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Genome-wide analysis of signatures of selection in populations of African honey bees (Apis mellifera) using new web-based tools.

Fuller ZL, Niño EL, Patch HM, Bedoya-Reina OC, Baumgarten T, Muli E, Mumoki F, Ratan A, McGraw J, Frazier M, Masiga D, Schuster S, Grozinger CM, Miller W - BMC Genomics (2015)

Bottom Line: The dense coverage allowed us to apply several computational procedures to study population structure and the evolutionary relationships among the populations, and to detect signs of adaptive evolution across the genome.While there is considerable gene flow among the sampled populations, there are clear distinctions between populations from the northern desert region and those from the temperate, savannah region.We identified several genes showing population genetic patterns consistent with positive selection within African bee populations, and between these populations and European A. mellifera or Asian Apis florea.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Pennsylvania State University, University Park, PA, USA. zlf105@psu.edu.

ABSTRACT

Background: With the development of inexpensive, high-throughput sequencing technologies, it has become feasible to examine questions related to population genetics and molecular evolution of non-model species in their ecological contexts on a genome-wide scale. Here, we employed a newly developed suite of integrated, web-based programs to examine population dynamics and signatures of selection across the genome using several well-established tests, including F ST, pN/pS, and McDonald-Kreitman. We applied these techniques to study populations of honey bees (Apis mellifera) in East Africa. In Kenya, there are several described A. mellifera subspecies, which are thought to be localized to distinct ecological regions.

Results: We performed whole genome sequencing of 11 worker honey bees from apiaries distributed throughout Kenya and identified 3.6 million putative single-nucleotide polymorphisms. The dense coverage allowed us to apply several computational procedures to study population structure and the evolutionary relationships among the populations, and to detect signs of adaptive evolution across the genome. While there is considerable gene flow among the sampled populations, there are clear distinctions between populations from the northern desert region and those from the temperate, savannah region. We identified several genes showing population genetic patterns consistent with positive selection within African bee populations, and between these populations and European A. mellifera or Asian Apis florea.

Conclusions: These results lay the groundwork for future studies of adaptive ecological evolution in honey bees, and demonstrate the use of new, freely available web-based tools and workflows ( http://usegalaxy.org/r/kenyanbee ) that can be applied to any model system with genomic information.

No MeSH data available.


Related in: MedlinePlus

Geographic, phylogenetic, and principal component relationship of Kenyan honeybees. a) Geographic locations of sampled apiaries. Each individual is designated according to the ecological region in which it was sampled, with S = savannah, C = coast, D = desert, and M = mountains. Colors indicate Köppen-Geiger climate regions, see (Peel, et al. 2007) [106]. b) Neighbor-joining tree inferred from full mitochondrial sequences. The evolutionary distances were computed using the Maximum Composite Likelihood method and are in the units of the number of base substitutions per site. The tree is drawn to scale. c) Neighbor-joining tree inferred from full nuclear sequences. Numbers indicate the branch lengths
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Fig1: Geographic, phylogenetic, and principal component relationship of Kenyan honeybees. a) Geographic locations of sampled apiaries. Each individual is designated according to the ecological region in which it was sampled, with S = savannah, C = coast, D = desert, and M = mountains. Colors indicate Köppen-Geiger climate regions, see (Peel, et al. 2007) [106]. b) Neighbor-joining tree inferred from full mitochondrial sequences. The evolutionary distances were computed using the Maximum Composite Likelihood method and are in the units of the number of base substitutions per site. The tree is drawn to scale. c) Neighbor-joining tree inferred from full nuclear sequences. Numbers indicate the branch lengths

Mentions: We sequenced the genomes of 11 individual worker bees from 11 different apiaries distributed throughout four distinct ecological regions in Kenya (savannah, coast, desert, mountain; see Fig. 1a for a map of the locations of the sampled individuals and Table 1 for details on the specimens). These regions have been previously described as areas of subspecies endemism [7, 9, 11]. Previous analyses with commonly used mitochondrial markers indicated that bees in these apiaries represented five different subspecies of Apis mellifera: scutellata, monticola, littorea, and yemenitica or simensis (see Additional file 1: Table S1 for further information about the precise sampling locations, and Muli et al. (2014) [12]. Sites S1, S2, S3 and S4 are within the described distribution of Apis mellifera scutellata. The original description of this habitat is “thorn woodland and tall grass savannah”, but A. m. scutellata is found in more diverse habitats across eastern Africa [7]. Sites 1C, 2C, and 3C are located in tropical coastal habitat where Apis mellifera litorea is said to occur. The apiary (1C) at the Gete Ruins is in the Arabuko Sokoke Forest Reserve, a remnant of the coastal tropical forest that supports a number of unique endemic species. Outside of this region, along the coast, there has been extensive alteration of the native habitat and potential incursion of A. m. scutellata. Sites 1D, 2D and 3D are located in the hot, dry Mandera district. At least two subspecies likely occur in this region, A. m. yemenitica and A. m. simensis [7, 9, 11]. The final subspecies, A.m. monticola, has received considerable attention in the literature (see Ruttner 1987, Hepburn and Radloff 1998, Gruber et al 2013 [7, 9, 13]). It has been described as “the bee of the rain forests of the East African mountains found at altitudes of 2000-3000 m” [7]. Only one site (1 M, Mt Elgon, Moorland) in our study was above 2000 m where A. m. monticola is said to occur. The bees were sampled during a 2010 survey of the health of Kenyan bee populations (see Muli et al. 2014 [12]). Several parasites and pathogens were identified in Kenyan bee colonies during this survey: Acute bee paralysis virus (ABPV), Black queen cell virus, (BQCV), Deformed wing virus (DWV), Nosema apis (a microsporidian gut parasite), and Varroa destructor (a parasitic mite); see Table 1 and Additional file 1: Table S1 for a listing of the parasites and pathogens found at each site. Notably, the honey bee colonies sampled at 1D, 2D, and 3D were free of all tested parasites and pathogens (see Table 1).Fig. 1


Genome-wide analysis of signatures of selection in populations of African honey bees (Apis mellifera) using new web-based tools.

Fuller ZL, Niño EL, Patch HM, Bedoya-Reina OC, Baumgarten T, Muli E, Mumoki F, Ratan A, McGraw J, Frazier M, Masiga D, Schuster S, Grozinger CM, Miller W - BMC Genomics (2015)

Geographic, phylogenetic, and principal component relationship of Kenyan honeybees. a) Geographic locations of sampled apiaries. Each individual is designated according to the ecological region in which it was sampled, with S = savannah, C = coast, D = desert, and M = mountains. Colors indicate Köppen-Geiger climate regions, see (Peel, et al. 2007) [106]. b) Neighbor-joining tree inferred from full mitochondrial sequences. The evolutionary distances were computed using the Maximum Composite Likelihood method and are in the units of the number of base substitutions per site. The tree is drawn to scale. c) Neighbor-joining tree inferred from full nuclear sequences. Numbers indicate the branch lengths
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4496815&req=5

Fig1: Geographic, phylogenetic, and principal component relationship of Kenyan honeybees. a) Geographic locations of sampled apiaries. Each individual is designated according to the ecological region in which it was sampled, with S = savannah, C = coast, D = desert, and M = mountains. Colors indicate Köppen-Geiger climate regions, see (Peel, et al. 2007) [106]. b) Neighbor-joining tree inferred from full mitochondrial sequences. The evolutionary distances were computed using the Maximum Composite Likelihood method and are in the units of the number of base substitutions per site. The tree is drawn to scale. c) Neighbor-joining tree inferred from full nuclear sequences. Numbers indicate the branch lengths
Mentions: We sequenced the genomes of 11 individual worker bees from 11 different apiaries distributed throughout four distinct ecological regions in Kenya (savannah, coast, desert, mountain; see Fig. 1a for a map of the locations of the sampled individuals and Table 1 for details on the specimens). These regions have been previously described as areas of subspecies endemism [7, 9, 11]. Previous analyses with commonly used mitochondrial markers indicated that bees in these apiaries represented five different subspecies of Apis mellifera: scutellata, monticola, littorea, and yemenitica or simensis (see Additional file 1: Table S1 for further information about the precise sampling locations, and Muli et al. (2014) [12]. Sites S1, S2, S3 and S4 are within the described distribution of Apis mellifera scutellata. The original description of this habitat is “thorn woodland and tall grass savannah”, but A. m. scutellata is found in more diverse habitats across eastern Africa [7]. Sites 1C, 2C, and 3C are located in tropical coastal habitat where Apis mellifera litorea is said to occur. The apiary (1C) at the Gete Ruins is in the Arabuko Sokoke Forest Reserve, a remnant of the coastal tropical forest that supports a number of unique endemic species. Outside of this region, along the coast, there has been extensive alteration of the native habitat and potential incursion of A. m. scutellata. Sites 1D, 2D and 3D are located in the hot, dry Mandera district. At least two subspecies likely occur in this region, A. m. yemenitica and A. m. simensis [7, 9, 11]. The final subspecies, A.m. monticola, has received considerable attention in the literature (see Ruttner 1987, Hepburn and Radloff 1998, Gruber et al 2013 [7, 9, 13]). It has been described as “the bee of the rain forests of the East African mountains found at altitudes of 2000-3000 m” [7]. Only one site (1 M, Mt Elgon, Moorland) in our study was above 2000 m where A. m. monticola is said to occur. The bees were sampled during a 2010 survey of the health of Kenyan bee populations (see Muli et al. 2014 [12]). Several parasites and pathogens were identified in Kenyan bee colonies during this survey: Acute bee paralysis virus (ABPV), Black queen cell virus, (BQCV), Deformed wing virus (DWV), Nosema apis (a microsporidian gut parasite), and Varroa destructor (a parasitic mite); see Table 1 and Additional file 1: Table S1 for a listing of the parasites and pathogens found at each site. Notably, the honey bee colonies sampled at 1D, 2D, and 3D were free of all tested parasites and pathogens (see Table 1).Fig. 1

Bottom Line: The dense coverage allowed us to apply several computational procedures to study population structure and the evolutionary relationships among the populations, and to detect signs of adaptive evolution across the genome.While there is considerable gene flow among the sampled populations, there are clear distinctions between populations from the northern desert region and those from the temperate, savannah region.We identified several genes showing population genetic patterns consistent with positive selection within African bee populations, and between these populations and European A. mellifera or Asian Apis florea.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Pennsylvania State University, University Park, PA, USA. zlf105@psu.edu.

ABSTRACT

Background: With the development of inexpensive, high-throughput sequencing technologies, it has become feasible to examine questions related to population genetics and molecular evolution of non-model species in their ecological contexts on a genome-wide scale. Here, we employed a newly developed suite of integrated, web-based programs to examine population dynamics and signatures of selection across the genome using several well-established tests, including F ST, pN/pS, and McDonald-Kreitman. We applied these techniques to study populations of honey bees (Apis mellifera) in East Africa. In Kenya, there are several described A. mellifera subspecies, which are thought to be localized to distinct ecological regions.

Results: We performed whole genome sequencing of 11 worker honey bees from apiaries distributed throughout Kenya and identified 3.6 million putative single-nucleotide polymorphisms. The dense coverage allowed us to apply several computational procedures to study population structure and the evolutionary relationships among the populations, and to detect signs of adaptive evolution across the genome. While there is considerable gene flow among the sampled populations, there are clear distinctions between populations from the northern desert region and those from the temperate, savannah region. We identified several genes showing population genetic patterns consistent with positive selection within African bee populations, and between these populations and European A. mellifera or Asian Apis florea.

Conclusions: These results lay the groundwork for future studies of adaptive ecological evolution in honey bees, and demonstrate the use of new, freely available web-based tools and workflows ( http://usegalaxy.org/r/kenyanbee ) that can be applied to any model system with genomic information.

No MeSH data available.


Related in: MedlinePlus