Frogs that adapt to pesticides are more vulnerable to parasites

"We have only recently begun to understand that amphibians can rapidly evolve tolerance to chemicals like pesticides, which on the surface is good news," said Rick Relyea, a professor of biological sciences and director of the Darrin Fresh Water Institute at Rensselaer. "But now comes the bad news: with that tolerance there is a tradeoff, which is that they become more susceptible to parasites that, in the case of ranavirus, can wipe out entire amphibian populations."

Previous research, led by Jessica Hua, a Binghamton University assistant professor, with the assistance of researchers at Rensselaer and Purdue University, showed that amphibians can evolve tolerance to pesticides in one of two ways. Amphibians that live close to agriculture can evolve higher baseline tolerance by passing tolerance on from generation to generation. Alternatively, if exposed to low levels of pesticides early in life, amphibians that live far from agriculture evolve the ability to induce higher pesticide tolerance within a few days, which is known as "inducible tolerance."

"While it is optimistic that amphibians can evolve tolerance to chemicals using multiple mechanisms, it is important to consider that pesticides are not the only stressor amphibians face," said Hua. "Amphibians are declining worldwide and other stressors such as parasites can interact with pesticides to contribute to these declines."

"Across their lifetime, amphibians encounter many different types of parasites and the parasite-specific responses we detected highlight the complexity of pesticide-parasite interactions," said Jason Hoverman, associate professor of Forestry and Natural Resources at Purdue University.

To understand whether land use or evolving pesticide tolerance comes at a cost when facing other stressors such as parasites, the team identified 15 wood frog populations that vary in their proximity to agriculture and displayed either higher baseline tolerance or inducible tolerance. Using these populations, they measured the relationship between land use, evolutionary responses to a pesticide, and susceptibility to two common parasites: a trematode worm and a ranavirus.

The results showed that amphibian susceptibility to parasites was related to their proximity to agriculture and their evolutionary responses to pesticide. For the trematode, wood frogs living closer to agriculture with high baseline tolerance had lower trematode loads than populations living far from agriculture with inducible pesticide tolerance. In contrast for ranavirus, a highly virulent pathogen capable of decimating amphibian populations, populations living close to agriculture with high baseline tolerance had higher viral loads than populations far from agriculture with inducible tolerance.

"Our results suggest that it is not enough to consider the effects of contaminants or parasites in isolation. Nature is complex," said Hua. "Not only do different stressors interact in ways that can be difficult to predict, but evolutionary responses to one stressor can shape amphibian responses to other stressors."

The research was part of a suite of experiments the team conducted to assess tolerance to pesticides, inducible tolerance, and the effects of pathogens on amphibian populations that varied in their induced or baseline tolerance, said Relyea. Rensselaer researchers were largely responsible for identifying the populations and conducting initial testing on pesticides.

"Our group has been leading the way in understanding how animals can rapidly evolve tolerance to pesticides," said Relyea, the David M. Darrin '40 Senior Endowed Chair at Rensselaer. "Five years ago, we didn't know that amphibians or any vertebrate animals could evolve induced tolerance to pesticides. This is a new layer of the effort, which is to ask: are there tradeoffs to rapidly evolving increased tolerance to pesticides?"