Genetic Variation Influences Tolerance to a Neonicotinoid Insecticide in 3 Butterfly Species

Kobiela, Megan E.; Snell‐Rood, Emilie C.

doi:10.1002/etc.4845

Cited by 6 publications

(7 citation statements)

References 41 publications

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“…However, genetic variation may also contribute to differences in the size (i.e. based on forewing and hindwing length) of adult monarch butterflies exposed to neonicotinoids (Kobiela and Snell-Rood, 2020). For instance, in contrast with previous evidence (Wilcox, 2020), monarchs in our study had shorter forewings than controls (Table 5; Fig.…”

Section: Discussioncontrasting

confidence: 66%

Effects of early-life exposure to sublethal levels of a common neonicotinoid insecticide on the orientation and migration of monarch butterflies (Danaus plexippus)

Wilcox

Newman

Raine

et al. 2020

Journal of Experimental Biology

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Migratory insects use a variety of innate mechanisms to determine their orientation and maintain correct bearing. For long-distance migrants, such as the monarch butterfly (Danaus plexippus), these journeys could be affected by exposure to environmental contaminants. Neonicotinoids are synthetic insecticides that work by affecting the nervous system of insects, resulting in impairment of their mobility, cognitive performance, and other physiological and behavioural functions. To examine how neonicotinoids might affect the ability of monarch butterflies to maintain a proper directional orientation on their ∼4000 km migration, we grew swamp milkweed (Asclepias incarnata) in soil that was either untreated (0 ng g−1: control) or mixed with low (15 ng g−1 of soil) or high (25 ng g−1 of soil) levels of the neonicotinoid clothianidin. Monarch caterpillars were raised on control or clothianidin-treated milkweed and, after pupation, either tested for orientation in a static flight simulator or radio-tracked in the wild during the autumn migration period. Despite clothianidin being detectable in milkweed tissue consumed by caterpillars, there was no evidence that clothianidin influenced the orientation, vector strength (i.e. concentration of direction data around the mean) or rate of travel of adult butterflies, nor was there evidence that morphological traits (i.e. mass and forewing length), testing time, wind speed or temperature impacted directionality. Although sample sizes for both flight simulator and radio-tracking tests were limited, our preliminary results suggest that clothianidin exposure during early caterpillar development does not affect the directed flight of adult migratory monarch butterflies or influence their orientation at the beginning of migration.

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Section: Discussioncontrasting

confidence: 66%

Effects of early-life exposure to sublethal levels of a common neonicotinoid insecticide on the orientation and migration of monarch butterflies (Danaus plexippus)

Wilcox

Newman

Raine

et al. 2020

Journal of Experimental Biology

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“…The quantitative nature of most phenotypic traits has been documented in many cases of adaptation ( Dermauw et al 2013 ; Faucon et al 2015 ; Cheng et al 2017 ; Barghi et al 2020 ), and since large-effect mutations often require compensatory fitness changes that are unlikely to evolve quickly enough to prevent such mutations from being removed by antagonistic selection, the most likely outcome of evolution in theoretical models is polygenic adaptation ( Wellenreuther and Hansson 2016 ). Quantitative variation in insecticide tolerance, among populations and individuals within populations, is frequently observed, even under controlled laboratory conditions ( Tabashnik and Cushing 1989 ; Kobiela and Snell‐Rood 2020 ). The action of multiple genes and their regulatory elements can be difficult to detect using population genomics methods, as only modest changes in allele frequencies are expected under soft or partial selective sweeps ( Teshima et al 2006 ; Messer et al 2016 ; Stephan 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle

Pélissié

Chen

Cohen

et al. 2022

Molecular Biology and Evolution

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Insecticide resistance and rapid pest evolution threatens food security and the development of sustainable agricultural practices, yet the evolutionary mechanisms that allow pests to rapidly adapt to control tactics remains unclear. Here we examine how a global super-pest, the Colorado potato beetle (CPB), Leptinotarsa decemlineata, rapidly evolves resistance to insecticides. Using whole genome resequencing and transcriptomic data focused on its ancestral and pest range in North America, we assess evidence for three, non-mutually exclusive models of rapid evolution: pervasive selection on novel mutations, rapid regulatory evolution, and repeated selection on standing genetic variation. Population genomic analysis demonstrates that CPB is geographically structured, even among recently established pest populations. Pest populations exhibit similar levels of nucleotide diversity, relative to non-pest populations, and show evidence of recent expansion. Genome scans provide clear signatures of repeated adaptation across CPB populations, with especially strong evidence of selection on insecticide resistance genes in different populations. Analyses of gene expression show that constitutive upregulation of candidate insecticide resistance genes drives distinctive population patterns. CPB evolves insecticide resistance repeatedly across agricultural regions, leveraging similar genetic pathways but different genes, demonstrating a polygenic trait architecture for insecticide resistance that can evolve from standing genetic variation. Despite expectations, we do not find support for strong selection on novel mutations, or rapid evolution from selection on regulatory genes. These results suggest that integrated pest management practices must mitigate the evolution of polygenic resistance phenotypes among local pest populations, in order to maintain the efficacy and sustainability of novel control techniques.

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“…Although clothianidin was detected in caterpillar tissue, it was not found in adult monarch butterflies. Recent studies provide evidence that exposure to neonicotinoids during early caterpillar development can result in a decrease in the size of adult monarch butterflies (Kobiela and Snell-Rood 2020;Olaya-Arenas et al 2020), but at low concentrations (i.e., approximately 15 ng/g) clothianidin has only a weak effect on monarch forewing length (Olaya-Arenas et al 2020). Olaya-Arenas et al (2020) suggest that tolerance to clothianidin may be a result of evolution of toxin resistance, specifically to the cardenolides found in milkweed.…”

Section: Discussionmentioning

confidence: 99%

“…However, in our study, adult monarchs exposed to clothianidin during development grew larger (i.e., forewing length) than controls did. Genetic variation may explain the differences in the size of adult monarch butterflies, with maternal line known to be a contributing factor influencing body size in monarchs exposed to neonicotinoids during development (Kobiela and Snell-Rood 2020).…”

Section: Discussionmentioning

confidence: 99%

Developmental and reproductive effects of clothianidin exposure in monarch butterflies (Lepidoptera: Nymphalidae)

2021

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Neonicotinoid insecticides are used to reduce crop damage caused by insect pests, but sublethal levels could affect development and reproduction in nontarget insects, such as monarch butterflies (Danaus plexippus) (Lepidoptera: Nymphalidae). To investigate the impact of field-realistic concentrations of the neonicotinoid clothianidin on monarch butterflies, we grew swamp milkweed (Asclepias incarnata) (Apocynaceae) in either low (15 ng/g of soil) or high (25 ng/g of soil) levels of clothianidin, or in a control (0 ng/g), then raised monarchs on the milkweed. Morphological traits of monarch caterpillars were measured during development and, once they eclosed, were mated as adults to quantify egg size and mass and the number of eggs laid. Although the effects of the treatment had complex effects on caterpillar length, width and volume of late-instar caterpillars were negatively affected. Fifth-instar caterpillars from the high-dose insecticide treatment had lower mass than other groups. Adult monarch butterflies raised on treated milkweed were larger than controls, but clothianidin exposure did not affect the number of eggs laid or egg size. Although the magnitude of the effect depends on clothianidin concentration, our results suggest that exposure to clothianidin during early life can impact monarch caterpillar development but is unlikely to reduce female reproductive output.

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Genetic Variation Influences Tolerance to a Neonicotinoid Insecticide in 3 Butterfly Species

Cited by 6 publications

References 41 publications

Effects of early-life exposure to sublethal levels of a common neonicotinoid insecticide on the orientation and migration of monarch butterflies (Danaus plexippus)

Effects of early-life exposure to sublethal levels of a common neonicotinoid insecticide on the orientation and migration of monarch butterflies (Danaus plexippus)

Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle

Developmental and reproductive effects of clothianidin exposure in monarch butterflies (Lepidoptera: Nymphalidae)

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