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Abstract Bumble bees (Bombus) exhibit exceptional diversity in setal body color patterns, largely as a result of convergence onto multiple Mullerian mimicry patterns globally. When multiple species cross the same sets of mimicry complexes, they can acquire the same color polymorphisms, providing replicates of phenotypic evolution. This study examines the genetic basis of parallel color pattern acquisition in three bumble bee taxon pairs in western North America that shift between orange-red and black mid-abdominal segmental coloration in Rocky Mountain and Pacific Coastal mimicry regions: polymorphic Bombus vancouverensis and B. melanopygus, and sister species B. huntii and B. vosnesenskii. Initial gene targets are identified using a genome-wide association study, while cross-developmental transcriptomics reveals genetic pathways leading to final pigmentation genes. The data show all three lineages independently target the regulatory region of a segmental-fate determining Hox gene, Abdominal B (Abd-B), for this color transition. For B. vancouverensis and B. melanopygus, this involves different deletions in the same location, and all mimicry pairs differentially express Abd-B and ncRNAs in this locus. Transcriptomics reveals a shared core gene network across species, where Abd-B interacts with nubbin and pigment enzyme ebony to decrease black melanin production in favor of paler, redder morphs. Expression of multiple genes in the melanin biosynthesis pathway is modified to promote this phenotype, with differing roles by taxon. Replicated morphologies unveil key genes and a Hox gene hotspot, while enabling evolutionary tracking of genetic changes to phenotypic changes and informing how gene regulatory networks evolve. 

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.