ArticleLiterature Review

Recent advances in population and quantitative genomics of honey bees

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

The increase in the availability of individual Apis mellifera genomes has resulted in significant progress toward understanding the evolution and adaptation of the honey bee. These efforts have identified new subspecies, evolutionary lineages, and a significant number of genes involved with adaptations and colony-level quantitative traits. Many studies have also developed genetic assays that are being used to monitor the movement and admixture of honey bee populations. These resources are valuable for conservation and breeding programs that seek to improve the economic value of colonies or preserve locally adapted populations and subspecies. This review provides a brief discussion on how population and quantitative genomic studies has improved our understanding of the honey bee.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... The exception, Apis mellifera, is native to Europe, Africa, and Western Asia. Given the wide geographic spread of the species, A. mellifera has diversified into several subspecies (4,5), of which there are approximately 10 subspecies in Africa, 9 in Asia, and potentially as many as 13 subspecies in Europe (6). Each subspecies can be genetically and morphologically classified into at least five distinct evolutionary lineages: the M lineage of Eurasia, the C lineage of Europe, the O and Y lineages of Western Asia, and the A lineage of Africa (4,5). ...
... Given the wide geographic spread of the species, A. mellifera has diversified into several subspecies (4,5), of which there are approximately 10 subspecies in Africa, 9 in Asia, and potentially as many as 13 subspecies in Europe (6). Each subspecies can be genetically and morphologically classified into at least five distinct evolutionary lineages: the M lineage of Eurasia, the C lineage of Europe, the O and Y lineages of Western Asia, and the A lineage of Africa (4,5). Although it is reasonably accepted that the genus emerged in Asia, the ancestral origin and adaptive radiation of contemporary A. mellifera lineages and subspecies remain unresolved. ...
... Recent genomic studies of A. mellifera have shown that with the addition of new subspecies and enhanced datasets (9,15), estimates of evolutionary origin can change. As such, the increased representation of samples from Africa and Western Asia-two historically undersampled regions (4,16)-may be the key to resolving the out-of-Africa and out-of-Asia debate. ...
Article
Full-text available
The origin of the western honey bee Apis mellifera has been intensely debated. Addressing this knowledge gap is essential for understanding the evolution and genetics of one of the world’s most important pollinators. By analyzing 251 genomes from 18 native subspecies, we found support for an Asian origin of honey bees with at least three expansions leading to African and European lineages. The adaptive radiation of honey bees involved selection on a few genomic “hotspots.” We found 145 genes with independent signatures of selection across all bee lineages, and these genes were highly associated with worker traits. Our results indicate that a core set of genes associated with worker and colony traits facilitated the adaptive radiation of honey bees across their vast distribution.
... Accordingly, the honey bee subspecies were discriminated and clustered into three major groups (Fig 1) that led to establishment of hypotheses on the origin and routes of distribution of the species (Ruttner, 1978(Ruttner, , 1988Franck et al., 2001;Weinstock et al., 2006;Han et al., 2012). Several studies supported the hypothesis that the honey bee originated from northeast Africa or the Middle East, and distributed worldwide in different routes (Ruttner, 1978;Weinstock et al., 2006;Cridland et al., 2017;Dogantzis and Zayed, 2019;Tihelka et al., 2020), while others argue against (Han et al., 2012). ...
... Moreover, Cridland et al. (2017) supported the origin of A.mellifera to be in Northeast Africa or the Middle East, with the ancestral population giving rise to A and Y lineages, but their precise placement is not clear and awaits future research that should include Ethiopian honey bee samples and employ genome-wide SNP analysis. Evolutionary lineages of the honey bee Apis mellifera classified using A) Principal component analyses based on classical morphometry, showing the grouping of the honey bee subspecies into three major branches following the lineage distribution (Ruttner, 1978), B) Canonical variate analyses based on forewing venation, showing the separation of lineages A, C, M, and O, not including samples of lineage Y (Nawrocka et al., 2017), and C) Neighbor-joining tree based on a genome-wide genetic distance, elucidating four lineages (Weinstock et al., 2006); as well as (D) geographic distribution of five lineages M, C, O, Y, A (Dogantzis and Zayed, 2019). ...
Thesis
Ethiopia is a major beekeeping country located in northeast Africa where several evolutionary lineages of Apis mellifera contact. A unique practice of honey bee colony marketing which involves broad agro-ecological zones (AEZs) is a developing trend in the northern part of the country such as Tigray region in association with apicultural development. Several studies based on classical morphometry on the Ethiopian honey bee subspecies classification debated from the unique Apis mellifera simensis to five others. Moreover, the genetic diversity, adaptation, gene flow and inter-relationships of the honey bees between AEZs were not disentangled - a challenge for planning sustainable apicultural development and conservation. Therefore, this study was conducted to elucidate the honey bees of Ethiopia in a context of apicultural transformation using integrated methods: morphometrics, genetics, colony market survey and metadata analyses on beekeeping development. The results of geometric morphometric analyses confirmed that Ethiopian honey bees represented by Apis mellifera simensis references belong to a separate lineage (Y) compared to A, O, M and C, and the present sample belonged to Y. This supported the hypothesis of five major honey bee lineages of the honey bee Apis mellifera. Similarly, a maximum likelihood phylogenetic tree analysis based on the mitochondrial COI-COII showed that most of the Ethiopian honey bees belong to lineage Y. However, a substantial proportion of the samples from the northern part of the country clustered with lineage O, which support the hypothesis that there is close contact between Y and O. Both geometric morphometry and classical morphometry differentiated the Ethiopian honey bees from all references including A. m. monticola, A. m. scutellata, A. m. jementica, A. m. adansonii but grouped with A. m. simensis. Genetically, five DraI haplotypes (COI-COII) were found to be randomly distributed across AEZs, indicating a substantial gene flow. Consequently, the level of genetic differentiation among the Ethiopian honey bee subpopulations defined by local areas and AEZs was generally low based on r7-frag nuclear marker, which is identified to be associated with adaptation to habitat elevation in East African honey bees. Similarly, nucleotide diversity consistently decreased with increasing elevation - indicating a reduced effective population size in the highlands. Results obtained from colony market survey showed that the honey bee swarms are reproduced in a few highlands and re-distributed throughout the region. Colony buyers have preferences of color and AEZ of origin of the honey bees, which led to a one-way flow and eroded the overall level of genetic differentiation. However, a marked differentiation was detected between the highland and lowland honey bees in relic communities where an allelic length polymorphism was observed as a signature of local adaptation. Altogether, Ethiopian honey bees belong to the lineage Y and subspecies A. m. simensis, and are characterized by a high level of gene flow enhanced by colony marketing; but a conserved signature of local adaptation to higher elevations was identified in less disturbed communities. Further studies based on genome-wide analyses and field experiments, focusing on undisturbed communities, can provide more insights into adaptation, admixture and management implications. Sustainable bee breeding and extension services that enable local beekeeping without colony trade and transportation will help to promote apiculture and genetic conservation.
... The evolutionary history of the honey bee A. mellifera is not fully understood and there are hypotheses of an Asian as well as an African evolutionary origin, with the latest and most comprehensive study advocating an origin in the Middle East or Northern Africa (Whitfield et al., 2006;Han et al., 2012;Wallberg et al., 2014;Cridland et al., 2017). The species is found throughout Africa, Asia and Europe and subdivided into at least 27 morphologically, geographically, physiologically and behaviourally distinct subspecies (Ruttner, 1988;Parker et al., 2010;Dogantzis & Zayed, 2019), with new subspecies recently described (Sheppard & Meixner, 2003;Meixner et al., 2011;Chen et al., 2016). While there may not be a consensus in the scientific community on the origins and major migration events and routes of A. mellifera, it is broadly accepted that there are at least five genetically distinct evolutionary lineages: A lineage (Africa), Y lineage (Arabian Peninsula and Horn of Africa), O lineage (Asia) and the C and M lineage (Europe) (Dogantzis & Zayed, 2019). ...
... The species is found throughout Africa, Asia and Europe and subdivided into at least 27 morphologically, geographically, physiologically and behaviourally distinct subspecies (Ruttner, 1988;Parker et al., 2010;Dogantzis & Zayed, 2019), with new subspecies recently described (Sheppard & Meixner, 2003;Meixner et al., 2011;Chen et al., 2016). While there may not be a consensus in the scientific community on the origins and major migration events and routes of A. mellifera, it is broadly accepted that there are at least five genetically distinct evolutionary lineages: A lineage (Africa), Y lineage (Arabian Peninsula and Horn of Africa), O lineage (Asia) and the C and M lineage (Europe) (Dogantzis & Zayed, 2019). The European M lineage, traditionally comprised of A. mellifera mellifera (dark honey bee) and A. mellifera iberiensis, has its distribution from the Iberian peninsula in the South to southern Scandinavia in the North and from the British Isles in the West across much of Europe to the Ural mountains in the East (Ruttner, 1988). ...
Article
Full-text available
Displacement and admixture are threatening the survival and genetic integrity of the European dark bee, Apis mellifera mellifera. Studies on the phenotype-genotype map and genotype by environment interactions in honey bees are demonstrating that variation at subspecies level exists and is worth conserving. SNP-based tools for monitoring genetic integrity in bees have been developed, but are not yet widely used by European dark bee breeders. We used a panel of ancestry informative SNP markers to assess the level of admixture in Nordic dark bee breeding stocks. We found that bee breeders falsely classified admixed stocks based on morphometry as purebred and vice versa. Even though most Nordic A. m. mellifera breeding stocks have low proportions of C-lineage ancestry, we recommend to incorporate genotyping in Nordic dark bee breeding programmes to ensure that minimal genetic diversity is lost, while the genetic integrity of the subspecies is maintained.
... single nucleotide polymorphism (SNP) panels have been designed starting from whole genome resequencing datasets produced from different honey bee populations, and informative markers that can discriminate honey bee subspecies have been identified [26][27][28][29][30][31][32] . A few SNP panels have been also designed and used for several other applications in honey bee population genetic studies [33][34][35][36][37] . For example, genome-wide association analysis for varroa-specific defence behaviour in honey bees has been carried out using a SNP panel 38 . ...
Article
Full-text available
Awareness has been raised over the last years on the genetic integrity of autochthonous honey bee subspecies. Genomic tools available in Apis mellifera can make it possible to measure this information by targeting individual honey bee DNA. Honey contains DNA traces from all organisms that contributed or were involved in its production steps, including the honey bees of the colony. In this study, we designed and tested a genotyping by sequencing (GBS) assay to analyse single nucleotide polymorphisms (SNPs) of A. mellifera nuclear genome using environmental DNA extracted from honey. A total of 121 SNPs (97 SNPs informative for honey bee subspecies identification and 24 SNPs associated with relevant traits of the colonies) were used in the assay to genotype honey DNA, which derives from thousands of honey bees. Results were integrated with information derived from previous studies and whole genome resequencing datasets. This GBS method is highly reliable in estimating honey bee SNP allele frequencies of the whole colony from which the honey derived. This assay can be used to identify the honey bee subspecies of the colony that produced the honey and, in turn, to authenticate the entomological origin of the honey.
... This species has evolved to be thermally homeostatic, which has enabled its wide distribution throughout ecosystems, accompanied by diversification into distinct subspecies and ecotypes that differ morphologically and behaviorally [1], as well as genetically [2][3][4][5][6]. Several studies have been performed in order to elucidate their genetic divergence as well as their morphological plasticity, supporting the view of at least five major lineages denoted as C, M, A, O, Y of honey bees worldwide [3,7,8]. At the level of local subpopulation differentiation, honey bee traits such as high polyandry [9,10] enhance its fitness and productivity by increasing intracolonial genetic variability while reducing intercolonial differentiation. ...
Article
Full-text available
The diversity and local differentiation of honey bees are subjects of broad general interest. In particular, the classification of Ethiopian honey bees has been a subject of debate for decades. Here, we conducted an integrated analysis based on classical morphometrics and a putative nuclear marker (denoted r7-frag) for elevational adaptation to classify and characterize these honey bees. Therefore, 660 worker bees were collected out of 66 colonies from highland, midland and lowland agro-ecological zones (AEZs) and were analyzed in reference to populations from neighboring countries. Multivariate morphometric analyses show that our Ethiopian samples are separate from Apis mellifera scutellata, A. m. jemenitica, A. m. litorea and A. m. monticola, but are closely related to A. m. simensis reference. Linear discriminant analysis showed differentiation according to AEZs in the form of highland, midland and lowland ecotypes. Moreover, size was positively correlated with elevation. Similarly, our Ethiopian samples were differentiated from A. m. monticola and A. m. scutellata based on r7-frag. There was a low tendency towards genetic differentiation between the Ethiopian samples, likely impacted by increased gene flow. However, the differentiation slightly increased with increasing elevational differences, demonstrated by the highland bees that showed higher differentiation from the lowland bees (FST = 0.024) compared to the midland bees (FST = 0.015). An allelic length polymorphism was detected (denoted as d) within r7-frag, showing a patterned distribution strongly associated with AEZ (X2 = 11.84, p < 0.01) and found predominantly in highland and midland bees of some pocket areas. In conclusion, the Ethiopian honey bees represented in this study are characterized by high gene flow that suppresses differentiation.
... The origin of the samples that they have used (Harpur et al. 2014) differs from those used in describing the lineage Y (Franck et al. 2001). A recently conducted review (Dogantzis and Zayed 2019) indicated lineage Y to be of Asian origin in contrast to the initial description of the lineage Y to represent Ethiopian honey bees (Franck et al. 2001). The tendency to associate lineage Y with the Middle East could be arisen due to the fact that Ethiopian honey bees were assumed to be A . ...
Article
Full-text available
Traditional beekeeping has been playing important socio-economic roles in Ethiopia for millennia. The country is situated in northeast Africa, where ranges of major evolutionary lineages of Apis mellifera adjoin. However, studies on the classification and distribution of subspecies and lineages of honey bees in the country are partly inconsistent, either proposing multiple subspecies and lineages or a unique A. m. simensis. This study was conducted with the aim of elucidating Ethiopian honey bees in reference to African subspecies and major global lineages using wing geometric morphometrics and COI-COII mitochondrial DNA analyses. For this purpose, 660 worker bees were collected from 66 colonies representing highland, midland, and lowland zones in different locations. Both methods indicated that the samples from this study form a distinct cluster together with A. m. simensis reference. In addition, forewing venation patterns showed that most of the Ethiopian samples are separate from all reference subspecies, except A. m. simensis. Analysis of COI-COII sequences revealed five DraI haplotypes (Y2, Y1, A1, and O5’), of which one was new denoted as Y3. Moreover, centroid size strongly associated with elevation. In conclusion, the results supported that Ethiopian honey bees are distinct both at lineage and subspecies levels; however, there is an indication of lineage O in the north.
... Since the early 2000s, with increased emergence of genomic analysis resources for this eusocial species (Dogantzis and Zayed, 2019;Weinstock et al., 2006), studies proceeded to forward screen the honey bee genome for genes that are functionally associated with differential ovary activation or de-activation in the worker caste (e.g., Niu et al., 2014;Thompson et al., 2008). This type of study is insightful because it helps to identify loci specifically associated with worker sterility and is not obscured by genes more broadly involved in caste differentiation (Mullen and Thompson, 2015). ...
... Honey bees are now widespread across Africa, Asia, Europe, America, and Oceania. All honey bee subspecies are divided into five main lineages that are described according to their place of origin (Ruttner, 1988;Dogantzis and Zayed, 2019). The first ones described were the African lineage (A), the Western and Northern Europe lineage (M), and the Eastern Europe lineage (C) (Ruttner, 1988). ...
Article
Full-text available
The natural diversity of the honey bee (Apis mellifera) includes five evolutionary lineages and 26 subspecies, currently described that come from Africa, Europe, and the Middle East. They were introduced by humans to almost every continent and each of them has adapted favorably to the environmental and climatic conditions of their geographical areas of origin, which has led to greater genetic diversity and hybridization processes between subspecies. The genetic diversity of honey bees in Chile was characterized by the presence of European subspecies, such as Apis mellifera mellifera and Apis mellifera ligustica, but no updated information is available. The objective of this study was to assess the current genetic characterization of honey bees in the coastal zone of the O'Higgins Region, due to its national importance in beekeeping, using geometric morphometrics. Samples were taken from five counties taking samples of five apiaries from each one, including 3 colonies per apiary with a total of 30 bees per colony. The results indicate that there is evidence of hybridization between the subspecies Apis mellifera carnica and Apis mellifera ligustica, which reveals that the genetic pattern of the region has changed. This raises the questions as to whether this hybridization with predominantly Apis mellifera carnica is the most suitable for the ecological conditions of the region and how this could affect colony productivity and local beekeeping.
... Despite the influx of all of these genomic resources and substantial progress in understanding A. mellifera diversity and evolutionary history, the evolutionary origin of A. mellifera still remains uncertain, with both 'out of Africa' and 'out of Asia' scenarios possible (Cridland et al. 2017). While we certainly have the tools to rapidly sequence and analyse bee genomes, the limiting factor in understanding the evolutionary origins of A. mellifera is actually the availability of a 'pure' honey bee samples especially from Africa and Asia (Dogantzis and Zayed 2019). This example illustrates how genomics cannot operate in a vacuum of biological understanding, i.e. genomic expertise can never replace the importance of well-trained biologists that are able to identify and sample the large number of native honey bee subspecies in the field. ...
Article
Full-text available
In 2006, the full complement of DNA sequence information (or ‘genome’) of the Western honey bee, Apis mellifera , was published. This important resource was one of the most important advances in the history of honey bee research, with seemingly limitless applications to unlocking the secrets of honey bee biology and social life and for improving health, breeding and management. Honey bee genomics has seen immense growth in the past one and a half decades. In this article, we reflect on what the genome has added to our understanding of fundamental aspects of honey bee biology, including evolutionary origins, behaviour and health/disease. We conclude that while the genome has fuelled growth in many areas of honey bee research, it is only one part of an emerging systems-based, multi-omics approach. Moving forward, we posit that honey bee research will benefit most from an even fuller integration of genomics with classical approaches in evolution, ethology, physiology and microbiology.
... Honey bees (Apis mellifera L.) are the most important managed pollinators and currently under threat due to a multitude of pressures worldwide [1,2]. The species shows considerable variation across its natural range and is comprised of at least 30 described subspecies belonging to different evolutionary lineages [3][4][5][6]. Europe holds a large fraction of this honey bee diversity with numerous endemic subspecies representing four evolutionary lineages, namely the African lineage (A), Central and Eastern European lineage (C), Western and Northern European lineage (M), and Near East and Central Asian lineage (O) [7,8]. However, this diversity and the natural distribution range of European honey bees have been influenced by anthropogenic factors to an extent that several locally adapted populations are at risk due to introgression and crossbreeding [9][10][11]. ...
Article
Full-text available
Background With numerous endemic subspecies representing four of its five evolutionary lineages, Europe holds a large fraction of Apis mellifera genetic diversity. This diversity and the natural distribution range have been altered by anthropogenic factors. The conservation of this natural heritage relies on the availability of accurate tools for subspecies diagnosis. Based on pool-sequence data from 2145 worker bees representing 22 populations sampled across Europe, we employed two highly discriminative approaches (PCA and F ST ) to select the most informative SNPs for ancestry inference. Results Using a supervised machine learning (ML) approach and a set of 3896 genotyped individuals, we could show that the 4094 selected single nucleotide polymorphisms (SNPs) provide an accurate prediction of ancestry inference in European honey bees. The best ML model was Linear Support Vector Classifier (Linear SVC) which correctly assigned most individuals to one of the 14 subspecies or different genetic origins with a mean accuracy of 96.2% ± 0.8 SD. A total of 3.8% of test individuals were misclassified, most probably due to limited differentiation between the subspecies caused by close geographical proximity, or human interference of genetic integrity of reference subspecies, or a combination thereof. Conclusions The diagnostic tool presented here will contribute to a sustainable conservation and support breeding activities in order to preserve the genetic heritage of European honey bees.
... There is a number of honey bee, Apis mellifera L., subspecies from 20 up 33 (Ruttner, 1988;Engel, 1999;Sheppard and Meixner2003;Dogantzis and Zayed, 2019;Ilyasov et al., 2020). ...
Article
Full-text available
Objectives This study aimed to analyze the genetic relationships between honey bee subspecies using reference specimens and recently collected specimens from different parts of the world. The purity of these specimens was discussed in light of the obtained results. Methods The genetic networks were constructed between 21 subspecies of honey bees, Apis mellifera L.: 9 in Africa, 7 in Europe and 5 in Asia. The analysis was performed using the mtDNA of these subspecies and the Population Analysis with Reticulate Trees software. Some subspecies were represented by more than two specimens based on the available online sequences. Results and Conclusions: The subspecies A. m. sahariensis from Africa showed unique characteristics and is genetically isolated than all other studied bee subspecies. Specimens collected from Saudi Arabia showed genetic relatedness to A.m.jemenitica, A. m. lamarckii, and some European subspecies, suggesting high degree of hybridization. The close genetic relationship between the Egyptian bees, A. m. lamarckii, and the Syrian bees, A. m. syriaca, were emphasized. The overall genetic network showed the presence of three distinct branches in relation to geographical locations. The high accurateness of the used analysis was confirmed by previous phylogenetic studies as well as the genetic relationships between hybrid bees of A. m. capensis and A. m. scutellata. The genetic networks showed the presence of bee subspecies from Africa in all branches including Europe and Asia. The study suggests the impurity of some specimens mostly due to the hybridization between subspecies. Specific recommendations for future conservation efforts of bees were presented in light of this study.
... Moreover, this species can digest a large range of nutrients and dilute toxins and unpalatable compounds due to social behaviors and stores [8][9][10]. Another aspect of the wide geographic distribution of A. mellifera is the diversity of its subspecies/breeds, species' domestication, and introduction by humans [11,12]. In fact, honeybee keeping has steadily grown in recent decades worldwide, which is linked to the fact that A. mellifera is an effective pollinator of many crops and honey production is a profitable activity [13]. ...
Article
Full-text available
Studies at local spatial scales have shown that the generalist honeybee Apis mellifera L. can strongly affect the structural organization and properties of pollination networks. However, there is still little knowledge on how the connectivity of the honeybee within networks (i.e., interactive role) could affect pollination networks at a global scale. To fill this gap, we evaluated how the interactive role of A. mellifera could affect niche overlap, specialization, and robustness of pollination networks. We used 109 weighted pollination networks spread across about 94 degrees of latitude and 227 degrees of longitude. We developed a new standardized framework based on species removal to assess the impact of the honeybee on plant-pollinator networks. We found that when the honeybee was removed from the networks, plant species had less niche overlap (i.e., shared fewer interactions via their pollinators) and the networks became more specialized and more robust to species extinctions. Our findings indicate that A. mellifera’s effects on pollination networks vary geographically and could influence several ecological and evolutionary factors acting at local scales, including pollination services. We hope this contribution will stimulate new macroecological studies involving abundant and generalist species and their functional roles within ecological communities
... Honey bees live in perennial colonies, with a single reproductive female queen and tens of thousands of facultatively sterile female workers (Winston, M. L., 1987). Honey bees evolved in tropical regions, and later expanded into temperate Europe (reviewed in Dogantzis, K. A. & Zayed, A., 2019). In both temperate and tropical regions, bees experience periods of season dearth during which they reduce or cease brood rearing, requiring that the adult workers exhibit an increased lifespan. ...
Preprint
Faced with adverse conditions, such as winter in temperate regions or hot and dry conditions in tropical regions, many insect species enter a state of diapause, a period of dormancy associated with a reduction or arrest of physical activity, development, and reproduction. Changes in common physiological pathways underlie diapause phenotypes in different insect species. However, most transcriptomic studies of diapause have not simultaneously evaluated and compared expression patterns in different tissues. Honey bees (Apis mellifera) represent a unique model system to study the mechanisms underpinning diapause. In winter, honey bees exhibit a classic diapause phenotype, with reduced metabolic activity, increased physiological nutritional resources, and altered hormonal profiles. However, winter bees actively heat their colony by vibrating their wing muscles; thus, this tissue is not quiescent. Here, we evaluated the transcriptional profiles of flight muscle tissue and fat body tissue (involved in nutrient storage, metabolism and immune function) of winter bees. We also evaluated two behavioral phenotypes of summer bees: nurses, which exhibit high nutritional stores and low flight activity, and foragers, which exhibit low nutritional stores and high flight activity. We found winter bees and nurses have similar fat body transcriptional profiles compared to foragers, whereas winter bees and foragers have similar flight muscle transcriptional profiles compared to nurses. Additionally, differentially expressed genes were enriched in diapause-related GO terms. Thus, honey bees exhibit tissue-specific transcriptional profiles associated with diapause, laying the groundwork for future studies evaluating the mechanisms, evolution, and consequences of this tissue-specific regulation.
... Honey bees live in perennial colonies, with a single reproductive female queen and tens of thousands of facultatively sterile female workers (Winston, M. L., 1987). Honey bees evolved in tropical regions, and later expanded into temperate Europe (reviewed in Dogantzis, K. A. & Zayed, A., 2019). In both temperate and tropical regions, bees experience periods of season dearth during which they reduce or cease brood rearing, requiring that the adult workers exhibit an increased lifespan. ...
Preprint
Faced with adverse conditions, such as winter in temperate regions or hot and dry conditions in tropical regions, many insect species enter a state of diapause, a period of dormancy associated with a reduction or arrest of physical activity, development, and reproduction. Changes in common physiological pathways underlie diapause phenotypes in different insect species. However, most transcriptomic studies of diapause have not simultaneously evaluated and compared expression patterns in different tissues. Honey bees (Apis mellifera) represent a unique model system to study the mechanisms underpinning diapause. In winter, honey bees exhibit a classic diapause phenotype, with reduced metabolic activity, increased physiological nutritional resources, and altered hormonal profiles. However, winter bees actively heat their colony by vibrating their wing muscles; thus, this tissue is not quiescent. Here, we evaluated the transcriptional profiles of flight muscle tissue and fat body tissue (involved in nutrient storage, metabolism and immune function) of winter bees. We also evaluated two behavioral phenotypes of summer bees: nurses, which exhibit high nutritional stores and low flight activity, and foragers, which exhibit low nutritional stores and high flight activity. We found winter bees and nurses have similar fat body transcriptional profiles compared to foragers, whereas winter bees and foragers have similar flight muscle transcriptional profiles compared to nurses. Additionally, differentially expressed genes were enriched in diapause-related GO terms. Thus, honey bees exhibit tissue-specific transcriptional profiles associated with diapause, laying the groundwork for future studies evaluating the mechanisms, evolution, and consequences of this tissue-specific regulation.
... Thus, each colony has thousands of potential foragers to pollinate crops (Tautz, 2008). Honey bees have been managed by humans for thousands of years and have been transported to all continents except Antarctica (Dogantzis and Zayed, 2019;Kritsky, 2017). While historically beekeepers focused on honey production, managing bees for commercial pollination services has become quite common. ...
Article
Full-text available
Pollinators, particularly managed honey bees, are crucial for global food systems. However, declines in populations of both wild and managed pollinators have been reported across the world. In the United States, approximately 30% of managed honey bee colonies die each year. The factors underlying these losses are well understood and include reductions in the abundance and diversity of flowering plants that pollinators depend on for food, increased insecticide use, and reduced nesting habitat for wild bees. However, translating pollinator research findings into actionable knowledge for beekeepers presents a sizable spatial decision support challenge. In this work we evaluate the utility and usability of a prototype system called Beescape which intends to support environmental decision-making for beekeepers and other stakeholders. Beescape includes tools for exploring and visualizing maps that link to modeled environmental factors that impact managed bees, including honey bees, and wild bee health. Thirty beekeepers were recruited to take part in an online user study that included task analysis and survey components to elicit user input on areas of improvement for future Beescape development. The results of our evaluation of usability and utility metrics for Beescape highlighted the need for spatially-specific foraging information, better descriptions of modeled habitat quality measures, and actionable guidance to help them manage their hives. The results of our study highlight the challenges and opportunities associated with providing decision support systems that attempt to translate emerging environmental science for audiences that may be motivated by a common goal to improve honey bee survival, but who have a diverse range of technical backgrounds, applied practices, and reasons for their interest.
... Honeybees (Apis mellifera) are social species and represent one of the most important pollinators for agricultural systems [17,18]. Humans have managed honeybees for thousands of years, and developed bee breeding for all continents, mostly the United States and Europe [19,20]. ...
Article
Full-text available
Plant species are fundamental source of nectar in beekeeping since bees access nectar and pollen from flowers. Consequently, bee products are strongly linked to the bee foraging flora source, and, depending on this, they acquire defined features, including their health and medicinal properties. Medicinal plants contribute greatly to increase the beneficial properties of bee products, such as honey, pollen, royal jelly, and propolis. Bee products represent a potential source of natural antioxidants that can counteract the effects of oxidative stress underlying the pathogenesis of many diseases. The antioxidant properties of bee products have been widely studied and there is an abundance of information available in the literature. Notwithstanding, the uniqueness of the presented perspective is to provide an updated overview of the antioxidant properties of bee products derived from medicinal plants as beekeeping sources. This topic is divided and discussed in the text in different sections as follows: (i) beekeeping and the impacts of environmental factors; (ii) an overview of the role of medicinal plants for bee products; (iii) definition and categorization of the main medicinal bee plants and related bee products; (iv) the study approach of the antioxidant properties; (v) the conventional and innovative assays used for the measurement of the antioxidant activity; and (vi) the antioxidant properties of bee products from medicinal plants.
... The origin of the samples that they have used (Harpur et al. 2014) differs from those used in describing the lineage Y (Franck et al. 2001). A recently conducted review (Dogantzis and Zayed 2019) indicated lineage Y to be of Asian origin in contrast to the initial description of the lineage Y to represent Ethiopian honey bees (Franck et al. 2001). The tendency to associate lineage Y with the Middle East could be arisen due to the fact that Ethiopian honey bees were assumed to be A . ...
... Mitochondrial DNA; single molecule real-time sequencing; Apis mellifera sinisxinyuan Apis mellifera has a wide distribution in Europe, western Asia and Africa. There are at least 27 morphologically and geographically distinct subspecies divided into five lineages (A, Y, M, C and O lineage) (Ruttner 1988;Sheppard and Meixner 2003;Chen et al. 2016;Dogantzis and Zayed 2019). The newly discovered A. mellifera subspecies Apis mellifera sinisxinyuan, was clustered in the M-lineage and postulated to diverge from A. m. mellifera about 132 KYA. A. m. sinisxinyuan is winter-tolerant and adapted to temperate climates (Chen et al. 2016). ...
Article
Full-text available
We analyzed the complete mitochondrial genome of the recently discovered Xinyuan honey bee, Apis mellifera sinisxinyuan using single molecule real-time sequencing. The mitochondrial genome of A. m. sinisxinyuan is a circular molecule of 16,886 bp, comprising 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes and a control region rich in A + T. Phylogenetic analysis using 13 protein-coding genes supports a close relationship to another M-lineage honey bee, A. m. mellifera.
Article
Full-text available
Western honey bees (Apis mellifera) are one of the most important pollinators of agricultural crops and wild plants. Despite the growth in the availability of sequence data for honey bees, the phylogeny of the species remains a subject of controversy. Most notably, the geographic origin of honey bees is uncertain, as are the relationships among its constituent lineages and subspecies. We aim to infer the evolutionary and biogeographical history of the honey bee from mitochondrial genomes. Here we analyse the full mitochondrial genomes of 18 A. mellifera subspecies, belonging to all major lineages, using a range of gene sampling strategies and inference models to identify factors that may have contributed to the recovery of incongruent results in previous studies. our analyses support a northern African or Middle eastern origin of A. mellifera. We show that the previously suggested european and Afrotropical cradles of honey bees are the result of phylogenetic error. Monophyly of the M, c, and o lineages is strongly supported, but the A lineage appears paraphyletic. A. mellifera colonised europe through at least two pathways, across the Strait of Gibraltar and via Asia Minor.
Article
Faced with adverse conditions, such as winter in temperate regions or hot and dry conditions in tropical regions, many insect species enter a state of diapause, a period of dormancy associated with a reduction or arrest of physical activity, development, and reproduction. Changes in common physiological pathways underlie diapause phenotypes in different insect species. However, most transcriptomic studies of diapause have not simultaneously evaluated and compared expression patterns in different tissues. Honey bees (Apis mellifera) represent a unique model system to study the mechanisms underpinning diapause‐related phenotypes. In winter, honey bees exhibit a classic diapause phenotype, with reduced metabolic activity, increased physiological nutritional resources, and altered hormonal profiles. However, winter bees actively heat their colony by vibrating their wing muscles; thus, this tissue is not quiescent. Here, we evaluated the transcriptional profiles of flight muscle tissue and fat body tissue (involved in nutrient storage, metabolism and immune function) of winter bees. We also evaluated two behavioral phenotypes of summer bees: nurses, which exhibit high nutritional stores and low flight activity, and foragers, which exhibit low nutritional stores and high flight activity. We found winter bees and nurses have similar fat body transcriptional profiles, whereas winter bees and foragers have similar flight muscle transcriptional profiles. Additionally, differentially expressed genes were enriched in diapause‐related GO terms. Thus, honey bees exhibit tissue‐specific transcriptional profiles associated with seasonal phenotypes, laying the groundwork for future studies evaluating the mechanisms, evolution, and consequences of this tissue‐specific regulation.
Article
Declines in bee populations across the world threaten food security and ecosystem function. It is currently not possible to routinely predict which specific stressors lead to declines in different populations or contexts, hindering efforts to improve bee health. Genomics has the potential to dramatically improve our ability to identify, monitor and predict the effects of stressors, as well as to mitigate their impacts through the use of marker-assisted selection, RNA interference and potentially gene editing. Here we discuss the most compelling recent applications of genomics to investigate the mechanisms underpinning bee population declines and to improve the health of both wild and managed bee populations.
Article
Full-text available
The natural distribution of the honeybee (Apis mellifera L.) has been changed by humans in recent decades to such an extent that the formerly widest-spread European subspecies, Apis mellifera mellifera, is threatened by extinction through introgression from highly divergent commercial strains in large tracts of its range. Conservation efforts for A. m. mellifera are underway in multiple European countries requiring reliable and cost-efficient molecular tools to identify purebred colonies. Here, we developed four ancestry-informative SNP assays for high sample throughput genotyping using the iPLEX Mass Array system. Our customized assays were tested on DNA from individual and pooled, haploid and diploid honeybee samples extracted from different tissues using a diverse range of protocols. The assays had a high genotyping success rate and yielded accurate genotypes. Performance assessed against whole-genome data showed that individual assays behaved well, although the most accurate introgression estimates were obtained for the four assays combined (117 SNPs). The best compromise between accuracy and genotyping costs was achieved when combining two assays (62 SNPs). We provide a ready-to-use cost-effective tool for accurate molecular identification and estimation of introgression levels to more effectively monitor and manage A. m. mellifera conservatories.
Article
Full-text available
The most important managed pollinator, the honeybee (Apis mellifera L.), has been subject to a growing number of threats. In Western Europe one such threat is large-scale introductions of commercial strains (C-lineage ancestry), which is leading to introgressive hybridization and even the local extinction of native honeybee populations (M-lineage ancestry). Here, we developed reduced assays of highly informative SNPs from 176 whole genomes to estimate C-lineage introgression in the most diverse and evolutionarily complex subspecies in Europe, the Iberian honeybee (Apis mellifera iberiensis). We started by evaluating the effects of sample size and sampling a geographically restricted area on the number of highly informative SNPs. We demonstrated that a bias in the number of fixed SNPs (FST=1) is introduced when the sample size is small (N≤10) and when sampling only captures a small fraction of a population's genetic diversity. These results underscore the importance of having a representative sample when developing reliable reduced SNP assays for organisms with complex genetic patterns. We used a training dataset to design four independent SNP assays selected from pairwise FST between the Iberian and C-lineage honeybees. The designed assays, which were validated in holdout and simulated hybrid datasets, proved to be highly accurate and can be readily used for monitoring populations not only in the native range of A. m. iberiensis in Iberia but also in the introduced range in the Balearic islands, Macaronesia, and South America, in a time- and cost-effective manner. While our approach used the Iberian honeybee as model system, it has a high value in a wide range of scenarios for the monitoring and conservation of potentially hybridized domestic and wildlife populations.
Article
Full-text available
The rate of genomic recombination displays evolutionary plasticity and can even vary in response to environmental factors. The western honey bee (Apis mellifera L.) has an extremely high genomic recombination rate but the mechanistic basis for this genome-wide upregulation is not understood. Based on the hypothesis that meiotic recombination and DNA damage repair share common mechanisms in honey bees as in other organisms, we predicted that oxidative stress leads to an increase in recombination rate in honey bees. To test this prediction, we subjected honey bee queens to oxidative stress by paraquat injection and measured the rates of genomic recombination in select genome intervals of offspring produced before and after injection. The evaluation of 26 genome intervals in a total of over 1750 offspring of 11 queens by microsatellite genotyping revealed several significant effects but no overall evidence for a mechanistic link between oxidative stress and increased recombination was found. The results weaken the notion that DNA repair enzymes have a regulatory function in the high rate of meiotic recombination of honey bees, but they do not provide evidence against functional overlap between meiotic recombination and DNA damage repair in honey bees and more mechanistic studies are needed.
Article
Full-text available
Africanized honey bees (Apis mellifera) arrived in the western hemisphere in the 1950s and quickly spread north reaching California in the 1990s. These bees are highly defensive and somewhat more difficult to manage for commercial purposes than the European honey bees traditionally kept. The arrival of these bees and their potentially replacing European bees over much of the state is thus of great concern. After a 25 year period of little systematic sampling, a recent small scale study found Africanized honey bees in the Bay Area of California, far north of their last recorded distribution. The purpose of the present study was to expand this study by conducting more intensive sampling of bees from across northern California. We found Africanized honey bees as far north as Napa and Sacramento. We also found Africanized bees in all counties south of these counties. Africanized honey bees were particularly abundant in parts of the central valley and Monterey. This work suggests the northern spread of Africanized honey bees may not have stopped. They may still be moving north at a slow rate, although due to the long gaps in sampling it is currently impossible to tell for certain. Future work should routinely monitor the distribution of these bees to distinguish between these two possibilities.
Article
Full-text available
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.
Article
Full-text available
Understanding the genetic basis of adaption is a central task in biology. Populations of the honey bee Apis mellifera that inhabit the mountain forests of East Africa differ in behavior and morphology from those inhabiting the surrounding lowland savannahs, which likely reflects adaptation to these habitats. We performed whole genome sequencing on 39 samples of highland and lowland bees from two pairs of populations to determine their evolutionary affinities and identify the genetic basis of these putative adaptations. We find that in general, levels of genetic differentiation between highland and lowland populations are very low, consistent with them being a single panmictic population. However, we identify two loci on chromosomes 7 and 9, each several hundred kilobases in length, which exhibit near fixation for different haplotypes between highland and lowland populations. The highland haplotypes at these loci are extremely rare in samples from the rest of the world. Patterns of segregation of genetic variants suggest that recombination between haplotypes at each locus is suppressed, indicating that they comprise independent structural variants. The haplotype on chromosome 7 harbors nearly all octopamine receptor genes in the honey bee genome. These have a role in learning and foraging behavior in honey bees and are strong candidates for adaptation to highland habitats. Molecular analysis of a putative breakpoint indicates that it may disrupt the coding sequence of one of these genes. Divergence between the highland and lowland haplotypes at both loci is extremely high suggesting that they are ancient balanced polymorphisms that greatly predate divergence between the extant honey bee subspecies.
Article
Full-text available
The complementary sex determiner (csd) gene determines the sex of the western honey bee (Apis mellifera L.). Bees that are heterozygous at the csd locus develop into females; whereas hemizygous bees develop into males. The co-occurrence of two identical csd alleles in a single diploid genome leads to the genetic death of the bee. Thus, the maintenance of csd diversity in the population is favoured. The number and distribution of csd alleles is particularly interesting in light of the recent decline in the honey bee population. In this study, we analysed the distribution of csd alleles in two Polish populations separated by about 100 km. We analysed the maternal alleles of 193 colonies and found 121 different alleles. We also analysed the distribution and frequency of the alleles, and found that they are distributed unevenly. We show that the methods that have been used so far to estimate the total worldwide number of csd alleles have significantly underestimated their diversity. We also show that the uneven distribution of csd alleles is caused by a large number of infrequent alleles, which most likely results from the fact that these alleles are generated very frequently.
Article
Full-text available
Genetic exchange by hybridization or admixture can make an important contribution to evolution, and introgression of favourable alleles can facilitate adaptation to new environments. A small number of honeybees (Apis mellifera) with African ancestry were introduced to Brazil ~60 years ago, which dispersed and hybridized with existing managed populations of European origin, quickly spreading across much of the Americas in an example of a massive biological invasion. Here we analyse whole genome sequences of 32 Africanized honeybees sampled from throughout Brazil in order to study the effect of this process on genome diversity. By comparison with ancestral populations from Europe and Africa, we infer that these samples have 84% African ancestry, with the remainder from western European populations. However, this proportion varies across the genome and we identify signals of positive selection in regions with high European ancestry proportions. These observations are largely driven by one large gene-rich 1.4-Mbp segment on chromosome 11 where European haplotypes are present at a significantly elevated frequency and likely confer an adaptive advantage in the Africanized honeybee population. This region has previously been implicated in reproductive traits and foraging behaviour in worker bees. Finally, by analysing the distribution of ancestry tract lengths in the context of the known time of the admixture event, we are able to infer an average generation time of 2.0 years. Our analysis highlights the processes by which populations of mixed genetic ancestry form and adapt to new environments. This article is protected by copyright. All rights reserved.
Article
Full-text available
Western honey bees (Apis mellifera) far exceed the commonly observed 1-2 meiotic recombination events per chromosome and exhibit the highest Metazoan recombination rate (20 cM/Mb) described thus far. However, the reasons for this exceptional rate of recombination are not sufficiently understood. In a comparative study, we report on the newly constructed genomic linkage maps of Apis florea and Apis dorsata that represent the two honey bee lineages without recombination rate estimates so far. Each linkage map was generated de-novo, based on SNP genotypes of haploid male offspring of a single female. The A. florea map spans 4782 cM with 1279 markers in 16 linkage groups. The A. dorsata map is 5762 cM long and contains 1189 markers in 16 linkage groups. Respectively, these map sizes result in average recombination rate estimates of 20.8 cM/Mb and 25.1 cM/Mb. Synteny analyses indicate that frequent intra-chromosomal rearrangements but no translocations among chromosomes accompany the high rates of recombination during the independent evolution of the three major honey bee lineages. Our results imply a common cause for the evolution of very high recombination rates in Apis. Our findings also suggest that frequent homologous recombination during meiosis might increase ectopic recombination and rearrangements within but not between chromosomes. It remains to be investigated whether the resulting inversions may have been important in the evolutionary differentiation between honey bee species.
Article
Full-text available
The western honey bee, Apis mellifera, provides critical pollination services to agricultural crops worldwide. However, despite substantial interest and prior investigation, the early evolution and subsequent diversification of this important pollinator remain uncertain. The primary hypotheses place the origin of A. mellifera in either Asia or Africa, with subsequent radiations proceeding from one of these regions. Here, we use two publicly available whole-genome data sets plus newly sequenced genomes and apply multiple population genetic analysis methods to investigate the patterns of ancestry and admixture in native honey bee populations from Europe, Africa, and the Middle East. The combination of these data sets is critical to the analyses, as each contributes samples from geographic locations lacking in the other, thereby producing the most complete set of honey bee populations available to date. We find evidence supporting an origin of A. mellifera in the Middle East or North Eastern Africa, with the A and Y lineages representing the earliest branching lineages. This finding has similarities with multiple contradictory hypotheses and represents a disentangling of genetic relationships, geographic proximity, and secondary contact to produce a more accurate picture of the origins of A. mellifera. We also investigate how previous studies came to their various conclusions based on incomplete sampling of populations, and illustrate the importance of complete sampling in understanding evolutionary processes. These results provide fundamental knowledge about genetic diversity within Old World honey bee populations and offer insight into the complex history of an important pollinator.
Article
Full-text available
Pollination is a key ecosystem service for agricultural systems and Western honey bees, Apis mellifera, are the most important managed pollinators. Major losses of managed honey bee colonies reinforced the need to take advantage of locally adapted subspecies and ecotypes to buffer populations against various stressors. However, introductions of non-native honey bees from distant lineages are likely to undermine respective conservation efforts unless reliable and cost effective tools can be used to identify hybridization. The purpose of this study is to characterize current population structure and genetic diversity, and to assess the degree of admixture between native and introduced honey bees. Moreover, we aim to select a reduced number of genetic markers to improve conservation management strategies. We take advantage of recent developments in next-generation sequencing and network-based clustering to investigate conservation efforts for the native European Dark honey bee, A. m. mellifera, which is threatened by introgression in most of its range. We collected whole-genome sequence information from haploid drones of A. m. mellifera, A. m. carnica and Buckfast sampled throughout Switzerland (N=81), as well as from four Swiss A. m. mellifera conservation areas (N=39) and from one conservatory in the French Alps (N = 31). Population structure analyses based upon 3.375 M genome-wide SNPs discerned samples by subspecies and geographic origin (Switzerland or France). Ancestry inference indicated admixed individuals in all of the protected areas, calling for improved management efforts. After testing different subsets of ancestry informative SNPs using three different selection strategies (FST, PCA-based or at random), as few as 50 SNPs are found to be sufficient to differentiate native from introduced honey bees. Therefore our data suggests that a low-density SNP panel can be a precise and cost-effective tool to support conservation management efforts for managed pollinators.
Article
Full-text available
Quantitative genetic traits provide insights into the evolutionary potential of populations, as heritability estimates measure the population’s ability to respond to global changes. Although wild and managed bees are increasingly threatened by the degradation of natural habitats and climate change, risking plant biodiversity and agriculture production, no study has yet performed a systematic review of heritability estimates across the group. Here we help fill this knowledge gap, gathering all available heritability estimates for ants, bees, and wasps, evaluating which factors affect these estimates and assessing the reported genetic correlations between traits. Using a model selection approach to analyze a dataset of more than 800 heritability estimates, we found that heritability is influenced by trait type, with morphological traits exhibiting the highest heritability estimates, and defense and metabolism-related traits showing the lowest estimates. Study system, sociality degree, experimental design, estimation type (narrow or broad-sense heritability), and sample size were not found to affect heritability estimates. Results remained unaltered when correcting for phylogenetic inertia, and when analyzing social bees separately. Genetic correlations between honeybee traits revealed both positive coefficients, usually for traits in the same category, and negative coefficients, suggesting trade-offs among other traits. We discuss these findings and highlight the importance of maintaining genetic variance in fitness-related traits. Our study shows the importance of considering heritability estimates and genetic correlations when designing breeding and conservation programs. We hope this meta-analysis helps identify sustainable breeding approaches and conservation strategies that help safeguard the evolutionary potential of wild and managed bees.
Article
Full-text available
The Africanized honeybee (AHB) is a population of Apis mellifera found in the Americas. AHBs originated in 1956 in Rio Clara, Brazil where imported African A. m. scutellata escaped and hybridized with local populations of European A. mellifera. Africanized populations can now be found from Northern Argentina to the Southern United States. AHBs—often referred to as ‘Killer Bees’— are a major concern to the beekeeping industry as well as a model for the evolutionary genetics of colony defence. We performed high coverage pooled-resequencing of 360 diploid workers from 30 Brazilian AHB colonies using Illumina Hi-Seq (150 bp PE). This yielded a high density SNP data set with an average read depth at each site of 20.25 reads. With 3,606,720 SNPs and 155,336 SNPs within 11,365 genes, this data set is the largest genomic resource available for AHBs and will enable high-resolution studies of the population dynamics, evolution, and genetics of this successful biological invader, in addition to facilitating the development of SNP-based tools for identifying AHBs.
Article
Full-text available
Some invasive hymenopteran social insects found new populations with very few reproductive individuals. This is despite the high cost of founder effects for such insects, which generally require heterozygosity at a single locus—the complementary sex determiner, csd—to develop as females. Individuals that are homozygous at csd develop as either infertile or subfertile diploid males or not at all. Furthermore, diploid males replace the female workers that are essential for colony function. Here we document how the Asian honey bee (Apis cerana) overcame the diploid male problem during its invasion of Australia. Natural selection prevented the loss of rare csd alleles due to genetic drift and corrected the skew in allele frequencies caused by founder effects to restore high average heterozygosity. Thus, balancing selection can alleviate the genetic load at csd imposed by severe bottlenecks, and so facilitate invasiveness.
Article
Full-text available
In colonies of the honeybee Apis mellifera, the queen is usually the only reproductive female, which produces new females (queens and workers) by laying fertilized eggs. However, in one subspecies of A. mellifera, known as the Cape bee (A. m. capensis), worker bees reproduce asexually by thelytoky, an abnormal form of meiosis where two daughter nucleii fuse to form single diploid eggs, which develop into females without being fertilized. The Cape bee also exhibits a suite of phenotypes that facilitate social parasitism whereby workers lay such eggs in foreign colonies so their offspring can exploit their resources. The genetic basis of this switch to social parasitism in the Cape bee is unknown. To address this, we compared genome variation in a sample of Cape bees with other African populations. We find genetic divergence between these populations to be very low on average but identify several regions of the genome with extreme differentiation. The regions are strongly enriched for signals of selection in Cape bees, indicating that increased levels of positive selection have produced the unique set of derived phenotypic traits in this subspecies. Genetic variation within these regions allows unambiguous genetic identification of Cape bees and likely underlies the genetic basis of social parasitism. The candidate loci include genes involved in ecdysteroid signaling and juvenile hormone and dopamine biosynthesis, which may regulate worker ovary activation and others whose products localize at the centrosome and are implicated in chromosomal segregation during meiosis. Functional analysis of these loci will yield insights into the processes of reproduction and chemical signaling in both parasitic and non-parasitic populations and advance understanding of the process of normal and atypical meiosis.
Article
Full-text available
Four main evolutionary lineages of A. mellifera have been described including eastern Europe (C) and western and northern Europe (M). Many apiculturists prefer bees from the C lineage due to their docility and high productivity. In France, the routine importation of bees from the C lineage has resulted in the widespread admixture of bees from the M lineage. The haplodiploid nature of the honeybee Apis mellifera, and its small genome size, permits affordable and extensive genomics studies. As a pilot study of a larger project to characterise French honeybee populations, we sequenced 60 drones sampled from two commercial populations managed for the production of honey and royal jelly. Results indicate a C lineage origin, whilst mitochondrial analysis suggests two drones originated from the O lineage. Analysis of heterozygous SNPs identified potential copy number variants near to genes encoding odorant binding proteins and several cytochrome P450 genes. Signatures of selection were detected using the hapFLK haplotype-based method, revealing several regions under putative selection for royal jelly production. The framework developed during this study will be applied to a broader sampling regime, allowing the genetic diversity of French honeybees to be characterised in detail.
Article
Full-text available
Protection against inflammation and oxidative stress is key in slowing down aging processes. The honey bee (Apis mellifera) shows flexible aging patterns linked to the social role of individual bees. One molecular factor associated with honey bee aging regulation is vitellogenin, a lipoglycophosphoprotein with anti-inflammatory and antioxidant properties. Recently, we identified three genes in Hymenopteran genomes arisen from ancient insect vitellogenin duplications, named vg-like-A, -B, and -C. The function of these vitellogenin homologs is unclear. We hypothesize that some of them might share gene- and protein-level similarities and a longevity-supporting role with vitellogenin. Here, we show how the structure and modifications of the vg-like genes and proteins have diverged from vitellogenin. Furthermore, all three vg-like genes show signs of positive selection, but the spatial location of the selected protein sites differ from those found in vitellogenin. We show that all these genes are expressed in both long-lived winter worker bees and in summer nurse bees with intermediate life expectancy, yet only vg-like-A shows elevated expression in winter bees as found in vitellogenin. Finally, we show that vg-like-A responds more strongly than vitellogenin to inflammatory and oxidative conditions in summer nurse bees, and that also vg-like-B responds to oxidative stress. We associate vg-like-A and, to lesser extent, vg-like-B to the antiaging roles of vitellogenin, but that vg-like-C probably is involved in some other function. Our analysis indicates that an ancient duplication event facilitated the adaptive and functional divergence of vitellogenin and its paralogs in the honey bee.
Article
Full-text available
The arrival to the United States of the Africanized honey bee, a hybrid between European subspecies and the African subspecies Apis mellifera scutellata, is a remarkable model for the study of biological invasions. This immigration has created an opportunity to study the dynamics of secondary contact of honey bee subspecies from African and European lineages in a feral population in South Texas. An 11-year survey of this population (1991–2001) showed that mitochondrial haplotype frequencies changed drastically over time from a resident population of eastern and western European maternal ancestry, to a population dominated by the African haplotype. A subsequent study of the nuclear genome showed that the Africanization process included bidirectional gene flow between European and Africanized honey bees, giving rise to a new panmictic mixture of A. m. scutellata- and European-derived genes. In this study, we examined gene flow patterns in the same population 23 years after the first hybridization event occurred. We found 28 active colonies inhabiting 92 tree cavities surveyed in a 5.14 km2 area, resulting in a colony density of 5.4 colonies/km2. Of these 28 colonies, 25 were of A. m. scutellata maternal ancestry, and three were of western European maternal ancestry. No colonies of eastern European maternal ancestry were detected, although they were present in the earlier samples. Nuclear DNA revealed little change in the introgression of A. m. scutellata-derived genes into the population compared to previous surveys. Our results suggest this feral population remains an admixed swarm with continued low levels of European ancestry and a greater presence of African-derived mitochondrial genetic composition.
Article
Full-text available
Studying the genetic signatures of climate-driven selection can produce insights into local adaptation and the potential impacts of climate change on populations. The honey bee (Apis mellifera) is an interesting species to study local adaptation because it originated in tropical/subtropical climatic regions and subsequently spread into temperate regions. However, little is known about the genetic basis of its adaptation to temperate climates. Here, we resequenced the whole genomes of 10 individual bees from a newly discovered population in temperate China and downloaded resequenced data from 35 individuals from other populations. We found that the new population is an undescribed subspecies in the M-lineage of Apis mellifera (Apis mellifera sinisxinyuan). Analyses of population history show that long-term global temperature has strongly influenced the demographic history of Apis mellifera sinisxinyuan and its divergence from other subspecies. Further analyses comparing temperate and tropical populations identified several candidate genes related to fat body and the Hippo signaling pathway that are potentially involved in adaptation to temperate climates. Our results provide insights into the demographic history of the newly discovered Apis mellifera sinisxinyuan, as well as the genetic basis of adaptation of A. mellifera to temperate climates at the genomic level. These findings will facilitate the selective breeding of A. mellifera to improve the survival of overwintering colonies.
Article
Full-text available
Among forager honey bees, scouts seek new resources and return to the colony, enlisting recruits to collect these resources. Differentially expressed genes between these behaviors and genetic variability in scouting phenotypes have been reported. Whole-genome sequencing of 44 Apis mellifera scouts and recruits was undertaken to detect variants and further understand the genetic architecture underlying the behavioral differences between scouts and recruits. The median coverage depth in recruits and scouts was 10.01 and 10.7 X, respectively. Representation of bacterial species among the unmapped reads reflected a more diverse microbiome in scouts than recruits. Overall, 1,412,705 polymorphic positions were analyzed for associations with scouting behavior, and 212 significant (p-value < 0.0001) associations with scouting corresponding to 137 positions were detected. Most frequent putative transcription factor binding sites proximal to significant variants included Broad-complex 4, Broad-complex 1, Hunchback, and CF2-II. Three variants associated with scouting were located within coding regions of ncRNAs including one codon change (LOC102653644) and 2 frameshift indels (LOC102654879 and LOC102655256). Significant variants were also identified on the 5'UTR of membrin, and 3'UTRs of laccase 2 and diacylglycerol kinase theta. The 60 significant variants located within introns corresponded to 39 genes and most of these positions were > 1000 bp apart from each other. A number of these variants were mapped to ncRNA LOC100578102, solute carrier family 12 member 6-like gene, and LOC100576965 (meprin and TRAF-C homology domain containing gene). Functional categories represented among the genes corresponding to significant variants included: neuronal function, exoskeleton, immune response, salivary gland development, and enzymatic food processing. These categories offer a glimpse into the molecular support to the behaviors of scouts and recruits. The level of association between genomic variants and scouting behavior observed in this study may be linked to the honey bee's genomic plasticity and fluidity of transition between castes.
Article
Full-text available
Honey bees are exposed to many damaging pathogens and parasites. The most devastating is Varroa destructor, which mainly affects the brood. A promising approach for preventing its spread is to breed Varroa-resistant honey bees. One trait that has been shown to provide significant resistance against the Varroa mite is hygienic behavior, which is a behavioral response of honeybee workers to brood diseases in general. Here we report the use of an Affymetrix 44K SNP array to analyze SNPs associated with detection and uncapping of Varroa-parasitized brood by individual worker bees (Apis mellifera). For this study, 22,000 individually labeled bees were video-monitored and a sample of 122 cases and 122 controls was collected and analyzed to determine the dependence / independence of SNP genotypes from hygienic and non-hygienic behavior on a genome-wide scale. After false-discovery rate correction of the p-values, six SNP markers had highly significant associations with the trait investigated (alpha < 0.01). Inspection of the genomic regions around these SNPs led to the discovery of putative candidate genes.
Article
Full-text available
The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolution. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subsequently studied the relative rates of molecular evolution at these caste-associated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection coefficients suggest that both nurse and larval genes putatively associated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as caste.
Article
Full-text available
Canadian honey bees, like all honey bees in the New World, originated from centuries of importation of predominately European subspecies, but their precise genetic ancestry has not been investigated. We used a citizen science approach that engaged a diverse group of beekeepers to undertake the largest population genetic study of Canadian honey bees. We used the dataset to characterize the ancestry of Canadian honey bee populations, test if Northern Canadian colonies have a greater proportion of ancestry from subspecies native to Northern Europe, and determine the effectiveness of using single nucleotide polymorphism (SNPs) to distinguish between Canadian bees and the aggressive and invasive Africanized honey bee found from South America to the Southern United States. We genotyped 855 worker honey bees at 91 ancestrally informative SNPs and found very low levels of genetic differentiation within Canada at these SNPs and small but significant differences in ancestry between provinces. Honey bee populations in Northern and Western Canada were more closely related to subspecies from Southern and Mediterranean Europe. We attributed this pattern to differences in importation practices within Canada. Finally, we were able to accurately discriminate between Africanized bees and Canadian bees using the ancestrally informative SNPs, supporting the use of SNPs for accurately detecting Africanized honey bees and providing valuable insights into the genetic structure of Canadian bees, all while engaging beekeepers in the scientific process. © 2015, International Union for the Study of Social Insects (IUSSI).
Article
Full-text available
With increased globalisation and homogenisation, the maintenance of genetic integrity in local populations of agriculturally important species is of increasing concern. The western honeybee (Apis mellifera) provides an interesting perspective as it is both managed and wild, with a large native range and much larger introduced range. We employed a newly created 95 single nucleotide polymorphism (SNP) test to characterise the genetic ancestry of the Australian commercial and feral honeybee populations. We found that most individuals were hybrids of mainly Western and Eastern European ancestry. Introductions of bees from North Africa are known from the historical record, and we show here the presence of alleles of African ancestry in some Australian bees, at levels comparable to those seen in the commercial populations of European-derived bees in North America.
Article
Full-text available
American foulbrood (AFB) is a severe brood disease in honeybees. Since sustainable treatment is not available, selection of genetically resistant honeybee stock is highly desirable. Using a set of 291 heterozygous microsatellite markers in a bulk segregant analysis with subsequent finemapping of haploid drone offspring from a single honeybee queen, we identified one significant and three suggestive quantitative trait loci as well as one significant epistatic interaction influencing prepupal survival after AFB infection. While we were not able to verify specific genes responsible for tolerance, we suggest that developmental genes may have played an important role. The identified markers can be used as regions of interest in future mapping or expression studies. In order to use them for marker-assisted selection in breeding programmes for AFB-resistant honeybee stock, it will be required to evaluate these loci more extensively under variable experimental conditions.
Article
Full-text available
Meiotic recombination is a fundamental cellular process, with important consequences for evolution and genome integrity. However, we know little about how recombination rates vary across the genomes of most species and the molecular and evolutionary determinants of this variation. The honeybee, Apis mellifera, has extremely high rates of meiotic recombination, although the evolutionary causes and consequences of this are unclear. Here we use patterns of linkage disequilibrium in whole genome resequencing data from 30 diploid honeybees to construct a fine-scale map of rates of crossing over in the genome. We find that, in contrast to vertebrate genomes, the recombination landscape is not strongly punctate. Crossover rates strongly correlate with levels of genetic variation, but not divergence, which indicates a pervasive impact of selection on the genome. Germ-line methylated genes have reduced crossover rate, which could indicate a role of methylation in suppressing recombination. Controlling for the effects of methylation, we do not infer a strong association between gene expression patterns and recombination. The site frequency spectrum is strongly skewed from neutral expectations in honeybees: rare variants are dominated by AT-biased mutations, whereas GC-biased mutations are found at higher frequencies, indicative of a major influence of GC-biased gene conversion (gBGC), which we infer to generate an allele fixation bias 5 - 50 times the genomic average estimated in humans. We uncover further evidence that this repair bias specifically affects transitions and favours fixation of CpG sites. Recombination, via gBGC, therefore appears to have profound consequences on genome evolution in honeybees and interferes with the process of natural selection. These findings have important implications for our understanding of the forces driving molecular evolution.
Article
Full-text available
All hymenopteran species, such as bees, wasps and ants, are characterized by the common principle of haplodiploid sex determination in which haploid males arise from unfertilized eggs and females from fertilized eggs. The underlying molecular mechanism has been studied in detail in the western honey bee Apis mellifera, in which the gene complementary sex determiner (csd) acts as primary signal of the sex determining pathway, initiating female development by csd-heterozygotes. Csd arose from gene duplication of the feminizer (fem) gene, a transformer (tra) ortholog, and mediates in conjunction with transformer2 (tra2) sex-specific splicing of fem. Comparative molecular analyses identified fem/tra and its downstream target doublesex (dsx) as conserved unit within the sex determining pathway of holometabolous insects. In this study, we aim to examine evolutionary differences among these key regulators. Our main hypothesis is that sex determining key regulators in Hymenoptera species show signs of coevolution within single phylogenetic lineages. We take advantage of several newly sequenced genomes of bee species to test this hypothesis using bioinformatic approaches. We found evidences that duplications of fem are restricted to certain bee lineages and notable amino acid differences of tra2 between Apis and non-Apis species propose structural changes in Tra2 protein affecting co-regulatory function on target genes. These findings may help to gain deeper insights into the ancestral mode of hymenopteran sex determination and support the common view of the remarkable evolutionary flexibility in this regulatory pathway.
Article
Full-text available
Social hymenoptera, the honey bee (Apis mellifera) in particular, have ultra-high crossover rates and a large degree of intra-genomic variation in crossover rates. Aligned with haploid genomics of males, this makes them a potential model for examining the causes and consequences of crossing over. To address why social insects have such high crossing-over rates and the consequences of this, we constructed a high-resolution recombination atlas by sequencing 55 individuals from three colonies with an average marker density of 314 bp/marker. We find crossing over to be especially high in proximity to genes upregulated in worker brains, but see no evidence for a coupling with immune-related functioning. We detect only a low rate of non-crossover gene conversion, contrary to current evidence. This is in striking contrast to the ultrahigh crossing-over rate, almost double that previously estimated from lower resolution data. We robustly recover the predicted intragenomic correlations between crossing over and both population level diversity and GC content, which could be best explained as indirect and direct consequences of crossing over, respectively. Our data are consistent with the view that diversification of worker behavior, but not immune function, is a driver of the high crossing-over rate in bees. While we see both high diversity and high GC content associated with high crossing-over rates, our estimate of the low non-crossover rate demonstrates that high non-crossover rates are not a necessary consequence of high recombination rates.
Article
Full-text available
It is increasingly apparent that genes and networks that influence complex behavior are evolutionary conserved, which is paradoxical considering that behavior is labile over evolutionary timescales. How does adaptive change in behavior arise if behavior is controlled by conserved, pleiotropic, and likely evolutionary constrained genes? Pleiotropy and connectedness are known to constrain the general rate of protein evolution, prompting some to suggest that the evolution of complex traits, including behavior, is fuelled by regulatory sequence evolution. However, we seldom have data on the strength of selection on mutations in coding and regulatory sequences, and this hinders our ability to study how pleiotropy influences coding and regulatory sequence evolution. Here we use population genomics to estimate the strength of selection on coding and regulatory mutations for a transcriptional regulatory network that influences complex behavior of honey bees. We found that replacement mutations in highly connected transcription factors and target genes experience significantly stronger negative selection relative to weakly connected transcription factors and targets. Adaptively evolving proteins were significantly more likely to reside at the periphery of the regulatory network, while proteins with signs of negative selection were near the core of the network. Interestingly, connectedness and network structure had minimal influence on the strength of selection on putative regulatory sequences for both transcription factors and their targets. Our study indicates that adaptive evolution of complex behavior can arise because of positive selection on protein-coding mutations in peripheral genes, and on regulatory sequence mutations in both transcription factors and their targets throughout the network.
Article
Full-text available
The honeybee Apis mellifera has major ecological and economic importance. We analyze patterns of genetic variation at 8.3 million SNPs, identified by sequencing 140 honeybee genomes from a worldwide sample of 14 populations at a combined total depth of 634×. These data provide insight into the evolutionary history and genetic basis of local adaptation in this species. We find evidence that population sizes have fluctuated greatly, mirroring historical fluctuations in climate, although contemporary populations have high genetic diversity, indicating the absence of domestication bottlenecks. Levels of genetic variation are strongly shaped by natural selection and are highly correlated with patterns of gene expression and DNA methylation. We identify genomic signatures of local adaptation, which are enriched in genes expressed in workers and in immune system– and sperm motility–related genes that might underlie geographic variation in reproduction, dispersal and disease resistance. This study provides a framework for future investigations into responses to pathogens and climate change in honeybees.
Article
Full-text available
The recognition that the Dark European honey bee, Apis mellifera mellifera, is increasingly threatened in its native range has led to the establishment of conservation programmes and protected areas throughout western Europe. Previous molecular surveys showed that, despite management strategies to preserve the genetic integrity of A. m. mellifera, protected populations had a measurable component of their gene pool derived from commercial C-lineage honey bees. Here we used both sequence data from the tRNAleu-cox2 intergenic mtDNA region and a genome-wide scan, with over 1183 single nucleotide polymorphisms (SNPs), to assess genetic diversity and introgression levels in several protected populations of A. m. mellifera, which were then compared with samples collected from unprotected populations. MtDNA analysis of the protected populations revealed a single colony bearing a foreign haplotype, whereas SNPs showed varying levels of introgression ranging from virtually zero in Norway to about 14% in Denmark. Introgression overall was higher in unprotected (30%) than in protected populations (8%), and is reflected in larger SNP diversity levels of the former, although opposite diversity levels were observed for mtDNA. These results suggest that, despite controlled breeding, some protected populations still require adjustments to the management strategies to further purge foreign alleles, which can be identified by SNPs.
Article
Full-text available
Significance Most hypotheses explaining the evolution of sociality in insects assume that positive selection drives the evolution of worker traits. Yet we know little about the extent of natural selection acting on social insects. We produced a map of positive selection for the honey bee through analysis of 40 individual genomes. We found strong evidence of positive selection acting on genes and regulatory sequences, and we discovered that mutations in worker-biased proteins tend to have greater fitness effects than mutations in queen-biased proteins. We also found many instances of positive selection acting on genes that influence worker traits, suggesting that worker phenotypes represent a major vector for adaptation in social insects.
Article
Full-text available
De la Rúa et al. (2013) express some concerns about the conclusions of our recent study showing that management increases genetic diversity of honey bees (Apis mellifera) by promoting admixture (Harpur et al. 2012). We provide a brief review of the literature on the population genetics of A. mellifera and show that we utilized appropriate sampling methods to estimate genetic diversity in the focal populations. Our finding of higher genetic diversity in two managed A. mellifera populations on two different continents is expected to be the norm given the large number of studies documenting admixture in honey bees. Our study focused on elucidating how management affects genetic diversity in honey bees, not on how to best manage bee colonies. We do not endorse the intentional admixture of honey bee populations, and we agree with De la Rúa et al. (2013) that native honey bee subspecies should be conserved.
Article
Full-text available
Nosema ceranae has been recently introduced into the honeybee Apis mellifera as a novel microsporidian gut parasite. To locate the genetic region involved in N. ceranae infection tolerance, we fed N. ceranae spores to haploid drones of a F1 hybrid queen produced from a cross between a queen of a Nosema resistant bred strain and drones of susceptible colonies. The spore loads of the infected F1 drones were used as the phenotype to identify quantitative trait loci (QTLs) associated with N. ceranae spore load. One hundred forty-eight infected drones were individually genotyped with microsatellite markers at an average marker distance of 20 cM along the genome. Four QTLs were significantly associated with low spore load, explaining 20.4 % of total spore load variance. Moreover, a candidate gene Aubergine (Aub) within the major QTL region was significantly overexpressed in drones with low spore loads than in those with high spore loads. Our results confirm the genetic basis of Nosema tolerance in the selected strain and show that both additive effects and epistatic interactions among the QTLs interfere with the tested phenotype.
Article
Full-text available
Eusocial Hymenoptera, such as the European honey bee, Apis mellifera, have the highest recombination rates of multicellular animals.(1) Recently, we showed(2) that a side-effect of recombination in the honey bee, GC biased gene conversion (bGC), helps maintain the unusual bimodal GC-content distribution of the bee genome by increasing GC-content in high recombination areas while low recombination areas are losing GC-content because of biased AT mutations and low rates of bGC. Although the very high recombination rate of A. mellifera makes GC-content evolution easier to study, the pattern is consistent with results found in many other species including mammals and yeast.(3) Also consistent across phyla is the association of higher genetic diversity and divergence with high GC and high recombination areas.(4) (,) (5) Finally, we showed that genes overexpressed in the brains of workers cluster in GC-rich genomic areas with the highest rates of recombination and molecular evolution.(2) In this Addendum we present a conceptual model of how eusociality and high recombination rates may co-evolve.
Article
Full-text available
Varroa mites (V. destructor) are a major threat to honey bees (Apis melilfera) and beekeeping worldwide and likely lead to colony decline if colonies are not treated. Most treatments involve chemical control of the mites; however, Varroa has evolved resistance to many of these miticides, leaving beekeepers with a limited number of alternatives. A non-chemical control method is highly desirable for numerous reasons including lack of chemical residues and decreased likelihood of resistance. Varroa sensitive hygiene behavior is one of two behaviors identified that are most important for controlling the growth of Varroa populations in bee hives. To identify genes influencing this trait, a study was conducted to map quantitative trait loci (QTL). Individual workers of a backcross family were observed and evaluated for their VSH behavior in a mite-infested observation hive. Bees that uncapped or removed pupae were identified. The genotypes for 1,340 informative single nucleotide polymorphisms were used to construct a high-resolution genetic map and interval mapping was used to analyze the association of the genotypes with the performance of Varroa sensitive hygiene. We identified one major QTL on chromosome 9 (LOD score = 3.21) and a suggestive QTL on chromosome 1 (LOD = 1.95). The QTL confidence interval on chromosome 9 contains the gene 'no receptor potential A' and a dopamine receptor. 'No receptor potential A' is involved in vision and olfaction in Drosophila, and dopamine signaling has been previously shown to be required for aversive olfactory learning in honey bees, which is probably necessary for identifying mites within brood cells. Further studies on these candidate genes may allow for breeding bees with this trait using marker-assisted selection.
Article
Full-text available
The rise of insect societies, marked by the formation of reproductive and sterile castes, represents a major unsolved mystery in evolution. Across several independent origins of sociality, the genomes of social hymenopterans share two peculiar attributes: high recombination and low but heterogeneous GC content. For example, the genome of the honey bee, Apis mellifera, represents a mosaic of GC-poor and GC-rich regions with rates of recombination an order of magnitude higher than in humans. However, it is unclear how heterogeneity in GC content arises, and how it relates to the expression and evolution of worker traits. Using population genetic analyses, we demonstrate a bias in the allele frequency and fixation rate of derived C or G mutations in high-recombination regions, consistent with recombination's causal influence on GC-content evolution via biased gene conversion. We also show that recombination and biased gene conversion actively maintain the heterogeneous GC content of the honey bee genome despite an overall A/T mutation bias. Further, we found that GC-rich genes and intergenic regions have higher levels of genetic diversity and divergence relative to GC-poor regions, also consistent with recombination's causal influence on the rate of molecular evolution. Finally, we found that genes associated with behavior and those with worker-biased expression are found in GC-rich regions of the bee genome and also experience high rates of molecular evolution. Taken together, these findings suggest that recombination acts to maintain a genetically diverse and dynamic part of the genome where genes underlying worker behavior evolve more quickly.
Article
Full-text available
The process of domestication often brings about profound changes in levels of genetic variation in animals and plants. The honey bee, Apis mellifera, has been managed by humans for centuries for both honey and wax production and crop pollination. Human management and selective breeding are believed to have caused reductions in genetic diversity in honey bee populations, thereby contributing to the global declines threatening this ecologically and economically important insect. However, previous studies supporting this claim mostly relied on population genetic comparisons of European and African (or Africanized) honey bee races; such conclusions require reassessment given recent evidence demonstrating that the honey bee originated in Africa and colonized Europe via two independent expansions. We sampled honey bee workers from two managed populations in North America and Europe as well as several old-world progenitor populations in Africa, East and West Europe. Managed bees had highly introgressed genomes representing admixture between East and West European progenitor populations. We found that managed honey bees actually have higher levels of genetic diversity compared with their progenitors in East and West Europe, providing an unusual example whereby human management increases genetic diversity by promoting admixture. The relationship between genetic diversity and honey bee declines is tenuous given that managed bees have more genetic diversity than their progenitors and many viable domesticated animals.
Article
Full-text available
Varroa destructor is a highly virulent ectoparasitic mite of the honey bee Apis mellifera and a major cause of colony losses for global apiculture. Typically, chemical treatment is essential to control the parasite population in the honey bee colony. Nevertheless a few honey bee populations survive mite infestation without any treatment. We used one such Varroa mite tolerant honey bee lineage from the island of Gotland, Sweden, to identify quantitative trait loci (QTL) controlling reduced mite reproduction. We crossed a queen from this tolerant population with drones from susceptible colonies to rear hybrid queens. Two hybrid queens were used to produce a mapping population of haploid drones. We discriminated drone pupae with and without mite reproduction, and screened the genome for potential QTL using a total of 216 heterozygous microsatellite markers in a bulk segregant analysis. Subsequently, we fine mapped three candidate target regions on chromosomes 4, 7, and 9. Although the individual effect of these three QTL was found to be relatively small, the set of all three had significant impact on suppression of V. destructor reproduction by epistasis. Although it is in principle possible to use these loci for marker-assisted selection, the strong epistatic effects between the three loci complicate selective breeding programs with the Gotland Varroa tolerant honey bee stock.