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Multiple Origins of Pyrethroid Insecticide Resistance Across the Species Complex of a Nontarget Aquatic Crustacean, Hyalella Azteca

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Multiple Origins of Pyrethroid Insecticide Resistance Across the Species Complex of a Nontarget Aquatic Crustacean, Hyalella Azteca Multiple origins of pyrethroid insecticide resistance across the species complex of a nontarget aquatic crustacean, Hyalella azteca Donald P. Westona,1, Helen C. Poyntonb, Gary A. Wellbornc, Michael J. Lydyd, Bonnie J. Blalockb, Maria S. Sepulvedae, and John K. Colbournef aDepartment of Integrative Biology, University of California, Berkeley, CA 94720; bSchool for the Environment, University of Massachusetts, Boston, MA 02125; cDepartment of Biology, University of Oklahoma, Norman, OK 73019; dCenter for Fisheries, Aquaculture and Aquatic Sciences, Southern Illinois University, Carbondale, IL 62901; eDepartment of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907; and fThe Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405 Edited* by Bruce D. Hammock, University of California, Davis, CA, and approved August 20, 2013 (received for review January 31, 2013) Use of pesticides can have substantial nonlethal impacts on non- survival when exposed to contaminants (13). The possibility of target species, including driving evolutionary change, often with differential contaminant sensitivity among species within the unknown consequences for species, ecosystems, and society. complex has not been fully appreciated by the ecotoxicological Hyalella azteca, a species complex of North American freshwater community, yet it could have implications for the many moni- amphipods, is widely used for toxicity testing of water and sed- toring programs that rely on this organism. iment and has frequently shown toxicity due to pyrethroid pes- In the present study, we demonstrate wide variation in pyre- ticides. We demonstrate that 10 populations, 3 from laboratory throid sensitivity among populations of H. azteca. We contrast cultures and 7 from California water bodies, differed by at least sensitivity of three laboratory-cultured and seven wild-collected 550-fold in sensitivity to pyrethroids. The populations sorted in- populations and interpret differences in light of phylogenetic to four phylogenetic groups consistent with species-level diver- relationships, emergence of resistance, and contrasting gene gence. By sequencing the primary pyrethroid target site, the expression patterns among the populations. GENETICS voltage-gated sodium channel, we show that point mutations Results and their spread in natural populations were responsible for H. azteca differences in pyrethroid sensitivity. At least one population had Sources of Investigated and Relationship to Pyrethroid both mutant and WT alleles, suggesting ongoing evolution of resis- Exposure. Natural populations of H. azteca were obtained from tance. Although nonresistant H. azteca were susceptible to the typ- seven sites in California (Table 1). Using sediment pyrethroid ical neurotoxic effects of pyrethroids, gene expression analysis concentrations as an integrated measure of exposure, the sites suggests the mode of action in resistant H. azteca was not neurotox- represent a broad range of prior exposure. Two sites with minimal icity but was oxidative stress sustained only at considerably higher surrounding development (Blodgett and Laguna) contained bifen- pyrethroid concentrations. The finding that a nontarget aquatic spe- thrin barely above the 1-ng/g reporting limit. Chualar Creek con- cies has acquired resistance to pesticides used only on terrestrial pests tained no measurable pyrethroids, although agricultural pyrethroid is troubling evidence of the impact of chronic pesticide transport from land-based applications into aquatic systems. Our findings have far- Significance reaching implications for continued uncritical use of H. azteca as a principal species for monitoring and environmental policy The crustacean, Hyalella azteca, is commonly used in environ- decisions. mental monitoring to test the toxicity of water or sediment. We show that among three laboratory cultures and seven wild lthough evolution of pesticide resistance in pest species has populations of H. azteca, there is a more than 550-fold varia- Abeen a major area of investigation, evolutionary impacts of tion in sensitivity to widely used pyrethroid insecticides. Some pesticide pollution on nontarget species are poorly understood individuals have attained resistance by mutations in the volt- but may hold important consequences for affected species and age-gated sodium channel, the target site for pyrethroid tox- their ecosystems (1, 2). Acquisition of pesticide resistance may icity. Similar mutations have been found in agricultural pests be especially troublesome when it occurs in nontarget species targeted by pyrethroids, but this study indicates that runoff of terrestially applied urban and agricultural pesticides has been used in biomonitoring programs that inform public policy. One sufficient to induce resistance in a nontarget aquatic species on such species is the amphipod, Hyalella azteca, widely used for multiple, independent occasions. Our results have far-reaching sediment toxicity testing and sometimes for water testing (3, 4). implications for biomonitoring programs in general and espe- There are many instances of sediment or water toxicity to H. cially those relying on H. azteca. azteca due to pyrethroids, which are widely used insecticides in – fi urban and agricultural settings (4 6). However, we nd wild Author contributions: D.P.W. and H.C.P. designed research; D.P.W., H.C.P., G.A.W., M.J.L., populations of H. azteca in some pyrethroid-contaminated water and B.J.B. performed research; H.C.P., M.S.S., and J.K.C. contributed new reagents/analytic bodies from which water or sediment samples cause acute tools; D.P.W., H.C.P., G.A.W., and B.J.B. analyzed data; and D.P.W., H.C.P., G.A.W., M.J.L., mortality to laboratory-cultured populations. One possibility is and M.S.S. wrote the paper. fl that wild populations have evolved resistance, as has been The authors declare no con ict of interest. reported in target pests (7, 8). *This Direct Submission article had a prearranged editor. The picture is further complicated by the fact that H. azteca is Data deposition: The sequences reported in this paper have been deposited in the Gen- Bank database (accession nos. GAJQ00000000.1, GAJP00000000.1, JX678289, KF596727– actually a species complex. Genetic analyses of what are nomi- KF596752, and KF596753–KF596771), and the data reported in this paper have been nally H. azteca have suggested the presence of 33 species in the deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo Great Basin of California and Nevada (9), 7 species in Wisconsin (accession nos. GPL17458 and GSE48943). and parts of Canada (10), 4 species in Michigan (11), and 2 1To whom correspondence should be addressed. E-mail: [email protected]. species in Oregon (12). Genetic differences among individuals This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. within a single population of H. azteca led to differences in 1073/pnas.1302023110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1302023110 PNAS Early Edition | 1of6 Downloaded by guest on September 25, 2021 Table 1. Collecting sites for the wild H. azteca populations, including the organic content and total pyrethroid concentration in the sediments, measured at the time the animals were collected Land use surrounding Sediment organic Pyrethroid concentration Site and coordinates sampling site Sample date carbon (%) (ng/g)* Blodgett Reservoir, Sacramento, CA Undeveloped Nov. 19, 2010 2.7 1.3 38.5176°N, 121.2109°W grasslands Laguna Lake, Petaluma, CA Grasslands with scattered July 3, 2010 0.2 1.8 38.2064°N, 122.7636°W homes and agriculture † † Pleasant Grove Creek, Roseville, CA Open space with residential June 1, 2010; 2.9 6.8 38.8052°N, 121.3069°W use 1 km upstream March 13, 2013 Morrison Creek, Sacramento, CA Airfield with residential Oct. 19, 2010 1.6 Not detected (<1) 38.5271°N, 121.3274°W use 5 km upstream Mosher Slough, Stockton, CA Commercial and June 11, 2010 3.4 57.6 38.0325°N, 121.3654°W residential land use Chualar Creek, Chualar, CA Agriculture Aug. 18. 2010 1.1 Not detected (<1) 36.5583°N, 121.5296°W Grayson Creek, Concord, CA Commercial and Aug. 12, 2010 1.2 50.7 37.9665°N, 122.0666°W residential land use *Total sediment pyrethroids were comprised entirely of bifenthrin except Mosher Slough (35.5 ng/g bifenthrin, 5.9 ng/g cyfluthrin, 4.2 ng/g cyhalothrin, 5.4 ng/g cypermethrin, 6.6 ng/g permethrin) and Grayson Creek (26.6 ng/g bifenthrin, 7.7 ng/g cyfluthrin, 3.6 ng/g cypermethrin, 12.8 ng/g permethrin). † Chemistry data from the June 2010 collecting event. use is widespread in the watershed (14). The organophosphate in- 4.8 ng/L. Wild populations from the two sites with little prior secticide chlorpyrifos was present at 248 ng/g at the site. Among four pyrethroid exposure had sensitivity comparable to the cultures: urban creeks, Morrison Creek sediments had no measurable pyr- Blodgett Reservoir animals (clade B) had LC50sof1.1–1.3 ng/L, ethroids, perhaps because the site was in a reach of the creek along and Laguna Lake amphipods (clade A) had LC50sof3.9–4.8 ng/L. an airfield, although there was extensive residential development Wild populations from sites with the highest pyrethroid and therefore likely pyrethroid use, both upstream and downstream. exposures as indicated by sediment concentrations (Mosher and The Pleasant Grove Creek site had 6.8 ng/g bifenthrin, approxi- Grayson) or with pyrethroid use nearby in the watershed (Mor- mately one-third the median lethal concentration (LC50) for labo- rison and Chualar) showed extraordinary pyrethroid resistance. ratory-cultured H. azteca (15), and sediment toxicity attributed to H. azteca from the Morrison, Mosher, and Chualar sites had pyrethroids has been reported 2 km downstream (16). Mosher fl – Slough and Grayson Creek contained pyrethroids at least twice the cy uthrin LC50sof92535 ng/L. Grayson Creek animals were even more resistant, with only 33% mortality at the highest LC50 for laboratory-cultured H. azteca. For comparison with wild populations, laboratory-cultured H.
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