Rapid resistance to pesticide control is predicted to evolve in an invasive fish

Abstract

Xenobiotic resistance is commonly found in species with short generation times such as bacteria, 1 annual plants, and insects. Nevertheless, the fundamental evolutionary principles that govern the 2 spread of resistance alleles hold true for species with longer generation times. One such example 3 could occur with sea lamprey (Petromyzon marinus), a parasitic invasive species in the 4 Laurentian Great Lakes that decimated native fish populations prior to its control with the 5 pesticide 3-trifluoromethyl-4-nitrophenol (TFM). Since the 1950s, tributaries have been treated 6 annually with TFM, where treatments effectively remove most, but not all, larval sea lamprey. 7 We developed an eco-genetic model of sea lamprey to examine factors affecting the evolution of 8 resistance and found that resistance alleles rapidly rise to fixation after 40-80 years of treatment, 9 despite the species' relatively long generation time (4-7 years). The absence of natal homing 10 allows resistant individuals to spread quickly throughout the entire system, but also makes the 11 early detection of resistance challenging. High costs of resistance and density independent 12 reproduction can delay, but not prevent, the onset of resistance. These results illustrate that sea 13 lamprey have the potential to evolve resistance to their primary control agent in the near future, 14 highlighting the urgent need for alternative controls. 15

Incipient resistance to an effective pesticide results from genetic adaptation and the canalization of gene expression

“…It may only be a matter of time before further mutations or a continued response to selection allows individuals to survive higher concentrations of TFM. In fact, recent modeling efforts have revealed that given the estimated strength of selection imposed by lamprey control, full‐fledged resistance to TFM is predicted to occur within the next tens of years (Christie et al, 2019). Because of the high gene flow and lack of population structure found throughout the Great Lakes, fully resistant individuals may already be spreading throughout the population even though it may take many more years for successful detection (Christie et al, 2019).…”

“…In fact, recent modeling efforts have revealed that given the estimated strength of selection imposed by lamprey control, full‐fledged resistance to TFM is predicted to occur within the next tens of years (Christie et al, 2019). Because of the high gene flow and lack of population structure found throughout the Great Lakes, fully resistant individuals may already be spreading throughout the population even though it may take many more years for successful detection (Christie et al, 2019). From a pragmatic standpoint, the detection of incipient resistance (IR) means that the development of alternative control measures and the implementation of adaptive management strategies focusing on delaying resistance should be a priority for the continued control of invasive sea lamprey.…”

“…Lake Michigan ammocoetes have been treated with TFM since 1960 (Lavis et al., 2003), Lake Champlain ammocoetes have been treated with TFM since 1990 (Marsden et al., 2003), and Connecticut River has never been treated with TFM. Importantly, sea lamprey have very little natal philopatry (i.e., adults rarely spawn in their natal stream) and high population connectivity (Bjerselius et al., 2000; Bryan et al., 2005), meaning that TFM treatments applied in one part of the lake affect the development of resistance throughout the entire lake (Christie et al, 2019). To examine lamprey of similar ages and developmental stages, we only collected ammocoetes from a narrow size range (80–120 mm) and we only collected larvae that had never been previously exposed to TFM.…”

“…Unfortunately, resistance is often detected too late, after most individuals in a population have acquired a resistant phenotype (McKenna, 2013). Once this stage is reached, there is little to be done except to implement alternative control measures, which are often less effective (Ghosh et al., 2019; Peterson et al., 2018), or stop employing control measures until resistant genotypes are eliminated from the population, which can take tens to hundreds of generations (Andersson & Hughes, 2010; Andersson & Levin, 1999; Christie et al., 2019).…”

“…Since the application of TFM to locations with abundant larval lamprey, invasive sea lamprey populations have declined by up to 90% (Heinrich et al., 2003; Smith & Tibbles, 1980). However, TFM applications kill most, but not all, larval sea lamprey (Dunlop et al., 2017) and it is possible that resistant individuals could survive and reproduce (Christie et al., 2019). If this process is repeated over enough generations, then resistant individuals could increase in frequency—a scenario documented in many systems where pests have been controlled by chemical means (Whalon et al., 2008).…”