Genomic Signatures of Recent Adaptation in a Wild Bumblebee

Abstract

Environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects respond to environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of Bombus terrestris bumblebees collected across Great Britain. We reveal extensive genetic diversity within this population, and strong signatures of recent adaptation throughout the genome affecting key processes including neurobiology and wing development. We also discover unusual features of the genome, including a region containing 53 genes that lacks genetic diversity in many bee species, and a horizontal gene transfer from a Wolbachia bacteria. Overall, the genetic diversity we observe and how it is distributed throughout the genome and the population should support the resilience of this important pollinator species to ongoing and future selective pressures. Applying our approach to more species should help understand how they can differ in their adaptive potential, and to develop conservation strategies for those most at risk.

Keywords: bees; ecological genomics; genetic health; horizontal gene transfer; population genomics; selective sweeps.

Fig. 1

Environmental pressures affecting insect pollinators and population structure of wild-caught British B. terrestris. (A) Overview of key environmental selective pressures on wild bumblebee populations, and some of the biological pathways and processes expected to be under selection in response. (B) Twenty-eight collection sites across Great Britain, colored according to latitude. (C) Population structure of 46 males according to the first two principal components (PC1 and PC2). Each point refers to one male, with up to two males (A and B) per site, colored according to collection site latitude.

Fig. 2

Genome-wide signatures of selective sweeps in British B. terrestris bumblebees. (A) |nS_L| measures of selection for all SNPs in the bumblebee genome. Each dot represents one SNP; labeled dots represent the SNP with highest |nS_L| score for genes of interest, including transcription factors, insecticide susceptibility genes, and a Wolbachia-like gene, with high |nS_L| scores. Labels indicate Flybase gene symbols when clear Drosophila orthology exists, otherwise, the NCBI gene symbol is provided. Blue and purple horizontal dashed lines, respectively, indicate the 1st percentile of overall |nS_L| scores and 10th percentile of genic |nS_L| scores. (B) Distributions of |nS_L| scores show that most SNPs are in genic regions, and that most |nS_L| scores are consistent with neutral or purifying rather than directional evolution as 96% of SNPs have |nS_L| < 2. (C) Diverse Gene Ontology terms are enriched in genes with high |nS_L| scores (−log10 transformed Bonferroni-adjusted P values). Terms associated with roles in neurology and transcription factor activity are, respectively, highlighted in bold and bold italics. The total number of annotated genes for each term is in parentheses.

Fig. 3

Conserved gene-rich region of low nucleotide diversity in bumblebee and honeybee. (A) Number of SNPs identified in 100 kb sliding windows across the bumblebee genome. The two windows with the lowest number of SNPs (in blue) are adjacent to each other on chromosome one. (B) Relative genomic positions of homologous regions of low diversity on chromosomes one of Bombus terrestris and Apis mellifera. (C) Genomic coordinates of 53 genes present in (beige) and flanking (gray) the region of low diversity. (D) Nucleotide diversity (π, calculated in 10 kb sliding windows) is low in this region in comparison with flanking regions and to the genome-wide mean (dashed line). (E) Genotypes for each of 46 B. terrestris males (rows) at each SNP (columns; chromosomal coordinate shown in the x-axis). Colors indicate reference allele (beige) or alternative allele (brown). (F–I) In the honeybee Apis mellifera, homology with the region of low diversity in B. terrestris is split between two regions. For both regions, we show genomic positions of genes (F, H). In four populations, both regions have lower nucleotide diversity (π, calculated in 10 kb sliding windows) than flanking regions or the rest of the genome (dashed line; G, I).