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Understanding the evolutionary origins and factors maintaining alternative life history strategies (ALHS) within species is a major goal of evolutionary research. While alternative alleles causing discrete ALHS are expected to purge or fix over time, one-third of the ~90 species of Colias butterflies are polymorphic for a female-limited ALHS called Alba. Whether Alba arose once, evolved in parallel, or has been exchanged among taxa is currently unknown. Using comparative genome-wide association study (GWAS) and population genomic analyses, we placed the genetic basis of Alba in time-calibrated phylogenomic framework, revealing that Alba evolved once near the base of the genus and has been subsequently maintained via introgression and balancing selection. CRISPR-Cas9 mutagenesis was then used to verify a putative cis-regulatory region of Alba, which we identified using phylogenetic foot printing. We hypothesize that this cis-regulatory region acts as a modular enhancer for the induction of the Alba ALHS, which has likely facilitated its long evolutionary persistence.

How much does natural selection, as opposed to genetic drift, admixture, and gene flow, contribute to the evolution of invasive species following introduction to a new environment? Here we assess how evolution can shape biological invasions by examining population genomic variation in non‐native guppies (Poecilia reticulata) introduced to the Hawaiian Islands approximately a century ago. By examining 18 invasive populations from four Hawaiian islands and four populations from the native range in northern South America, we reconstructed the history of introductions and evaluated population structure as well as the extent of ongoing gene flow across watersheds and among islands. Patterns of differentiation indicate that guppies have developed significant population structure, with little natural or human‐mediated gene flow having occurred among populations following introduction. Demographic modeling and admixture graph analyses together suggest that guppies were initially introduced to O‘ahu and Maui and then translocated to Hawai‘i and Kaua‘i. We detected evidence for only one introduction event from the native range, implying that any adaptive evolution in introduced populations likely utilized the genetic variation present in the founding population. Environmental association tests accounting for population structure identified loci exhibiting signatures of adaptive variation related to predators and landscape characteristics but not nutrient regimes. When paired with high estimates of effective population sizes and detectable population structure, the presence of environment‐associated loci supports the role of natural selection in shaping contemporary evolution of Hawaiian guppy populations. Our findings indicate that local adaptation may engender invasion success, particularly in species with life histories that facilitate rapid evolution. Finally, evidence of low gene flow between populations suggests that removal could be an effective approach to control invasive guppies across the Hawaiian archipelago.

How do novel fire regimes and a long history of fire suppression influence species genetic diversity? Genetic diversity provides the raw materials for sustaining viable populations and for allowing adaptation to novel environmental challenges, and at present, few studies address the genetic responses of animals to fire management. Here we study the genetic responses of 2 butterfly species to a landscape gradient of fire timing and severity in Yosemite National Park using a large set of genome-wide single nucleotide polymorphisms (SNPs). Butterflies are important bio-indicators of invertebrate diversity and play important roles in both bottom–up and top–down ecosystem processes, and typically increase in abundance following wildfires, due to an increase in abundance of flowering plants. However, it is not clear how genetic diversity and genetic connectivity of butterflies respond to landscape change following fire, and whether fire management has positive or negative effects. We found evidence to suggest that fire increases genetic diversity and reduces isolation in 2 butterfly species, but that aspects of the fire regime (severity, extent, timing, and frequency) differ in importance depending on the ecology of the specific species. This research is the first study to address fire management impacts on genetic diversity in invertebrates, and the results will allow fire managers to predict that fire reintroduction in protected areas will generally benefit butterfly populations.

To understand how organisms adapt to their environment, a gene-environmental association (GEA) analysis is commonly conducted. GEA methods based on mixed models, such as linear latent factor mixed models (LFMM) and LFMM2, have grown in popularity for their robust performance in terms of power and computational speed. However, it is unclear how the assumption of a Gaussian distribution for the response variables influences model performance. In this paper, we develop a generalized linear model (GLM) that allows for non-Gaussian distribution in the genotypic response variables, and treatment of multiallelic nucleotide polymorphisms. Moreover, this multinomial logistic regression model (MLR) is combined with an admixture-based model or principal components analysis to correct for population structure (MLR-ADM and MLR-PC). Using simulations, we evaluate the type 1 error, false discovery rates (FDR), and power to detect selected SNPs, to guide model choice and best practices. With genomic control, MLR-PC and LFMM2 have similar type 1 error, FDRs, and power when analysing biallelic SNPs, while dramatically outperforming models not accounting for population structure. Differences in performance occur under continuous population structure where MLR-PC outperforms LFMM/LFMM2, especially when a larger number of clusters or triallelic SNPs are analysed. The Human Genome Diversity Project (HGDP) data set shows that both MLR-PC and LFMM2 control the inflation of P -values. Analysis of the 1,000 Genome Project Phase 3 data set illustrates that MLR-PC and LFMM2 produce consistent results for most significant SNPs, while MLR-PC discovered additional SNPs corresponding to certain genes, suggesting MLR-PC may be a useful alternative to GEA inference.

Insect pests are characterized by expansion, preference and performance on agricultural crops, high fecundity and rapid adaptation to control methods, which we collectively refer to as pestiferousness. Which organismal traits and evolutionary processes facilitate certain taxa becoming pests remains an outstanding question for evolutionary biologists. In order to understand these features, we set out to test the relative importance of genomic properties that underlie the rapid evolution of pestiferousness in the emerging pest model: the Colorado potato beetle (CPB),Leptinotarsa decemlineataSay. Within theLeptinotarsagenus, only CPB has risen to pest status on cultivatedSolanum. Using whole genomes from ten closely relatedLeptinotarsaspecies, we reconstructed a high-quality species tree of this genus. Within this phylogenetic framework, we tested the relative importance of four drivers of rapid adaptation: standing genetic variation, gene family expansion and contraction, transposable element variation, and protein evolution. Throughout approximately 20 million years of divergence,Leptinotarsashow little evidence of gene family turnover or transposable element variation contributing to pest evolution. However, there is a clear pattern of pest lineages experiencing greater rates of positive selection on protein coding genes, as well as retaining higher levels of standing genetic variation. We also identify a suite of positively selected genes unique to the Colorado potato beetle that are directly associated with pestiferousness. These genes are involved in xenobiotic detoxification, chemosensation, and hormones linked with pest behavior and physiology.

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.

Insecticide use is pervasive as a selective force in modern agroecosystems. Insect herbivores exposed to these insecticides have been able to rapidly evolve resistance to them, but how they are able to do so is poorly understood. One possible but largely unexplored explanation is that exposure to sublethal doses of insecticides may alter epigenetic patterns that are heritable. For instance, epigenetic mechanisms, such as DNA methylation that modifies gene expression without changing the underlying genetic code, may facilitate the emergence of resistant phenotypes in complex ways. We assessed the effects of sublethal insecticide exposure, with the neonicotinoid imidacloprid, on DNA methylation in the Colorado potato beetle, Leptinotarsa decemlineata, examining both global changes in DNA methylation and specific changes found within genes and transposable elements. We found that exposure to insecticide led to decreases in global DNA methylation for parent and F2 generations and that many of the sites of changes in methylation are found within genes associated with insecticide resistance, such as cytochrome P450s, or within transposable elements. Exposure to sublethal doses of insecticide caused heritable changes in DNA methylation in an agricultural insect herbivore. Therefore, epigenetics may play a role in insecticide resistance, highlighting a fundamental mechanism of evolution while informing how we might better coexist with insect species in agroecosystems.

Background 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 in Leptinotarsa decemlineata baseline sensitivity to insecticides as they became commercially available. Results 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. Conclusions 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.

The climate-driven species pump hypothesis has been supported in a number of phylogeographic studies of alpine species. Climate-driven shifts in distribution, coupled with rapid demographic change, have led to strong genetic drift and lineage diversification. Although the species pump has been linked to rapid speciation in a number of studies, few studies have demonstrated that ecological divergence accompanies rapid speciation. Here we examine genetic, morphological and physiological variation in members of the ground beetle taxon Nippononebria, to test three competing hypotheses of evolutionary diversification: isolation and incomplete lineage sorting (no speciation), recent speciation without ecological divergence, or recent speciation with ecological divergence into alpine habitats. Genetic data are consistent with recent divergence, with major lineages forming in the last million years. A species tree analysis, in conjunction with morphological divergence in male reproductive traits, support the formation of three recognized Nippononebria taxa. Furthermore, both morphological and physiological traits demonstrate ecological divergence in alpine lineages, with convergent shifts in body shape and thermal tolerance breadth. This provides strong evidence that the climate-driven species pump can generate ecological novelty, though it is argued that spatial scale may be a key determinant of broader patterns of macroevolution in alpine communities.

Despite considerable research, efforts to manage insecticide resistance continue to fail. The Colorado potato beetle (CPB), Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), epitomizes this problem, as it has repeatedly and rapidly evolved resistance to50 insecticides. The patterns of resistance evolution are intriguing, as they defy models where resistance evolves from rare mutations. Here we synthesize recent research on insecticide resistance in CPB showing that polygenic resistance drawn from standing genetic diversity explains genomic patterns of insecticide resistance evolution. However, rapid gene regulatory evolution suggests that other mechanisms might also facilitate adaptive change. We explore the hypothesis that sublethal stress from insecticide exposure could alter heritable epigenetic modifications, and discuss the range of experimental approaches needed to fully understand insecticide resistance evolution in this super pest.

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, nonmutually 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 nonpest 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.

Past glacial cycles have generated lineage diversity in alpine habitats, acting as a climate-driven species pump. It is not clear how much this process contributes to ecological diversification of alpine species. To examine this problem, we test patterns of genetic and phenotypic divergence in two co-distributed species complexes of flightless alpine ground beetles. Greater differentiation in functional traits would indicate that ecological selection is an outcome of oscillating climate change, whereas greater differentiation in non-ecological traits would indicate niche conservatism. Location: The Cascades Range and Trinity Mountains of western North America. Taxon: Nebria paradisi and N. vandykei species complexes (Insecta: Coleoptera: Carabidae: Nebriinae). Methods: We generated genome-wide single nucleotide polymorphism data and mitochondrial sequence data, as well as morphological and physiological data, to compare populations spanning the range of both species. Phylogenetic and population genetic analyses were used to infer relationships among taxa and populations in each species complex, as well as historical demography. Support vector machines were used to test for classification of taxa and populations based on ecomorphological, ecophysiological and male reproductive traits. Mantel tests were then used to assess associations between phenotypic and genetic divergence among populations. Results: The N. vandykei and N. paradisi species complexes are each comprised of genetically distinctive populations exhibiting long-term demographic declines. Each phylogeny supports multiple monophyletic groups with geographical cohesion. By examining phenotypic traits among populations in both species’ complexes, we show that reproductive trait divergence can discriminate species and population status more effectively than ecomorphological or ecophysiological traits. Reproductive and genetic divergence are significantly correlated in the N. vandykei species complex. Main Conclusions: We found limited evidence of ecological selection acting on functional traits. Instead, reproductive and genetic divergence evolved among isolated populations in both species complexes, suggesting niche conservatism may be a common outcome in alpine species diversification.

Two new species of Bimastos Moore are described based on morphological and molecular data. Bimastos nanae n. sp. resembles B. lawrenceae Fender, B. zeteki (Smith and Gittins) and B. welchi (Smith). Bimastos nanae n. sp. differs from these species in the position of the clitellum, size and number and position of thickened septa. Bimastos magnum n. sp. is similar to B. schwerti Csuzdi & Chang and B. palustris Moore in having a fully annular clitellum and male pores on huge porophores. Bimastos magnum n. sp. differs from both species by having a more posterior position of the clitellum (in xxiv-xxxiii, xxxiv) and larger body size. With the description of these new species, the number of Bimastos species is raised to 14.

Pesticide resistance provides one of the best examples of rapid evolution to environmental change. The Colorado potato beetle (CPB) has a long and noteworthy history as a super-pest due to its ability to repeatedly develop resistance to novel insecticides and rapidly expand its geographic and host plant range. Here, we investigate regional differences in demography, recombination, and selection using whole-genome resequencing data from two highly resistant CPB populations in the United States (Hancock, Wisconsin and Long Island, New York). Demographic reconstruction corroborates historical records for a single pest origin during the colonization of the Midwestern and Eastern United States in the mid- to late-19th century and suggests that the effective population size might be higher in Long Island, NY than Hancock, WI despite contemporary potato acreage of Wisconsin being far greater. Population-based recombination maps show similar background recombination rates between these populations, as well as overlapping regions of low recombination that intersect with important metabolic detoxification genes. In both populations, we find compelling evidence for hard selective sweeps linked to insecticide resistance with multiple sweeps involving genes associated with xenobiotic metabolism, stress response, and defensive chemistry. Notably, only two candidate insecticide resistance genes are shared among both populations, but both appear to be independent hard selective sweep events. This suggests that repeated, rapid, and independent evolution of genes may underlie CPB's pest status among geographically distinct populations.

Structural variation has been associated with genetic diversity and adaptation. Despite these observations, it is not clear what their relative importance is for evolution, especially in rapidly adapting species. Here we examine the significance of structural polymorphisms in pesticide resistance evolution of the agricultural super-pest, the Colorado potato beetle, Leptinotarsa decemlineata. By employing a parent offspring trio sequencing procedure, we develop highly contiguous reference genomes to characterize structural variation. These updated assemblies represent100-fold improvement of contiguity and include derived pest and ancestral non-pest individuals. We identify200,000 structural variations, which appear to be non-randomly distributed across the genome as they co-occur with transposable elements and genes. Structural variations intersect with exons in a large proportion of gene annotations (~20%) that are associated with insecticide resistance (including cytochrome P450s), development, and transcription. To understand the role structural variations play in adaptation, we measure their allele frequencies among an additional 57 individuals using whole genome resequencing data, which represents pest and non-pest populations of North America. Incorporating multiple independent tests to detect the signature of natural selection using SNP data, we identify 14 genes that are likely under positive selection, include structural variations, and SNPs of elevated frequency within the pest lineages. Among these, three are associated with insecticide resistance based on previous research. One of these genes, CYP4g15, is co-induced during insecticide exposure with glycosyltransferase-13, which is a duplicated gene enclosed within a structural variant adjacent to the CYP4g15 genic region. These results demonstrate the significance of structural variations as a genomic feature to describe species history, genetic diversity, and adaptation.

Species responses to environmental change are likely to depend on existing genetic and phenotypic variation, as well as evolutionary potential. A key challenge is to determine whether gene flow might facilitate or impede genomic divergence among populations responding to environmental change, and if emergent phenotypic variation is dependent on gene flow rates. A general expectation is that patterns of genetic differentiation in a set of codistributed species reflect differences in dispersal ability. In less dispersive species, we predict greater genetic divergence and reduced gene flow. This could lead to covariation in life‐history traits due to local adaptation, although plasticity or drift could mirror these patterns. We compare genome‐wide patterns of genetic structure in four phenotypically variable grasshopper species along a steep elevation gradient near Boulder, Colorado, and test the hypothesis that genomic differentiation is greater in short‐winged grasshopper species, and statistically associated with variation in growth, reproductive, and physiological traits along this gradient. In addition, we estimate rates of gene flow under competing demographic models, as well as potential gene flow through surveys of phenological overlap among populations within a species. All species exhibit genetic structure along the elevation gradient and limited gene flow. The most pronounced genetic divergence appears in short‐winged (less dispersive) species, which also exhibit less phenological overlap among populations. A high‐elevation population of the most widespread species, Melanoplus sanguinipes, appears to be a sink population derived from low elevation populations. While dispersal ability has a clear connection to the genetic structure in different species, genetic distance does not predict growth, reproductive, or physiological trait variation in any species, requiring further investigation to clearly link phenotypic divergence to local adaptation., Four grasshoppers species exhibit genetic structure and limited gene flow along elevation gradients in the Rocky Mountains. The strength of genetic divergence is associated with dispersal phenotypes and phenological patterns. The most widespread species, Melanoplus sanguinipes, follows a stepping stone pattern, with the highest elevation population appearing to be a sink population derived from low elevation.

The hyperdiverse order Coleoptera comprises a staggering ~25% of known species on Earth. Despite recent breakthroughs in next generation sequencing, there remains a limited representation of beetle diversity in assembled genomes. Most notably, the ground beetle family Carabidae, comprising more than 40,000 described species, has not been studied in a comparative genomics framework using whole genome data. Here we generate a high-quality genome assembly for Nebria riversi, to examine sources of novelty in the genome evolution of beetles, as well as genetic changes associated with specialization to high-elevation alpine habitats. In particular, this genome resource provides a foundation for expanding comparative molecular research into mechanisms of insect cold adaptation. Comparison to other beetles shows a strong signature of genome compaction, with N. riversi possessing a relatively small genome (~147 Mb) compared to other beetles, with associated reductions in repeat element content and intron length. Small genome size is not, however, associated with fewer protein-coding genes, and an analysis of gene family diversity shows significant expansions of genes associated with cellular membranes and membrane transport, as well as protein phosphorylation and muscle filament structure. Finally, our genomic analyses show that these high-elevation beetles have endosymbiotic Spiroplasma, with several metabolic pathways (e.g., propanoate biosynthesis) that might complement N. riversi, although its role as a beneficial symbiont or as a reproductive parasite remains equivocal.

Alternative life-history strategies (ALHS) are genetic polymorphisms generating phenotypes differing in life histories that generally arise due to metabolic resource allocation tradeoffs. Althouigh ALHS are often be limited to a single sex or populations of a species, they can, in rare cases, be found among several species across a genus. In the butterfly genus Colias, at least a third of the species have a female limited ALHS called Alba. While many females develop brightly pigmented wings, Alba females reallocate nitrogen resources used in pigment synthesis to reproductive development, producing white-winged, more fecund females. Whether this ALHS evolved once or many times, and whether it has moved among species via introgression or been maintained via long-term balancing selection, has not been established. Answering these questions presents an opportunity to investigate the genetic basis and evolutionary forces acting upon ALHS, which have rarely been studied at a genus level. Here we identify the genetic locus of Alba in a second Colias species, allowing us to compare this with previous results in a larger phylogenetic context. Our findings suggest Alba has a singular origin and has been maintained in Colias through a combination of balancing selection and introgression for nearly one million years and at least as many generations. Finally, using CRISPR/Cas9 deletions in the cis-regulatory region of the Alba allele, we demonstrate that the Alba allele is a modular enhancer for the BarH1 gene and is necessary for the induction of the ALHS, which potentially facilitates its long-term persistence in the genus.

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.

BackgroundInsecticide resistance and rapid pest evolution threatens food security and the development of sustainable agricultural practices. An improved understanding of the evolutionary mechanisms that allow pests to rapidly adapt to novel control tactics will help prevent economically damaging outbreaks. The Colorado potato beetle (CPB), Leptinotarsa decemlineata, is a global super-pest that 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.ResultsPopulation genomic analysis demonstrates that CPB is geographically structured, even among recently established pest populations. Pest populations exhibit only modest reductions in nucleotide diversity, relative to non-pest ancestral populations, and show evidence of recent demographic expansion. Genome scans of selection provide clear signatures of repeated adaptation across different CPB populations, with especially strong evidence that insecticide resistance involves selection of different genes in different populations. Similarly, analyses of gene expression show that constitutive upregulation of candidate insecticide resistance genes drives distinctive population patterns.ConclusionCPB evolves insecticide resistance repeatedly across agricultural regions, and oftentimes at the same loci, supporting a prominent role of polygenic evolution 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. An important future goal will be to understand how polygenic resistance phenotypes spread among local pest populations, in order to refine integrated pest management practices to maintain the efficacy and sustainability of novel control techniques.

The hyper-diverse order Coleoptera comprises a staggering ~25% of known species on Earth. Despite recent breakthroughs in next generation sequencing, there remains a limited representation of beetle diversity in assembled genomes. Most notably, the ground beetle family Carabidae, comprising more than 40,000 described species, has not been studied in a comparative genomics framework using whole genome data. Here we generate a high-quality genome assembly for Nebria riversi, to examine sources of novelty in the genome evolution of beetles, as well as genetic changes associated with specialization to high elevation alpine habitats. In particular, this genome resource provides a foundation for expanding comparative molecular research into mechanisms of insect cold adaptation. Comparison to other beetles shows a strong signature of genome compaction, with N. riversi possessing a relatively small genome (~147 Mb) compared to other beetles, with associated reductions in repeat element content and intron length. Small genome size is not, however, associated with fewer protein-coding genes, and an analysis of gene family diversity shows significant expansions of genes associated with cellular membranes and membrane transport, as well as protein phosphorylation and muscle filament structure. Finally, our genomic analyses show that these high elevation beetles have endosymbiotic Spiroplasma, with several metabolic pathways (e.g. propanoate biosynthesis) that might complement N. riversi, although its role as a beneficial symbiont or as a reproductive parasite remains equivocal.

The ability of pests to develop resistance is still poorly understood, particularly regarding the process of adaptive change that leads to resistance. Understanding the mechanisms involved in pesticide adaptation is important because common methods of field-level resistance management assume that simple (single-gene) mutations cause resistance, but may not perform effectively when multiple loci and several molecular pathways confer resistance. Emerging experimental and genomic evidence suggests the single-gene model may be insufficient to explain many cases of rapid pest evolution. Here we review such evidence in the Colorado potato beetle, Leptinotarsa decemlineata, widely considered to be a super-pest due to its rapid evolution to most classes of insecticides. A combination of studies suggests that polygenic resistance drawn from standing variation best explains regional differences in patterns of insecticide resistance. However, these studies have lacked a temporal framework to demonstrate polygenic evolution unequivocally, as well as the ability to estimate key evolutionary parameters to model processes of rapid evolution. We suggest a temporal framework to empirically test for polygenic insecticide resistance evolution, as well as determine the proximate genetic and evolutionary mechanisms contributing to resistance. Emerging data from population genomics promise to increase our knowledge of insect pest molecular genetics by identifying gene networks involved in pesticide resistance, thereby providing a means to monitor the spread of resistance, develop management approaches that increase pesticide longevity, and identify new methods of gene-targeted pest control.

The phylogeny of the carabid beetle supertribe Nebriitae is inferred from analyses of DNA sequence data from eight gene fragments including one nuclear ribosomal gene (28S), four nuclear-protein coding genes (CAD, topoisomerase 1, PEPCK, andwingless), and three mitochondrial gene fragments (16S + tRNA-Leu + ND1, COI (“barcode” region) and COI (“Pat/Jer” region)). Our taxon sample included 264 exemplars representing 241 species and subspecies (25% of the known nebriite fauna), 39 of 41 currently accepted genera and subgenera (all exceptNotiokasisandArchileistobrius), and eight outgroup taxa. Separate maximum likelihood (ML) analyses of individual genes, combined ML analyses of nuclear, nuclear protein-coding, and mitochondrial genes, and combined ML and Bayesian analyses of the eight-gene-fragment matrix resulted in a well-resolved phylogeny of the supertribe, with most nodes in the tree strongly supported. Within Nebriitae, 167 internal nodes of the tree (out of the maximum possible 255) are supported by maximum-likelihood bootstrap values of 90% or more. The tribes Notiophilini, Opisthiini, Pelophilini, and Nebriini are well supported as monophyletic but relationships among these are not well resolved.Nippononebriais a distinct genus more closely related toLeistusthanNebria.Archastes,Oreonebria,Spelaeonebria, andEurynebria, previously treated as distinct genera by some authors, are all nested within a monophyletic genusNebria.WithinNebria, four major clades are recognized: (1) theOreonebriaSeries, including eight subgenera arrayed in two subgeneric complexes (theEonebriaandOreonebriaComplexes); (2) the Nebriola Series, including only subgenus Nebriola; (3) theNebriaSeries, including ten subgenera arrayed in two subgeneric complexes, theBoreonebriaandNebriaComplexes, with the latter further subdivided into three subgeneric subcomplexes (theNebria,Epinebriola, andEunebriaSubcomplexes)); and (4) theCatonebriaSeries, including seven subgenera arrayed in two subgeneric complexes (theReductonebriaandCatonebriaComplexes). A strong concordance of biogeography with the inferred phylogeny is noted and some evident vicariance patterns are highlighted. A revised classification, mainly within the Nebriini, is proposed to reflect the inferred phylogeny. Three genus-group taxa (Nippononebria,VancouveriaandArchastes) are given revised status and seven are recognized as new synonymies (NebrioritesJeannel, 1941 andMarggiaHuber, 2014 =OreonebriaDaniel, 1903;PseudonebriolaLedoux & Roux, 1989 =BoreonebriaJeannel, 1937;PatrobonebriaBänninger, 1923,ParanebriaJeannel, 1937 andBarbonebriolaHuber & Schmidt, 2017 =EpinebriolaDaniel & Daniel, 1904; andAsionebriaShilenkov, 1982 =PsilonebriaAndrewes, 1923). Six new subgenera are proposed and described for newly recognized clades: Parepinebriola Kavanaugh subgen. nov. (type species:Nebria delicataHuber & Schmidt, 2017), Insulanebria Kavanaugh subgen. nov. (type species:Nebria carbonariaEschscholtz, 1829), Erwinebria Kavanaugh subgen. nov. (type speciesNebria sahlbergiiFischer von Waldheim, 1828),NivalonebriaKavanaughsubgen. nov.(type species:Nebria paradisiDarlington, 1931),NeaptenonebriaKavanaughsubgen. nov.(type species:Nebria ovipennisLeConte, 1878), andPalaptenonebriaKavanaughsubgen. nov.(type species:Nebria mellyiGebler, 1847). Future efforts to better understand relationships within the supertribe should aim to expand the taxon sampling of DNA sequence data, particularly within subgeneraLeistusandEvanoleistus of genusLeistusand theNebriaComplex of genusNebria.

Key changes in ecological niche space are often critical to understanding how lineages diversify during adaptive radiations. However, the converse, or understanding why some lineages are depauperate and relictual, is more challenging, as many factors may constrain niche evolution. In the case of the insect order Grylloblattodea, highly conserved thermal breadth is assumed to be closely tied to their relictual status, but has not been formerly tested. Here, we investigate whether evolutionary constraints in the physiological tolerance of temperature can help explain relictualism in this lineage. Using a comparative transcriptomics approach, we investigate gene expression following acute heat and cold stress across members of Grylloblattodea and their sister group, Mantophasmatodea. We additionally examine patterns of protein evolution, to identify candidate genes of positive selection. We demonstrate that cold specialization in Grylloblattodea has been accompanied by the loss of the inducible heat shock response under both acute heat and cold stress. Additionally, there is widespread evidence of selection on protein-coding genes consistent with evolutionary constraints due to cold specialization. This includes positive selection on genes involved in trehalose transport, metabolic function, mitochondrial function, oxygen reduction, oxidative stress, and protein synthesis. These patterns of molecular adaptation suggest that Grylloblattodea have undergone evolutionary trade-offs to survive in cold habitats and should be considered highly vulnerable to climate change. Finally, our transcriptomic data provide a robust backbone phylogeny for generic relationships within Grylloblattodea and Mantophasmatodea. Major phylogenetic splits in each group relate to arid conditions driving biogeographical patterns, with support for a sister-group relationship between North American Grylloblatta and Altai-Sayan Grylloblattella, and a range disjunction in Namibia splitting major clades within Mantophasmatodea. © 2020 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

The most remarkable feature of our planet is the diversity of its life forms, ranging from viruses and nanobacteria to blue whales and giant sequoias to satanic leaf‐tailed geckos and leafy seadragons (look them up!). Life is found in essentially all environments on earth, and the number of species living on our planet is many times greater than we could have imagined a century ago. A well‐regarded estimate pegs the number of eukaryotic species on earth at 8.7 million (±1.3 million), of which fewer than 15% are currently described (Mora et al., 2011). The diversity of prokaryotes is less clear (and highly controversial), but an analysis of 1.6 billion 16S ribosomal RNA sequences estimated that 0.8–1.6 million prokaryotic operational taxonomic units exist globally (Louca et al., 2019). While we do not know how many species are currently extant, or have existed in the past, we do know that this biodiversity is valuable, providing food, fibre and medicine, furnishing ecosystem services such as water and air purification, nutrient cycling, pollination and carbon uptake, and contributing to technological innovations ranging from biotechnology to robotics to material science. Moreover, biodiversity underlies the cultural identity of human populations and is important to human health and well‐being. Geographically, species richness increases from the Polar Regions to the tropics in terrestrial and surface marine ecosystems. Thus, some countries, especially those in tropical and subtropical regions, are endowed with much greater biodiversity than others. Unfortunately, benefits arising from the access and utilization of this biodiversity have been unequally shared, with (paradoxically) biodiversity‐poor countries often accruing the lion's share of economic gains. There can be imbalances within countries as well, wherein some segments of the population obtain greater economic benefits from biodiversity and associated traditional knowledge than indigenous peoples. The “Nagoya Protocol on Access to Genetic Resources and the Fair and Equitable Sharing of Benefits Arising from their Utilization,” which came into force in 2014, is an international agreement designed to ensure that the benefits arising from biodiversity are shared equitably (https://www.cbd.int/abs/). However, few scientific journals require compliance with the Nagoya Protocol or the reporting of benefits from biodiversity research. In this editorial, we (the editors of Molecular Ecology and Molecular Ecology Resources) express support for the Nagoya Protocol and the principle of benefit sharing. We believe that scientific journals publishing research on biodiversity can play an important role in implementing the Nagoya Protocol and in reporting on benefits generated from such research. Below, we provide background on the Nagoya Protocol, discuss the kinds of benefits that may arise from biodiversity research, describe the rationale for reporting on these benefits and introduce changes to the journals’ Data Accessibility Statements to incorporate the requirements and goals of the Nagoya Protocol.

Understanding the effects of environmental disturbances on the health and physiology of insects is crucial in predicting the impact of climate change on their distribution, abundance, and ecology. As microbial symbionts have been shown to play an integral role in a diversity of functions within the insect host, research examining how organisms adapt to environmental fluctuations should include their associated microbiota. Previous studies have shown that temperature affects the diversity of protists in termite gut, but less is known about the bacterial symbionts. In this study, subterranean termites (Reticulitermes flavipes(Kollar)) were exposed to three different temperature treatments characterized as low (15 °C), medium (27 °C), and high (35 °C). Results showed low temperature exposed termites had significantly lower CTmin and significantly higher SCP values compared to termites from medium or high temperature groups. This suggests that pre-exposure to cold allowed termites to stay active longer in decreasing temperatures but caused termites to freeze at higher temperatures. High temperature exposure had the most deleterious effects on termites with a significant reduction in termite survival as well as reduced ability to withstand cold stress. The microbial community of high temperature exposed termites showed a reduction in bacterial richness and decreased relative abundance of Spirochaetes, Elusimicrobia, and methanogenic Euryarchaeota. Our results indicate a potential link between gut bacterial symbionts and termite’s physiological response to environmental changes and highlight the need to consider microbial symbionts in studies relating to insect thermosensitivity.

The evolutionary histories of alpine species are often directly associated with responses to glaciation. Deep divergence among populations and complex patterns of genetic variation have been inferred as consequences of persistence within glacier boundaries (i.e., on nunataks), while shallow divergence and limited genetic variation are assumed to result from expansion from large refugia at the edge of ice shields (i.e., massifs de refuge). However, for some species, dependence on specific microhabitats could profoundly influence their spatial and demographic response to glaciation, and such a simple dichotomy may obscure the localization of actual refugia. In this study, we use the Nebria ingens complex (Coleoptera: Carabidae), a water-affiliated ground beetle lineage, to test how drainage basins are linked to their observed population structure. By analysing mitochondrial COI gene sequences and genome-wide single nucleotide polymorphisms, we find that the major drainage systems of the Sierra Nevada Mountains in California best explain the population structure of the N. ingens complex. In addition, we find that an intermediate morphotype within the N. ingens complex is the product of historical hybridization of N. riversi and N. ingens in the San Joaquin basin during glaciation. This study highlights the importance of considering ecological preferences in how species respond to climate fluctuations and provides an explanation for discordances that are often observed in comparative phylogeographical studies.

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 tuberosum L., 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 decemlineata Say, 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 among L. decemlineata populations 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.

The Colorado potato beetle, Leptinotarsa decemlineata Say, is a serious pest of potato, Solanum tuberosum L., worldwide. Leptinotarsa decemlineata has a history of repeated adaptation to insecticides, and exhibits a geographic pattern of decreasing insecticide resistance from east to west in the USA. Imidacloprid is one of the most widely used insecticide in western states. In this study, we measured imidacloprid resistance among larval and adult L. decemlineata from ten locations in the Columbia Basin (southeastern Washington and northeastern Oregon) using topical LD50 bioassays, and compared them to estimates from ten locations in Minnesota and Wisconsin. Larval and adult imidacloprid LD50’s and mean percent mortality were generally lowest in Washington and Oregon, but some sites exhibited reductions in mortality comparable to those observed at some Wisconsin sites. Adult LD50’s suggest L. decemlineata in the Columbia Basin may be evolving in response to selection by neonicotinoid insecticides, but larval data suggest high susceptibility to imidacloprid remains in most populations. Future work should expand resistance monitoring efforts to include more regions in the West and other insecticide modes of action.

Background Arthropod pests are widely perceived to evolve resistance to insecticides at different rates. Although widespread "successful" species are assumed to evolve quickly and minor pests slowly, few studies have utilized published data on resistance events to test for differences among species. Using 532 records from the Arthropod Pesticide Resistance Database covering 20 species, we applied a survival analysis to model the number of generations from insecticide introduction to the first report of arthropod resistance, providing one of the most comprehensive analyses of this question to date. Our approach tested: 1) whether successful pests evolve resistance faster than close relatives, 2) whether species differ significantly in the time to demonstrate resistance, and 3) whether different insecticide classes differ in durability (length of time an insecticide is used before resistance arises). Results We found that species differed significantly in the amount of time it took for resistance to be reported. Overall, the median duration between the introduction of an insecticide and the first report of resistance was 66 generations (95% c.i. 60-78 generations), and highly-resistant arthropods did not evolve resistance faster than their relatives. Insecticide durability did not differ by the mode of action or year of introduction. Conclusion Arthropod species significantly varied in how rapidly they evolve resistance to new insecticides, regardless of their chemistry. Visualization of the history of insecticide resistance provides information to be used for understanding how pesticide resistance evolved and how it can best be managed. © 2018 Society of Chemical Industry.

Pest species in agroecosystems often exhibit patterns of rapid evolution to environmental and human-imposed selection pressures. Although the role of adaptive processes is well accepted, few insect pests have been studied in detail and most research has focused on selection at insecticide resistance candidate genes. Emerging genomic datasets provide opportunities to detect and quantify selection in insect pest populations, and address long-standing questions about mechanisms underlying rapid evolutionary change. We examine the strengths of recent studies that stratify population samples both in space (along environmental gradients and comparing ancestral vs. derived populations) and in time (using chronological sampling, museum specimens and comparative phylogenomics), resulting in critical insights on evolutionary processes, and providing new directions for studying pests in agroecosystems.

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.

The ability of insect pests to rapidly and repeatedly adapt to insecticides has long challenged entomologists and evolutionary biologists. Since Crow's seminal paper on insecticide resistance in 1957, new data and insights continue to emerge that are relevant to the old questions about how insecticide resistance evolves: such as whether it is predominantly mono- or polygenic, and evolving from standing vs. de novo genetic variation. Many studies support the monogenic hypothesis, and current management recommendations assume single- or two-locus models. But inferences could be improved by integrating data from a broader sample of pest populations and genomes. Here we generate evidence relevant to these questions by applying a landscape genomics framework to the study of insecticide resistance in a major agricultural pest, Colorado potato beetle, Leptinotarsa decemlineata (Say). Genome-environment association tests using genomic variation from 16 populations spanning gradients of landscape variables associated with insecticide exposure over time revealed 42 strong candidate insecticide resistance genes, with potentially overlapping roles in multiple resistance mechanisms. Measurements of resistance to a widely-used insecticide, imidacloprid, among 47 L. decemlineata populations revealed heterogeneity at a small (2 km) scale and no spatial signature of origin or spread throughout the landscape. Analysis of nucleotide diversity suggested candidate resistance loci have undergone varying degrees of selective sweeps, often maintaining similar levels of nucleotide diversity to neutral loci. This study suggests that many genes are involved in insecticide resistance in L. decemlineata and that resistance likely evolves from both de novo and standing genetic variation. This article is protected by copyright. All rights reserved.

Pleistocene glaciations have profoundly affected patterns of genetic diversity within many species. Temperate alpine organisms likely experienced dramatic range shifts, given that much of their habitat was glaciated during this time. While the effects of glaciations are relatively well understood, the spatial locations of refugia and processes that gave rise to current patterns of diversity are less well known. We use a microsatellite data set to test hypotheses of population connectivity and refugial isolation in the web-toed salamanders (Hydromantes) of the Sierra Nevada. We reject models of refugia with subsequent expansion into either the high southern Sierra or low-elevation Owens Valley, in favor of a simple isolation model with no migration between current populations. We find no evidence of migration at even moderate spatial scales using a variety of analyses in the southern Sierra, and limited migration in the northern Sierra. These results suggest that divergence in isolation following fragmentation is the dominant process structuring genetic variation in these salamander species. In the context of anthropogenic climate change and habitat degradation, these results imply that salamanders and other low-vagility alpine organisms are at risk of decline as they are unlikely to migrate across large distances.