Tiny fish provides giant insight into how organisms adapt to changing environment

An Indiana University-Dartmouth College team has identified genes and regulatory patterns that allow some organisms to alter their body form in response to environmental change.

Understanding how an organism adopts a new function to thrive in a changing environment has implications for molecular evolution and many areas of science including climate change and medicine, especially in regeneration and wound healing.

The study, which appears in the journal Molecular Biology and Evolution, provides insight into phenotypic plasticity, a phenomenon that enables some organisms to change their observable characteristics in response to their environment.

"Phenotypic plasticity is an incredibly important ability," said Joe Shaw, associate professor at the Indiana University School of Public and Environmental Affairs and the paper's lead author. "Think in terms of the metamorphosis that butterflies go through, except in this case the shift is triggered by a change in the environment."

Shaw and Tom Hampton, senior bioinformatics analyst at Dartmouth's Geisel School of Medicine, headed the team of scientists that conducted the research. Other IU co-authors are Nathan Keith and Stephen Glaholt of SPEA.

The researchers examined how the Atlantic killifish modifies its gills to live in freshwater or seawater, including activating or deactivating channels that secrete salt. While some of the structures used to maintain salt balance are already known, the new study sheds light on how the killifish coordinates multiple changes in order for its gills to transition. The process involves both structural and functional changes since the freshwater gill is fundamentally different from the seawater gill.

Shaw and co-author Bruce Stanton, a professor of microbiology and immunology at the Geisel School, previously observed that killifish are more vulnerable to arsenic during changes in salinity. Killifish living in freshwater or seawater can tolerate arsenic well, but even low levels of arsenic interfere with their plastic response required to survive in the new environment. Since arsenic prevents killifish from shifting between freshwater and seawater, they reasoned that arsenic could be used to identify which genes orchestrate these changes.

Arsenic exposure during salt acclimation revealed many genes that orchestrate the killifish plastic response, and these plasticity-enabling genes are maintained at precise levels. The results suggest that strict regulatory control of these genes may be a general feature of plastic responses in other organisms.

"If you take two fish that are different many ways, and these two fish just changed over from living in freshwater to seawater, what's striking is how identical their gills are if you look at them under a microscope, or test to see how they are functioning," Shaw said. "Gills from two fish find a way, in spite of all sorts of environmental differences, to end up virtually identical. That is a very neat trick when you think about it, and we think this precise control over plasticity genes makes this consistency possible."

The researchers report that plasticity-enabling genes seem to be organized in unusually simple networks, and that these structures may explain why genes involved in the plasticity response are so precisely controlled. They also found that nature selects for these networks depending on how much plasticity is required. Killifish living in stable environments have evolved less precise control over plasticity-enabling genes than those living in the least stable environments. The results have substantial implications for our understanding of molecular evolution by suggesting that natural selection targets the regulatory networks of genes in addition to individual genes or proteins.

The research team is working on experiments that apply the results to other fields. Shaw's team is experimenting with killifish that evolved under different conditions in an effort to better understand species that are adapted to withstand abrupt and more widespread changes in their environment. He hopes such research will help predict and prepare for the threats of global climate change.

Stanton, who also is director of the Dartmouth Toxic Metals Superfund Research Program and the Dartmouth Lung Biology Center, said low levels of arsenic in drinking water increase risks for lung disease. His lab team is testing whether low-level arsenic interferes with immune responses.