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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.


FST analysis of the chromosomal region containing the Neuroligin-3 gene. a) Plot of FST (Reich-Patterson formulation) between Desert and Plains bees at 4,507 SNPs in a 200-kb interval on Chromosome 9 (Group9.10) that spans the first two exons of the Neuroligin-3 gene (GB42603; blue rectangles; transcribed right-to-left). Orange rectangles indicate the two exons of annotated gene GB42882, putatively transcribed on the opposite strand, though we find the evidence for existence of a functional gene unconvincing. Genome-wide, 10 % of the FST values are larger than 0.20 — indicated with red. Light blue bars represent non-significant FST values. b) The interval 3,143,154-3,143,747 has a statistically significant concentration of SNPs with FST in the highest 10 %, meeting our criterion for putative positive selection by the FST criterion
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Fig5: FST analysis of the chromosomal region containing the Neuroligin-3 gene. a) Plot of FST (Reich-Patterson formulation) between Desert and Plains bees at 4,507 SNPs in a 200-kb interval on Chromosome 9 (Group9.10) that spans the first two exons of the Neuroligin-3 gene (GB42603; blue rectangles; transcribed right-to-left). Orange rectangles indicate the two exons of annotated gene GB42882, putatively transcribed on the opposite strand, though we find the evidence for existence of a functional gene unconvincing. Genome-wide, 10 % of the FST values are larger than 0.20 — indicated with red. Light blue bars represent non-significant FST values. b) The interval 3,143,154-3,143,747 has a statistically significant concentration of SNPs with FST in the highest 10 %, meeting our criterion for putative positive selection by the FST criterion

Mentions: Another gene of interest is Neuroligin 3 (Nlg3, GB42603; Fig. 5). Nlg3 is involved in central nervous system development and is expressed in higher order processing centers in the honey bee brain [95]. The interval with high FST that intersects Nlg3 spans around 600 bp with the 202 kb intron between exon 1 and exon 2 (Fig. 5b). Nlg3 has several orthologs found within the insect class that also have long first intron sequences, including the parasitoid wasp (Nasonia vitrpennis, 130 kb), the red flour beetle (Tribolium castaneum, 100 kb), the dwarf honeybee (Apis florea, 202 kb), the leafcutter bee (Megachile rotundata, 95 kb), the pea aphid (Acrythosiphon pisum, 143 kb) and the bumble bee (Bombus terrestris, 187 kb). The evolutionary conservation of a large intronic region hints at the presence of essential regulatory elements.Fig. 5


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)

FST analysis of the chromosomal region containing the Neuroligin-3 gene. a) Plot of FST (Reich-Patterson formulation) between Desert and Plains bees at 4,507 SNPs in a 200-kb interval on Chromosome 9 (Group9.10) that spans the first two exons of the Neuroligin-3 gene (GB42603; blue rectangles; transcribed right-to-left). Orange rectangles indicate the two exons of annotated gene GB42882, putatively transcribed on the opposite strand, though we find the evidence for existence of a functional gene unconvincing. Genome-wide, 10 % of the FST values are larger than 0.20 — indicated with red. Light blue bars represent non-significant FST values. b) The interval 3,143,154-3,143,747 has a statistically significant concentration of SNPs with FST in the highest 10 %, meeting our criterion for putative positive selection by the FST criterion
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: FST analysis of the chromosomal region containing the Neuroligin-3 gene. a) Plot of FST (Reich-Patterson formulation) between Desert and Plains bees at 4,507 SNPs in a 200-kb interval on Chromosome 9 (Group9.10) that spans the first two exons of the Neuroligin-3 gene (GB42603; blue rectangles; transcribed right-to-left). Orange rectangles indicate the two exons of annotated gene GB42882, putatively transcribed on the opposite strand, though we find the evidence for existence of a functional gene unconvincing. Genome-wide, 10 % of the FST values are larger than 0.20 — indicated with red. Light blue bars represent non-significant FST values. b) The interval 3,143,154-3,143,747 has a statistically significant concentration of SNPs with FST in the highest 10 %, meeting our criterion for putative positive selection by the FST criterion
Mentions: Another gene of interest is Neuroligin 3 (Nlg3, GB42603; Fig. 5). Nlg3 is involved in central nervous system development and is expressed in higher order processing centers in the honey bee brain [95]. The interval with high FST that intersects Nlg3 spans around 600 bp with the 202 kb intron between exon 1 and exon 2 (Fig. 5b). Nlg3 has several orthologs found within the insect class that also have long first intron sequences, including the parasitoid wasp (Nasonia vitrpennis, 130 kb), the red flour beetle (Tribolium castaneum, 100 kb), the dwarf honeybee (Apis florea, 202 kb), the leafcutter bee (Megachile rotundata, 95 kb), the pea aphid (Acrythosiphon pisum, 143 kb) and the bumble bee (Bombus terrestris, 187 kb). The evolutionary conservation of a large intronic region hints at the presence of essential regulatory elements.Fig. 5

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.