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Assessing the resistance of sea lampreys (Petromyzon marinus) to TFM
2 Department of Biological Sciences, Purdue University
915 West State Street, West Lafayette IN, 47907
3 Department of Forestry and Natural Resources, Purdue University
715 West State Street, West Lafayette IN, 47907
Sea lampreys (Petromyzon marinus) have been chemically controlled in the Great Lakes with the lampricide 3-trifluoromethyl-4-nitrophenol (TFM) for 57 years. Many studies of animals (including vertebrates) have shown that resistance to toxic chemicals can evolve rapidly, particularly when the application does not kill all individuals (i.e., there is differential survival). Furthermore, the likelihood of evolving resistance is correlated with fecundity and sea lampreys are highly fecund (> 100,000 eggs/individual). Knowledge of whether or not resistance is evolving is critical for the successful control and management of this invasive species. By combining standard toxicology assays with whole-tissue gene expression (RNA-seq), we detected incipient resistance (IR) in invasive sea lamprey. Our toxicological studies using individuals collected from three populations with varying histories of pesticide treatment (56, 26, and 0 years, respectively) revealed no differences in survival after exposure. By contrast, hundreds of genes were upregulated in individuals from the population with the longest history of treatment (Lake Michigan) and, in both treated populations, we found transcriptomic and genomic evidence of a genetic response to pesticide-induced selection. TFM works by interrupting the normal production of ATP from mitochondria, the cell’s powerhouse. In treated populations, we find remarkably strong evidence of selection (FST > 9 SD from the mean) in a gene coding for ATP synthase, the enzyme responsible for the creation of ATP. In a gene coding for a different subunit of ATP synthase, we also find a different adaptive response to selection. Expression of this gene is continually up-regulated in individuals from treated populations (i.e., high constitutive expression is canalized), but responds plastically to TFM in individuals from the population with no history of treatment. Collectively, these data illustrate that while full-fledged resistance has not yet evolved, adaptive genetic responses to the pesticide’s primary mode of action have already occurred in treated populations. To determine whether and when resistance may develop, we also created an eco-genetic model that mimics sea lamprey population dynamics and life history characteristics. We found that resistant individuals initially spread quickly and remain at low density throughout the entire system, making the initial detection of resistance challenging. Most importantly, we find that given the duration and intensity of treatment, resistance is likely to evolve in the next 10-20 years. Given that TFM is the most effective control option currently in place, we advocate for the rapid development of alternative control measures.