Genus-wide characterization of bumblebee genomes reveals variation associated with key ecological and behavioral traits of pollinators

Abstract

66Bumblebees are a diverse group of globally important pollinators in natural 67 ecosystems and for agricultural food production. With both eusocial and solitary life-68 cycle phases, and some social parasite species, they are especially interesting models 69to understand social evolution, behavior, and ecology. Reports of many species in 70 decline point to pathogen transmission, habitat loss, pesticide usage, and global 71 climate change, as interconnected causes. These threats to bumblebee diversity make 72 our reliance on a handful of well-studied species for agricultural pollination 73 particularly precarious. To broadly sample bumblebee genomic and phenotypic 74 diversity, we de novo sequenced and assembled the genomes of 17 species, 75representing all 15 subgenera, producing the first genus-wide quantification of genetic 76and genomic variation potentially underlying key ecological and behavioral traits. The 77 species phylogeny resolves subgenera relationships while incomplete lineage sorting 78 likely drives high levels of gene tree discordance. Five chromosome-level assemblies 79show a stable 18-chromosome karyotype, with major rearrangements creating 25 80 chromosomes in social parasites. Differential transposable element activity drives 81 changes in genome sizes, with putative domestications of repetitive sequences 82influencing gene coding and regulatory potential. Dynamically evolving gene families 83and signatures of positive selection point to genus-wide variation in processes linked 84to foraging, diet and metabolism, immunity and detoxification, as well as adaptations 85for life at high altitudes. These high-quality genomic resources capture natural genetic 86and phenotypic variation across bumblebees, offering new opportunities to advance 87 our understanding of their remarkable ecological success and to identify and manage 88 current and future threats. 89 90 91 92