Genus-Wide Characterization of Bumblebee Genomes Provides Insights into Their Evolution and Variation in Ecological and Behavioral Traits

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

doi:10.1093/molbev/msaa240

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, 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.

Highlights

Bumblebees (Hymenoptera: Apidae) are a group of pollinating insects comprising the genus Bombus, which are economically important for crop pollination (Velthuis and Van Doorn 2006; Garibaldi et al 2013; Martin et al 2019)
Complementary analysis with ASTRAL based on maximum likelihood gene trees (Zhang et al 2018) resulted in an identical species tree with the exception of the placement of B. pyrosoma, which no longer forms a monophyletic pairing with B. breviceps, but rather forms an asymmetrical four-taxa clade with B. breviceps, B. sibricus, and B. cullumanus (Supplementary figures Figure S5)
For each node in the IQ-TREE species tree, gene concordance factors reflect the percentage of gene trees that contain that node as defined by its descendant taxa, and site concordance factors reflect the percentage of informative sites that support that node via parsimony

Summary

Introduction

Bumblebees (Hymenoptera: Apidae) are a group of pollinating insects comprising the genus Bombus, which are economically important for crop pollination (Velthuis and Van Doorn 2006; Garibaldi et al 2013; Martin et al 2019). Bumblebees are ecologically important pollinators, serving as the sole or predominant pollinators of many wild plants (Fontaine et al 2005; Goulson et al 2008) They are charismatic social insects that exhibit complex behaviors such as learning through observation (Alem et al 2016) and damaging leaves to stimulate earlier flowering (Pashalidou et al 2020). To broadly sample the genomic and phenotypic diversity of bumblebees, we selected representative species from China for whole genome sequencing based on their phylogeny, ecology, behavior, geography, and specimen availability. We performed de novo sequencing and assembly of the genomes of 17 bumblebee species, representing all 15 subgenera within the genus Bombus. Our results characterize patterns of molecular and genomic evolution across the Bombus phylogeny and provide the first genus-wide quantification of genetic and genomic variation potentially underlying key ecoethological traits

Methods

Results

Discussion

Conclusion