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.
Colorado potato beetle (Leptinotarsa decemlineata Say [Coleoptera: Chrysomelidae]) is a pest of potato throughout the Northern Hemisphere, but little is known about the beetle's origins as a pest. We sampled the beetle from uncultivated Solanum host plants in Mexico, and from pest and non-pest populations in the United States and used mitochondrial DNA and nuclear loci to examine three hypotheses on the origin of the pest lineages: 1) the pest beetles originated from Mexican populations, 2) they descended from hybridization between previously divergent populations, or 3) they descended from populations that are native to the Plains states in the United States. Mitochondrial haplotypes of non-pest populations from Mexico and Arizona differed substantially from beetles collected from the southern plains and potato fields in the United States, indicating that beetles from Mexico and Arizona did not contribute to founding the pest lineages. Similar results were observed for AFLP and microsatellite data . In contrast, non-pest populations from the states of Colorado, Kansas, Nebraska, New Mexico, and Texas were genetically similar to U.S. pest populations, indicating that they contributed to the founding of the pest lineages. Most of the pest populations do not show a significant reduction in genetic diversity compared to the plains populations in the United States. We conclude that genetically heterogeneous beetle populations expanded onto potato from native Solanum hosts. This mode of host range expansion may have contributed to the abundant genetic diversity of contemporary populations, perhaps contributing to the rapid evolution of climate tolerance, host range, and insecticide resistance.
BackgroundInvasive pest species offers a unique opportunity to study the effects of genetic architecture, demography and selection on patterns of genetic variability. Invasive Colorado potato beetle (Leptinotarsa decemlineata) populations have experienced a rapid range expansion and intense selection by insecticides. By comparing native and invasive beetle populations, we studied the origins of organophosphate (OP) resistance-associated mutations in the acetylcholinesterase 2 (AChE2) gene, and the role of selection and demography on its genetic variability.ResultsAnalysis of three Mexican, two US and five European populations yielded a total of 49 haplotypes. Contrary to the expectations all genetic variability was associated with a point mutation linked to insecticide resistance (S291G), this mutation was found in 100% of Mexican, 95% of US and 71% of European beetle sequences analysed. Only two susceptible haplotypes, genetically very differentiated, were found, one in US and one in Europe. The genetic variability at the AChE2 gene was compared with two other genes not directly affected by insecticide selection, diapause protein 1 and juvenile hormone esterase. All three genes showed reduction in genetic variability indicative of a population bottleneck associated with the invasion.ConclusionsStochastic effects during invasion explain most of the observed patterns of genetic variability at the three genes investigated. The high frequency of the S291G mutation in the AChE2 gene among native populations suggests this mutation is the ancestral state and thus, either a pre-adaptation of the beetle for OP resistance or the AChE2 is not the major gene conferring OP resistance. The long historical association with host plant alkaloids together with recombination may have contributed to the high genetic variation at this locus. The genetic diversity in the AChE2 locus of the European beetles, in turn, strongly reflects founder effects followed by rapid invasion. Our results suggest that despite the long history of insecticide use in this species, demographic events together with pre-invasion history have been strongly influential in shaping the genetic diversity of the AChE2 gene in the invasive beetle populations.
Existing scholarship on agroecology and food systems education within U.S. colleges and universities has focused primarily on preparing students to be professionals working in agrifood systems. Developing students' skills and competencies, though vitally important, may not suffice for supporting transformative learning. Transformative learning shifts students' perceptions and awareness and informs future actions, constituting a potential avenue for leveraging education to support transformations toward more socially just and ecologically viable agrifood systems. It is unclear, however, what pedagogies and educational practices enable transformative learning. This paper explores the integration of multiple pedagogical innovations within an advanced agroecology course taught at the University of Vermont. Over a decade, the teaching team has made iterative adjustments to course content and pedagogies with the goal of catalyzing action toward transforming agrifood systems. In this paper, we evaluate our pedagogical approach, asking: (1) How well do course content and pedagogy align with our definition of transformative agroecology as transdisciplinary, participatory, action-oriented, and political? (2) How well does our approach enable transformative agroecological learning, and how is that identified? We present our course evaluation as a case study comprising qualitative analyses of course syllabi, student comments on University-administered course evaluations, and most significant change (MSC) reflections. MSC reflections proved to be a valuable method for identifying and assessing transformative learning. Through a curricular review, we found that substantial changes to course content and evaluative assignments between 2010 and 2020 align with a transformative approach to agroecology. This is validated in students' MSC reflections, which provide evidence of transformative learning. In sharing evaluative results, processes, and insights, we aim to contribute to a broader movement of scholar educators committed to iteratively and collaboratively developing transformative pedagogies within agroecology and sustainable food system education. We contend that reflexive practice among educators is necessary to leverage education for transforming agrifood systems.
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