Rapid evolution meets invasive species control: the potential for pesticide resistance in sea lamprey

Dunlop, Erin S.; McLaughlin, Robert L.; Adams, Jean V.; Jones, Michael L.; Birceanu, Oana; Christie, Mark R.; Criger, Lori A.; Hinderer, Julia L. Mida; Hollingworth, Robert M.; Johnson, Nicholas S.; Lantz, Stephen R.; Li, Weiming; Miller, James R.; Morrison, Bruce J.; Mota-Sánchez, David; Muir, Andrew M.; Sepúlveda, Marı́a S.; Steeves, Todd B.; Walter, Lisa M.; Westman, Erin L.; Wirgin, Isaac; Wilkie, Michael P.

doi:10.1139/cjfas-2017-0015

Cited by 54 publications

(36 citation statements)

References 140 publications

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“…Results from sampling just over 200 larvae from DC (a) are consistent with previous studies that indicate sea lamprey display a polygamous mating behavior (Gilmore, ; Rodrıguez‐Munoz & Tregenza, ), and (b) showed that downstream dispersal is a continuous process for individuals of different ages (Derosier et al, ). Population genetic analyses demonstrate that the SNPs developed from larval sea lampreys from two populations were variable across the Great Lakes and exhibit levels of interpopulation variance in allele frequency that are comparable to mtDNA (Waldman et al, ) and microsatellite analyses (Bryan et al, ).Identification of outlier loci (Figure ; features detailed in GitHub repository) portends developments in areas of gene‐assisted control (McCauley et al, ), for example, the exploration of potential rapid evolution in response to intense selection associated with pesticide treatments (Dunlop et al, ).…”

Section: Discussionmentioning

confidence: 99%

RAPTURE (RAD capture) panel facilitates analyses characterizing sea lamprey reproductive ecology and movement dynamics

Sard

Smith

Homola

et al. 2020

Ecology and Evolution

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Genomic tools are lacking for invasive and native populations of sea lamprey (Petromyzon marinus). Our objective was to discover single nucleotide polymorphism (SNP) loci to conduct pedigree analyses to quantify reproductive contributions of adult sea lampreys and dispersion of sibling larval sea lampreys of different ages in Great Lakes tributaries. Additional applications of data were explored using additional geographically expansive samples. We used restriction site‐associated DNA sequencing (RAD‐Seq) to discover genetic variation in Duffins Creek (DC), Ontario, Canada, and the St. Clair River (SCR), Michigan, USA. We subsequently developed RAD capture baits to genotype 3,446 RAD loci that contained 11,970 SNPs. Based on RAD capture assays, estimates of variance in SNP allele frequency among five Great Lakes tributary populations (mean FST 0.008; range 0.00–0.018) were concordant with previous microsatellite‐based studies; however, outlier loci were identified that contributed substantially to spatial population genetic structure. At finer scales within streams, simulations indicated that accuracy in genetic pedigree reconstruction was high when 200 or 500 independent loci were used, even in situations of high spawner abundance (e.g., 1,000 adults). Based on empirical collections of larval sea lamprey genotypes, we found that age‐1 and age‐2 families of full and half‐siblings were widely but nonrandomly distributed within stream reaches sampled. Using the genomic scale set of SNP loci developed in this study, biologists can rapidly genotype sea lamprey in non‐native and native ranges to investigate questions pertaining to population structuring and reproductive ecology at previously unattainable scales.

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Section: Discussionmentioning

confidence: 99%

RAPTURE (RAD capture) panel facilitates analyses characterizing sea lamprey reproductive ecology and movement dynamics

Sard

Smith

Homola

et al. 2020

Ecology and Evolution

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“…The single largest determinant of whether resistance takes a comparatively short (e.g., 30 years) or longer time (e.g., 80 years) to develop is the annual number of tributaries treated. Across all Great Lakes, sea lamprey have been treated with TFM for an average of 50 years 34 , which is towards the beginning of when our model predicts resistance will evolve. As such, sea lamprey in the Great Lakes could be in the incipient stages for the evolution of resistance.…”

Section: Discussionmentioning

confidence: 99%

“…This longevity means that sea lamprey generation times are longer and their response to selection slower in real time in comparison with many other pest species. Assuming an average generation time of between 3 and 5 years, invasive sea lamprey may have been exposed to TFM for 20-30 generations, which may not be sufficient time for resistance to evolve (but see 34–36 ). Another reason that resistance may not evolve is the high rate of dispersal and subsequent gene flow found in this species.…”

Section: Introductionmentioning

confidence: 99%

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

Christie¹,

Sepúlveda²,

Dunlop

2019

Preprint

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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

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“…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. 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, Mota-Sanchez, & Hollingworth, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…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, Mota-Sanchez, & Hollingworth, 2008). The evolution of resistance would greatly reduce the effectiveness of TFM, which is currently the primary control method for invasive sea lamprey (Dunlop et al, 2017), and decreased pesticide effectiveness would likely hamper the restoration of native and commercially-important fish populations throughout the Great Lakes.…”

Section: Introductionmentioning

confidence: 99%

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

Yin¹,

Martinez²,

Perkins

et al. 2019

Preprint

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1The resistance of bacteria, disease vectors, and pests to chemical controls has vast ecological, 2 economic, and human-health costs. In most cases, resistance is only detected after non-3 susceptible phenotypes have spread throughout the entire population. Detecting resistance in its 4 incipient stages, by comparison, provides time to implement preventative strategies. Incipient 5 resistance (IR) can be detected by coupling standard toxicology assays with large-scale gene 6 expression experiments. We apply this approach to a system where an invasive parasite, sea 7 lamprey (Petromyzon marinus), has been treated with the highly-effective pesticide 3-8 trifluoromethyl-4-nitrophenol (TFM) for 60 years. Toxicological experiments revealed that 9 lamprey from treated populations did not have higher survival to TFM exposure than lamprey 10 from their native range, demonstrating that full-fledged resistance has not yet evolved. In stark 11 contrast, we find hundreds of genes differentially expressed in response to TFM in the 12 population with the longest history of exposure, many of which relate to TFM's primary mode of 13 action, the uncoupling of oxidative phosphorylation. One gene critical to oxidative 14 phosphorylation, ATP5PB, which encodes subunit b of ATP synthase, was nearly fixed for 15 alternative alleles in comparisons between native and treated populations (FST > 9 SD from the 16 mean). A gene encoding an additional subunit of ATP synthase, ATP5F1B, was canalized for 17 high expression in treated populations, but remained plastic in response to treatment in sea 18 lamprey from the native range. These combined genomic and transcriptomic results illustrate that 19 an adaptive, genetic response to TFM is driving incipient resistance in a damaging pest species. 20 S3). Remarkably, when comparing samples treated with 0.3 mg/L TFM to control samples, we 113 found 336 genes that were differentially expressed (275 upregulated, 61 downregulated in 114 comparison to control individuals) in muscle tissue in the Lake Michigan population, dwarfing 115 the number of differentially expressed genes (DEGs) found in both the Lake Champlain (n = 21) 116 and the Connecticut River (n = 68) populations (Fig. 3A-C; Table S4). No DEGs were shared 117 among all three populations and different population responses were observed when lower 118 concentrations (i.e., 0.2 mg/L) of TFM were applied and when different tissues were examined 119 (Figures S2-S5). 120The primary mode of action for TFM is to uncouple oxidative phosphorylation in the 121 mitochondria resulting in severe ATP depletion and eventual death (25, 26, 32). Of the 336 122 DEGs identified in Lake Michigan, several genes were directly related to this mode of action 123 including CRCM1 (LogFC = 2.60), a calcium release-activated channel protein that controls the 124 influx of calcium into cells when depleted, and PLCD4 (LogFC = 2.41), an enzyme responsible 125 for hydrolyzing phosphatidylinositol 4,5-bisphosphate into two secondary messenger molecules, 126 one of which (...

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Rapid evolution meets invasive species control: the potential for pesticide resistance in sea lamprey

Cited by 54 publications

References 140 publications

RAPTURE (RAD capture) panel facilitates analyses characterizing sea lamprey reproductive ecology and movement dynamics

RAPTURE (RAD capture) panel facilitates analyses characterizing sea lamprey reproductive ecology and movement dynamics

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

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

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