This experiment changed our understanding of parasite resistanceS

It's common scientific wisdom that parasite resistance comes from repeated exposure to a parasite. But a new study has turned this idea on its head. Guppies who were removed from rivers swarming with parasites actually evolved an improved parasite tolerance in just a few generations. Here's how it happened.

In 2008, the National Science Foundation's Frontiers in Integrative Biological Research (FIBR) project set out to observe the process of adaptive evolution by tinkering with one species' ecosystem. University of California at Riverside evolutionary biologist David Reznick and his team collected guppies (Poecilia reticulata) from the Guanapo River on the island of Trinidad, off the northeastern coast of Venezuela. Then, they introduced the fish to four previously guppy-free tributary streams in the Guanapo River over a period of two years.

The "Nesting Dolls" That Kill

Though these bodies of water are part of the same overall system, the tributary streams and the main river provided vastly different habitats for the guppies. Most importantly, the Guanapo River is loaded with guppy predators, while the streams are not. The streams also have varying degrees of canopy covers, which block out the sun that promotes the growth of the guppies' main food source, algae. So these transplanted guppies were safer — but lacked a basic foodstuff.

And the researchers meddled even further in the guppies' new homes. "The FIBR researchers removed the parasites [Gyrodactylus] before they put the guppies into the streams," McGill University biologist Felipe Dargent told io9. Their removal was of special interest to Dargent, who studies the ecological interactions between parasites and hosts.

In their original river home, the guppies were plagued by Gyrodactylus, which live on their skin and spread between fish through physical contact. Aiding their spread is another biological quirk — the mother parasites have a fully developed embryo inside of them, and inside of that embryo is another embryo. "The parasites are quite neat — they're like Russian dolls," Dargent said. As adults, Gyrodactylus parasites have little claws that they use to move around on their host's body, feeding on skin and mucus all the while.

The parasites also transform the lives of their guppy hosts. For starters, they can affect sexual selection. If a male is infected, he will be less attractive to a female; if a female is infected, she will make poorer mate choices. The parasites also damage the skin, allowing bacterial and fungal infections to take root and kill the fish. And even without the help of microbial infections, Gyrodactylus can directly kill guppies if their numbers are great enough and the fish don't have the enough energy or resources to fight the parasites.

The Disappearing Parasite Test

When Dargent learned about Reznick's project, he thought FIBR would provide the perfect opportunity to test what happens to the fish when they no longer have to deal with parasites. Previous laboratory studies have shown that living a parasite-free life makes potential hosts more vulnerable to parasite infestation. Scientists believe that's because these hosts evolve poorer parasite resistance, and their bodies are less prepared to fight parasites and reduce their numbers. But that's in the lab. "The removal of parasites in nature has not been tested before," Dargent said.

For their experiments, Dargent and his colleagues collected fish from two of the streams one year (2009) and two years (2010) after the FIBR team relocated the guppies there. They collected additional guppies from the two other streams a year after their introduction (2010). They also collected fish from the Guanapo River source population, which they then treated for parasites. Given the fishes' breeding cycles, the guppies the researchers collected from the streams were fourth- and eighth- generation descendants of the Guanapo River source population.

This experiment changed our understanding of parasite resistance

Then, they bred the transplanted fish and the river fish in the lab for two more generations. This additional breeding was necessary to make sure that any differences in resistances the researchers found were not due to the sharp shift in environment, Dargent explained. "We wanted to see genetic changes, not just changes induced by the environment," he said. The researchers tried to mimic the conditions the guppies experienced in their original habitats by providing similar water, temperatures and amounts of food.

Next, the scientists infected the guppies with their ancient parasitic enemy. To their complete surprise, they found that the survival rates were significantly higher for the transplanted fish from the parasite-free streams in 2010, compared with the source population. These fish also had lower parasite loads than the River populations after 10 days of infection.

It seemed that the fish had rapidly evolved increased parasite resistance from living in the parasite-free streams. None of guppies evolved the decreased parasite resistance the researchers expected to see.

The Importance of the Slow-Paced Life

Dargent and his team ruled out a number of possible explanations for this odd discovery. For instance, they determined that the increased resistance was not due to some fish simply being more physically fit.

Previous studies have suggested that animals trade off resistance for tolerance — that is, if an individual is able to survive a high parasite load (tolerance), there's no point in putting energy towards getting rid of the parasites (resistance). The opposite could also be true. But the researchers found that the transplanted guppies' health had nothing to do with decreased tolerance, or the ability to mitigate the damage caused by parasites.

"If anything, they're evolving to have increased tolerance," Dargent said. "So this is what we're are left with: We think this evolution of increased resistance is being driven by the change in predation levels." Somehow, the lack of predators made these guppies more resistant to parasites. How could this happen?

This experiment changed our understanding of parasite resistanceS

In their initial river home, the guppies lived a "fast-paced life." Due to the large number of predators they had to deal with, the fish didn't have a very long life expectancy, so they matured quickly and had many babies. Because of their intense focus on reproduction, the fish didn't put much energy into parasite resistance — it didn't matter much if they succumbed to parasites because they were going to die soon anyway.

The fish in the streams, on the other hand, lived a "slow-paced life," where they matured gradually and had fewer babies with each birth cycle. But they produced more offspring over their long lives. Without the pressure from predators, they didn't need to devote so much of their resources towards growth and reproduction, and instead could invest some of that energy into parasite resistance (and possibly parasite tolerance). "When you have a slow pace of life, you will lose out on any reproductive advantage if you get sick and die," Dargent said.

Of course, further research is needed to really establish a causal relationship between longevity and increased parasite resistance, the scientists stress in their paper on the research, published recently in the journal Proceedings of the Royal Society B.

Whatever the case, the fact that animals can rapidly evolve increased parasite resistance after the pests have been removed has a number of implications. Farmed salmon, for example, are routinely treated for parasites. Over time, you'd expect the fish to evolve reduced resistance to parasites, and there is a constant concern that they could pass on those genes to wild populations should they ever escape the farm. "What we find is that this actually might not necessarily be the case," Dargent said.

The results may also extend to invasive species. These destructive organisms are able to thrive in new environments partly because they no longer have to deal with their natural parasites. One conservation strategy idea has been to introduce those parasites to the invasive species' environments, because of the belief that invasive species will no longer be able to adequately defend against their old enemies, Dargent said. The study shows that this tactic may not work after all.

Check out the research over in the Proceedings of the Royal Society B.

Top image Holger Krisp, Ulm, Germany/Wikimedia Commons. Inset images via Andrew Hendry @ McGill University and Marrabbio2/Wikimedia Commons.