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Schoville, S. D.

Publications and source records attributed to Schoville, S. D..

15 recordsLinked to original sources

Reconstructing the demographic history of blacklegged ticks (Ixodes scapularis) in the northern United States

AimTo resolve the topological branching patterns, the timing of demographic events, and the effective population size changes associated with major demographic events. LocationMidwestern (eastern North Central) and Northeastern USA TaxonBlacklegged tick, Ixodes scapularis (Say, 1821) MethodsUsing three independent genomic datasets, single-nucleotide variants were analyzed for demographic inference. Maximum likelihood topologies and prior ecological knowledge were used to generate nested demographic hypotheses. The best-fit scenario and the associated demographic parameter estimates were determined using approximate Bayesian computation under a random forest statistical model. The topologies and parameters supported in the three independent datasets were compared to generate insights about the demographic history of blacklegged ticks in the region. ResultsThe emergence of extant northern populations of blacklegged ticks began between 10-15 k.y.a. (thousand years ago), with independent population splits from the common ancestor during the Early-Mid-Holocene, and never more recent than 4 k.y.a. All populations sustained moderately large population sizes without bottlenecks, with Michigan as the exception. Michigan appears to have an uncertain placement that depends on sampling, reflecting its admixed origin. Main conclusionsThere are multiple populations of northern blacklegged ticks that have persisted independently as deglaciated regions in the northern U.S. were recolonized following the Last Glacial Maximum (26.5 to 19 k.y.a.). The current ecological expansions across the northern U.S. are likely seeded by separate relictual populations with distinctive genomic ancestry rather than a range expansion from a single source, with important implications for vector-borne disease management.

evolutionary biology↗

Regional analysis of spatiotemporal trends in Colorado potato beetle abundance

Crop pests can significantly damage crops, cause economic loss, and reduce the sustainability of agroecosystems. New ecoinformatic approaches are needed to understand the drivers of pest population dynamics and improve pest management practices. Here we analyze spatiotemporal drivers of Colorado potato beetle (CPB, Leptinotarsa decemlineata) abundance across Wisconsin potato fields using multi-year scouting data (2014-2024) linked with climate and cropping histories. We develop statistical models that account for spatial and temporal correlations, and find these approaches substantially improve fit and prediction. After accounting for spatiotemporal random effects, we find that three predictors increased CPB abundance: cumulative growing degree days (GDD), recent potato intensity in the surrounding landscape, and winter coldest-day temperature. Cumulative GDD and potato intensity are positively associated with abundance, and warmer winter minima (higher coldest-day temperatures) are likewise associated with higher abundance, consistent with improved overwintering survival. Using the best-performing model, we generate a preliminary, statewide risk surface for Wisconsin in order to support regional decision-making. Our results highlight the value of integrating field-level history with landscape context and explicit spatial structure when forecasting pest pressures in agroecosystems.

ecology↗

Abiotic factors are the primary determinants of endemic Hawaiian Drosophila microbiome assembly

The Hawaiian Drosophila radiation exemplifies rapid adaptation and species diversification. Many factors have been attributed to these phenomena, including allopatry, sexual selection, and ecological specialization. In recent years, the microbiome has come to the forefront as an important driver of adaptation that is capable of facilitating host survivorship, enhancing resilience to local environmental challenges, and enabling the use of different dietary resources. To determine how microbial communities assemble in natural populations and potentially contribute to the rapid adaptation of Hawaiian drosophilids, we conducted a survey of bacterial and fungal communities from over 500 wild flies collected from across six islands of the Hawaiian archipelago. These samples represent a breadth of host plant specializations, habitats, lifestyles, and endemicity. Our findings reveal that microbiome assembly is largely driven by abiotic factors including elevation, temperature, rainfall, and evapotranspiration, but is not strongly constrained by phylogenetic relatedness. Identical species inhabiting two separate locations exhibited different microbiomes. By contrast, distantly related species inhabiting the same site had more similar microbiomes. The microbiomes of native species also differ from recently introduced, non-native Drosophila in terms of diversity, composition, and function. Given the myriad roles of the microbiome in nutrition, reproduction, and mate choice, these results support a role for the microbiome in the remarkable ecological divergence of Hawaiian Drosophila.

ecology↗

Shared features underlying compact genomes and extreme habitat use in chironomid midges

Non-biting midges (family Chironomidae) are found throughout the world in a diverse array of aquatic and terrestrial habitats, can often tolerate harsh conditions such as hypoxia or desiccation, and have consistently compact genomes. Yet we know little about the shared molecular basis for these attributes and how they have evolved across the family. Here, we address these questions by first creating high-quality, annotated reference assemblies for Tanytarsus gracilentus (subfamily Chironominae, tribe Tanytarsini) and Parochlus steinenii (subfamily Podonominae). Using these and other publicly available assemblies, we created a time-calibrated phylogenomic tree for family Chironomidae with outgroups from order Diptera. We used this phylogeny to test for features associated with compact genomes, as well as examining patterns of gene family evolution and positive selection that may underlie chironomid habitat tolerances. Our results suggest that compact genomes evolved in the most recent common ancestor of Chironomidae and Ceratopogonidae, and that this occurred mainly through reductions in non-coding regions (introns, intergenic sequences, and repeat elements). Gene families that significantly expanded in Chironomidae included biological processes that may relate to tolerance of stressful environments, such as temperature homeostasis, inflammatory response, melanization defense response, and trehalose transport. We identified a number of genes with evidence for positive selection in Chironomidae, notably sulfonylurea receptor, peroxiredoxin-1, and protein kinase D. Our results help to understand the genomic basis for the small genomes and extreme habitat use in this widely distributed group. Significance StatementChironomid midges are known for having small genomes and being able to tolerate many forms of environmental stress, yet little is known of the shared features of their genomes that may underlie these traits. We found that reductions in non-coding regions coincide with small chironomid genomes, and we identified duplicated and/or selected genes that may equip chironomids to tolerate harsh conditions. These results describe the key genomic changes in chironomid midges that may explain their ability to inhabit a range of extreme habitats across the world.

genomics↗

The genomic landscape of metallic color variation in ground beetles

The metallic color variation of beetles is a spectacular feature that has inspired diverse human cultures. However, little is known about the genetic basis of this trait or its ecological importance. In this study, we characterize the geographical distribution, optical mechanism, genetic basis, and ecological and evolutionary importance of metallic color variation in the Nebria ingens complex, an alpine ground beetle in the Sierra Nevada, California. We find that elytral color varies continuously across two allopatric species (from black N. ingens to green N. riversi), with hybrid populations showing intermediate coloration, and we demonstrate that the metallic color is generated from multilayer reflectors in the epicuticle of the elytra. By applying association mapping in natural populations (wild-GWAS) using high-density genotype variants, we identify five promising candidate genes covarying with metallic variation, with known roles in cuticle formation and pigmentation pathways. This finding, together with a significant correlation between color variation and water availability, suggests that metallic variation evolves as a local adaptation to environmental variation in the N. ingens complex.

evolutionary biology↗

Evidence for admixture and rapid evolution during glacial climate change in an alpine specialist

The pace of current climate change is expected to be problematic for alpine flora and fauna, as their adaptive capacity may be limited by small population size. Yet despite substantial genetic drift following post-glacial recolonization of alpine habitats, alpine species are notable for their success in surviving highly heterogeneous environments. Population genomic analyses demonstrating how alpine species have adapted to novel environments with limited genetic diversity remain rare, yet are important in understanding the potential for species to respond to contemporary climate change. In this study, we explored the evolutionary history of alpine ground beetles in the Nebria ingens complex, including the demographic and adaptive changes that followed the last glacier retreat. Using whole genome data from hundreds of beetles, to test alternative models of evolutionary divergence in the species complex, we found evidence that the Nebria ingens complex has been formed by past admixture of lineages responding to glacial cycles. Recolonization of alpine sites involved a distributional range shift to higher elevation, which was accompanied by a reduction in suitable habitat and the emergence of complex spatial genetic structure. We also used genome-wide association and genotype-environment association methods to look for genetic pathways involved in adaptation to heterogeneous new environments during this range shift. The identified genes were enriched for functions broadly associated with abiotic stress responses, with strong evidence for adaptation to hypoxia-related pathways. The results demonstrate that despite rapid environmental changes, alpine beetles in the N. ingens complex have shown rapid physiological evolution.

evolutionary biology↗

Genomic Diversity Illuminates the Species History and Environmental Adaptation of Drosophila suzukii

Biological invasions carry substantial practical and scientific importance, and represent natural evolutionary experiments on contemporary timescales. Here, we investigated genomic diversity and environmental adaptation of the crop pest Drosophila suzukii using whole-genome sequencing data and environmental metadata for 29 population samples from its native and invasive range. Through a multifaceted analysis of this population genomic data, we increase our understanding of the D. suzukii genome, its diversity and its evolution, and we identify an appropriate genotype-environment association pipeline for our data set. Using this approach, we detect genetic signals of local adaptation associated with nine distinct environmental factors related to altitude, wind speed, precipitation, temperature, and human land use. We uncover unique functional signatures for each environmental variable, such as a prevalence of cuticular genes associated with annual precipitation. We also infer biological commonalities in the adaptation to diverse selective pressures, particularly in terms of the apparent contribution of nervous system evolution to enriched processes (ranging from neuron development to circadian behavior) and to top genes associated with all nine environmental variables. Our findings therefore depict a finer-scale adaptive landscape underlying the rapid invasion success of this agronomically important species.

evolutionary biology↗

Evidence of hard-selective sweeps suggest independent adaptation to insecticides in Colorado potato beetle (Coleoptera: Chrysomelidae) populations

Pesticide resistance provides one of the best examples of rapid evolution to environmental change. The Colorado potato beetle 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 CPBs pest status among geographically distinct populations.

evolutionary biology↗

A complex interplay between balancing selection and introgression maintains a genus-wide alternative life-history strategy.

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.

evolutionary biology↗

Genome resequencing reveals rapid, repeated evolution in the Colorado potato beetle, Leptinotarsa decemlineata

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.

evolutionary biology↗

Experimental warming reduces gut prokaryotic diversity, survival and thermal tolerance of the eastern subterranean termite, Reticulitermes flavipes (Kollar)

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 {degrees}C), medium (27 {degrees}C), and high (35 {degrees}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 termites physiological response to environmental changes and highlight the need to consider microbial symbionts in studies relating to insect thermosensitivity.

microbiology↗

Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

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 decemlineata Say. Within the Leptinotarsa genus, only CPB has risen to pest status on cultivated Solanum. Using whole genomes from ten closely related Leptinotarsa species, 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, Leptinotarsa show 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.

evolutionary biology↗

Regional differences in gene regulation may underlie patterns of sensitivity to novel insecticides in Colorado potato beetle

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 LC50 bioassay data spanning 15 years and six insecticides (abamectin, imidacloprid, spinosad, cyantraniliprole, chlorantraniliprole, and metaflumizone) for evidence of regional differences in Colorado potato beetle (CPB) baseline sensitivity to insecticides as they became commercially available. We consistently found that CPB populations from the Western 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 populations 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.

evolutionary biology↗

A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. The L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.

genomics↗

Origin of pest lineages of the Colorado potato beetle, Leptinotarsa decemlineata

Colorado potato beetle (Leptinotarsa decemlineata Say) is a pest of potato throughout the Northern Hemisphere, but little is known about the beetles origins as a pest. To determine the origins of pest populations of CPB, we sampled the beetle from uncultivated Solanum host plants in Mexico, and from pest and non-pest populations in the U.S. We used mtDNA and nuclear loci to examine three hypotheses on the origin of the pest lineages: 1) the pest beetles originated from Mexican populations, 2) the pest beetles descended from hybridization between previously divergent populations, or 3) the pest beetles descended from populations that are native to the Plains states in the United States. We examined patterns of genetic diversity among geographic regions in order to detect invasion-related genetic information. Mitochondrial haplotypes of non-pest populations from Mexico and southern Arizona differed substantially from beetles collected from the southern plains and potato fields in the U. S., 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 southern plains of Colorado, Kansas, Nebraska, New Mexico, and Texas were genetically similar to U. S. pest populations, clearly indicating that they contributed to the founding of the pest lineages. Although some pest populations are less genetically diverse (e.g., Washington, Idaho), most of the pest populations do not show a significant reduction in genetic diversity compared to the plains populations in the U. S. In contrast to the colonization patterns typical of exotic pests, our analyses suggests that a large genetically heterogeneous beetle populations expanded onto potato from native Solanum hosts. As an endemic colonization of a novel host plant, this host range expansion may have contributed to the relatively abundant genetic diversity of contemporary populations, perhaps contributing to the rapid evolution of host range and insecticide resistance in this widely successful insect pest.

evolutionary biology↗