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Unintentional exposure to terrestrial pesticides drives widespread and predictable evolution of resistance in freshwater crustaceans.

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.

SUBMITTER: Major KM

PROVIDER: S-EPMC5979619 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:The discovery of many fragments of viral genomes integrated in the genome of their eukaryotic host (endogenous viral elements; EVEs) has recently opened new avenues to further our understanding of viral evolution and of host-virus interactions. Here, we report the results of a comprehensive screen for EVEs in crustaceans. Following up on the recent discovery of EVEs in the terrestrial isopod, Armadillidium vulgare, we scanned the genomes of six crustacean species: a terrestrial isopod (Armadillidium nasatum), two water fleas (Daphnia pulex and D. pulicaria), two copepods (the salmon louse, Lepeophtheirus salmonis and Eurytemora affinis), and a freshwater amphipod (Hyalella azteca). RESULTS:In total, we found 210 EVEs representing 14 different lineages belonging to five different viral groups that are present in two to five species: Bunyaviridae (-ssRNA), Circoviridae (ssDNA), Mononegavirales (-ssRNA), Parvoviridae (ssDNA) and Totiviridae (dsRNA). The identification of shared orthologous insertions between A. nasatum and A. vulgare indicates that EVEs have been maintained over several millions of years, although we did not find any evidence supporting exaptation. Overall, the different degrees of EVE degradation (from none to >10 nonsense mutations) suggest that endogenization has been recurrent during the evolution of the various crustacean taxa. Our study is the first to report EVEs in D. pulicaria, E. affinis and H. azteca, many of which are likely to result from recent endogenization of currently circulating viruses. CONCLUSIONS:In conclusion, we have unearthed a large diversity of EVEs from crustacean genomes, and shown that four of the five viral groups we uncovered (Bunyaviridae, Circoviridae, Mononegavirales, Parvoviridae) were and may still be present in three to four highly divergent crustacean taxa. In addition, the discovery of recent EVEs offers an interesting opportunity to characterize new exogenous viruses currently circulating in economically or ecologically important copepod species.

Project description:BackgroundLow socioeconomic status (SES) residents living in social housing, which is subsidized by government or government-funded agencies, may have higher exposures to pesticides used in indoor residences since pesticides are applied due to structural deficiencies, poor maintenance, etc. OBJECTIVE: To estimate exposure of residents in low-SES social housing built in the 1970s to legacy and current-use pesticides and to investigate factors related to exposures.MethodsTwenty-eight particle-phase pesticides were measured in the indoor air of 46 units in seven low-income social housing, multi-unit residential buildings (MURBs) in Toronto, Canada using portable air cleaners deployed for 1 week in 2017. Pesticides analyzed were legacy and current use in the classes: organochlorines, organophosphates, pyrethroids, and strobilurins.ResultsAt least one pesticide was detected in 89% of the units with detection frequencies (DF) for individual pesticides of up to 50%, including legacy organochlorines and current-use pesticides. Current-use pyrethroids had the highest DF and concentrations, with the highest particle-phase concentration for pyrethrin I at 32,000 pg/m3. Heptachlor, restricted for use in Canada in 1985, had the highest estimated maximum total air (particle plus gas phase) concentration of 443,000 pg/m3. Heptachlor, lindane, endosulfan I, chlorothalonil, allethrin, and permethrin (except in one study) had higher concentrations than those measured in low-income residences reported elsewhere. In addition to the intentional use of pesticides to control pests and their use in building materials and paints, tobacco smoking was significantly correlated with the concentrations of five pesticides used on tobacco crops. The distribution of pesticides with high DF in individual buildings suggested that pest eradication programs by the building management and/or pesticide use by residents were the major sources of measured pesticides.ImpactLow-income social housing fills a much-needed demand, but the residences are prone to pest infestation and hence pesticide use. We found exposure to at least 1 of 28 particle-phase pesticides in 89% of all 46 units tested, with the highest DF and concentrations for current-use pyrethroids and long-banned organochlorines (e.g., DDT, heptachlor) due to very high persistence indoors. Also measured were several pesticides not registered for use indoors, e.g., strobilurins used to treat building materials and pesticides used on tobacco crops. These results, which are the first Canadian data for most pesticides indoors, show widespread exposure to numerous pesticides.

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Unintentional exposure to terrestrial pesticides drives widespread and predictable evolution of resistance in freshwater crustaceans.

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