- commercial honey bee stocks. - honey bee stocks remain poorly characterized despite the agricultural importance of Apis mellifera as the major crop pollinator. - The variety of bees produced by artificial selection provides an opportunity to characterize the genetic diversity and regions of the genome undergoing selection in commonly managed stocks.. - Results: Pooled sequencing of eight honey bee stocks found strong genetic similarity among six of the stocks. - Conclusion: This study provides important insights into the distinct genetic characteristics and population diversity of honey bee stocks used in the United States, and provides further evidence of high levels of admixture in commercially managed honey bee stocks. - Managing genetic diversity is critical for the success and sustainability of breeding programs of domesticated organ- isms. - Retaining enough genetic diversity while simultan- eously applying selection for desirable traits is a balance. - Honey bees (Apis mellifera) are the predomin- ant managed insect pollinator for a majority of food crop species and depend on high genetic diversity within col- onies and between populations. - 1 USDA-ARS, Honey Bee Breeding, Genetics and Physiology Laboratory, Baton Rouge, LA 70820, USA. - Full list of author information is available at the end of the article. - There are currently a number of honey bee stocks (sup- posedly isolated populations bred for desirable traits) pro- duced by queen breeders for widespread use across the United States. - While these do not all represent genetically distinct lines, the varied sources contribute to genetic diversity among stocks. - The variance in breeding and population structure among managed honey bee colonies has, as of yet, lacked a comprehensive high resolution understand- ing of the genetic diversity and structure in managed U.S.. - honey bee populations. - A population genetic approach to the analysis of honey bee genetic variation could prove useful by identifying regions that have undergone selec- tion through breeding efforts which can be used as a basis for novel breeding programs. - Previous work has provided genomic information about aggressive behavior, swarm- ing, and Africanization in various honey bee populations globally [22–25]. - A more comprehensive understanding of the genetic differ- entiation among commercially relevant stocks, however, is an important first step toward efforts to begin implement- ing genomic-based marker-assisted selection to rapidly and efficiently improve honey bee breeding programs.. - We investigated the current patterns of genetic diversity of eight U.S. - honey bee stocks using whole genome se- quencing of pooled individuals (Pool-seq) to determine genome-wide allele frequencies. - We characterize the genetic diversity found within and be- tween these stocks and identify single nucleotide polymor- phisms (SNPs) that may be useful in stock identification.. - The overall aim was to provide an initial genetic screen to strengthen future efforts toward incorporating the use of marker-assisted selection in honey bee breed- ing, especially for traits that are challenging to phenotype.. - honey bee stocks collected in 2016 and one collected in 2019 (Hilo). - Four of the stocks are widely used in the beekeeping industry including three Italian (designated as Italian1, Italian2 and Italian3) and one Carniolan, representing some of the major bee breeding programs in North America. - Pol-line honey bees were de- rived from Italian bees with high Varroa resistance largely derived from the expression of the ‘Varroa-sensi- tive hygiene’ (VSH) trait [38]. - their combined profile is representative of the broader genetic diversity of managed Italian bees across the U.S.. - The first principal component (PC1) accounted for 5.1% of the variation in allele frequency data, while PC2 and PC3 accounted for 3.9 and 2.6%. - of the variation, respectively. - Broadly, PC1 appeared to differentiate among the Carniolan-Italian spectrum of genetic diversity while PC2 primarily differentiated Pol-line and Hilo stocks (Fig. - To establish unique stock-specific SNPs among all of the stocks examined as possible candidates for stock identification, we analyzed SNPs with the top 1.0 and 0.1% F ST values and extracted only the unique SNPs.. - A full list of the stock-specific SNPs in the top 0.1% can be found in Supplemental Table 3.. - A full list of the top 0.1% CSS SNPs can be found in the Supplemental Table 4 and the distribution of CSS scores can be found in Supplemental Figure 1. - honey bee stocks. - We show that within-stock genetic diversity is limited. - measured among the eight honey bee stocks. - Genetic diversity metrics: within stocks. - We found relatively similar, low levels of within- population genetic diversity measured by π and θ across the genome for the eight stocks. - It should be noted that a few factors may potentially be influencing our findings such as the matrilineal bias influenced by honey bee mul- tiple mating, our pooling approach, and potential non- random sampling of individuals by bee breeders. - However, the differences in within-stock variation examined among stocks provides an informative, relative measure of genetic diversity. - This suggests that within sample relationships may not be con- tributing significantly to the reduced genetic diversity.. - Admixture appears to cause commercially managed honey bees to have greater genetic diversity than their pro- genitor populations [45]. - Although our genome-wide estimates of π and θ show low genetic diversity within stocks, analysis of the csd locus pro- vided greater resolution of recent population changes.. - This suggests a disconnect between genomic level nucleotide diversity and that of the csd locus, which is possible in honey bees given their high rate of re- combination and low levels of linkage-disequilibrium [46].. - Further exploration of this will be informative for adequate determination and mitigation of inbreeding depression in honey bee breeding operations.. - This provides further evidence of the genetic differentiation of Hilo and Pol-line from other stocks. - This may indicate a greater contribution of the Pol-line ancestry to Hilo, with F ST estimates suggesting that Hilo is more differentiated from the combined Italian. - Csd exons are depicted across the base of the figure. - This may also explain the distribution of the Russian and Minnesota Hygienic stocks across two genetic clusters determined through the KNN analysis as a result of shared selection pressure among operations.. - 2 Principal component analysis of allele frequencies by principal components (PC) and k-nearest neighbor (KNN) analysis of the eight sequenced honey bee stocks demonstrating the distribution of genetic relatedness. - This supports the case that introgres- sion from external Italian honey bee populations exists ei- ther from their population of origin (e.g. - [50]) or after their introduction in the U.S. - For example, while Russian honey bee stock is produced as part of a closed network of breeders [44], queens are produced via natural mating. - honey bee populations.. - Our annotation using haplotype blocks identified 46 of the that were shared among the four stocks with a strong signal of selection Table 2 Stock specific measures of genetic diversity within honey bees. - However, there remains an unlikely possibility that a CSS signal may arise of a specific region that is highly selected in only the Italian stocks and not of the other populations. - Further investigations to de- termine the functional mechanisms regulating social im- munity will aid in the development of molecular tools to apply for more full integration of resistance traits among honey bee breeding programs and populations. - This study categorizes the underlying genetic variation that exists in common honey bee stocks through the use of gen- omics and population genetic approaches. - The findings suggest the need for future efforts to integrate additional forms of data including gene expression, epigenetic, and regulatory information to provide a more complete under- standing of the mechanisms regulating stock phenotypic di- versity. - Validation of QTLs for complex traits associated with disease and parasite resistance among honey bee pop- ulations has been extremely difficult to achieve [42]. - Through the incorporation of the results presented here and future efforts into data repository resources such as Hymenopteramine [56], beekeepers and honey bee re- searchers can begin to work towards the development of marker-assisted selection to “build a better bee.”. - Pool-seq was used to widely sample each population and identify conserved patterns of genetic variation within each of the 8 sampled stocks. - Given that Hilo, Pol-line, and Russian stocks are either maintained by the USDA-ARS Baton Rouge research unit or close collaborators, they were care- fully sampled to ensure independent sampling within each of the populations so as to minimize relatedness between colonies. - Colonies from the Russian stock were selected from 12 of the 18 breeding lines, Pol-line colonies repre- sented 12 different lines and Hilo represents 10 different lines. - Raw sequence files were trimmed using Trim Galore v0.6.0 and then aligned to the honey bee reference genome (Amel_HAv3.1) using bwa v0.7.16a to generate bam files [58]. - For the within and between pairwise comparisons of the stocks, the software packages Popoolation was used to estimate π and θ [68] and Popoolation2 was used to estimate F ST. - We also used a max- coverage threshold of no more than 2% of the total num- ber of reads. - These filters frame assured the consideration of the most conservative and consistent SNPs among our data set. - Stock specific SNPs were identified using the top 1.0 and 0.1% F ST values from each of the pairwise compari- sons of stocks. - Briefly, a fractional rank of the F ST calculations for Minnesota Hygienic-Italian, Pol- line-Italian, Hilo-Italian, and Russian-Italian compari- sons were calculated and used to derive a Z-score. - CSS outliers were identified as having a CSS score in the top 0.1% of the distribution. - To assist in functional annotation, we capitalized on the small span of linkage-disequilibrium across the honey bee genome.. - We thank five commercial queen breeders for contributing stocks used in this study, and BartJan Fernhout, David Thomas, and Danielle Downey of the Hilo Bee breeding project for their support. - We acknowledge Matt Tarver and Beth Holloway for the initial conceptualization of the study.. - Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. - Honey bee Nest thermoregulation: diversity promotes stability. - Genetic diversity promotes homeostasis in insect colonies. - Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. - Genetic diversity in honey bee colonies enhance productivity and fitness. - Genetic diversity affects colony survivorship in commercial honey bee colonies. - A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. - Honey bee genetic diversity and breeding - towards the reintroduction of European germplasm. - Genetic characterization of commercial honey bee (Hymenoptera: Apidae) populations in the United States by using mitochondrial and microsatellite markers. - Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. - et al. - Grooming behavior and gene expression of the Indiana “ mite-biter ” honey bee stock. - Genomics and host specialization of honey bee and bumble bee gut symbionts. - Varroidae) populations in Russian honey bee (Hymenoptera: Apidae) colonies. - Genetic characterization of Russian honey bee stock selected for improved resistance to Varroa destructor. - The complex demographic history and evolutionary origin of the Western honey bee, Apis Mellifera. - A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera. - Comparative study of enzyme polymorphism in United States and European honey bee (Hymenoptera: Apidae) populations. - Performance of hygienic honey bee colonies in a commercial apiary. - Honey bee hygienic behavior and defense against Varroa jacobsoni. - Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. - Correlation of proteome-wide changes with social immunity behaviors provides insight into resistance to the parasitic mite, Varroa destructor, in the honey bee (Apis mellifera). - Integrative genomics reveals the genetics and evolution of the honey bee's social immune system.. - Phenotypic and genetic analyses of the Varroa sensitive hygienic trait in Russian honey bee (Hymenoptera: Apidae) colonies. - Management increases genetic diversity of honey bees via admixture. - Exceptionally high levels of recombination across the honey bee genome. - Sex determination in the Hymenoptera. - Tracking the genetic stability of a honey bee (Hymenoptera: Apidae) breeding program with genetic markers
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