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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
December 2019
ABSTRACT:
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.