Complex population structure and haplotype patterns in the Western European honey bee from sequencing a large panel of haploid drones

Abstract

Honey bee subspecies originate from specific geographical areas in Africa, Europe and the Middle East, and beekeepers interested in specific phenotypes have imported genetic material to regions outside of the bees' original range for use either in pure lines or controlled crosses. Moreover, imported drones are present in the environment and mate naturally with queens from the local subspecies. The resulting admixture complicates population genetics analyses, and population stratification can be a major problem for association studies. To better understand Western European honey bee populations, we produced a whole genome sequence and single nucleotide polymorphism (SNP) genotype data set from 870 haploid drones and demonstrate its utility for the identification of nine genetic backgrounds and various degrees of admixture in a subset of 629 samples. Five backgrounds identified correspond to subspecies, two to isolated populations on islands and two to managed populations. We also highlight several large haplotype blocks, some of which coincide with the position of centromeres. The largest is 3.6 Mb long and represents 21% of chromosome 11, with two major haplotypes corresponding to the two dominant genetic backgrounds identified. This large naturally phased data set is available as a single vcf file that can now serve as a reference for subsequent populations genomics studies in the honey bee, such as (i) selecting individuals of verified homogeneous genetic backgrounds as references, (ii) imputing genotypes from a lower‐density data set generated by an SNP‐chip or by low‐pass sequencing, or (iii) selecting SNPs compatible with the requirements of genotyping chips.

Reconstructing queen genotypes by pool sequencing colonies in eusocial insects: Statistical Methods and their application to honeybee

“…The second model exploits information available across multiple colonies to reconstruct the queen genotypes. Performances of the models are evaluated through simulations, including some based on real data from an Apis mellifera diversity panel (Wragg et al, 2022). Using these simulations, we show that the genetic ancestry of a queen estimated from pool sequencing data matches results from standard population genetics methods based on queen genotypes data.…”

“…In our applications below, the reference populations considered are Apis mellifera mellifera, Apis mellifera ligustica & carnica and Apis mellifera causasia, the three main genetically distinct populations found in Western Europe (Wragg et al, 2022). We will do that in a supervised manner and therefore, we will assume that we are provided with allele frequencies in a set of K reference populations at the L loci: this takes the form of an L × K matrix F where F lk is the frequency of the reference allele at locus l in population k. Here we are interested in inferring q, the Kvector of admixture proportions for the queen: q k is the proportion of alleles over all loci that come from population k.…”

“…We assume these data come in the form of the reference allele counts x c l and sequencing depths d c l at each locus l , knowing the queen genotypes g c l and allele frequencies in the inseminating drones f c l . To further condition our simulations on what can be expected from real data, we exploited information available in a reference population of Apis mellifera (Wragg et al, 2022). These data consist of 628 European samples of haploid drones (Table S2) with genotypes available at 6,914,704 single nucleotide polymorphisms (SNPs).…”

“…These data consist of 628 European samples of haploid drones (Table S2) with genotypes available at 6,914,704 single nucleotide polymorphisms (SNPs). Wragg et al (2022) showed that this panel is structured into three main genetic backgrounds for which unadmixed (reference) individuals can be identified, with a threshold of 99% of their genetic background being from a unique type: the M background (Apis mellifera mellifera) with 85 reference individuals, the L background (Apis mellifera ligustica & carnica) with 44 reference individuals and the C background (Apis mellifera caucasia) with 16 reference individuals (Table S3). In the simulations described below, the reference panel information used was either the allele frequencies in the three main backgrounds (F = F lk ∈ 0, 1…”

“…Pool sequencing experiments provide information on a large number of markers distributed throughout the genome. To evaluate the performance of the models in realistic conditions for the distribution of allele frequencies and the genetic structure, a second set of simulations was performed using individual genotypes of 628 individuals from the diversity panel previously described in Wragg et al (2022) and used beforehand to define reference genetic backgrounds. First, individuals were clustered into seven groups, of all potential combinations of admixture between the three genetic backgrounds, using hard thresholds on their initial vectors of genetic ancestries estimated with ADMIXTURE (Alexander et al, 2009) (Figure S3).…”