Abstract
Pesticide runoff from terrestrial environments into waterways is often lethal to freshwater organisms, but exposure may also drive evolution of pesticide resistance. We analyzed the degree of resistance and molecular genetic changes underlying resistance in Hyalella azteca, a species complex of freshwater crustaceans inadvertently exposed to pesticide pollution via runoff. We surveyed 16 waterways encompassing most major watersheds throughout California and found that land use patterns are predictive of both pyrethroid presence in aquatic sediments and pyrethroid resistance in H. azteca. Nonsynonymous amino acid substitutions in the voltage‐gated sodium channel including the M918L, L925I, or L925V confer resistance in H. azteca. The most frequently identified mutation, L925I, appears to be preferred within the species complex. The L925V substitution has been associated with pyrethroid resistance in another insect, but is novel in H. azteca. We documented a variety of pyrethroid resistance mutations across several species groups within this complex, indicating that pyrethroid resistance has independently arisen in H. azteca at least six separate times. Further, the high frequency of resistance alleles indicates that pesticide‐mediated selection on H. azteca populations in waterways equals or exceeds that of targeted terrestrial pests. Widespread resistance throughout California suggests current practices to mitigate off‐site movement of pyrethroids are inadequate to protect aquatic life from negative ecological impacts and implies the likelihood of similar findings globally.
Highlights
Widespread, global pesticide use has had devastating effects on ecosystems through impacts to keystone species such as pollinators, alterations in food webs, endocrine disruption in vertebrates, and indirect impacts to ecosystem function (Kohler & Triebskorn, 2013)
We developed a genotyping assay that can be widely used within the H. azteca species complex to link pyrethroid resistance phenotypes to resistance alleles at the M918 and the L925 voltage-gated sodium channel loci
At all seven sites with demonstrated tolerance, resistance allele frequencies were 80% or higher for one of three voltage-gated sodium channel (Vgsc) amino acid substitutions associated with pyrethroid resistance: M918L, L925I, or L925V (Table 1; Figure 3)
Summary
Widespread, global pesticide use has had devastating effects on ecosystems through impacts to keystone species such as pollinators, alterations in food webs, endocrine disruption in vertebrates, and indirect impacts to ecosystem function (Kohler & Triebskorn, 2013). Parallel evolution of resistance mutations among insects and pyrethroid-resistant H. azteca suggests similar selective pressures experienced in both the targeted pest and the nontarget, ecologically important amphipod unintentionally exposed to pesticides via runoff. Waterways in urban, residential, and agricultural areas of California often have water or sediment concentrations of pyrethroids that exceed toxicity thresholds for sensitive, wild-type H. azteca (Amweg, Weston, You, & Lydy, 2006; Holmes et al, 2008; Phillips et al, 2012; Weston, Holmes, & Lydy, 2009; Weston, Holmes, You, & Lydy, 2005; Weston & Lydy, 2012) Taken together, these studies indicate that pesticides entering waterways via runoff have sufficient toxicity to alter the evolutionary trajectory of arthropod populations by strongly selecting for resistance mutations. We investigated the widespread geographic distribution of pyrethroid resistance in populations of H. azteca throughout California to determine whether expected pyrethroid use on terrestrial land is predictive of pyrethroid resistance
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