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1. Population genomics of divergence among extreme and intermediate color forms in a polymorphic insect

   https://doi.org/10.1002/ece3.1928  

   Lozier, Jeffrey D.; Jackson, Jason M.; Dillon, Michael E.; Strange, James P. (January 2016, Ecology and Evolution)

   Abstract Geographic variation in insect coloration is among the most intriguing examples of rapid phenotypic evolution and provides opportunities to study mechanisms of phenotypic change and diversification in closely related lineages. The bumble beeBombus bifariuscomprises two geographically disparate color groups characterized by red‐banded and black‐banded abdominal pigmentation, but with a range of spatially and phenotypically intermediate populations across western North America. Microsatellite analyses have revealed thatB. bifariusin the USA are structured into two major groups concordant with geography and color pattern, but also suggest ongoing gene flow among regional populations. In this study, we better resolve the relationships among major color groups to better understand evolutionary mechanisms promoting and maintaining such polymorphism. We analyze >90,000 and >25,000 single‐nucleotide polymorphisms derived from transcriptome (RNAseq) and double digest restriction site associatedDNAsequencing (ddRAD), respectively, in representative samples from spatial and color pattern extremes inB. bifariusas well as phenotypic and geographic intermediates. Both ddRADandRNAseq data illustrate substantial genome‐wide differentiation of the red‐banded (eastern) color form from both black‐banded (western) and intermediate (central) phenotypes and negligible differentiation among the latter populations, with no obvious admixture among bees from the two major lineages. Results thus indicate much stronger background differentiation amongB. bifariuslineages than expected, highlighting potential challenges for revealing loci underlying color polymorphism from population genetic data alone. These findings will have significance for resolving taxonomic confusion in this species and in future efforts to investigate color‐pattern evolution inB. bifariusand other polymorphic bumble bee species. 

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2. De Novo Genome Assemblies for Three North American Bumble Bee species: Bombus bifarius , Bombus vancouverensis , and Bombus vosnesenskii

   https://doi.org/10.1534/g3.120.401437  

   Heraghty, Sam D.; Sutton, John M.; Pimsler, Meaghan L.; Fierst, Janna L.; Strange, James P.; Lozier, Jeffrey D. (August 2020, G3)

   Bumble bees are ecologically and economically important insect pollinators. Three abundant and widespread species in western North America, Bombus bifarius, Bombus vancouverensis, and Bombus vosnesenskii, have been the focus of substantial research relating to diverse aspects of bumble bee ecology and evolutionary biology. We present de novo genome assemblies for each of the three species using hybrid assembly of Illumina and Oxford Nanopore Technologies sequences. All three assemblies are of high quality with large N50s (> 2.2 Mb), BUSCO scores indicating > 98% complete genes, and annotations producing 13,325 - 13,687 genes, comparing favorably with other bee genomes. Analysis of synteny against the most complete bumble bee genome, Bombus terrestris, reveals a high degree of collinearity. These genomes should provide a valuable resource for addressing questions relating to functional genomics and evolutionary biology in these species. 

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3. Local adaptation across a complex bioclimatic landscape in two montane bumble bee species

   https://doi.org/10.1111/mec.15376  

   Jackson, Jason M.; Pimsler, Meaghan L.; Oyen, Kennan J.; Strange, James P.; Dillon, Michael E.; Lozier, Jeffrey D. (February 2020, Molecular Ecology)

   Abstract Understanding evolutionary responses to variation in temperature and precipitation across species ranges is of fundamental interest given ongoing climate change. The importance of temperature and precipitation for multiple aspects of bumble bee (Bombus) biology, combined with large geographic ranges that expose populations to diverse environmental pressures, make these insects well‐suited for studying local adaptation. Here, we analyzed genome‐wide sequence data from two widespread bumble bees,Bombus vosnesenskiiandBombus vancouverensis, using multiple environmental association analysis methods to investigate climate adaptation across latitude and altitude. The strongest signatures of selection were observed inB. vancouverensis, but despite unique responses between species for most loci, we detected several shared responses. Genes relating to neural and neuromuscular function and ion transport were especially evident with respect to temperature variables, while genes relating to cuticle formation, tracheal and respiratory system development, and homeostasis were associated with precipitation variables. Our data thus suggest that adaptive responses for tolerating abiotic variation are likely to be complex, but that several parallels among species can emerge even for these complex traits and landscapes. Results provide the framework for future work into mechanisms of thermal and desiccation tolerance in bumble bees and a set of genomic targets that might be monitored for future conservation efforts. 

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4. Divergence in Body Mass, Wing Loading, and Population Structure Reveals Species-Specific and Potentially Adaptive Trait Variation Across Elevations in Montane Bumble Bees

   https://doi.org/10.1093/isd/ixab012  

   Lozier, Jeffrey D; Parsons, Zachary M; Rachoki, Lois; Jackson, Jason M; Pimsler, Meaghan L; Oyen, Kennan J; Strange, James; Dillon, Michael E (September 2021, Insect Systematics and Diversity)

   Hines, Heather (Ed.)

   Abstract Biogeographic clines in morphology along environmental gradients can illuminate forces influencing trait evolution within and between species. Latitude has long been studied as a driver of morphological clines, with a focus on body size and temperature. However, counteracting environmental pressures may impose constraints on body size. In montane landscapes, declines in air density with elevation can negatively impact flight performance in volant species, which may contribute to selection for reduced body mass despite declining temperatures. We examine morphology in two bumble bee (Hymenoptera: Apidae: Bombus Latreille) species, Bombus vancouverensis Cresson and Bombus vosnesenskii Radoszkowski, across mountainous regions of California, Oregon, and Washington, United States. We incorporate population genomic data to investigate the relationship between genomic ancestry and morphological divergence. We find that B. vancouverensis, which tends to be more specialized for high elevations, exhibits stronger spatial-environmental variation, being smaller in the southern and higher elevation parts of its range and having reduced wing loading (mass relative to wing area) at high elevations. Bombus vosnesenskii, which is more of an elevational generalist, has substantial trait variation, but spatial-environmental correlations are weak. Population structure is stronger in the smaller B. vancouverensis, and we find a significant association between elevation and wing loading after accounting for genetic structure, suggesting the possibility of local adaptation for this flight performance trait. Our findings suggest that some conflicting results for body size trends may stem from distinct environmental pressures that impact different aspects of bumble bee ecology, and that different species show different morphological clines in the same region. 

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5. Examining the Effects of Environment, Geography, and Elevation on Patterns of DNA Methylation Across Populations of Two Widespread Bumble Bee Species

   https://doi.org/10.1093/gbe/evae207  

   Heraghty, Sam_D; Rahman, Sarthok_Rasique; Verble, Kelton_M; Lozier, Jeffrey_D; Eyre-Walker, ed., Adam (September 2024, Genome Biology and Evolution)

   Abstract Understanding the myriad avenues through which spatial and environmental factors shape evolution is a major focus in biological research. From a molecular perspective, much work has been focused on genomic sequence variation; however, recently there has been increased interest in how epigenetic variation may be shaped by different variables across the landscape. DNA methylation has been of particular interest given that it is dynamic and can alter gene expression, potentially offering a path for a rapid response to environmental change. We utilized whole genome enzymatic methyl sequencing to evaluate the distribution of CpG methylation across the genome and to analyze patterns of spatial and environmental association in the methylomes of two broadly distributed montane bumble bees (Bombus vancouverensis Cresson and Bombus vosnesenskii Radoszkowski) across elevational gradients in the western US. Methylation patterns in both species are similar at the genomic scale with ∼1% of CpGs being methylated and most methylation being found in exons. At the landscape scale, neither species exhibited strong spatial or population structuring in patterns of methylation, although some weak relationships between methylation and distance or environmental variables were detected. Differential methylation analysis suggests a stronger environment association in B. vancouverensis given the larger number of differentially methylated CpG's compared to B. vosnesenskii. We also observed only a handful of genes with both differentially methylated CpGs and previously detected environmentally associated outlier SNPs. Overall results reveal a weak but present pattern in variation in methylation over the landscape in both species. 

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