A soft selective sweep during rapid evolution of gentle behaviour in an Africanized honeybee

Abstract

Highly aggressive Africanized honeybees (AHB) invaded Puerto Rico (PR) in 1994, displacing gentle European honeybees (EHB) in many locations. Gentle AHB (gAHB), unknown anywhere else in the world, subsequently evolved on the island within a few generations. Here we sequence whole genomes from gAHB and EHB populations, as well as a North American AHB population, a likely source of the founder AHB on PR. We show that gAHB retains high levels of genetic diversity after evolution of gentle behaviour, despite selection on standing variation. We observe multiple genomic loci with significant signatures of selection. Rapid evolution during colonization of novel habitats can generate major changes to characteristics such as morphological or colouration traits, usually controlled by one or more major genetic loci. Here we describe a soft selective sweep, acting at multiple loci across the genome, that occurred during, and may have mediated, the rapid evolution of a behavioural trait.

Fig. 1

Honeybee genome SNPs showing signatures of selection in gAHB. In the central scatter plot, candidate genomic regions associated with the evolution of reduced aggression in gAHB are identified by the distributions of composite selection scores for Rsb (cyan + black points) and F _ST (violet + black points) at SNPs from genome sequencing of AHB, gAHB and European honeybees (EHB). Axes and cut-off points identify the 0 and 99th percentiles of data distribution; points beyond the 99th percentile were designated as extreme values of interest. The bar along each axis is a reduced box plot with the line extending from the minima to the maxima of the distributions. The gap in the line corresponds to the range from the 25th to the 75th percentile, with the crossbar indicating the median and the point indicating the mean of the distribution. ‘gAHB selection alleles’ (black points) were defined as the intersection of significant alleles from both the composite selection scores, indicating both an EHB-like allelic profile and significant positive selection unique to gAHB. The radial plot illustrates the distribution of composite selection scores for both metrics across the honeybee genome. Colors identify outliers in the composite score distribution for F _ST (violet + black) and Rsb (cyan + black) with ‘gAHB selection alleles’ (black) representing the intersection shown in the center plot. The y-axis extends from the minimum (0) to the maximum composite score value for each metric while the x-axis provides the genetic position in Morgans. Roman numerals identify linkage groups in the honeybee genome. Many significant peaks are apparent across the genome; the dashed boxes and italicized numerals highlight three candidate regions whose component genes are further explored in Fig. 2

Fig. 2

Haplotype relationships within three loci under selection in gAHB. We examined haplotype blocks that overlap with exonic regions of three representative genes: GB40504, GB42728, and GB50509. Models are provided for each gene with a black line representing the genomic span, gray segments denoting exons, and an arrowhead identifying 3′ direction. Italicized Roman numerals beside each gene label correspond to regions identified in Fig. 1. Open boxes highlight candidate haplotype blocks within the genes. a Median joining network analysis was used to reconstruct the relationships of haplotypes within each haplotype blocks. Circle size is scaled to abundance of each haplotype across the populations, and colors demonstrate the proportion of the given haplotype originating from each population (AHB, EHB, and gAHB). Black dots represent median vertices in the network cross lines represent number of changes between networks. b Visualization of the spectrum of haplotypes corresponding to each of the illustrated networks. Each haplotype block is represented by a trio of bar plots for which the y-axis corresponds to the frequency of constituent haplotypes across gAHB, AHB, and EHB populations (x-axis). Constituent haplotypes in each block have unique colors and colors shared across populations indicate the presence of the same haplotype

Fig. 3

Population structure and patterns of admixture across EHB, AHB, and gAHB. a A diagrammatic superimposition of an un-rooted Neighbor Joining (NJ) cladogram of the samples with population geography. The NJ tree was constructed from 2,808,570 SNPs derived from whole-genome sequencing. Taxa represent the 90 samples assessed in this study, with fill color corresponding to population membership. b Principal component analysis (PCA) showing population structure of 230 samples with 1,049,512 SNPs common between the 90 samples in a and 140 previously-described samples of wild and domesticated honeybees from Europe, Africa, and North and South America. Ellipses in the PCA enclose the 95th percentile of actual population membership with ellipse color corresponding to population as above. The gAHB, AHB, and EHB group labels are the populations sampled in this study. Remaining labels are aggregates of samples from the previous study grouped as follows: wAHB is a Brazilian AHB population; wEHB are domestic EHB population samples from both Minnesota, USA, and Sweden; groups A, O, M, and C are genetic groupings spanning multiple, distinct subspecies of A. mellifera as identified in prior reference studies^,