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Despite extensive research on agricultural pests, our knowledge about their evolutionary history is often limited. A mechanistic understanding of the demographic changes and modes of adaptation remains an important goal, as it improves our understanding of organismal responses to environmental change and our ability to sustainably manage pest populations. Emerging genomic datasets now allow for characterization of demographic and adaptive processes, but face limits when they are drawn from contemporary samples, especially in the context of strong demographic change, repeated selection, or adaptation involving modest shifts in allele frequency at many loci. Temporal sampling, however, can improve our ability to reconstruct evolutionary events. Here, we leverage museum samples to examine whether population genomic diversity and structure has changed over time, and to identify genomic regions that appear to be under selection. We focus on the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say 1824; Coleoptera: Chrysomelidae), which is widely regarded as a super-pest due to its rapid, and repeated, evolution to insecticides. By combining whole genome resequencing data from 78 museum samples with modern sampling, we demonstrate that CPB expanded rapidly in the 19th century, leading to a reduction in diversity and limited genetic structure from the Midwest to Northeast United States. Temporal genome scans provide extensive evidence for selection acting in resistant field populations in Wisconsin and New York, including numerous known insecticide resistance genes. We also validate these results by showing that known selective sweeps in modern populations are identified by our genome scan. Perhaps most importantly, temporal analysis indicates selection on standing genetic variation, as we find evidence for parallel evolution in the two geographical regions. Parallel evolution involves a range of phenotypic traits not previously identified as under selection in CPB, such as reproductive and morphological functional pathways that might be important for adaptation to agricultural habitats.

 

An ancient, trans-specific polymorphism provides insights into the evolution of life history strategies. 

ABSTRACT Organisms respond to shifts in climate means and variability via distinct mechanisms. Accounting for these differential responses and appropriately aggregating them is central to understanding and predicting responses to climate variability and change. Separately considering fitness components can clarify organismal responses: fecundity is primarily an integrated, additive response to chronic environmental conditions over time via mechanisms such as energy use and acquisition, whereas survival can be strongly influenced by short-term, extreme environmental conditions. In many systems, the relative importance of fecundity and survival constraints changes systematically along climate gradients, with fecundity constraints dominating at high latitudes or altitudes (i.e. leading range edges as climate warms), and survival constraints dominating at trailing range edges. Incorporating these systematic differences in models may improve predictions of responses to recent climate change over models that assume similar processes along environmental gradients. We explore how detecting and predicting shifts in fitness constraints can improve our ability to forecast responses to climate gradients and change. 

The enigmatic insect order Grylloblattodea comprises two described species in Canada, which are limited to the Montane Cordillera and Pacific Maritime ecozones. One of the described species has three Canadian subspecies of uncertain taxonomic ranking, and there are two additional undescribed or unreported species known in close proximity to the Canadian border in western Alberta and British Columbia that likely also occur in Canada. Thus, as much as 50% of the total taxonomic diversity of Grylloblattodea in Canada is still undocumented. Targeted surveys and taxonomic work, as well as studies that describe the ecology and conservation status of Grylloblattodea are important goals for future research. 

Over the last century, US agriculture greatly intensified and became industrialized, increasing in inputs and yields while decreasing in total cropland area. In the industrial sector, spatial agglomeration effects are typical, but such changes in the patterns of crop types and diversity would have major implications for the resilience of food systems to global change. Here, we investigate the extent to which agricultural industrialization in the United States was accompanied by agglomeration of crop types, not just overall cropland area, as well as declines in crop diversity. Based on county‐level analyses of individual crop land cover area in the conterminous United States from 1840 to 2017, we found a strong and abrupt spatial concentration of most crop types in very recent years. For 13 of the 18 major crops, the widespread belts that characterized early 20th century US agriculture have collapsed, with spatial concentration increasing 15‐fold after 2002. The number of counties producing each crop declined from 1940 to 2017 by up to 97%, and their total area declined by up to 98%, despite increasing total production. Concomitantly, the diversity of crop types within counties plummeted: in 1940, 88% of counties grew >10 crops, but only 2% did so in 2017, and combinations of crop types that once characterized entire agricultural regions are lost. Importantly, declining crop diversity with increasing cropland area is a recent phenomenon, suggesting that corresponding environmental effects in agriculturally dominated counties have fundamentally changed. For example, the spatial concentration of agriculture has important consequences for the spread of crop pests, agrochemical use, and climate change. Ultimately, the recent collapse of most agricultural belts and the loss of crop diversity suggest greater vulnerability of US food systems to environmental and economic change, but the spatial concentration of agriculture may also offer environmental benefits in areas that are no longer farmed.

 

Agricultural insect pests frequently exhibit geographic variation in levels of insecticide resistance, which are often presumed to be due to the intensity of insecticide use for pest management. However, regional differences in the evolution of resistance to novel insecticides suggests that other factors are influencing rates of adaptation. We examined median lethal concentration (LC₅₀) bioassay data spanning 15 years and six insecticides (abamectin, imidacloprid, spinosad, cyantraniliprole, chlorantraniliprole, and metaflumizone) for evidence of regional differences inLeptinotarsa decemlineatabaseline sensitivity to insecticides as they became commercially available.

We consistently found that larvae from Colorado potato beetle populations from the northwestern USA had the highest baseline sensitivity to novel insecticides, while populations from the eastern USA had the lowest. Comparisons of gene expression between populations from these regions revealed constitutively elevated expression of an array of detoxification genes in the East, but no evidence of additional induction when exposed to imidacloprid.

Our results suggest a mechanism for geographic variation in rates of adaptation to insecticides, whereby baseline levels of gene expression determine a population's response to novel insecticides. These findings have implications for the regional development of insecticide resistance management strategies and for the fundamental question of what determines the rate of adaptation to insecticides. © 2020 Society of Chemical Industry

 

Landscape structure, which can be manipulated in agricultural landscapes through crop rotation and modification of field edge habitats, can have important effects on connectivity among local populations of insects. Though crop rotation is known to influence the abundance of Colorado potato beetle (CPB;Leptinotarsa decemlineataSay) in potato (Solanum tuberosumL.) fields each year, whether crop rotation and intervening edge habitat also affect genetic variation among populations is unknown. We investigated the role of landscape configuration and composition in shaping patterns of genetic variation in CPB populations in the Columbia Basin of Oregon and Washington, and the Central Sands of Wisconsin, USA. We compared landscape structure and its potential suitability for dispersal, tested for effects of specific land cover types on genetic differentiation among CPB populations, and examined the relationship between crop rotation distances and genetic diversity. We found higher genetic differentiation between populations separated by low potato land cover, and lower genetic diversity in populations occupying areas with greater crop rotation distances. Importantly, these relationships were only observed in the Columbia Basin, and no other land cover types influenced CPB genetic variation. The lack of signal in Wisconsin may arise as a consequence of greater effective population size and less pronounced genetic drift. Our results suggest that the degree to which host plant land cover connectivity affects CPB genetic variation depends on population size and that power to detect landscape effects on genetic differentiation might be reduced in agricultural insect pest systems.

 

Changing landscape heterogeneity can influence connectivity and alter genetic variation in local populations, but there can be a lag between ecological change and evolutionary responses. Temporal lag effects might be acute in agroecosystems, where land cover has changed substantially in the last two centuries. Here, we evaluate how patterns of an insect pest’s genetic differentiation are related to past and present agricultural land cover change over a 150‐year period. We quantified change in the amount of potato,Solanum tuberosumL., land cover since 1850 using county‐level agricultural census reports, obtained allele frequency data from 7,408 single‐nucleotide polymorphism loci, and compared effects of historic and contemporary landscape connectivity on genetic differentiation of Colorado potato beetle,Leptinotarsa decemlineataSay, in two agricultural landscapes in the United States. We found that potato land cover peaked in Wisconsin in the early 1900s, followed by rapid decline and spatial concentration, whereas it increased in amount and extent in the Columbia Basin of Oregon and Washington beginning in the 1960s. In both landscapes, we found small effect sizes of landscape resistance on genetic differentiation, but a 20× to 1,000× larger effect of contemporary relative to historic landscape resistances. Demographic analyses suggest population size trajectories were largely consistent among regions and therefore are not likely to have differentially impacted the observed patterns of population structure in each region. Weak landscape genetic associations might instead be related to the coarse resolution of our historical land cover data. Despite rapid changes in agricultural landscapes over the last two centuries, genetic differentiation amongL. decemlineatapopulations appears to reflect ongoing landscape change. The historical landscape genetic framework employed in this study is broadly applicable to other agricultural pests and might reveal general responses of pests to agricultural land‐use change.

 

Quaternary climate change has been strongly linked to distributional shifts and recent species diversification. Montane species, in particular, have experienced enhanced isolation and rapid genetic divergence during glacial fluctuations, and these processes have resulted in a disproportionate number of neo‐endemic species forming in high‐elevation habitats. In temperate montane environments, a general model of alpine population history is well supported, where cold‐specialized species track favourable climate conditions downslope during glacial episodes and upslope during warmer interglacial periods, which leads to a climate‐driven population or species diversification pump. However, it remains unclear how geography mediates distributional changes and whether certain episodes of glacial history have differentially impacted rates of diversification. We address these questions by examining phylogenomic data in a North American clade of flightless, cold‐specialized insects, the ice crawlers (Insecta: Grylloblattodea: Grylloblattidae:Grylloblatta). These low‐vagility organisms have the potential to reveal highly localized refugia and patterns of spatial recolonization, as well as a longer history of in situ diversification. Using continuous phylogeographic analysis of species groups, we show that all species tend to retreat to nearby low‐elevation habitats across western North America during episodes of glaciation, but species at high latitude exhibit larger distributional shifts. Lineage diversification was examined over the course of the Neogene and Quaternary periods, with statistical analysis supporting a direct association between climate variation and diversification rate. Major increases in lineage diversification appear to be correlated with warm and dry periods, rather than with extreme glacial events. Finally, we identify substantial cryptic diversity among ice crawlers, leading to high endemism across their range. This diversity provides new insights into highly localized glacial refugia for cold‐specialized species across western North America.