Genus-wide characterization of bumblebee genomes provides insights into their evolution and variation in ecological and behavioral traits

Cheng Sun, Jiaxing Huang, Yun Wang, Xiaomeng Zhao, Long Su, Gregg W C Thomas, Mengya Zhao, Xingtan Zhang, Irwin Jungreis, Manolis Kellis, Saverio Vicario, Igor V Sharakhov, Semen M Bondarenko, Martin Hasselmann, Chang N Kim, Benedict Paten, Luca Penso-Dolfin, Li Wang, Yuxiao Chang, Qiang GaoLing Ma, Lina Ma, Yuxiao Zhang, Hongbo Zhang, Huahao Zhang, Livio Ruzzante, Hugh M Robertson, Yihui Zhu, Yanjie Liu, Huipeng Yang, Lele Ding, Quangui Wang, Dongna Ma, Weilin Xu, Cheng Liang, Michael W Itgen, Lauren Mee, Gang Cao, Ze Zhang, Ben M Sadd, Matthew Hahn, Sarah Schaack, Seth M Barribeau, Paul H Williams, Robert M Waterhouse, Rachel Lockridge Mueller

Research output: Contribution to journalArticlepeer-review

Abstract

Bumblebees are a diverse group of globally important pollinators in natural ecosystems and for agricultural food production. With both eusocial and solitary life-cycle phases, and some social parasite species, they are especially interesting models to understand social evolution, behavior, and ecology. Reports of many species in decline point to pathogen transmission, habitat loss, pesticide usage, and global climate change, as interconnected causes. These threats to bumblebee diversity make our reliance on a handful of well-studied species for agricultural pollination particularly precarious. To broadly sample bumblebee genomic and phenotypic diversity, we de novo sequenced and assembled the genomes of 17 species, representing all 15 subgenera, producing the first genus-wide quantification of genetic and genomic variation potentially underlying key ecological and behavioral traits. The species phylogeny resolves subgenera relationships while incomplete lineage sorting likely drives high levels of gene tree discordance. Five chromosome-level assemblies show a stable 18-chromosome karyotype, with major rearrangements creating 25 chromosomes in social parasites. Differential transposable element activity drives changes in genome sizes, with putative domestications of repetitive sequences influencing gene coding and regulatory potential. Dynamically evolving gene families and signatures of positive selection point to genus-wide variation in processes linked to foraging, diet and metabolism, immunity and detoxification, as well as adaptations for life at high altitudes. Our study reveals how bumblebee genes and genomes have evolved across the Bombus phylogeny and identifies variations potentially linked to key ecological and behavioral traits of these important pollinators.

Original languageEnglish (US)
Article numbermsaa240
JournalMolecular biology and evolution
DOIs
StateAccepted/In press - Sep 18 2020

Keywords

  • Bombus
  • gene family evolution
  • genome evolution
  • genome assembly
  • insect diversity

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