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 Gao, Ling Ma, Lina Ma, Zhang 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 W Hahn, Sarah Schaack, Seth M Barribeau, Paul H Williams, Robert M Waterhouse, Rachel Lockridge Mueller
Author Information
- Cheng Sun: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Jiaxing Huang: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Yun Wang: School of Life Sciences, Chongqing University, Chongqing, China.
- Xiaomeng Zhao: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Long Su: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Gregg W C Thomas: Division of Biological Sciences, University of Montana, Missoula, MT.
- Mengya Zhao: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China.
- Xingtan Zhang: Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, China.
- Irwin Jungreis: MIT Computer Science and Artificial Intelligence Laboratory, Cambridge, MA.
- Manolis Kellis: MIT Computer Science and Artificial Intelligence Laboratory, Cambridge, MA.
- Saverio Vicario: Institute of Atmospheric Pollution Research-Italian National Research Council C/O Department of Physics, University of Bari, Bari, Italy.
- Igor V Sharakhov: Department of Entomology, Virginia Polytechnic and State University, Blacksburg, VA.
- Semen M Bondarenko: Department of Entomology, Virginia Polytechnic and State University, Blacksburg, VA.
- Martin Hasselmann: Department of Livestock Population Genomics, Institute of Animal Science, University of Hohenheim, Stuttgart, Germany.
- Chang N Kim: UC Santa Cruz Genomics Institute, University of California Santa Cruz, Santa Cruz, CA.
- Benedict Paten: UC Santa Cruz Genomics Institute, University of California Santa Cruz, Santa Cruz, CA.
- Luca Penso-Dolfin: Deutsches Krebsforschungszentrum, Heidelberg, Germany.
- Li Wang: Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China.
- Yuxiao Chang: Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China.
- Qiang Gao: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
- Ling Ma: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
- Lina Ma: China National Center for Bioinformation & Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
- Zhang Zhang: China National Center for Bioinformation & Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
- Hongbo Zhang: School of Life Sciences, Chongqing University, Chongqing, China.
- Huahao Zhang: College of Pharmacy and Life Science, Jiujiang University, Jiujiang, China.
- Livio Ruzzante: Department of Ecology and Evolution, University of Lausanne, and Swiss Institute of Bioinformatics, Lausanne, Switzerland.
- Hugh M Robertson: Department of Entomology, University of Illinois at Urbana-Champaign, Champaign, IL.
- Yihui Zhu: Department of Medical Microbiology and Immunology, Genome Center, and MIND Institute, University of California Davis, Davis, CA.
- Yanjie Liu: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Huipeng Yang: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Lele Ding: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Quangui Wang: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Dongna Ma: Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, China.
- Weilin Xu: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
- Cheng Liang: Institute of Sericultural and Apiculture, Yunnan Academy of Agricultural Sciences, Mengzi, China.
- Michael W Itgen: Department of Biology, Colorado State University, Fort Collins, CO.
- Lauren Mee: Department of Ecology, Evolution and Behaviour, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.
- Gang Cao: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China.
- Ze Zhang: School of Life Sciences, Chongqing University, Chongqing, China.
- Ben M Sadd: School of Biological Sciences, Illinois State University, Normal, IL.
- Matthew W Hahn: Department of Biology, Indiana University, Bloomington, IN.
- Sarah Schaack: Department of Biology, Reed College, Portland, OR.
- Seth M Barribeau: Department of Ecology, Evolution and Behaviour, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.
- Paul H Williams: Department of Life Sciences, Natural History Museum, London, United Kingdom.
- Robert M Waterhouse: Department of Ecology and Evolution, University of Lausanne, and Swiss Institute of Bioinformatics, Lausanne, Switzerland.
- Rachel Lockridge Mueller: Department of Biology, Colorado State University, Fort Collins, CO.
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, whereas 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.
Adaptation, Biological
Animals
Bees
Biological Evolution
Codon Usage
DNA Transposable Elements
Diet
Feeding Behavior
Gene Components
Genome Size
Genome, Insect
Selection, Genetic
DNA Transposable Elements
