ben Seegher's PhD thesis and continued by very cool scientists like John Endler, David Reznick, Helen Rodd, and Anne Magurran, the guppy became a model system for rapid adaptation. Guppies in low predation areas are more colourful and differ in life history and behavioural traits, among many other things, as compared to guppies that co-habit with dangerous predators. For the purposes of our paper, we focus on male colour, a well known adaptive trait in the guppy.

Pretty guppies.
Photo by Paul Bentzen

The spatial variation in predator composition means guppies have to adapt to their environment to be able to reproduce, and thus, a lot of work has focused on the effects of predation or surveyed differences among populations in relation to the predation level. However, we know life for guppies is very complicated, and that there are other selective pressures acting on them, including parasitism. If we think of adaptation beyond a single causal force, what happens? Will it alter our perceptions of the original causal force? Will the causes interact? Could it be a stronger force than the original one? To address these questions of uni- vs. multi-factorial causes of variation in phenotype, we looked at the effects of both predation and parasitism on male guppy colour.

A pike cichlid, one of the predators
Photo by Kiyoko Gotanda

While there are many ways to consider the effects of parasitism, we chose to focus on the ectoparasite Gyrodactylus spp because previous work has shown that Gyros (as we affectionately call them) can affect a number of traits that also differ between high predation (HP) populations and low predation (LP) populations. The parasite is transferred through fish contact, and we also know that parasitism levels vary considerably in natural populations. We can see Gyros through a stereo-microscope, which means we can assess parasitism levels in the field.

Based on previous work, we know Gyros can impose selection by affecting survival, growth rate, and reproductive success. We also know Gyros can have an effect on behaviour, body size, and colouration, so it is not unreasonable for one to think parasitism can impose selection on phenotypic traits. However, relatively few of these studies are field studies, so we seek to fill that lack of information by building on previous field-surveys.

A Gyro
Photo by Joanne Cable

Specifically, the question we sought to answer was "whether or not parasitism by Gyrodactylus leaves a signature on guppy phenotypes in nature," and by phenotypes, we mean things like male colour. As stated above, we know predation is an important selective agent driving guppy colour where HP fish have less colour than LP fish. Based on previous work, we would expect parasitism to have a negative effect on guppy colour. High rates of parasitism would be expected to lead to lower levels of colour. Thus, if we jointly consider predation and parasitism, is parasitism as important in driving colour differences as predation? Can parasitism modify our perceptions of the effect of predation on guppy colour? To determine this, we surveyed 26 natural populations of guppies in Trinidad. As cool as the science was, I think everyone enjoyed the break from Canadian winters the most... We sample with butterfly nets. How cool is that?

Here guppy, guppy, guppy
Photo by Kiyoko Gotanda

If you want to know our methods, you can check us out online for the details. It involves equipment, chemicals, a digital camera, and a lot of audiobooks. Or you can ask in the comments or email me. I won't bite. I promise.

So what did we find? Well, first, we found that when we sample around the same time in two subsequent years, the parasitism levels are pretty consistent, that parasitism levels among populations varied quite a bit, and that parasitism levels were generally higher in HP sites than in LP sites.  This is consistent with previous surveys, and we speculate this could be because (1) flooding might sweep infected fish downstream from LP to HP populations, (2) HP guppies like to shoal more than LP guppies, possibly increasing transmission, (3) susceptibility might be higher in HP populations, and (4) HP sites might differ ecologically in ways conducive to parasite infection.

But what about colour? Did parasitism have an effect on male guppy colour? Well, interestingly, it appeared not to. Lab studies have shown an effect of parasitism on guppy colour, but we didn't find any direct effects of parasitism on male colour. In fact, a previous field survey didn't find an association with orange colour and parasitism either. So what gives? We have a couple of ideas on why things might be detected in the lab, but not in nature. First, our field survey was a snapshot survey, so we don't know a given guppy's infection history or what the population parasitism levels were like before or after the survey. We know that Gyro epidemics increase and decrease quite rapidly, so it's possible our measures of parasitism are not a true representation of parasitism levels. Second, lab studies can control for a lot of things such as light and resources. We can't control nature, so there might be variation in other selective agents that prevented us from detecting a parasite signature on colour patterning. Third, mortality of infected or uninfected fish can differ, potentially altering parasite and colour distributions.

So we didn't find a significant effect of parasitism on guppy colour. But what if we throw predation back into the story? Does parasitism modify our conclusions about the effect of predation on colour? When considering predation, our results were congruent with what we expected a priori: males in LP sites had more colour than HP sites in general. But we had a lot of variation. It wasn't a clear cut story. Some HP sites had more colour than some LP sites. Previous work has also found similar differences and nuances, and from this, we can conclude that predation IS an important selective agent on guppies, but it's a lot more complicated than just predation alone.

We now ask "does the predation regime story benefit from a simultaneous consideration of parasitism?" Well, we didn't find an effect of parasitism on colour, and adding a parasitism term to our models almost never affected our conclusion about the effect of predation. We still must consider the potential drawbacks of field surveys, but based on our data, we find that parasitism does not modify our interpretation of the effects of predation.However, we are not saying parasitism has no effect, but rather that the signature of an effect of parasitism on male guppy colour might be swamped by other selective agents (e.g. predation) leaving us unable to detect a significant effect of parasitism on colour.

So, in a nutshell, we found that parasites vary between populations and were relatively consistent when assessed over two years, higher infection levels are often found at HP sites as compared to LP sites, parasitism doesn't appear to have an effect on male guppy colour, and considering parasites does not alter our current conclusions about predation.

That's all she wrote!

Pretty snake
photo by Kiyoko Gotanda

Reference:  Gotanda K.M., Delaire L.C., Raeymaekers J.A.M., PĂ©rez-Jvostov F., Dargent F., Bentzen P., Scott M.E., Fussmann G.F. & Hendry A.P. (2013). Adding parasites to the guppy-predation story: insights from field surveys. Oecologia.172(1): 155-166. DOI: 10.1007/s00442-012-2485-7

Friday, October 5, 2012

Indirect Genetic Effects and Eco-Evo Feedbacks

I’ve enjoyed reading through some of the recent entries of this blog and I’m very happy to be invited to contribute. I hope that the ideas of using indirect genetic effects as part of research into eco-evo feedbacks will be interesting.

In a new paper, out in Ecology Letters, we examined how genotype by genotype (G x G) interactions affected plant productivity and pollinator visitation.  We used three genotypes each of Solidago altissima and Solidago gigantea, planted together in monocultures and all interspecific combinations. After two years of growth in large, outdoor pots, we examined pollinator visitation rates and destructively sampled the plants to obtain biomass measurements for flowers, stems and leaves, rhizomes, and coarse roots. We found that neighbor plants exerted particularly strong influences on the belowground phenotype of focal plants. The presence of strong, genetically-based, belowground interactions among neighboring plants makes sense given the expectation of resource, rather than light, limitation. The neighbor genotype effects described above can be considered indirect genetic effects (IGEs), which are influences on the phenotype of a focal individual due to the expression of genes in an interacting individual. To be precise with terminology, we’d call the IGEs in our study interspecific indirect genetic effects (IIGEs), because the interacting individuals were members of different species. 

Earlier I mentioned that we also measured pollinator visitation. We found that genotype by genotype (G x G) interactions influenced how many pollinators visited focal plants. Although we don’t know the mechanism for sure, it may be that synchronicity (or the lack thereof) in flowering times between neighboring genotypes influenced pollinator visitation. Because we didn’t detect G x G interactions for any biomass traits, it’s likely that the mechanism goes beyond variation in productivity due intransitive competitive relationships between interacting genotypes. Whatever the mechanism, G x G interactions are a fundamental unit of the coevolutionary process, suggesting that it is possible that, over many generations, we could observe coevolutionary interactions between genotypes driving changes in the composition of associated communities.

IGEs show that evolutionary forces acting on an individual’s phenotype can come from multiple sources – changes in that individual’s genotype or changes in the genotypes of interacting individuals. Additionally, models approaches have suggested that evolution can occur much faster when phenotypes interact (see Moore et al. 1997). So, in line with this blog’s recent “Kumbaya” spirit, I’d suggest that IGEs and IIGEs could be an important concept that can help unite community genetics, niche construction, ecological genetics, and so on. Perhaps IIGEs could be the arrow that connects “communities” and “phenotypes”, or they could result in changes to a focal plant’s phenotype that affects its interactions with other species. Either way, in my view eco-evo feedbacks are complex and applying names and definitions to the interactions which make up the feedback helps to simplify the issue.

Thursday, October 4, 2012

Carnival of Evolution #52

Carnival of Evolution #52 is up!  Our contribution this time around comes from Andrew Hendry, musing about the ecosystem services perspective and its implications: Ecosystem disservices and assisted elimination.

Posts in the Carnival are, as usual, about every topic under the evolutionary sun; however, the theme of this edition of the Carnival is phylogenetic networks: