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

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.

The genomic basis of evolutionary differentiation among honey bees

“…Our results parallel previous analyses that indicate accelerated evolution during the diversification of species within a family (Nevado et al 2016;Tollis et al 2018;Vianna et al 2020), suggesting a common evolutionary pattern. We also find evidence for selection for sequence changes in existing protein-coding regions and evolutionary turnover of genes, similar to a genomic study of the radiation of closely related bumble bees (Sun et al 2021). These two sources of evolutionary change may be important in bee social evolution in addition to regulatory diversification (Kapheim et al 2015).…”

“…As a consequence, the genotype-phenotype map is being elucidated at ever-increasing detail (Zhou et al 2020). In addition to broad-scale macroevolutionary studies, taxon-specific comparative genomics is generating novel insights, particularly with respect to structural genome evolution (Figueiró et al 2017;Chavez et al 2019;Sun et al 2021).…”

“…Genomic signatures of this transition share few commonalities across taxa, except for an increase in gene regulatory capacity (Gadau et al 2012;Simola et al 2013;Terrapon et al 2014;Kapheim et al 2015;Harpur et al 2017;Harrison et al 2018). In contrast to the major focus on studying the genomic bases of the origin of sociality and associated traits, the maintenance and diversification of social traits has received limited attention (Simola et al 2013;Jasper et al 2015;Araujo and Arias 2021;Sun et al 2021).…”

A genomic and morphometric analysis of alpine bumblebees: ongoing reductions in tongue length but no clear genetic component

“…Assembly statistics for BBAL_1.0 ( B. balteatus ) and BSYL_1.0 ( B. sylvicola ) are presented in table 1, which includes statistics for the assemblies of B. terrestris (BTER_1.0) and B. impatiens (BIMP_2.2) for comparison. Total assembly sizes of 250.1 and 252.1 Mbp for B. balteatus and B. sylvicola respectively are both above the average assembly size of Bombus genomes assembled to date of 247.9 Mbp (22 genomes, range 229.8 – 282.1 Mbp) (Heraghty et al, 2020; Sadd et al, 2015; Sun et al, 2020). Contig N50s of 8.60 and 3.02 for BBAL_1.0 and BSYL_1.0 respectively are the longest and third longest contig N50s of all published Bombus assemblies, demonstrating these to be highly contiguous assemblies.…”

“…These are highly comparable to the 11,874 genes in the B. terrestris gene set (v. 1.0), but lower than the 12,728 genes in the B. impatiens gene set (v. 2.1). Gene annotation of the Bombus assemblies presented in (Heraghty et al, 2020; Sun et al, 2020) also resulted in a greater number of genes annotated, ranging from 13,325 to 16,970 genes. BUSCO analyses of the annotated genes in our assemblies do suggest that we are missing some genes from our annotations (complete BUSCO genes in BBAL_01 and BSYL_01 respectively: 86.6% and 86.9%).…”